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Part of the book series: Cancer Drug Discovery and Development ((CDD&D))

Abstract

The tubulin molecule is an α/β heterodimer. In most eukaryotes both α-and β-tubulin consist of isotypes encoded by different genes and differing in amino acid sequence. Differences among isotypes are often highly conserved in evolution, suggesting that they have functional significance. The complex isotype families in mammals, Drosophila and higher plants have been particularly well studied. Different isotypes often have different cellular and tissue distributions. In addition, purified isotypes display different properties including assembly, GTPase, conformation, dynamics, and ability to interact with anti-tumor drugs. The different cellular, tissue, and species distribution, as well as their primary structures and their in vitro properties give clues as to the possible functions of the different isotypes, which will be discussed in this chapter.

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References

  1. Bryan J, Wilson L. Are cytoplasmic microtubules heteropolymers? Proc Nat Acad Sci USA 1971;68:1762–1766.

    Article  PubMed  CAS  Google Scholar 

  2. Ludueña RF, Shooter EM, Wilson L. Structure of the tubulin dimer. J Biol Chem 1977;252:7006–7014.

    PubMed  Google Scholar 

  3. Ponstingl H, Krauhs E, Little M, Kempf T. Complete amino acid sequence of α-tubulin from porcine brain. Proc Nat Acad Sci USA 1981;78:2757–2761.

    Article  PubMed  CAS  Google Scholar 

  4. Krauhs E, Little M, Kempf T, Hofer-Warbinek R, Ade W, Ponstingl H. Complete amino acid sequence of β-tubulin from porcine brain. Proc Nat Acad Sci USA 1981;78:4156–4160.

    Article  PubMed  CAS  Google Scholar 

  5. Behnke O, Forer A. Evidence for four classes of microtubules in individual cells. J Cell Sci 1967;2:169–192.

    PubMed  CAS  Google Scholar 

  6. Fulton C, Simpson PA. Selective synthesis and utilization of flagellar tubulin. The multi-tubulin hypothesis. In: Goldman R, Pollard T, Rosenbaum J, eds. Cell Motility Vol. 3. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press 1976; 987–1005.

    Google Scholar 

  7. Ludueña RF. Are tubulin isotypes functionally significant. Mol Biol Cell 1993;4:445–457.

    PubMed  Google Scholar 

  8. Ludueña RF. The multiple forms of tubulin: different gene products and covalent modifications. Int Rev Cytol 1998;178:207–275.

    Article  PubMed  Google Scholar 

  9. Lu Q, Moore GD, Walss C, Ludueña RF. Structural and functional properties of tubulin isotypes. Adv Struct Biol 1998;5:203–227.

    Article  CAS  Google Scholar 

  10. Alexandraki D, Ruderman JV. Evolution of αq-and β-tubulin genes as inferred by the nucleotide sequences of sea urchin cDNA clones. J Mol Evol 1983;19:397–410.

    Article  PubMed  CAS  Google Scholar 

  11. Gianguzza F, Di Bernardo MG, Sollazzo M, et al. DNA sequence and pattern of expression of the sea urchin (Paracentrotus lividus) α-tubulin genes. Mol Reprod Dev 1989; 1:170–181.

    Article  PubMed  CAS  Google Scholar 

  12. Edvardsen RB, Flaat M, Tewari R, et al. Most intron positions in Oikopleura dioica α-tubulin genes are unique: did new introns help to preserve and expand gene families? NCBI Accession no. AAM73988, AAM73989, AAM73990, 2002.

    Google Scholar 

  13. Hallworth R, Ludueña RF. Differential expression of β tubulin isotypes in the adult gerbil organ of Corti Hearing Res 2000;148:161–172

    Article  CAS  Google Scholar 

  14. Jensen-Smith HC, Eley J, Steyger PS, Ludueña RF, Hallworth R. Cell type-specific reduction of β tubulin isotypes synthesized in the developing gerbil organ of Corti. J Neurocytol 2003;32:185–197.

    Article  PubMed  CAS  Google Scholar 

  15. Perry B, Jensen-Smith HC, Ludueña RF, Hallworth R. Differential expression of β tubulin isotypes in gerbil vestibular end organs. J Assoc Res Otorhinolaryngol (JARO) 2003;4:329–338 (on-line).

    Article  Google Scholar 

  16. Wang T, Lessman CA. Isoforms of soluble a-tubulin in oocytes and brain of the frog (genus Rana): changes during oocyte maturation. Cell Mol Life Sci 2002;59:2216–2223.

    Article  PubMed  CAS  Google Scholar 

  17. Miya T, Satoh N. Isolation and characterization of cDNA clones for β-tubulin genes as a molecular marker for neural cell differentiation in the ascidian embryo. Int J Dev Biol 1997;41:551–557.

    PubMed  CAS  Google Scholar 

  18. Costa S, Ragusa MA, Drago G, et al. Sea urchin neural α2 tubulin gene: isolation and promoter analysis. Biochem Biophys Res Commun 2004;316:446–453.

    Article  PubMed  CAS  Google Scholar 

  19. Kawasaki H, Sugaya K, Quan GX, Nohata J, Mita K. Analysis of α-and β-tubulin genes of Bombyx mori using an EST database. Insect Biochem Mol Biol 2003;33:131–137.

    Article  PubMed  CAS  Google Scholar 

  20. Simoncelli F, Sorbolini S, Fagotti A, Di Rosa I, Porceddu A, Pascolini R. Molecular characterization and expression of a divergent α-tubulin in planarian Schmidtea polychroa. Biochim Biophys Acta 2003;1629:26–33.

    PubMed  CAS  Google Scholar 

  21. Savage C, Hamelin M, Culotti JG, Coulson A, Albertson DG, Chalfie M. mec-7 is a β-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev 1989;3:870–881.

    Article  PubMed  CAS  Google Scholar 

  22. Fukushige T, Siddiqui ZK, Chou M, et al. MEC-12, an α-tubulin required for touch sensitivity in C. elegans. J Cell Sci 1999;112:395–403.

    PubMed  CAS  Google Scholar 

  23. Wright AJ, Hunter CP. Mutations in a β-tubulin disrupt spindle orientation and microtubule dynamics in the early Caenorhabditis elegans embryo. Mol Biol Cell 2003;14:4512–4525.

    Article  PubMed  CAS  Google Scholar 

  24. Okamura S, Naito K, Sonehara K, et al. Characterization of the carrot β-tubulin gene coding a divergent isotype, β-2. Cell Struct Funct 1997;22:291–298.

    PubMed  CAS  Google Scholar 

  25. Matzk F, Meyer H-M, Horstmann C, Balzer HJ, Bäumlein H, Schubert I. A specific α-tubulin is associated with the initiation of parthenogenesis in Salmon wheat lines. Hereditas 1997; 126:219–224.

    Article  PubMed  CAS  Google Scholar 

  26. Whittaker DJ, Triplett BA. Gene-specific changes in α-tubulin transcript accumulation in developing cotton fibers. Plant Physiol 1999;121:181–188.

    Article  PubMed  CAS  Google Scholar 

  27. Yoshikawa M, Yang G, Kawaguchi K, Komatsu S. Expression analyses of β-tubulin isotype genes in rice. Plant Cell Physiol 2003;44:1202–1207.

    Article  PubMed  CAS  Google Scholar 

  28. Schröder J, Stenger H, Wernicke W. α-Tubulin genes are differentially expressed during leaf cell development in barley (Hordeum vulgare L.). Plant Mol Biol 2001;45:723–730.

    Article  PubMed  Google Scholar 

  29. Morello L, Bardini M, Sala F, Breviario D. A long leader intron of the Ostub 16 rice β-tubulin gene is required for high-level gene expression and can autonomously promote transcription both in vivo and in vitro. Plant J 2002;29:33–44.

    Article  PubMed  CAS  Google Scholar 

  30. Ebel C, Gómez Gómez L, Schmit AC, Neuhaur-Url G, Boller T. Differential mRNA degradation of two β-tubulin isoforms correlates with cytosolic Ca2+ changes in glucan-elicited soybean cells. Plant Physiol 2001; 126:87–96.

    Article  PubMed  CAS  Google Scholar 

  31. Hellmann A, Wernicke W. Changes in tubulin protein expression accompany reorganization of microtubular arrays during cell shaping in barley leaves. Planta 1998;204:220–225.

    Article  CAS  Google Scholar 

  32. Abe T, Thitamadee S, Hashimoto T. Microtubule defects and cell morphogenesis in the lefty1 lefty2 tubulin mutant of Arabidopsis thaliana. Plant Cell Physiol 2004;45:211–220.

    Article  PubMed  CAS  Google Scholar 

  33. Buhr TL, Dickman MB. Isolation, characterization, and expression of a second β-tubulin-encoding gene from Colletotrichum gloeosporiodes f. Sp. aeschynomene. Appl Environ Microbiol 1994;60: 4155–4159.

    PubMed  CAS  Google Scholar 

  34. Yan K, Dickman MB. Isolation of a β-tubulin gene from Fusarium moniliforme that confers coldsensitive benomyl resistance. Appl Environ Microbiol 1996;62:3053–3056.

    PubMed  CAS  Google Scholar 

  35. Monnat J, Ortega Perez R, Turian G. Molecular cloning and expression studies of two divergent α-tubulin genes in Neurospora crassa. FEMS Microbiol Lett 1997; 150:33–41.

    PubMed  CAS  Google Scholar 

  36. Silva WP, Soares RBA, Jesuino RSA, Izacc SMS, Felipe MSS, Soares CMA. Expression of α tubulin during the dimorphic transition of Paracoccidioides brasiliensis. Med Mycol 2001;39:457–462.

    Article  PubMed  CAS  Google Scholar 

  37. Chung S, Cho J, Cheon H, Paik S, Lee J. Cloning and characterization of a divergent α-tubulin that is expressed specifically in dividing amebae of Naegleria gruben. Gene 2002;293:77–86.

    Article  PubMed  CAS  Google Scholar 

  38. Hu K, Suravajjala S, DiLullo C, Roos D, Murray J. Functional specialization of tubulin isoforms in Toxoplasma isoforms in Toxoplasma gondii. Am Soc Cell Biol Ann Meeting Abstr p. 424a.

    Google Scholar 

  39. Paul ECA, Buchschacher GL, Cunningham DB, Dove WF, Burland TG. Preferential expression of one β-tubulin gene during flagellate development in Physarum. J Gen Microbiol 1992; 138:229–238.

    PubMed  CAS  Google Scholar 

  40. Cunningham DB, Buchschacher GL, Burland TG, Dove WF, Kessler D, Paul ECA. Cloning and characterization of the altA α-tubulin gene of Physarum. J Gen Microbiol 1993;139:137–151.

    PubMed  CAS  Google Scholar 

  41. Matthews KA, Rees D, Kaufman TC. A functionally specialized α-tubulin is required for oocyte meiosis and cleavage mitoses in Drosophila. Development 1993;117:977–991.

    PubMed  CAS  Google Scholar 

  42. Hecht NB, Distel RJ, Yelick PC, et al. Localization of a highly divergent mammalian testicular α tubulin that is not detectable in brain. Mol Cell Biol 1988;8:996–1000.

    PubMed  CAS  Google Scholar 

  43. Wu W-L, Morgan GT. Ovary-specific expression of a gene encoding a divergent α-tubulin isotype in Xenopus. Differentiation 1994;58:9–18.

    Article  PubMed  CAS  Google Scholar 

  44. Evrard J-L, Nguyen I, Bergdoll M, Mutterer J, Steinmetz A, Lambert A-M. A novel pollen-specific α-tubulin in sunflower: structure and characterization. Plant Mol Biol 2002;49:611–620.

    Article  PubMed  CAS  Google Scholar 

  45. Wang D, Villasante A, Lewis SA, Cowan NJ. The mammalian β-tubulin repertoire:hematopoietic expression of a novel heterologous β-tubulin isotype. J Cell Biol 1986;103:1903–1910.

    Article  PubMed  CAS  Google Scholar 

  46. Murphy DB, Wallis KT, Machlin PS, Ratrie H, Cleveland DW. The sequence and expression of the divergent β-tubulin in chicken erythrocytes. J Biol Chem 1987;262:14,305–14,312.

    PubMed  CAS  Google Scholar 

  47. Guiltinan MJ, Ma D-P, Barker RF, et al. The isolation, characterization and sequence of two divergent β-tubulin genes from soybean (Glycine max L.). Plant Mol Biol 1987;10:171–184.

    Article  CAS  Google Scholar 

  48. Fackenthal JD, Hutchens JA, Turner FR, Raff EC. Structural analysis of mutations in the Drosophila β2-tubulin isoform reveals regions in the β-tubulin molecule required for general and for tissuespecific microtubule functions. Genetics 1995;139:267–286.

    PubMed  CAS  Google Scholar 

  49. Fackenthal JD, Turner FR, Raff EC. Tissue-specific microtubule functions in Drosophila spermatogenesis require the β-tubulin isotype-specific carboxy-terminus. Dev Biol 1993;158:213–227.

    Article  PubMed  CAS  Google Scholar 

  50. Fuller MT, Caulton JH, Hutchens JA, Kaufman TC, Raff EC. Genetic analysis of microtubule structure. A β-tubulin mutation causes the formation of aberrant microtubules in vivo and in vitro. J Cell Biol 1993; 104:385–394.

    Article  Google Scholar 

  51. Rudolph JE, Kimble M, Hoyle HD, Suber MA, Raff EC. Three Drosophila β-tubulin sequences: a developmentally regulated isoform (β3), the testis-specific isoform (β2), and an assembly-defective mutation of the testis-specific isoform (β2t8) reveal both an ancient divergence in metazoan isotypes and structural constraints for β-tubulin function. Mol Cell Biol 1987;7:2231–2242.

    PubMed  CAS  Google Scholar 

  52. Hoyle HD, Raff EC. Two Drosophila β tubulin isoforms are not functionally equivalent. J Cell Biol 1990;11:1009–1026.

    Article  Google Scholar 

  53. Kramer J, Hawley RS. The spindle-associated transmembrane protein Axs identifies a membranous structure ensheathing the meiotic spindle. Nature Cell Biol 2003;5:261–267.

    Article  PubMed  CAS  Google Scholar 

  54. Dettman RW, Turner FR, Hoyle HD, Raff EC. Embryonic expression of the divergent Drosophila β3-tubulin isoform is required for larval behavior. Genetics 2001; 158:253–263.

    PubMed  CAS  Google Scholar 

  55. Buttgereit D, Paululat A, Renkawitz-Pohl R. Muscle development and attachment to the epidermis is accompanied by expression of β3 and β1 tubulin isotypes, respectively. Int J Dev Biol 1996;40:189–196.

    PubMed  CAS  Google Scholar 

  56. Komma DJ, Endow SA. Enhancement of the ncd microtubule motor mutant by mutants of (αTub67C. J Cell Sci 1997;110:576–583.

    Google Scholar 

  57. Matthies HJG, Messina LG, Namba R, Greer KJ, Walker MY, Hawley RS. Mutations in the α-Tubulin 67C gene specifically impair achiasmate segregation in Drosophila melanogaster. J Cell Biol 1999; 147:1137–1144.

    Article  PubMed  CAS  Google Scholar 

  58. Hutchens JA, Hoyle HD, Turner FR, Raff EC. Structurally similar Drosophila α-tubulins are functionally distinct in vivo. Mol Biol Cell 1997;8:481–500.

    PubMed  CAS  Google Scholar 

  59. Roach MC, Boucher VL, Walss C, Ravdin PM, Ludueña RF. Preparation of a monoclonal antibody specific for the class I isotype of β-tubulin. The β isotypes of tubulin differ in their cellular distributions within human tissues. Cell Motil Cytoskeleton 1998;39:273–285.

    Article  PubMed  CAS  Google Scholar 

  60. Havercroft JC, Cleveland DW. Programmed expression of β-tubulin genes during development and differentiation of the chicken. J Cell Biol 1984;99:1927–1935.

    Article  PubMed  CAS  Google Scholar 

  61. Kumar S, Hedges, SB. A molecular timescale for vertebrate evolution. Nature 1998;392:917–920.

    Article  PubMed  CAS  Google Scholar 

  62. Lewis SA, Lee MGS, Cowan NJ. Five mouse tubulin isotypes and their regulated expression during development. J Cell Biol 1985;101:852–861.

    Article  PubMed  CAS  Google Scholar 

  63. Monteiro MJ, Cleveland DW. Sequence of chicken cβ7 tubulin. Analysis of a complete set of vertebrate β-tubulin isotypes. J Mol Biol 1988;199:439–446.

    Article  PubMed  CAS  Google Scholar 

  64. Banerjee A, Roach MC, Wall KA, Lopata MA, Cleveland DW, Ludueña RF. A monoclonal antibody against the type II isotype of β-tubulin. Preparation of isotypically altered tubulin. J Biol Chem 1988;263:3029–3034.

    PubMed  CAS  Google Scholar 

  65. Grieshaber NA, Ko C, Grieshaber SS, Ji I, Ji TH. Follicle-stimulating hormone-responsive cytoskeletal genes in rat granulosa cells: class I β-tubulin, tropomyosin-4, and kinesin heavy chain. Endocrinology 2003;144:29–39.

    Article  PubMed  CAS  Google Scholar 

  66. Oehlmann VD, Berger S, Sterner C, Korsching SI. Zebrafish β tubulin 1 expression is limited to the nervous system throughout development, and in the adult brain is restricted to a subset of proliferative regions. Gene Expr Patterns 2004;4:191–198.

    Article  PubMed  CAS  Google Scholar 

  67. Lee MG, Lewis SA, Wilde CD, Cowan NJ. Evolutionary history of a multigene family: an expressed human β-tubulin gene and three processed pseudogenes. Cell 1983;33:477–487.

    Article  PubMed  CAS  Google Scholar 

  68. Hirakawa M, Yamaguchi H, Imai K, Shimada J. NCBI Accession no. BAB63321, 1999.

    Google Scholar 

  69. Crabtree DV, Ojima I, Geng X, Adler AJ. Tubulins in the primate retina: evidence that xanthophylls may be endogenous ligands for the paclitaxel-binding site. Bioorg Med Chem 2001;9:1967–1976.

    Article  PubMed  CAS  Google Scholar 

  70. Narishige T, Blade KL, Ishibashi Y, et al. Cardiac hypertrophy and developmental regulation of the β-tubulin multigene family. J Biol Chem 1999;274:9692–9697.

    Article  PubMed  CAS  Google Scholar 

  71. Woo K, Jensen-Smith HC, Ludueña RF, Hallworth R. Differential expression of β tubulin isotypes in gerbil nasal epithelia. Cell Tissue Res 2002;309:331–335.

    Article  PubMed  CAS  Google Scholar 

  72. Jensen-Smith HC, Ludueña RF, Hallworth R. Requirement for the βI and βIV tubulin isotypes in mammalian cilia. Cell Motil Cytoskeleton 2003;55:213–220.

    Article  PubMed  CAS  Google Scholar 

  73. Raff EC, Fackenthal JD, Hutchens JA, Hoyle HD, Turner FR. Microtubule architecture specified by a β-tubulin isoform. Science 1997;275:70–73.

    Article  PubMed  CAS  Google Scholar 

  74. Lezama R, Castillo A, Ludueña RF, Meza I. Over-expression of βI tubulin in MDCK cells and incorporation of exogenous βI tubulin into microtubules interferes with adhesion and spreading. Cell Motil Cytoskeleton 2001;50:147–160.

    Article  PubMed  CAS  Google Scholar 

  75. Yanagida M, Hayano T, Yamauchi Y, et al. Human fibrillarin forms a sub-complex with splicing factor 2-associated p32, protein arginine methyltransferases, and tubulins α3 and β1 that is independent of its association with preribosomal ribonucleoprotein complexes. J Biol Chem 2004;279:1607–1614.

    Article  PubMed  CAS  Google Scholar 

  76. Yeh I-T, Ludueña RF. The βII isotype of tubulin is present in the cell nuclei of a variety of cancers. Cell Motil Cytoskeleton 2004;57:96–106.

    Article  PubMed  CAS  Google Scholar 

  77. Arai K, Shibutani M, Matsuda H. Distribution of the class II β-tubulin in developmental and adult rat tissues. Cell Motil Cytoskeleton 2002;52:174–182.

    Article  PubMed  CAS  Google Scholar 

  78. Dozier JH, Hiser L, Davis JA, et al. β class II tubulin predominates in normal and tumor breast tissues. Breast Cancer Res 2003;5:R157–R169.

    Article  PubMed  CAS  Google Scholar 

  79. Nakamura Y, Yamamoto M, Oda E, et al. Expression of tubulin βII in neural stem/progenitor cells and radial fibers during human fetal brain development. Lab Invest 2003;83:479–489.

    PubMed  CAS  Google Scholar 

  80. Renthal R, Schneider BG, Miller MM, Ludueña RF. βIV is the major β-tubulin isotype in bovine cilia. Cell Motil Cytoskeleton 1993;25:19–29.

    Article  PubMed  CAS  Google Scholar 

  81. Armas-Portela R, Parrales MA, Albar JP, Martinez C, Avila J. Distribution and characteristics of βII tubulin-enriched microtubules in interphase cells. Exp Cell Res 1999;248:372–380.

    Article  PubMed  CAS  Google Scholar 

  82. Ranganathan S, Salazar H, Benetatos CA, Hudes GR. Immunohistochemical analysis of β-tubulin isotypes in human prostate carcinoma and benign prostatic hypertrophy. Prostate 1997;30:263–268.

    Article  PubMed  CAS  Google Scholar 

  83. Walss C, Kreisberg JI, Ludueña RF. Presence of the βII-isotype of tubulin in the nuclei of cultured rat kidney mesangial cells. Cell Motil Cytoskeleton 1999;42:274–284.

    Article  PubMed  CAS  Google Scholar 

  84. Bugnard E, Zaal KJM, Ralston E. Reorganization of microtubule nucleation during muscle differentiation. Cell Motil Cytoskeleton 2005;60:1–13.

    Article  PubMed  Google Scholar 

  85. Sullivan KF, Cleveland DW. Sequence of a highly divergent β tubulin gene reveals regional heterogeneity in the β tubulin polypeptide. J Cell Biol 1984;99:1754–1760.

    Article  PubMed  CAS  Google Scholar 

  86. Banerjee A. NCBI Accession no. AAL28094, 2001.

    Google Scholar 

  87. Burgoyne RD, Cambray-Deakin MA, Lewis SA, Sarkar S, Cowan NJ. Differential distribution of β-tubulin isotypes in cerebellum. EMBO J 1988;7:2311–2319.

    PubMed  CAS  Google Scholar 

  88. Chen SS, Revoltella RP, Papini S, et al. Multilineage differentiation of rhesus monkey embryonic stem cells in three-dimensional culture systems. Stem Cells 2003;21:281–295.

    Article  PubMed  CAS  Google Scholar 

  89. Katsetos CD, Legido A, Perentes E, Mörk SJ. Class III β-tubulin isotype: a key cytoskeletal protein at the crossroads of developmental neurobiology and tumor neuropathology. J Child Neurol 2003;18:851–866.

    Article  PubMed  Google Scholar 

  90. Butler R, Leigh PN, Gallo JM. Androgen-induced up-regulation of tubulin isoforms in neuroblastoma cells. J Neurochem 2001;78:854–861.

    Article  PubMed  CAS  Google Scholar 

  91. Matsuo N, Hoshino M, Yoshizawa M, Nabeshima Y Characterization of STEF, a guanine nucleotide exchange factor for Rac1, required for neurite growth. J Biol Chem 2002;277:2860–2868.

    Article  PubMed  CAS  Google Scholar 

  92. Sanchez-Ramos JR, Song S, Kamath SG, et al. Expression of neural markers in human umbilical cord blood. Exp Neurol 2001;171:109–115.

    Article  PubMed  CAS  Google Scholar 

  93. Correa LM, Miller MG. Microtubule depolymerization in rat seminiferous epithelium is associated with diminished tyrosination of α-tubulin. Biol Reprod 2001;64:1644–1652.

    Article  PubMed  CAS  Google Scholar 

  94. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680–685.

    Article  PubMed  CAS  Google Scholar 

  95. Little M. Identification of a second β chain in pig brain tubulin. FEBS Lett 1979;108:283–286.

    Article  PubMed  CAS  Google Scholar 

  96. Ludueria RF, Roach MC, Trcka PP, et al. β2-Tubulin, a form of chordate brain tubulin with lesser reactivity toward an assembly-inhibiting sulfhydry1-directed cross-linking reagent. Biochemistry 1979; 21:4787–4794.

    Google Scholar 

  97. Detrich HW, Prasad V, Ludueria RF. Cold-stable microtubules from Antarctic fishes contain unique a tubulins. J Biol Chem 1987;262:8360–8366.

    PubMed  CAS  Google Scholar 

  98. Modig C, Olsson P-E, Barasoain I, et al. Identification of βIII-and βIV-tubulin isotypes in coldadapted microtubules from Atlantic cod (Gadus morhua): antibody mapping and cDNA sequencing. Cell Motil Cytoskeleton 1999;42:315–330.

    Article  PubMed  CAS  Google Scholar 

  99. Alexander JE, Hunt DF, Lee MK, et al. Characterization of posttranslational modifications in neuronspecific class III β-tubulin by mass spectrometry. Proc Nat Acad Sci USA 1991;88:4685–4689.

    Article  PubMed  CAS  Google Scholar 

  100. Panda D, Miller HP, Banerjee A, Ludueria RF, Wilson L. Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proc Nat Acad Sci USA 1994;91:11358–11362.

    Article  PubMed  CAS  Google Scholar 

  101. Mellon MG, Rebhun LI. Sulfhydryls and the in vitro polymerization of tubulin. J Cell Biol 1976; 70:226–238.

    Article  PubMed  CAS  Google Scholar 

  102. Little M, Ludueria, RF. Structural differences between brain β1-and β2-tubulins: implications for microtubule assembly and colchicine binding. EMBO J 1985;4:51–56.

    PubMed  CAS  Google Scholar 

  103. Bai RL, Lin CM, Nguyen NY, Liu TY, Hamel E. Identification of the cysteine residue of β-tubulin affected by the antimitotic agent 2, 4-dichlorobenzyl thiocyanate, facilitated by separation of the protein subunits of tubulin by hydrophobic column chromatography. Biochemistry 1989;28:5606–5612.

    Article  PubMed  CAS  Google Scholar 

  104. Palanivelu P, Ludueña RF. Interactions of the τ-tubulin-vinblastine complex with colchicine, podophyllotoxin, and N, N′-ethylenebis(iodoacetamide). J Biol Chem 1982;257:6311–6315.

    PubMed  CAS  Google Scholar 

  105. Ludueña RF, Roach MC, Jordan MA, Murphy, DB. Different activities of brain and erythrocyte tubulins toward a sulfhydryl group-directed reagent that inhibits microtubule assembly. J Biol Chem 1985;260:1257–1264.

    PubMed  Google Scholar 

  106. Dong Z, Thoma RS, Crimmins DL, McCourt DW, Tuley EA, Sadler JE. Disulfide bonds required to assemble functional von Willebrand factor multimers. J Biol Chem 1994;260:6753–6758.

    Google Scholar 

  107. Mayadas TN, Wagner DD. Vicinal cysteines in the prosequence play a role in von Willebrand multimer assembly. Proc Nat Acad Sci USA 1992;89:3531–3535.

    Article  PubMed  CAS  Google Scholar 

  108. Li PP, Nakanishi A, Clark SW, Kasamatsu H. Formation of transitory intrachain and interchain disulfide bonds accompanies the folding and oligomerization of simian virus 40 Vp1 in the cytoplasm. Proc Nat Acad Sci USA 2002;99:1353–1358.

    Article  PubMed  CAS  Google Scholar 

  109. Beckman JS, Chen J, Ischiropoulos H, Crow JP. Oxidative chemistry of peroxynitrite. Methods Enzymol 1994;233:229–240.

    Article  PubMed  CAS  Google Scholar 

  110. Landino LM, Iwig JS, Kennett KL, Moynihan KL. Repair of peroxynitrite damage to tubulin by the thioredoxin reductase system. Free Radic Biol Med 2004;36:497–506.

    Article  PubMed  CAS  Google Scholar 

  111. Nogales E, Wolf SG, Downing KH. Structure of the αβ tubulin dimer by electron crystallography. Nature 1998;391:199–203.

    Article  PubMed  CAS  Google Scholar 

  112. Landino LM, Hasan R, McGaw A, et al. Peroxynitrite oxidation of tubulin sulfhydryls inhibits microtubule polymerization. Arch Biochem Biophys 2002;398:213–220.

    Article  PubMed  CAS  Google Scholar 

  113. Mungrue IN, Bredt DS. nNOS at a glance: implications for brain and brawn. J Cell Sci 2004;117:2627–2629.

    Article  PubMed  CAS  Google Scholar 

  114. Gaily JA, Montague PR, Reeke GN, Edelman GM. The NO hypothesis: possible effects of short-lived rapidly diffusible signal in the development and function of the nervous system. Proc Nat Acad Sci USA 1990;87:3547–3551.

    Article  Google Scholar 

  115. Bredt DS, Snyder SH. Nitric oxide, a novel neuronal messenger. Neuron 1992;8:3–11.

    Article  PubMed  CAS  Google Scholar 

  116. Blottner D, Luck G. Just in time and place: NOS/NO system assembly in neuromuscular junction formation. Microsc Res Tech 2001;55:171–180.

    Article  PubMed  CAS  Google Scholar 

  117. Cappelletti G, Tedeschi G, Maggioni MG, Negri A, Nonnis S, Maci R. The nitration of τ protein in neurone-like PC12 cells. FEBS Lett 2004;562:35–39.

    Article  PubMed  CAS  Google Scholar 

  118. Lewis SA, Cowan NJ. Complex regulation and functional versatility of mammalian α-and β-tubulin isotypes during the differentiation of testis and muscle cells. J Cell Biol 1988;106:2023–2033.

    Article  PubMed  CAS  Google Scholar 

  119. Lee NPY, Cheng CY. Regulation of Sertoli cell tight junction dynamics in the rat testis via the nitric oxide synthase/soluble guanylate cyclase/3′, 5′-cyclic guanosine monophosphate/protein kinase G signaling pathway: an in vitro study. Endocrinology 2003;144:3114–3129.

    Article  PubMed  CAS  Google Scholar 

  120. Kon Y, Namiki Y, Endoh D. Expression and distribution of inducible nitric oxide synthase in the testis. Jpn J Vet Res 2002;50:115–123.

    PubMed  Google Scholar 

  121. Mruk DD, Cheng CY. In vitro regulation of extracellular Superoxide dismutase in sertoli cells. Life Sci 2000;67:133–145.

    Article  PubMed  CAS  Google Scholar 

  122. Holstein GR, Friedrick VI, Martinelli GP, Holstein GR. Monoclonal L-citrulline immunostaining reveal NO-producing vestibular neurons. Ann NY Acad Sci 2001;942:65–78.

    Article  PubMed  CAS  Google Scholar 

  123. Nie G, Wang J. Localization of nitric oxide synthase in the chicken vestibular system. J Clin Otorhinolaryngol 2002; 16:426–427 (article in Chinese, abstract in English).

    Google Scholar 

  124. Takumida M, Anniko M. Simultaneous detection of both nitric oxide and reactive oxygen species in guinea pig vestibular sensory cells. ORL 2002;64:143–147.

    Article  PubMed  CAS  Google Scholar 

  125. Takumida M, Anniko M. Direct evidence of nitric oxide production in guinea pig vestibular sensory cells. Acta Otolaryngol 2000;120:134–138.

    Google Scholar 

  126. Katsetos CD, Kontogeorgos G, Geddes JF, et al. Differential distribution of the neuron-associated class III β-tubulin in neuroendocrine lung tumors. Arch Pathol Lab Med 2000;124:535–544.

    PubMed  CAS  Google Scholar 

  127. Matsuzaki F, Harada F, Nabeshima Y, Fujii-Kuriyama Y, Yahara I. Cloning of cDNAs for two β-tubulin isotypes expressed in murine T cell lymphoma L5178Y and analysis of their translation products. Cell Struct Funct 1987;12:317–325.

    Article  PubMed  CAS  Google Scholar 

  128. Asai DJ, Remolona NM. Tubulin usage in vivo: A unique spatial distribution of the minor neuronalspecific β-tubulin isotype in pheochromocytoma cells. Dev Biol 1989; 132:398–409.

    Article  PubMed  CAS  Google Scholar 

  129. Scott CA, Walker CC, Neal DA, et al. β-Tubulin epitope expression in normal and malignant epithelial cells. Arch Otolaryngol Head Neck Surg 1990;116:583–589.

    PubMed  CAS  Google Scholar 

  130. Katsetos CD, Herman MM, Frankfurter A, Uffer S, Perentes E, Rubinstein LJ. Neuron-associated class III β-tubulin isotype, microtubule associated protein 2 and synaptophysin in human retinoblastomas in situ. Lab Invest 1991;64:45–64.

    PubMed  CAS  Google Scholar 

  131. Maraziotis T, Perentes E, Karamitopoulou E, et al. Neuron-associated class III β-tubulin isotype, retinal S-antigen, synaptophysin, and glial fibrillary acidic protein in human medulloblastomas: a clinicopathological analysis of 36 cases. Acta Neuropathol 1992;84:355–363.

    Article  PubMed  CAS  Google Scholar 

  132. Furuhata S, Kameya T, Toya S, Frankfurter A. Immunohistochemical analysis of 61 pituitary adenomas with amonoclonal antibody to the neuron-specific β-tubulin isotype. Acta Neuropathol 1993;86:518–520.

    Article  PubMed  CAS  Google Scholar 

  133. Woulfe J. Class III β-tubulin immunoreactive intranuclear inclusions in human ependymomas and gangliogliomas. Acta Neuropathol 2000; 100:427–434.

    Article  PubMed  CAS  Google Scholar 

  134. Katsetos CD, Del Valle L, Geddes JF, et al. Aberrant localization of the neuronal class III β-tubulin in astrocytomas. A marker for anaplastic potential. Arch Pathol Lab Med 2001;125:613–624.

    PubMed  CAS  Google Scholar 

  135. Hisaoka M, Okamoto S, Koyama S, et al. Microtubule-associated protein-2 and class III β-tubulin are expressed in extraskeletal myxoid chondrosarcoma. Mod Pathol 2003;16:453–459.

    Article  PubMed  Google Scholar 

  136. Katsetos CD, Legido A, Perentes E, Mörk SJ. Class III β-tubulin isotype: a key cytoskeletal protein at the crossroads of developmental neurobiology and tumor neuropathology. J Child Neurol 2003;18:851–866.

    Article  PubMed  Google Scholar 

  137. Katsetos CD, Herman MM, Mörk SJ. Class III β-tubulin in human development and cancer. Cell Motil Cytoskeleton 2003;55:77–96.

    Article  PubMed  CAS  Google Scholar 

  138. Hardman JG, Limbird LE. Goodman and Gilman’s The Pharmacological Basis of Therapeutics, 9th ed. McGraw-Hill, New York, 1996:1228, 1257–1261, 1603.

    Google Scholar 

  139. Mekhail TM, Markman M. Paclitaxel in cancer therapy. Expert Opin Pharmacother 2002;3:755–766.

    Article  PubMed  CAS  Google Scholar 

  140. Schiff R, Reddy P, Ahotupa M, et al. Oxidative stress and AP-1 activity in tamoxifen-resistant breast tumors in vivo. J Nat Cancer Inst 2000;92:1926–1934.

    Article  PubMed  CAS  Google Scholar 

  141. Brown NS, Bicknell R. Hypoxia and oxidative stress in breast cancer. Oxidative stress: its effects on the growth, metastatic potential and response to therapy of breast cancer. Breast Cancer Res 2001; 3:323–327.

    Article  PubMed  CAS  Google Scholar 

  142. Portakal O, Ozkaya O, Erden Inal M, Bozan B, Kosan M, Sayek I. Coenzyme Q10 concentrations and antioxidant status in tissues of breast cancer patients. Clin Biochem 2000;33:279–284.

    Article  PubMed  CAS  Google Scholar 

  143. Ray G, Batra S, Shukla NK, et al. Lipid peroxidation, free radical production and antioxidant status in breast cancer. Breast Cancer Res Treat 2000;59:163–170.

    Article  PubMed  CAS  Google Scholar 

  144. Punnonen K, Ahotupa M, Asaishi K, Hyoty M, Kudo R, Punnonen R. Antioxidant activities and oxidative stress in human breast cancer. J Cancer Res. Clin Oncol 1994;120:374–377.

    Article  PubMed  CAS  Google Scholar 

  145. Katsetos CD, Del Valle L, Geddes JF, et al. Localization of the neuronal class III β-tubulin in oligodendrogliomas: comparison with Ki-67 proliferative index and 1p/19q status. J Neuropathol Exp Neurol 2002;61:307–320.

    PubMed  CAS  Google Scholar 

  146. Dumontet C, Isaac S, Souquet PJ, et al. Expression of class III β tubulin in non-small cell lung cancer is correlated with resistance to taxane chemotherapy. Electr J Oncol 2002;1:58–64.

    Google Scholar 

  147. Colmenares SU, DeLuca K, Jordan MA, Mooberry SL. Native overexpression of βIII isotype of tubulin in the BT-549 breast carcinoma line is associated with resistance to paclitaxel, vinblastine and cryptophycin 1. Proc Am Assn Cancer Res 1998;39:163.

    Google Scholar 

  148. Carré M, André N, Carles G, et al. Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel. J Biol Chem 2002;277:33,644–33,669.

    Article  Google Scholar 

  149. Lu Q, Ludueña RF. In vitro analysis of microtubule assembly of isotypically pure tubulin dimers. Intrinsic differences in the assembly properties of αβII, αβIII, and αβIV tubulin dimers in the absence of microtubule-associated proteins. J Biol Chem 1994;269:2041–2047.

    PubMed  CAS  Google Scholar 

  150. Banerjee A, Roach MC, Trcka P, Ludueña RF. Preparation of a monoclonal antibody specific for the class IV isotype of β-tubulin. Purification and assembly of αβII, αβIII, and αβIV tubulin dimers from bovine brain. J Biol Chem 1992;267:5625–5630.

    PubMed  CAS  Google Scholar 

  151. Hari M, Yang H, Zeng C, Canizales M, Cabrai F. Expression of class III β-tubulin reduces microtubule assembly and confers resistance to paclitaxel. Cell Motil Cytoskeleton 2003;56:45–56.

    Article  PubMed  CAS  Google Scholar 

  152. Evans J, Sumners C, Moore J, et al. Characterization of mitotic neurons derived from adult rat hypothalamus and brain stem. J Neurophysiol 2001;87:1076–1085.

    Google Scholar 

  153. Ohuchi T, Maruoka S, Sakudo A, Arai T. Assay-based quantitative analysis of PC12 differentiation. J Neurosci Methods 2002;118:1–8.

    Article  PubMed  CAS  Google Scholar 

  154. Braun H, Schäfer K, Höllt V. βIII tubulin-expressing neurons reveal enhanced neurogenesis in hippocampal and cortical structures after a contusion trauma in rats. J Neurotrauma 2002;19:975–983.

    Article  PubMed  Google Scholar 

  155. Xu G, Pierson CR, Murakawa Y, Sima AAF. Altered tubulin and neurofilament expression and impaired axonal growth in diabetic nerve regeneration. J Neuropathol Exp Neurol 2002;61:164–175.

    PubMed  CAS  Google Scholar 

  156. Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N. MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 2002;158:541–549.

    Article  PubMed  CAS  Google Scholar 

  157. Fanarraga ML, Avila J, Zabala JC. Expression of unphosphorylated class III β-tubulin isotype in neuroepithelial cells demonstrates neuroblast commitment and differentiation. Eur J Neurosci 1999;11:517–527.

    Article  PubMed  CAS  Google Scholar 

  158. Molea D, Stone JC, Rubel EW. Class III β-tubulin expression in sensory and nonsensory regions of the developing avian inner ear. J Comp Neurol 1999;406:183–198.

    Article  PubMed  CAS  Google Scholar 

  159. Khan IA, Ludueña RF. Different effects of vinblastine on the polymerization of isotypically purified tubulins from bovine brain. Invest New Drugs 2003;21:3–13.

    Article  PubMed  CAS  Google Scholar 

  160. Daniely Y, Liao G, Dixon D, et al. Critical role of p63 in the development of a normal esophageal and tracheobronchial epithelium. Am J Physiol Cell Physiol 2004;287:C171–C181.

    Article  PubMed  CAS  Google Scholar 

  161. Pazour GJ, Agrin NS, Leszyk JD, Witman GB. Proteomic characterization of a eukaryotic cilium. American Society for Cell Biol Ann Meeting Abstracts. p. 55a. 2004.

    Google Scholar 

  162. Dustin P. Microtubules. Springer-Verlag, Berlin, 1984:149.

    Google Scholar 

  163. Smith EF. Regulation of flagellar dynein by the axonemal central apparatus. Cell Motil Cytoskeleton 2002;52:33–42.

    Article  PubMed  CAS  Google Scholar 

  164. Mitchell DR, Nakatsugawa M. Bend propagation drives central pair rotation in Chlamydomonas reinhardtii flagella. J Cell Biol 2004;166:709–715.

    Article  PubMed  CAS  Google Scholar 

  165. Sloboda RD. A healthy understanding of intraflagellar transport. Cell Motil Cytoskeleton 2002; 52:1–8.

    Article  PubMed  CAS  Google Scholar 

  166. Nielsen MG, Turner FR, Hutchens JA, Raff EC. Axoneme-specific β-tubulin specialization: a conserved C-terminal motif specifies the central pair. Curr Biol 2001;11:529–533.

    Article  PubMed  CAS  Google Scholar 

  167. Thazhath R, Liu C, Gaertig J. Polyglycylation domain of β-tubulin maintains axonemal architecture and affects cytokinesis in Tetrahymena. Nat Cell Biol 2002;4:256–259.

    Article  PubMed  CAS  Google Scholar 

  168. Sharma J, Ludueña RF. Use of N, N′-polymethylenebis(iodoacetamide) derivatives as probes for the detection of conformational differences in tubulin isotypes. J Prot Chem 1994;13:165–176.

    Article  CAS  Google Scholar 

  169. Sadek CM, Jiménez A, Damdimopoulous AE, et al. Characterization of human thioredoxin-like 2. A novel microtubule-binding thioredoxin expressed predominantly in the cilia of lung airway epithelium and spermatid manchette and axoneme. J Biol Chem 2003;278: 13,133–13,142.

    Article  PubMed  CAS  Google Scholar 

  170. Walss-Bass C, Kreisberg JI, Ludueña RF. Mechanism of localization of βII-tubulin in the nuclei of cultured rat kidney mesangial cells. Cell Motil Cytoskeleton 2001;49:208–217.

    Article  PubMed  CAS  Google Scholar 

  171. Walss-Bass C, Prasad V, Kreisberg JI, Ludueña RF. Interaction of the βIV-tubulin isotype with actin stress fibers in cultured rat kidney mesangial cells. Cell Motil Cytoskeleton 2001;49:200–207.

    Article  PubMed  CAS  Google Scholar 

  172. Kodoma A, Lechler T, Fuchs E. Coordinating cytoskeletal tracks to polarize cellular movements. J Cell Biol 2004; 167:203–207.

    Article  Google Scholar 

  173. Sullivan KF, Havercroft JC, Machlin PS, Cleveland DW. Sequence and expression of the chicken β5-and β4-tubulin genes define a pair of divergent β-tubulins with complementary patterns of expression. Mol Cell Biol 1986;6:4409–4418.

    PubMed  CAS  Google Scholar 

  174. Banerjee A, Elguezabal G, Joe P, Lazzell A, Prasad V, Luduena RF. Distribution and characterization of the βV isotype of tubulin in mammalian cells. Mol Biol Cell 2003;14:182A.

    Google Scholar 

  175. Ikeda Y, Steiner M. Sulfhydryls of platelet tubulin: Their role in polymerization and colchicine binding. Biochemistry 1978; 17:3454–3459.

    Article  PubMed  CAS  Google Scholar 

  176. Italiano JE, Bergmeier W, Tiwari S, et al. Mechanisms and implications of platelet discoid shape. Blood 2003; 101:4789–4796.

    Article  PubMed  CAS  Google Scholar 

  177. Lecine P, Italiano JE, Kim S-W, Villeval J-L. Shivdasaani RA. Hematopoietic-specific β1 tubulin participates in a pathway of platelet biogenesis dependent on the transcription factor NF-E2. Blood 2000;96:1366–1373.

    PubMed  CAS  Google Scholar 

  178. Hartwig J, Italiano J. The birth of the platelet. J Thromb Haemostasis 2003;1:1580–1586.

    Article  CAS  Google Scholar 

  179. Schwer HD, Lecine P, Tiwari S, Italiano JE, Hartwig JH. Shivdasani RA. A lineage-restricted and divergent β-tubulin isoform is essential for the biogenesis, structure and function of blood platelets. Curr Biol 2001;11:579–586.

    Article  PubMed  CAS  Google Scholar 

  180. White JG, de Alarcon PA. Platelet spherocytosis: a new bleeding disorder. Am J Hematol 2002;70:158–166.

    Article  PubMed  Google Scholar 

  181. DuMontet C, Viormery AV. Expression of a new β tubulin isotype in brain. Mol Biol Cell 1999;10:141a.

    Google Scholar 

  182. Van Geel M, van Deutekom JC, van Staalduinen A, et al. Identification of a novel β-tubulin subfamily with one member (TUBB4Q) located near the telomere of chromosome region 4q35. Cytogenet Cell Genet 2002;88:316–321.

    Article  Google Scholar 

  183. Miller FD, Naus CC, Durand M, Bloom FE, Milner RJ. Isotypes of α-tubulin are differentially regulated during neuronal maturation. J Cell Biol 1987;105:3065–3073.

    Article  PubMed  CAS  Google Scholar 

  184. Przyborski SA, Cambray-Deakin MA. Developmental regulation of α-tubulin mRNAs during the differentiation of cultured cerebellar granule cells. Mol Brain Res 1996;36:179–183.

    Article  PubMed  CAS  Google Scholar 

  185. Stanchi F, Corso V, Scannapieco P, et al. TUBA8: a new tissue-specific isoform of α-tubulin that is highly conserved in human and mouse. Biochem Biophys Res Commun 2000;270:1111–1118.

    Article  PubMed  CAS  Google Scholar 

  186. Kourmouli N, Dialynas G, Petraki C, et al. Binding of heterochromatin protein 1 to the nuclear envelope is regulated by a soluble form of tubulin. J Biol Chem 2001;276: 13,007–13,014.

    Article  PubMed  CAS  Google Scholar 

  187. Hu K, Roos DS, Murray JM. A novel polymer of tubulin forms the conoid of Toxoplasma gondii. J Cell Biol 2002; 158:1039–1050.

    Article  CAS  Google Scholar 

  188. Imai H, Nakagawa Y. Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic Biol Med 2003;34:145–169.

    Article  PubMed  CAS  Google Scholar 

  189. Ursini F, Heim S, Kiess M, et al. Dual function of the selenoprotein PHGPx during sperm maturation. Science 1999;285:1393–1396.

    Article  PubMed  CAS  Google Scholar 

  190. Xu K, Ludueña RF. Characterization of nuclear βII-tubulin in tumor cells: a possible novel target for taxol. Cell Motil Cytoskeleton 2002;53:39–52.

    Article  PubMed  CAS  Google Scholar 

  191. Walss-Bass C, Kreisberg JI, Ludueña RF. Effect of the anti-tumor drug vinblastine on nuclear βII-tubulin in cultured rat kidney mesangial cells. Invest New Drugs 2003;21:15–20.

    Article  PubMed  CAS  Google Scholar 

  192. Walss-Bass C, Xu K, David S, Fellous A, Ludueña RF. Occurrence of nuclear βII-tubulin in cultured cells. Cell Tissue Res 2002;308:215–223.

    Article  PubMed  CAS  Google Scholar 

  193. Ewald A, Zünkler C, Lourim D, Dabauvalle M-C. Microtubule-dependent assembly of the nuclear envelope in Xenopus laevis egg extract. Eur J Cell Biol 2001;80:678–691.

    Article  PubMed  CAS  Google Scholar 

  194. Salina D, Bodoor K, Enarson P, Raharjo WH, Burke B. Nuclear Envelope Dyn 2001;79:533–542.

    CAS  Google Scholar 

  195. Burke B, Ellenberg J. Remodelling the walls of the nucleus. Nat Rev Mol Cell Biol 2002;3:487–497.

    Article  PubMed  CAS  Google Scholar 

  196. Beaudouin J, Gerlich D, Daigle N, Eils R, Ellenberg J. Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 2002;108:83–96.

    Article  PubMed  CAS  Google Scholar 

  197. Weatherbee JA, May GS, Gambino J, Morris NR. Involvement of a particular species of β-tubulin (β3) in conidial development in Aspergillus nidulans. J Cell Biol 1985;101:706–711.

    Article  PubMed  CAS  Google Scholar 

  198. Oakley BR. Tubulins in Aspergillus nidulans. Fungal Genet Biol 2004;41:420–427.

    Article  PubMed  CAS  Google Scholar 

  199. Kirk KE, Morris NR. Either β-tubulin isogene product is sufficient for microtubule function during all stages of growth and differentiation in Aspergillus nidulans. Mol Cell Biol 1993;13:4465–4476.

    PubMed  CAS  Google Scholar 

  200. Joshi HC, Yen TJ, Cleveland DW. In vivo coassembly of a divergent β-tubulin subunit (cβ6) into microtubules of different function. J Cell Biol 1987;105:2179–2190.

    Article  PubMed  CAS  Google Scholar 

  201. Lopata MA, Cleveland DW. In vivo microtubules are copolymers of available β-tubulin isotypes. Localization of each of six vertebrate β-tubulin isotypes using polyclonal antibodies elicited by synthetic peptide antigens. J Cell Biol 1987;105:1707–2730.

    Article  PubMed  CAS  Google Scholar 

  202. Lewis SA, Gu W, Cowan NJ. Free intermingling of mammalian β-tubulin isotypes among functionally distinct microtubules. Cell 1987;49:539–548.

    Article  PubMed  CAS  Google Scholar 

  203. Gu W, Lewis SA, Cowan NJ. Generation of antisera that discriminate among mammalian a-tubulins. Introduction of specialized isotypes into cultured cells results in their coassembly without disruption of normal microtubule function. J Cell Biol 1988;106:2011–2022.

    Article  PubMed  CAS  Google Scholar 

  204. Chu B, Snustad DP, Carter JV. Alteration of β-tubulin gene expression during low-temperature exposure in leaves of Arabidopsis thaliana. Plant Physiol 1993;103:371–377.

    PubMed  CAS  Google Scholar 

  205. Abdrakhamanova A, Wang QY, Khokhlova L, Nick P. Is microtubule disassembly a trigger for cold acclimation? Plant Cell Physiol 2003;44:676–686.

    Article  PubMed  CAS  Google Scholar 

  206. Roos MH, Boersema JH, Borgsteede FHM, Cornelissen J, Taylor M, Ruitenberg EJ. Molecular analysis of selection for benzimidazole resistance in the sheep parasite Haemonchus contortus Mol Biochem Parasitai 1990;43:77–88.

    Article  CAS  Google Scholar 

  207. Kwa MSG, Veenstra JG, Roos MH. Molecular characterisation of β-tubulin genes present in benzimidazole-resistant populations of Haemonchus contortus. Mol Biochem Parasitai 1993;60:133–144.

    Article  CAS  Google Scholar 

  208. Driscoll M, Dean E, Reilly E, Bergholz E, Chalfie M. Genetic and molecular analysis of a Caenorhabditis elegans β-tubulin that conveys benzimidazole sensitivity. J Cell Biol 1989;109:2993–3003.

    Article  PubMed  CAS  Google Scholar 

  209. Grant WN, Mascord LJ. β-tubulin gene polymorphism and benzimidazole resistance in Trichostrongylus colubriformes. Int J Parasitai 1996;26:71–77.

    Article  CAS  Google Scholar 

  210. Silvestre A, Cabaret J. Mutation in position 167 of isotype 1 β-tubulin gene of Trichostrongylid nematodes: role in benzimidazole resistance? Mol Biochem Parasitai 2002;120:297–300.

    Article  CAS  Google Scholar 

  211. Burkhart CA, Kavallaris M, Horwitz SB. The role of β-tubulin isotypes in resistance to antimitotic drugs. Biochim Biophys Acta 2001;1471:01–09.

    Google Scholar 

  212. Orr GA, Verdier-Pinard P, McDaid H, Horwitz SB. Mechanisms of taxol resistance related to microtubules. Oncogene 2003;22:7280–7295.

    Article  PubMed  CAS  Google Scholar 

  213. Schatz PJ, Pillus L, Grisafi P, Solomon F, Botstein D. Two functional α-tubulin genes of the yeast Saccharomyces cerevisiae encode divergent proteins. Mol Cell Biol 1986;6:3711–3721.

    PubMed  CAS  Google Scholar 

  214. Bode CJ, Gupta ML, Suprenant KA, Himes RH. The two α-tubulin isotypes in budding yeast have opposing effects on microtubule dynamics in vitro. EMBO Rep 2003;4:94–99.

    Article  PubMed  CAS  Google Scholar 

  215. Haber M, Burkhart CA, Regl DL, Madafiglio J, Norris MD, Horwitz SB. Altered expression of Mβ2, the class II β-tubulin isotype, in a murine J774.2 cell line with a high level of taxol resistance. J Biol Chem 1995;270:31,269–31,275.

    Article  PubMed  CAS  Google Scholar 

  216. Ranganathan S, Dexter DW, Benetatos CA, Chapman AE, Tew KD, Hudes GR. Increase of βIII-and βIVa-tubulin isotypes in human prostate carcinoma cells as a result of estramustine resistance. Cancer Res 1996;56:2584–2589.

    PubMed  CAS  Google Scholar 

  217. Ranganathan S, Dexter DW, Benetatos CA, Hudes GR. Cloning and sequencing of human βIII-tubulin cDNA: induction of βIII isotype in human prostate carcinoma cells by acute exposure to antimicrotubule agents. Biochim Biophys Acta 1998;1395:237–245.

    PubMed  CAS  Google Scholar 

  218. Banerjee A. Increased levels of tyrosinated α-, βIII-, and βIV-tubulin isotypes in paclitaxel-resistant MCF-7 breast cancer cells. Biochem Biophys Res Commun 2002;293:598–601.

    Article  PubMed  CAS  Google Scholar 

  219. Kavallaris M, Kuo DYS, Burkhart CA, et al. Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific β-tubulin isotypes. J Clin Invest 1997;100:1282–1293.

    Article  PubMed  CAS  Google Scholar 

  220. Sangrajang S, Denoulet P, Laing NM, et al. Association of estramustine resistance in human prostatic carcinoma cells with modified patterns of tubulin expression. Biochem Pharmacol 1998;55:325–331.

    Article  Google Scholar 

  221. Verdier-Pinard P, Wang F, Martello L, Burd B, Orr GA, Horwitz SB. Analysis of tubulin isotypes and mutations from taxol-resistant cells by combined isoelectrofocusing and mass spectrometry. Biochemistry 2003;42:5349–5357.

    Article  PubMed  CAS  Google Scholar 

  222. Sirotnak FM, Danenberg KD, Chen J, Fritz F, Danenberg PV. Markedly decreased binding of vincristine to tubulin in Vinca alkaloid-resistant Chinese hamster cells is associated with selective overexpression of a and β tubulin isoforms. Biochem Biophys Res Commun 2000;269:21–24.

    Article  PubMed  CAS  Google Scholar 

  223. Makarovsky AN, Siryaporn E, Hixson DC, Akerley W Survival of docetaxel-resistant prostate cancer cells in vitro depends on phenotype alterations and continuity of drug exposure. Cell Mol Life Sci 2002;59:1198–1211.

    Article  Google Scholar 

  224. Galmarini CM, Kamath K, Vanier-Viornery A, et al. Drug resistance associated with loss of p53 involves extensive alterations in microtubule composition and dynamics. Br J Cancer 2003;88: 1793–1799.

    Article  PubMed  CAS  Google Scholar 

  225. Giannakakou P, Sackett DF, Kang YK, et al. Paclitaxel-resistant human ovarian cancer cells have mutant β-tubulins that exhibit impaired paclitaxel-driven polymerization. J Biol Chem 1997;272:17,118–17,125.

    Article  PubMed  CAS  Google Scholar 

  226. Bernard-Marty C, Treilleux I, Dumontet C, et al. Microtubule-associated parameters as predictive markers of docetaxel activity in advanced breast cancer patients: results of a pilot study. Clin Breast Cancer 2002;3:341–345.

    Article  PubMed  CAS  Google Scholar 

  227. Iwamoto Y, Nishio K, Fukumoto H, Yoshimatsu K, Yamakido M, Saijo N. Preferential binding of E7010 to murine β3-tubulin and decreased β3-tubulin in E7010-resistant cell lines. Jpn J Cancer Res 1998;89:954–962.

    PubMed  CAS  Google Scholar 

  228. Derry WB, Wilson L, Khan IA, Ludueña RF, Jordan MA. Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified β-tubulin isotypes. Biochemistry 1997; 36:3554–3562.

    Article  PubMed  CAS  Google Scholar 

  229. Kavallaris M, Burkhart CA, Horwitz SB. Antisense oligonucleotides to class III β-tubulin sensitize drug-resistant cells to taxol. Br J Cancer 1999;80:1020–1025.

    Article  PubMed  CAS  Google Scholar 

  230. Ranganathan S, McCauley RA, Dexter DW, Hudes GR. Modulation of endogenous β-tubulin isotype expression as a result of human βIII cDNA transfection into prostate carcinoma cells. Br J Cancer 2001;85:735–740.

    Article  PubMed  CAS  Google Scholar 

  231. Nicoletti MI, Valoti G, Giannakakou P, et al. Expression of β-tubulin isotypes in human ovarian carcinoma xenografts and in a sub-panel of human cancer cell lines from the NCI-anticancer drug screen: correlation with sensitivity to microtubule active agents. Clin Can Res 2001;7:2912–2922.

    CAS  Google Scholar 

  232. Blade K, Menick DR, Cabrai F. Overexpression of class I, II or IVb β-tubulin isotypes in CHO cells is insufficient to confer resistance to paclitaxel. J Cell Sci 1999;112:2213–2221.

    PubMed  CAS  Google Scholar 

  233. Kavallaris M, Tait AS, Walsh BJ, et al. Multiple microtubule alterations are associated with Vinca alkaloid resistance in human leukemia cells. Cancer Res 2001;61:5803–5809.

    PubMed  CAS  Google Scholar 

  234. Hiser L, Aggarwal A, Young R, et al. Comparison of β-tubulin mRNA and protein levels in 12 human cancer cell lines. Cell Motil Cytoskeleton 2006;63:41–52.

    Article  PubMed  CAS  Google Scholar 

  235. Montgomery RB, Guzman J, O’Rourke DM, Stahl WL. Expression of oncogenic epidermal growth factor receptor family kinases induces paclitaxel resistance and alters β-tubulin isotype expression. J Biol Chem 2000;275:17,358–17,363.

    Article  PubMed  CAS  Google Scholar 

  236. Banerjee A, Roach MC, Trcka P, Ludueña RF. Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of β-tubulin. J Biol Chem 1990;265:1794–1799.

    PubMed  CAS  Google Scholar 

  237. Lee MK, Tuttle JB, Rebhun LI, Cleveland DW, Frankfurter A. The expression and posttranslational modification of neuron-specific β-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton 1990;17:118–132.

    Article  PubMed  CAS  Google Scholar 

  238. Lobert S, Frankfurter A, Correia JJ. Binding of vinblastine to phosphocellulose-purified and αβ-class III tubulin: the role of nucleotides and β-tubulin isotypes. Biochemistry 1995;34:8050–8060.

    Article  PubMed  CAS  Google Scholar 

  239. Lobert S, Frankfurter A, Correia JJ. Energetics of Vinca alkaloid interactions with tubulin isotypes: implications for drug efficacy and toxicity. Cell Motil Cytoskeleton 1998;39:107–121.

    Article  PubMed  CAS  Google Scholar 

  240. Banerjee A. Differential effects of colchicine and its B-ring modified analog MTPT on the assemblyindependent GTPase activity of purified β-tubulin isoforms from bovine brain. Biochem Biophys Res Commun 1997;231:698–700.

    Article  PubMed  CAS  Google Scholar 

  241. Khan IA, Ludueña RF. Phosphorylation of βIII-tubulin. Biochemistry 1996;35:3704–3711.

    Article  PubMed  CAS  Google Scholar 

  242. Schwarz PM, Liggins JR, Ludueña RF. β-Tubulin isotypes purified from bovine brain have different relative stabilities. Biochemistry 1998;37:4687–4692.

    Article  PubMed  CAS  Google Scholar 

  243. Ludueria RF, Roach MC. Interaction of tubulin with drugs and alkylating agents. 1. Alkylation of tubulin by iodo[14C]acetamide and N, N′-ethylenebis(iodoacetamide). Biochemistry 1981;20: 4437–4444.

    Article  Google Scholar 

  244. Roach MC, Ludueria RF. Different effects of tubulin ligands on the intrachain cross-linking of β1tubulin. J Biol Chem 1984;259:12,063–12,071.

    PubMed  CAS  Google Scholar 

  245. Little M, Ludueña RF. Location of two cysteines in brain β1-tubulin that can be cross-linked after removal of exchangeable GTP. Biochim Biophys Acta 1987;912:28–33.

    PubMed  CAS  Google Scholar 

  246. Taylor EW. The mechanism of colchicine binding inhibition of mitosis I. Kinetics of inhibition and the binding of H3-colchicine. J Cell Biol 1965;25:145–160.

    Article  PubMed  CAS  Google Scholar 

  247. Wilson L, Friedkin M. The biochemical events of mitosis. I. Synthesis and properties of colchicine labeled with tritium in its acetyl moiety. Biochemistry 1966;5:2463–2468.

    Article  PubMed  CAS  Google Scholar 

  248. Borisy GG, Taylor EW. The mechanism of action of colchicine: Binding of colchicine-3H to cellular protein. J Cell Biol 1967;34:525–533.

    Article  PubMed  CAS  Google Scholar 

  249. Weisenberg RC, Borisy GG, Taylor EW. The colchicine-binding protein of mammalian brain and its relation to microtubules. Biochemistry 1968;7:4466–4479.

    Article  PubMed  CAS  Google Scholar 

  250. Wilson L. Properties of colchicine-binding protein from chick embryo brain. Interactions with Vinca alkaloids and podophyllotoxin. Biochemistry 1970;9:4999–5007.

    Article  PubMed  CAS  Google Scholar 

  251. Wilson L, Meza I. The mechanism of action of colchicine: colchicine-binding properties of sea urchin sperm tail outer doublet tubulin. J Cell Biol 1973;58:709–714.

    Article  PubMed  CAS  Google Scholar 

  252. Wilson L, Bryan J. Biochemical and pharmacological properties of microtubules. Adv Cell Mol Biol 1974;3:21–72.

    CAS  Google Scholar 

  253. Bhattacharyya B, Wolff J. Promotion of fluorescence upon binding of colchicine to tubulin. Proc Nat Acad Sci USA 1974;71:2627–2631.

    Article  PubMed  CAS  Google Scholar 

  254. Arai T, Okuyama T. Fluorometric assay of tubulin-colchicine complex. Anal Biochem 1975;69:443–448.

    Article  PubMed  CAS  Google Scholar 

  255. Garland D. Kinetics and mechanism of colchicine binding to tubulin: evidence for ligand-induced conformational change. Biochemistry 1978;17:4266–4272.

    Article  PubMed  CAS  Google Scholar 

  256. Lambeir A, Engelborghs Y. A fluorescence stopped flow study of colchicine binding to tubulin. J Biol Chem 1981;256:3279–3282.

    PubMed  CAS  Google Scholar 

  257. Banerjee A, Ludueña RF. Kinetics of association and dissociation of colchicine-tubulin complex from brain and renal tubulin. Evidence for the existence of multiple isotypes of tubulin in brain with differential affinity to tubulin. FEBS Lett 1987;219:103–107.

    Article  PubMed  CAS  Google Scholar 

  258. Banerjee A, Barnes LD, Ludueña RF. The role of the B-ring of colchicine in the stability of the colchicine-tubulin complex. Biochim Biophys Acta 1987;913:138–144.

    PubMed  CAS  Google Scholar 

  259. Banerjee A, Ludueña RF. Distinct colchicine binding kinetics of bovine brain tubulin lacking the type III isotype of β-tubulin. J Biol Chem 1991;266:1689–1691.

    PubMed  CAS  Google Scholar 

  260. Banerjee A, Ludueña RF Kinetics of colchicine binding to purified β-tubulin isotypes from bovine brain. J Biol Chem 1992;267:13,335–13,339.

    PubMed  CAS  Google Scholar 

  261. Banerjee A, D’Hoore A, Engelborghs Y. Interaction of desacetamidocolchicine, a fast-binding analogue of colchicine with isotypically pure tubulin dimers αβII, αβIII, and αβIV. J Biol Chem 1994;269:10,324–10,329.

    PubMed  CAS  Google Scholar 

  262. Banerjee A, Engelborghs Y, D’Hoore A, Fitzgerald TJ. Interaction of a bicyclic analogue of colchicine with purified β-tubulin isoforms from bovine brain. Eur J Biochem 1997;246:420–424.

    Article  PubMed  CAS  Google Scholar 

  263. Carlier M-F. Role of nucleotide hydrolysis in the dynamics of actin filaments and microtubules. Int Rev Cytol 1989;115:139–170.

    Article  PubMed  CAS  Google Scholar 

  264. Guasch A, Aloria K, Pérez R, Avila J, Zabala JC, Coll M. Three-dimensional structure of human tubulin chaperone cofactor Am J Mol Biol 2002;318:1139–1149.

    Article  CAS  Google Scholar 

  265. Saito Y, Yamagishi N, Ishihara K, Hatayama T. Identification of α-tubulin as an hsp105α-binding protein by the yeast two-hybrid system. Exp Cell Res 2003;286:233–240.

    Article  PubMed  CAS  Google Scholar 

  266. Fukata Y, Itoh TJ, Kimura T, et al. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 2002;4:583–591.

    PubMed  CAS  Google Scholar 

  267. Bonnet C, Denarier E, Bosc C, Lazereg S, Denoulet P, Larcher JC. Interaction of STOP with neuronal tubulin is independent of polyglutamylation. Biochem Biophys Res Commun 2002;297:787–793.

    Article  PubMed  CAS  Google Scholar 

  268. Ems-McClung SC, Zheng Y, Walczak CE. Importin α/β and Ran-GTP regulate XCTK2 microtubule binding through a bipartite nuclear localization signal. Mol Biol Cell 2004;15:46–57.

    Article  PubMed  CAS  Google Scholar 

  269. Kinoshita K, Habermann B, Hyman AA. XMAP215: a key component of the dynamic microtubule cytoskeleton. Trends Cell Biol 2002;12:267–273.

    Article  PubMed  CAS  Google Scholar 

  270. Chaudhuri AR, Khan IA, Prasad V, Robinson AK, Ludueña RF, Barnes LD. The tumor suppressor protein Fhit. A novel interaction with tubulin. J Biol Chem 1999;274:24,738–24,382.

    Google Scholar 

  271. Lu C, Srayko M, Mains PE. The Caenorhabditis elegans microtubule-severing complex MEI-1/MEI-2 katanin interacts differently with two superficially redundant β-tubulin isotypes. Mol Biol Cell 2004;15:142–150.

    Article  PubMed  CAS  Google Scholar 

  272. Murata-Hori M, Tatsuka M, Wang YL. Probing the dynamics and functions of aurora B kinase in living cells during mitosis and cytokinesis. Mol Biol Cell 2002; 13:1099–1108.

    Article  PubMed  CAS  Google Scholar 

  273. Curmi P, Andersen SSL, Lachkar S, et al. The stathmin/tubulin interaction in vitro. J Biol Chem 1997;272:25,029–25,036.

    Article  PubMed  CAS  Google Scholar 

  274. Rappoport JZ, Taha BW, Simon SM. Movement of plasma-membrane-associated clathrin spots along the microtubule cytoskeleton. Traffic 2003;4:460–467.

    Article  PubMed  CAS  Google Scholar 

  275. Garcia-Mata R, Gao Y-S, Sztul E. Hassles with taking out the garbage: aggravating aggresomes. Traffic 2002;3:388–396.

    Article  PubMed  CAS  Google Scholar 

  276. Geimer S, Melkonian M. The ultrastructure of the Chlamydomonas reinhardtii basal apparatus: identification of an early marker of radial asymmetry inherent in the basal body. J Cell Sci 2004;117:2663–2674.

    Article  PubMed  CAS  Google Scholar 

  277. Matsuura K, Lefebvre PA, Kamiya R, Hirono M. Bld10p, a novel protein essential for basal body assembly in Chlamydomonas: localization to the cartwheel, the first ninefold symmetrical structure appearing during assembly. J Cell Biol 2004;165:663–671.

    Article  PubMed  Google Scholar 

  278. Baas PW. Neuronal polarity: microtubules strike back. Nat Cell Biol 2002;4:E194–E195.

    Article  PubMed  CAS  Google Scholar 

  279. Kierszenbaum AL. Intramanchette transport (IMT): managing the making of the spermatid head, centrosome, and tail. Mol Reprod Dev 2002;63:1–4.

    Article  PubMed  CAS  Google Scholar 

  280. Layden Donati RJ, Oh J, Yang S, Johnsonz ME, Rasenick MM. Structural model of Gα-tubulin interaction. Am Soc Cell Biol Ann Meeting Abstracts 2004;p. 425A.

    Google Scholar 

  281. Littauer UZ, Giveon D, Thierauf M, Ginzburg I, Ponstingl H. Common and distinct tubulin binding sites for microtubule-associated proteins. Proc Nat Acad Sci USA 1986;83:7162–7166.

    Article  PubMed  CAS  Google Scholar 

  282. Fujii T, Koizumi Y. Identification of the binding region of basic calponin on α-and β-tubulins. J Biochem 1999;125:869–875.

    PubMed  CAS  Google Scholar 

  283. Karabay A, Walker RA. Identification of Ncd tail domain-binding sites on the tubulin dimer. Biochem Biophys Res Commun 2003;305:523–528.

    Article  PubMed  CAS  Google Scholar 

  284. Burns RG, Surridge C. Analysis of β-tubulin sequences reveals highly conserved, coordinated amino acid substitutions. Evidence that these hot spots are directly involved in the conformational change required for dynamic instability. FEBS Lett 1990;271:1–8.

    Article  PubMed  CAS  Google Scholar 

  285. Hoyle HD, Hutchens JA, Turner FR, Raff EC. Regulation of β-tubulin β3 function and expression in Drosophila spermatogenesis. Dev Genet 1995;16:148–170.

    Article  PubMed  CAS  Google Scholar 

  286. Keskin O, Durell SR, Baahar I, Jernigan RL, Covell DG. Relating molecular flexibility to function: a case study of tubulin. Biophys J 2002;83:663–680.

    Article  PubMed  CAS  Google Scholar 

  287. Van Buren V, Odde DJ, Cassimeris L. Estimates of lateral and longitudinal bond energies within the microtubule lattice. Proc Nat Acad Sci USA 2002;99:6035–6040.

    Article  CAS  Google Scholar 

  288. Detrich HW, Parker SK, Williams RC, Nogales E, Downing KH. Cold adaptation of microtubule assembly and dynamics. Structural interpretation of primary sequence changes present in the α-and β-tubulins of Antarctic fishes. J Biol Chem 2000;275:37,038–37,047.

    Article  PubMed  CAS  Google Scholar 

  289. Pucciarelli S, Miceli C. Characterization of the cold-adapted α-tubulin from the psychrophilic ciliate Euplotes focardii. Extremophiles 2002;6:385–389.

    Article  PubMed  CAS  Google Scholar 

  290. Murphy WJ, Elzirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ. Molecular phylogenetics and the origins of placental mammals. Nature 2001;409:614–618.

    Article  PubMed  CAS  Google Scholar 

  291. Colbert EH. Evolution of the Vertebrates, 3rd ed. New York: John Wiley and Sons; 1980.

    Google Scholar 

  292. Benton MJ, Ayala FJ. Dating the tree of life. Science 2003;300:1698–1700.

    Article  PubMed  CAS  Google Scholar 

  293. Modig C, Wallin M, Olsson P-E. Expression of cold-adapted β-tubulins confer cold-tolerance to human cellular microtubules. Biochem Biophys Res Commun 2000;269:787–791.

    Article  PubMed  CAS  Google Scholar 

  294. Detrich HW, Neighbors BW, Sloboda RD, Williams RC. Microtubule-associated proteins from Antarctic fishes. Cell Motil Cytoskeleton 1990;17:174–186.

    Article  PubMed  CAS  Google Scholar 

  295. Willmer P. Invertebrate Relationships. Patterns in Animal Evolution. Cambridge: Cambridge University Press; 1990.

    Google Scholar 

  296. Barrington EJW. Essential features of lower types. In: Wake MH, ed. Hyman’s Comparative Vertebrate Anatomy, 3rd ed. Chicago: University of Chicago Press; 1979;57–86.

    Google Scholar 

  297. Northcutt RG. The comparative anatomy of the nervous system and sense organs. In: Wake MH, ed. Hyman’s Comparative Vertebrate Anatomy, 3rd ed. Chicago: University of Chicago Press; 615–769.

    Google Scholar 

  298. Cloud P. Oasis in Space: Earth History from the Beginning. W.W. Norton and Co., New York.

    Google Scholar 

  299. Buchsbaum R. Animals Without Backbones. Chicago: University of Chicago Press.

    Google Scholar 

  300. Palmer D. Prehistoric Past Revealed: the Four Billion Year History of Life on Earth. University of California Press, Berkeley, 2003.

    Google Scholar 

  301. Gould SJ. Wonderful Life: the Burgess Shale and the Nature of History, W.W. Norton and Co., New York, 1989.

    Google Scholar 

  302. Arai K. Molecular cloning of isotype-specific regions of five classes of canine β-tubulin and their tissue distribution. NCBI Accession no. BAA96409, BAA96410, BAA96411, BAA96412, 1999.

    Google Scholar 

  303. Sidjanin DJ, Zangerl B, Johnson JL, et al. Cloning of the canine δ-tubulin cDNA (TUBD) and mapping to CFA9. Anim Genet 2002;33:161–162.

    Article  PubMed  CAS  Google Scholar 

  304. Kubo A, Hata M, Kubo A, Tsukita S. Gene-knockout analysis of two γ-tubulin isoforms in mice. NCBI Accession no. BAD27264, BAD27265, 2004.

    Google Scholar 

  305. Lemischka IR, Farmer S, Racaniello VR, Sharp PA. Nucleotide sequence and evolution of a mammalian α-tubulin messenger RNA. J Mol Biol 1981;151:101–120.

    Article  PubMed  CAS  Google Scholar 

  306. Usui H, Miyazaki Y, Xin D, Ichikawa T, Kumanishi T. Cloning and sequencing of the rat cDNAs encoding class I β-tubulin. DNA Seq 1998;9:365–368.

    Article  PubMed  CAS  Google Scholar 

  307. Ginzburg I, Teichman A, Dodemont HJ, Behar L, Littauer UZ. Regulation of three β-tubulin mRNAs during rat brain development. EMBO J 1985;4:3667–3673.

    PubMed  CAS  Google Scholar 

  308. Dennis KE, Spano A, Frankfurter A, Moody SA. Rattus norvegicus neuron-specific class III β-tubulin mRNA. NCBI Accession no. NP_640347, 2001.

    Google Scholar 

  309. Arai K. Preparation and characterization of a monoclonal antibody to class II β-tubulin isotype. NCBI Accession no. BAB72260, 2001.

    Google Scholar 

  310. Nakadai T, Okada N, Makino Y, Tamura T. Structure of rat γ-tubulin and its binding to HP33. DNA Res 1999;6:207–209.

    Article  PubMed  CAS  Google Scholar 

  311. Linhartová I, Novotná B, Sulimenko V, Dráberová E, Dráber P. γ-tubulin in chicken erythrocytes: changes in localization during cell differentiation and characterization of cytoplasmic complexes. Dev Dyn 2002;223:229–240.

    Article  PubMed  CAS  Google Scholar 

  312. Stearns T, Evans L, Kirschner M. γ-Tubulin is a highly conserved component of the centrosome. Cell 1991;65:825–836.

    Article  PubMed  CAS  Google Scholar 

  313. Parker SK, Detrich HW. Evolution, organization and expression of α-tubulin genes in the Antarctic fish Notothenia coriiceps. Adaptive expansion of a gene family by recent gene duplication, inversion, and divergence. J Biol Chem 1998;273:34,358–34,369.

    Article  PubMed  CAS  Google Scholar 

  314. Bormann P, Zumsteg VM, Roth LWA, Reinhard E. Target contact regulates GAP-43 and α-tubulin mRNA levels in regenerating retinal ganglion cells. J Neurosci Res 1998;52:405–419.

    Article  PubMed  CAS  Google Scholar 

  315. Edvardsen RB, Flaat M, Tewari R, et al. Most intron positions in Oikopleura dioica α-tubulin genes are unique: did new introns help to preserve and expand gene families? NCBI Accession no. AAM73981, AAM73982, AAM73986, AAM73987, AAM73991, AAM73992, AAM73993, AAM73995, AAM73996, AAM73997, 2002b.

    Google Scholar 

  316. Edvardsen, RB, Lerat E, Flaat M, et al. Hypervariable intron/exon organizations in the chordate Oikopleura and the nematode Caenorhabditis, two species with a very short life cycle. NCBI Accession no. AAO00725, AAP80593, AAP80594, AAP80595, AAP80596, AAP80597, AAP80598, AAP80599, AAP80600, AAP80601, AAP80602, AAP80603, 2002d.

    Google Scholar 

  317. Rogers GC, Chui KK, Lee EW, et al. A kinesin-related protein, KRP(180), positions prometaphase spindle poles during early sea urchin embryonic cell division. J Cell Biol 2000;150:499–512.

    Article  PubMed  CAS  Google Scholar 

  318. Varadaraj V, Kumari SS, Skinner DM. Molecular characterization of four members of the α-tubulin gene family of the Bermuda land crab Gecarcinus lateralis. J Exp Zool 1997;278:63–77.

    Article  PubMed  CAS  Google Scholar 

  319. Llamazares S, Tavosanis G, Gonzalez C. Cytological characterisation of the mutant phenotypes produced during early embryogenesis by null and loss-of-function alleles of the γTub37C gene in Drosophila. J Cell Sci 1999;112:659–667.

    PubMed  CAS  Google Scholar 

  320. Moccia R, Chen D, Lyles V, et al. An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. J Neurosci 2002;23:9409–9417.

    Google Scholar 

  321. Fedorov A, Johnston H, Korneev S, Blackshaw S, Davies J. Cloning, characterisation and expression of the α-tubulin genes of the leech, Hirudo medicinalis. Gene 1999;227:11–19.

    Article  PubMed  CAS  Google Scholar 

  322. Bobinnec Y, Fukuda M, Nishida E. Identification and characterization of Caenorhabditis elegans γ-tubulin in dividing cells and differentiated tissues. J Cell Sci 2000;113:3747–3759.

    PubMed  CAS  Google Scholar 

  323. Pape M, Schnieder T, von Samson-Himmelstjerna G. Investigation of diversity and isotypes of the β-tubulin cDNA in several small strongyle (Cyathostominae) species. J Parasitai 2002;88:673–677.

    CAS  Google Scholar 

  324. Von Samson-Himmelstjerna G, Harder A, Pape M, Schneider T. Novel small strongyle (Cyathostominae) β-tubulin sequences. Parasitai Res 2001;87:122–125.

    Article  Google Scholar 

  325. Pape M, von Samson-Himmelstjerna G, Schnieder T. Characterisation of the β-tubulin gene of Cylicocyclus nassatus. Int J Parasitol 1999;29:1941–1947.

    Article  PubMed  CAS  Google Scholar 

  326. Njue AI, Prichard RK. Cloning two full-length β-tubulin isotype cDNAs from Cooperia oncophora, and screening for benzimidazole resistance-associated mutations in two isolates. Parasitology 2003;127:579–588.

    Article  PubMed  CAS  Google Scholar 

  327. Collins CM, Miller KA, Cunningham CO. Characterisation of a β-tubulin gene from the monogenean parasite, Gyrodactylus salaris Malmberg, 1957. Parasitai Res 2004;92:390–399.

    Article  CAS  Google Scholar 

  328. Brehm K, Kronthaler K, Jura H, Frosch M. Cloning and characterization of β-tubulin genes from Echinococcus multilocularis. Mol Biochem Parasitai 2000; 107:297–302.

    Article  CAS  Google Scholar 

  329. Qin X, Gianì S, Breviario D. Molecular cloning of three rice α-tubulin isotypes: differential expression in tissues and during flower development. Biochim Biophys Acta 1997;1354:19–23.

    PubMed  CAS  Google Scholar 

  330. Kim Y-K, Cha Y-K, Jun H-Y, Kim J-D, Choi J-S, Kim HR. Nucleotide sequence of a cDNA (OstubG2) encoding a γ-tubulin in the rice plant (Oryza sativa). NCBI Accession no. 049068, 2001.

    Google Scholar 

  331. Segal G, Feldman M. NCBI Accession no. AAD10487, AAD10488, AAD10489, AAD10490, AAD10492, AAD10493, 1996.

    Google Scholar 

  332. Liu B, Joshi HC, Wilson TJ, Silflow CD, Palevitz BA, Snustad DP. γ-Tubulin in Arabidopsis: gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 1994;6:303–314.

    Article  PubMed  CAS  Google Scholar 

  333. Okamura S, Okahara K, Iida T, et al. Isotype-specific changes in the amount of β-tubulin RNA in synchronized tobacco BY2 cells. Cell Struct Funct 1999;24:117–122.

    Article  PubMed  CAS  Google Scholar 

  334. Okamura S, Hara M, Yamaguchi A. NCBI Accession no. AAB50565, 2000.

    Google Scholar 

  335. Okamura S, Yamaguchi A, Narita K, Morita M, Imanaka T. β-Tubulin isotypes in the tobacco BY2 cell cycle. Cell Biol Int 2003;27:245–246.

    Article  PubMed  CAS  Google Scholar 

  336. Breviario D, Linss M, Nick P. α-Tubulins from tobacco: gene cloning and expression studies. NCBI Accession no. CAD13176, CAD13177, CAD13178, 2001.

    Google Scholar 

  337. Kautz K, Schroeder J, Wernicke W. Characterization of γ-tubulin from tobacco. NCBI Accession no. CAC00547, 2000.

    Google Scholar 

  338. Schröder J. NCBI Accession no. CAA10664CAA70891, CAB76916, CAB76380, 2000.

    Google Scholar 

  339. Ji S, Liang X, Shi Y, Weu G, Lu Y, Zhu Y Expression profile study and functional analysis of α-and β-tubulin isotypes during cotton fiber development. NCBI Accession no. AAL92026, AAN32988, AAN32989, AAN32991, AAN32995, AAQ92665, AAQ92664, AAQ92666, AAQ92667, AAQ92668, 2002.

    Google Scholar 

  340. Saibo NJM, Van Der Straeten D, Rodriges-Pousada C. Lupinus albus γ-tubulin: mRNA and protein accumulation during development and in response to darkness. Planta 2004;219:201–211.

    Article  PubMed  CAS  Google Scholar 

  341. Kalluri UC, Joshi CP. Molecular cloning of tubulin cDNA from aspen xylem. NCBI Accession no. AAO23139, 2002.

    Google Scholar 

  342. Wang Y-S, Tsai C-J. Isolation and characterization of cDNAs involved in vascular development of quaking aspen. NCBI Accession no. AAO63773, AAO63781, 2003.

    Google Scholar 

  343. Canaday J, Stoppin V, Endle MC, Lambert AM. NCBI Accession no. Q41808, 1994.

    Google Scholar 

  344. Canaday J, Stoppin V, Endle MC, Lambert AM. Identification of two maize cDNAs encoding γ-tubulin. NCBI Accession no. CAA58670, 1995.

    Google Scholar 

  345. Yamamoto E, Zeng L, Baird WV. α-Tubulin missense mutations correlate with antimicrotubule drug resistance in Eleusine indica. Plant Cell 1998;10:297–308.

    Article  PubMed  CAS  Google Scholar 

  346. Yamamoto E, Baird WV. Molecular characterization of four β-tubulin genes from dinitroaniline susceptible and resistant biotypes of Eleusine indica. Plant Mol Biol 1999;39:45–61.

    Article  PubMed  CAS  Google Scholar 

  347. Wu W, Schaal BA, Hwang CY, Chiang YC, Chiang TY. Molecular cloning and evolutionary analysis of Miscanthus α-tubulin genes. Am J Bot 2003;90:1513–1521.

    Article  CAS  Google Scholar 

  348. Fuchs U, Moepps B, Maucher HP, Schraudolf H. Isolation, characterization and sequence of a cDNA encoding γ-tubulin protein from the fern Anemia phyllitidis L Sw Plant Mol Biol 1993;23: 595–603.

    Article  PubMed  CAS  Google Scholar 

  349. Moepps B, Maucher HP, Bogenberger JM, Schraudolf H. Characterization of the α-and β-tubulin gene families from Anemia phyllitidis. NCBI Accession no. CAA48929, CAA48930, 1993.

    Google Scholar 

  350. Fujita T, Nishiyama T, Hasebe M. Isolation of α tubulin cDNAs in Physcomitrella patens. NCBI Accession no. BAC24799, BAC24800, 2002.

    Google Scholar 

  351. Baur A, Gorr G, Jost W. Six β-tubulin genes from Physcomitrella patens. NCBI Accession no. AAQ88113, AAQ88114, AAQ88115, AAQ88116, AAQ88117, AAQ88118, 2003.

    Google Scholar 

  352. Wagner TA, Sack FD, Oakley BR, Oakley CE, Schwuchow J. Characterization of γ-tubulin from Physcomitrella patens. NCBI Accession no. AAD33883, 1999.

    Google Scholar 

  353. Takano Y, Oshiro E, Okuno T. Microtubule dynamics during infection-related morphogenesis of Colletotrichum lagenarium. Fungal Genet Biol 2001;34:107–121.

    Article  PubMed  CAS  Google Scholar 

  354. Daly S, Yacoub A, Dundon WE, Mastromei G, Islam K, Lorenzetti R. Isolation and characterization of a gene encoding α-tubulin from Candida albicans. Gene 1997;187:151–158.

    Article  PubMed  CAS  Google Scholar 

  355. Dujon B, Sherman D, Fischer G, et al. Genome evolution in yeasts. Nature 2004;430:35–44.

    Article  PubMed  Google Scholar 

  356. Heckmann S, Schliwa M, Kube-Granderath E. Primary structure of Neurospora crassa γ-tubulin. Gene 1997;199:303–309.

    Article  PubMed  CAS  Google Scholar 

  357. Mukherjee M, Hadar R, Mukherjee PK, Horwitz BA. Homologous expression of a mutated β-tubulin gene does not confer benomyl resistance on Trichoderma virens. J Appl Microbiol 2003;95:861–867.

    Article  PubMed  CAS  Google Scholar 

  358. Park S-Y, Jung O-J, Chung Y-R, Lee C-W. Isolation and characterization of a benomyl-resistant form of β-tubulin-encoding gene from the phytopathogenic fungus Botryotiniafuckeliana. Molecules Cells 1997;7:104–109.

    CAS  Google Scholar 

  359. Zhang J, Stringer JR. Cloning and characterization of an α-tubulin-encoding gene from rat-derived Pneumocystis carinii. Gene 1993;123:137–141.

    Article  PubMed  CAS  Google Scholar 

  360. Keeling PJ, Luker MA, Palmer JD. Evidence from β-tubulin phylogeny that microsporidia evolved from within the fungi. Mol Biol Evol 2000;17:23–31.

    PubMed  CAS  Google Scholar 

  361. Keeling PJ. Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet Biol 2003;38:298–309.

    Article  PubMed  CAS  Google Scholar 

  362. Voigt K, Einax E. Oligonucleotide primers for the universal amplification of β-tubulin genes facilitate phylogenetic analyses in the regnum Fungi. Org Divers Evol 2003;3:185–194.

    Article  Google Scholar 

  363. Corradi N, Kuhn G, Sanders IR. Monophyly of β-tubulin and H+-ATPase gene variants in Glomus intraradices: consequences for molecular evolutionary studies of AM fungal genes. Fungal Genet Biol 2004;41:262–273.

    Article  PubMed  CAS  Google Scholar 

  364. Juuti JT, Jokela S, Tarkka M, Paulin L, Lahdensalo J. Two phylogenetically highly distinct β-tubulin genes of the basidiomycete Suillus bovinus. NCBI Accession no. CAG27308, CAG27309, 2004.

    Google Scholar 

  365. Cruz MC, Edlind T. β-Tubulin genes and the basis for benzimidazole sensitivity of the opportunistic fungus Cryptococcus neoformans. Microbiology 1997;143:2003–2008.

    PubMed  CAS  Google Scholar 

  366. MacDonald LM, Armson A, Thompson A, Reynoldson JA. Characterization of factors favoring the expression of soluble protozoan tubulin proteins in Escherichia coli. Protein Expr Purif 2003;29:117–122.

    Article  PubMed  CAS  Google Scholar 

  367. Katinka MD, Duprat S, Cornillot E, et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 2001;414:450–453.

    Article  PubMed  CAS  Google Scholar 

  368. Cacciò S, La Rosa G, Pozio E. The β-tubulin gene of Cryptosporidium parvum. Mol Biochem Parasitai 1997;89:4155–4159.

    Article  Google Scholar 

  369. Abrahamsen MS, Templeton TJ, Enomoto S, et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 2004;304:441–445.

    Article  PubMed  CAS  Google Scholar 

  370. Maessen S, Wesseling JG, Smits MA, Konings RN, Schoenmakers JG. Theγ-tubulin gene of the malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 1993;60:27–35.

    Article  PubMed  CAS  Google Scholar 

  371. Lajoie-Mazenc I, Détraves C, Rotaru V, et al. A single γ-tubulin gene and mRNA, but two γ-tubulin polypeptides differing by their binding to the spindle pole organizing centres. J Cell Sci 1996;109:2483–2492.

    PubMed  CAS  Google Scholar 

  372. Willem S, Srahna M, Loppes R, Matagne RF. NCBI Accession no. AAB86648, AAB86649, 1997.

    Google Scholar 

  373. Silflow CD, Liu B, LaVoie M, Richardson EA, Palevitz BA. γ-Tubulin in Chlamydomonas: characterization of the gene and localization of the gene product in cells. Cell Motil Cytoskeleton 1999;42:285–297.

    Article  PubMed  CAS  Google Scholar 

  374. Mages W, Salbaum JM, Harper JF, Schmitt R. Organization and structure of Volvox α-tubulin genes. Mol Gen Genet 1988;213:449–458.

    Article  PubMed  CAS  Google Scholar 

  375. Dupuis-Williams P. γ-tubulin is necessary for basal body duplication in Paramecium. NCBI Accession no. CAA09992, 1998.

    Google Scholar 

  376. Joachimiak E, Miceli C, Kaczanowska J. Cloning and expression analysis of γ-tubulin gene in Tetrahymena pyriformis. NCBI Accession no. AAG44954, 2000.

    Google Scholar 

  377. Pucciarelli S, Ballarini P, Miceli C. Cold-adapted microtubules: Characterization of tubulin posttranslational modifications in the Antarctic ciliate Euplotes focardii. Cell Motil Cytoskeleton 1997;38:329–340.

    Article  PubMed  CAS  Google Scholar 

  378. Tan M, Liang A, Heckmann K. The two γ tubulin genes of Euplotes octocarinatus code for a slightly different protein. NCBI Accession no. P34786, CAA70745, 1996.

    Google Scholar 

  379. Tan M, Heckmann K. The two γ-tubulin-encoding genes of the ciliate Euplotes crassus differ in their sequences, codon usage, transcription initiation sites and poly(A) addition sites. Gene 1998;210: 53–60.

    Article  PubMed  CAS  Google Scholar 

  380. Katz LA, Israel RL. The fate of duplicated α-tubulin genes in ciliates. NCBI Accession no. AAL33680, AAL33681, AAL33682, AAL33683, AAL33684, AAL33685, AAL33686, AAL33691, AAL33692, AAL33694, AAL33695, AAL33697, AAL33698, AAL33699, AAL33700, AAL33713, AAL33714. AAL33715, AAL33718, AAL33719, AAL33724, AAL33725, 2001.

    Google Scholar 

  381. Pérez-Romero P, Villalobo E, Díaz-Ramos C, Calvo P, Santos-Rosa F, Torres A. α-Tubulin of Histriculus cavicola. Microbiología 1997;13:57–66.

    PubMed  Google Scholar 

  382. Snoeyenbos-West OLO, Salcedo T, McManus GB, Katz LA. Insights into the diversity of choreotrich and oligotrich ciliates (Class: Spirotrichea) based on genealogical analyses of multiple loci. Int J Syst Evol Microbiol 2002;52:1901–1913.

    Article  PubMed  CAS  Google Scholar 

  383. Sanchez-Silva R, Torres A. α-Tubulin of peritrich ciliates. (Unpublished) NCBI Accession no. AAM50063, AAM50064, 2002.

    Google Scholar 

  384. Ueda M, Graf R, Mac Williams HK, Schliwa M, Euteneuer U. Centrosome positioning and directionality of cell movements. Proc Nat Acad Sci USA 1997;94:9674–9678.

    Article  PubMed  CAS  Google Scholar 

  385. Saldarriaga JF, McEwan ML, Fast NM, Taylor FJR, Keeling PJ. Multiple protein phylogenies show that Oxyrrhus marina and Perkinsus marinus are early branches of the dinoflagellate lineage. Int J Syst Evol Microbiol 2003;53:355–365.

    Article  PubMed  CAS  Google Scholar 

  386. Kube-Granderath E, Schliwa M. Unusual distribution of γ-tubulin in the giant fresh water amoeba Reticulomyxa filosa. Eur J Cell Biol 1997;72:287–296.

    PubMed  CAS  Google Scholar 

  387. Libusová L, Sulimenko T, Sulimenko V, Hozák P, Dráber P. γ-Tubulin in Leishmania: cell cycle-dependent changes in subcellular localization and heterogeneity of its isoforms. Exp Cell Res 2004;295: 375–386.

    Article  PubMed  CAS  Google Scholar 

  388. Ivens AC, Lewis SM, Bagherzadeh A, Zhang L, Chan HM, Smith DF. A physical map of the Leishmania major Friedlin genome. Genome Res 1998;8:135–145.

    PubMed  CAS  Google Scholar 

  389. Ersfeld K, Gull K. Partitioning of large and minichromosomes in Trypanosoma brucei. Science 1997;276:611–614.

    Article  PubMed  CAS  Google Scholar 

  390. Scott V. NCBI Accession no. CAA68866, 1996.

    Google Scholar 

  391. Noël C, Gerbod D, Fast NM, et al. Tubulins in Trichomonas vaginalis: molecular characterization of α-tubulin genes, posttranslational modifications, and homology modeling of the tubulin dimer. J Eukaryot Microbiol 2001;48:647–654.

    Article  PubMed  Google Scholar 

  392. Schneider A, Plessmann U, Felleisen R, Weber K. α-Tubulins of Tritrichomonas mobilensis are encoded by multiple genes and are not posttranslationally tyrosinated. Parasitai Res 1999;85: 246–248.

    Article  CAS  Google Scholar 

  393. Moriya S, Tanaka K, Ohkuma M, Sugano S, Kudo T. Diversification of the microtubule system in the early stage of eukaryote evolution: elongation factor 1α and α-tubulin protein phylogeny of termite symbiotic oxymonad and hypermastigote protists. J Mol Evol 2001;52:6–16.

    PubMed  CAS  Google Scholar 

  394. Moriya S, Gerbod D, Viscogliosi E. NCBI Accession no. BAC98828, 2003.

    Google Scholar 

  395. Gerbod D, Sanders E, Moriya S, et al. Molecular phylogenies of Parabasalia inferred from various protein coding gene sequences and comparison with small subunit rRNA-based trees. NCBI Accession no. AAQ19197, AAQ19198, AAQ19199, AAQ19200, AAQ19201, 2003.

    Google Scholar 

  396. Coffman HR, Kropf DL. The brown alga, Pelvetia fastigiata, expresses two α-tubulin sequences. NCBI Accession no. Q40831, Q40832, 1999.

    Google Scholar 

  397. Keeling PJ, Deane JA, McFadden GI. The phylogenetic position of α-and β-tubulins from the Chlorarachnion host and Cercomonas (Cercozoa). J Eukaryot Microbiol 1998;45:561–570.

    Article  PubMed  CAS  Google Scholar 

  398. Keeling PJ, Leander BS. Characterisation of a non-canonical genetic code in the oxymonad Streblomastix strix. J Mol Biol 2002;326:1337–1349.

    Article  Google Scholar 

  399. Eun S-O, Wick SM. Tubulin isoform usage in maize microtubules. Protoplasma 1998;204:235–244.

    Article  CAS  Google Scholar 

  400. Lee MG, Loomis C, Cowan NJ. Sequence of an expressed human β-tubulin gene containing ten Alu family members. Nucleic Acids Res 1984;12:5823–5836.

    Article  PubMed  CAS  Google Scholar 

  401. Strausberg RL, Feingold EA, Grouse LH, et al. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Nat Acad Sci USA 2002;99:16,899–16,903. Swissprot Accession no. Q9BUF5, Q8AVU1.

    Article  PubMed  Google Scholar 

  402. Adachi J, Aizawa K, Akahira S, et al. Swissprot Accession no. Q9CUN8, 2000.

    Google Scholar 

  403. Smith DJ. The complete sequence of a frog α-tubulin and its regulated expression in mouse L-cells. Biochem J 1988;249:465–472.

    PubMed  CAS  Google Scholar 

  404. Cowan NJ, Dobner PR, Fuchs EV, Cleveland DW. Expression of human α-tubulin genes: interspecies conservation of 3′untranslated regions. Mol Cell Biol 1983;3:1738–1745.

    PubMed  CAS  Google Scholar 

  405. Dode C, Weil D, Levilliers J, et al. Sequence characterization of a newly identified human α-tubulin gene (TUBA2). Genomics 1998;47:125–130.

    Article  PubMed  CAS  Google Scholar 

  406. Dobner PR, Kislauskis E, Wentworth BM, Villa-Komaroff L. Alternative 5′ exons either provide or deny an initiator methionine codon to the same α-tubulin coding region. Nucleic Acids Res 1987;15:199–218.

    Article  PubMed  CAS  Google Scholar 

  407. Klein SL, Strausberg RL, Wagner L, Pontius J, Clifton SW, Richardson P. Genetic and genomic tools for Xenopus research: The NIH Xenopus initiative. Dev Dyn 2002;225:384–391.

    Article  PubMed  CAS  Google Scholar 

  408. Song HD, Wu XY, Sun XJ, et al. Gene expression profiling in the zebrafish kidney marrow tissue. NCBI Accession no. AAQ097807, 2003.

    Google Scholar 

  409. Lewis SA, Cowan NJ. Tubulin genes: structure, expression and regulation. In: Avila J, ed. Microtubule Proteins. Boca Raton, Florida: CRC Press; 37–66.

    Google Scholar 

  410. Khan IA, Tomita I, Mizuhashi F, Ludueña RF. Differential interaction of tubulin isotypes with the antimitotic compound IKP-104. Biochemistry 2000;39:9001–9009.

    Article  PubMed  CAS  Google Scholar 

  411. Banerjee A, Kasmala LT, Hamel E, Sun L, Lee KH. Interaction of novel thiocolchicine analogs with the tubulin isoforms from bovine brain. Biochem Biophys Res Commun 1999;254:334–337.

    Article  PubMed  CAS  Google Scholar 

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Ludueña, R.F., Banerjee, A. (2008). The Isotypes of Tubulin. In: Fojo, T. (eds) The Role of Microtubules in Cell Biology, Neurobiology, and Oncology. Cancer Drug Discovery and Development. Humana Press. https://doi.org/10.1007/978-1-59745-336-3_6

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