Summary
We have isolated and characterized five overlapping clones that encompass 3.2 kb and encode a part of the short subfragment 2, the hinge, and the light meromyosin regions of the myosin heavy chain rod as well as 143 bp of the 3′ untranslated portion of the mRNA. Northern blot analysis showed expression of this mRNA mainly in ventricular muscle of the adult chicken heart, with trace levels detected in the atrium. Transient expression was seen in skeletal muscle during development and in regenerating skeletal muscle following freeze injury. To our knowledge, this is the first report of an avian ventricular myosin heavy chain sequence. Phylogenetic analysis indicated that this isoform is a distant homolog of other ventricular and skeletal muscle myosin heavy chains and represents a distinct member of the multigene family of sarcomeric myosin heavy chains. The ventricular myosin heavy chain of the chicken is either paralogous to its counterpart in other vertebrates or has diverged at a significantly higher rate.
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References
Bader D, Masaki T, Fischman DA (1982) Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol 95:763–770
Bárány M (1967) ATPase activity of myosin correlated with the speed of muscle shortening. J Gen Physiol [Suppl 2] 50: 197–218
Benton MJ (1990) Phylogeny of the major tetrapod groups: morphological data and divergence dates. J Mol Evol 30:409–424
Bober E, Buchberger-Seidl A, Braun T, Singh S, Goedde HW, Arnold HH (1990) Identification of three developmentally controlled isoforms of human myosin heavy chain. Eur J Biochem 189:55–65
Casimir CM, Gates PB, Ross-Macdonald PB, Jackson JF, Patient RK, Brockes JP (1980) Structure and expression of a newt cardiac-skeletal myosin gene. J Mol Biol 202:287–296
Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159
Clark WA, Chizzonite RA, Everett AW, Rabinowitz M, Zak R (1982) Species correlations between cardiac isomyosins. A comparison of electrophoretic and immunological properties. J Biol Chem 257:5449–5454
Collier VL, Kronert WA, O'Donnell PT, Edwards KA, Bernstein SI (1990) Alternative myosin hihge regions are utilized in a tissue-specific fashion that correlates with muscle contraction speed. Genes & Dev 4:885–895.
Cox RD, Garner I, Buckingham ME (1990) Transcriptional regulation of actin and myosin genes during differentiation of a mouse muscle cell line. Differentiation 43:183–191
deGroot IJM, Hardy GPMA, Sanders E, Los JA, Moorman AFM (1985) The conducting tissue in the adult chicken atria, a histological and immunohistochemical analysis. Anat Embryol 172:239–245
Evans D, Miller JB, Stockdale FE (1988) Developmental patterns of expression and coexpression of myosin heavy chains in atria and ventricles of the avian heart. Dev Biol 127:376–383
Feghali R, Leinwand LA (1989) Molecular genetic characterization of a developmentally regulated human perinatal myosin heavy chain. J Cell Biol 108:1791–1979
Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13
Freyer GA, Robbins J (1938) The analysiss of a chicken myosin heavy chain cDNA clone. J Biol Chem 258:7149–7154
George EL, Ober MB, Emerson CP Jr (1989) Functional domains of theDrosophila melanogaster muscle myosin heavychain gene are encoded by alternatively spliced exons. Mol Cell Biol 9:2957–2974
Goldberg JM, Johnson MH, Whitelaw KD (1983) Effect of cervical vagal stimulation on chicken heart rate and atrioventricular conduction. Am J Physiol U244:R235-R243
Gonzáles-Sánchez A, Bader D (1984) Immunochemical analysis of myosin heavy chains in the developing chicken heart. Dev Biol 103:151–158
Gulick J, Kropp K, Robbins J (1985) The structure of two fastwhite myosin heavy chain promoters. A comparative study. J Biol Chem 260:14513–14520
Gulick J, Kropp K, Robbins J (1987) The developmentally regulated expression of two linked myosin heavy chain genes. Eur J Biochem 169:79–84
Harrington WF, Rodgers ME (1984) Myosin. Annu Rev Biochem 53:35–73
Harrington WF, Karr T, Busa WB, Lovell SJ (1990) Contraction of myofibrils in the presence of antibodies to myosin subfragment 2. Proc Natl Acad Sci USA 87:7453–7456
Jandreski MA, Sole MJ, Liew C-C (1988) Seuqence of cDNA encoding the Syrian hamster cardiac β-myosin heavy chain. Nucleic Acids Res 16:4737
Kavinski CJ, Umeda PK, Levin JE, Sinha AM, Nigro JM, Jakovcic S, Rabinowitz M (1984) Analysis of cloned mRNA sequences encoding subfragment 2 and part of subfragment 1 of α- and β-myosin heavy chains of rabbit heart. J Biol Chem 259:2775–2781
Kennedy JM, Eisenberg BR, Reid SK, Sweeney LJ, Zak R (1988) Nescent muscle fiber appearance in overloaded chicken slowtonic muscle. Am J Anat 181:203–215
Kennedy JM, Sweeney LJ, Gao L (1989) Ventricular myosin expression in developing and regenerating muscle, cultured myotubes, and nascent myofibeirs of overloaded muscle in the chicken. Med Sci Sprots Exercise 21:S187-S197
Kishino, A, Yanagida T (1988) Force measurements by micromanipulation of a single actin filament by glass needles. Nature 334:74–76
Kraft R, Bravo-Zehnder M, Taylor DA, Leinwand LA (1989) Complete nucleotide sequence of full length cDNA for rat β cardiac myosin heavy chain. Nucleic Acids Res 17:7529–7530
Lang S, Levy MN (1989) Effects of vagus nerve on heart rate and ventricular contractility in chicken. Am J Physiol 256: H1295-H1302
Leinwand LA, Fournier REK, Nadal-Ginard B, Shows TB (1983) Multigene family for sarcomeric myosin heavy chain in mouse and human DNA: localization on a single chronosome. Science 221:766–769
Lichter P, Umeda PK, Levin JE, Vosberg H-P (1986) Partial characterization of the human β-myosin heavy chain gene which is expressed in heart and skeletal muscle. Eur J Biochem 160:419–426
Liew C-C, Sole MJ, Yamauchi-Takihara K, Kellam B, Anderson DH, Lin L, Liew JC (1990) Complete sequence and organization of the human cardiac β-myosin heavy chain gene. Nucleic Acids Res 18:3647–3651
Lompré A-M, Nadal-Ginard B, Mahdavi V (1984) Expression of the cardiac ventricular α- and β-moyosin heavy chain genes is developmentally and hormonally regulated. J Biol Chem 259:6437–6446
Lovell S, Karr T, Harrington WF (1988) Suppression of contractile force in muscle fibers by antibody to myosin subfragment 2. Proc Natl Acad Sci USA 85:1849–1853
Mahdavi V, Chambers AP, Nadal-Ginard B (1984) Cardiac α- and β-myosin heavy chain genes are organized in tandem. Proc Natl Acad Sci USA 81:2626–2630
Madhavi V, Strehler EE, Periasamy M, Wieczorek DF, Izumo S, Nadal-Ginard B (1986) Sarcomeric myosin heavy chain gene family: organization and pattern of expression. Med Sci Sports Exercise 18:299–308
Mar JH, Antin P, Cooper TA, Ordahl CP (1988) Analysis of the upstream regions governing expression of the ardiac troponin T gene in embryonic cardiac and skeletam muscle cells. J Cell Biol 107:573–585
Masaki T, Konoshita T (1974) Synthesis of cardiac myosin by a polyribosome fraction from chick embryonic skeletal muscle. J Biochem 75:1193–1195
Masaki T, Yoshizaki C (1974) Differentiation of myosin in chick embryos. J Biochem 76:123–131
Matsuda R, Bandman E, Strohman RC (1982) Two myosin isoenzymes of chicken anterior latismus dorsi muscle contain different myosin heavy chains encoded by separate mRNAs. Differentiation 23:36–42
McLachlan AD, Karn J (1983) Periodic features in the amino acid sequence of nematode myosin rod. J Mol Biol 164:605–626
McNally EM, Gianola KM, Leinwand LA (1989a) Complete nucleotide sequence of full length cDNA for rat α cardiac myosin heavy chain. Nucleic Acids Res 17:7527–7528
McNally EM, Kraft R, Bravo-Zehnder M, Taylor DA, Leinwand LA (1989b) Full-length rat alpha and beta cardiac myosin heavy chain sequences. J Mol Biol 210:665–671
Molina MI, Kropp KE, Gulick J, Robbins J (1987) The sequence of an embryonic myosin heavy chain gene and isolation of its corresponding cDNA. J Biol Chem 262:6478–6488
Price HM, Howes EL, Blumberg JM (1964) Ultrastructural alterations in skeletal muscle fibers injured by cold. 1. The acute degenerative changes. Lab Invest 133:1264–1278
Reiser PJ, Kasper CE, Greaser ML, Moss RL (1988) Functional significance of myosin transitions in single fibers of developing soleus muscle. Am J Physiol 254:C605-C613
Saez L, Leinwand LA (1986) Characterization of diverse forms of myosin heavy chain expressed in adult human skeletal muscle. Nucleic Acids Res 14:2951–2969
Saez LJ, Gianola KM, McNally EM, Feghali R, Eddy R, Shows TB, Leinwand LA (1987) Human cardiac myosin heavy chain genes and their linkage in the genome. Nucleic Acids Res 15:5443–5459
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Springer Harbor NY, p 7.46
Sanders E, deGroot IJM, Geerts WJC, deJong F, van Horssen AA, Los JA, Moorman AFM (1986) The local expression of adult chicken heart myosins during development. II. Ventricular conducting tissue. Anal Embryol 174:187–193
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–6567
Sartone S, Pierobon-Bormioli S, Schiaffino S (1978) Immuno-histochemical evidence for myosin polymorphism in the chicken heart. Nature 274: 82–83
Short JM, Sorge JA, Huse WD (1988) γ ZAP: a bacteriophage γ expression vector with in vivo excision properties. Nucleic Acids Res 16:7583–7600
Sinha AM, Umeda PK, Kavinsky CJ, Rajamanickam C, Hsu H-J, Kakovcic S, Rabinowitz M (1982) Molecular cloning of mRNA sequences for cardiac α- and β-form myosin heavy chains: expression in ventricles of normal, hypothyroid, and thyrotoxic rabbits. Proc Natl Acad Sci USA 79:5847–5851
Stedman HH, Eller M, Jullian EH, Fertels SH, Sarkar S, Sylvester JE, Kelly AM, Rubinstein NA (1990) The human embryonic myosin heavy chain. Complete primary structure reveals evolutionary relationships with other developmental isoforms. J Biol Chem 265:3568–3576
Stewart AFR, Kennedy JM, Bandman E, Zak R (1989) A myosin isoform represented in hypertrophied ALD muscle of the chicken reappears during regeneration following cold injury. Dev Biol 135:367–375
Strehler EF, Strehler-Page M-A, Perriard J-C, Periasamy M, Nadal-Ginard B (1986) Complete nucleotide and encoded amino acid sequence of a mammalian myosin heavy chain gene. Evidence against intron-dependent evolution of the rod J Mol Biol 190:291–317
Sweeney LJ, Clark WA Jr, Umeda PK, Zak R, Manasek FJ (1984) Immunofluorescence analysis of the primordial myosin detectable in embryonic striated muscle. Proc Natl Acad Sci USA 81:797–800
Sweeney LJ, Kennedy JM, Zak R, Kokjohn K, Kelley SW (1989) Evidence for expression of a commun myosin heavy chain phenotype ink future fast and slow skeletal muscle during initial stages of avian myogenesis. Dev Biol 133:361–374
Swofford DL (1990) PAUP: phylogenetic analysis using parsimony, version 3.0 Illinois Natural History Survey, Champaign IL
Swofford DL, Olsen JG (1990) Phyloigeny reconstruction. In: Hillis DM, Moritz C (eds) Molecular systematics. Sinauer Assocaites, Sundersland MA, pp 411–501
Tanigawa G, Jarcho JA, Kass S, Soolomon SD, Vosberg H-P, Seidman JG, Seidman CE (1990) A molecular basis for familial hyeprtrophic cardiomyopathy: an α/β cardiac myosin heavy chain hybrid gene. Cell 62:991–998
Ueno H, Harrington WF (1987) Cross-linking within thick filaments of muscle and its effects on contractile force. Biochemistry 26:36589–3596
Virarelli E, Brown WE, Whalen RG, Cossu G (1988) The expresseion of slow myosin during mammalian somitogenesis and limb bud diffierentiation. J Cell Biol 107:2191–2197
Watanabe B (1989) Complete amino-acid sequence of subfragment-2 in adult chicken skeletal muscle myosin. Biol Chem Hoppe-Seyler 370:1027–1034
Yano Toyoshima Y, Kron SJ, McNally EM, Niebling KR, Toyoshima C, Spudich JA (1987) Myosin subfragment-1 is sufficient to more actin filaments in vitro. Nature 328:536–539
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Department of Pharmacological and Physiological Sciences, The University of Chicago, Chicago, IL60637, USA
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Stewart, A.F.R., Camoretti-Mercado, B., Perlman, D. et al. Structural and phylogenetic analysis of the chicken ventricular myosin heavy chain rod. J Mol Evol 33, 357–366 (1991). https://doi.org/10.1007/BF02102866
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DOI: https://doi.org/10.1007/BF02102866