Skip to main content

Regulation of Neural Stem Cell Death

  • Chapter
Neural Development and Stem Cells

Part of the book series: Contemporary Neuroscience ((CNEURO))

Abstract

Nervous system development is a complex process that begins with a small number of cells and ends with a highly organized and specialized organ. Neural stem cells play a critical role in this process. These cells have the capacity to self-renew, proliferate, and give rise to lineage-restricted neuronal and/or glial progenitor cells and postmitotic specialized daughter cells. The number of neural stem cells contributing to neural development depends on the balance between proliferation, self-renewal, differentiation, and cell death. Studies of apoptosis-associated molecules have indicated significant cell death in neural precursor cells, defined as neural stem cells and lineage restricted progenitors, and immature neurons prior to the generation of synaptic contacts. These studies complement the extensive body of work dedicated to cell death regulation in mature neurons, where competition for limited amounts of target-derived neurotrophic factors plays a direct role in activating cell death pathways during neuronal histogenesis and cell injury. The striking neurodevelopmental abnormalities observed in mice with targeted disruptions in genes regulating cell death emphasizes the importance of programmed cell death during development. Studies of these animals further reveal that cell death regulation is remarkably specific to cell type and stage of neural differentiation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 149.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Burek, M. J. and Oppenheim, R. W. (1996) Programmed cell death in the developing nervous system. Brain Pathol. 6, 427–446.

    PubMed  CAS  Google Scholar 

  2. Sulston, J. E. and Horvitz, H. R. (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110–156.

    Article  PubMed  CAS  Google Scholar 

  3. Ernst, M. (1926) Über untergang von Zellen während der normalen Entwicklung bei Wirbeltieren. Z. Anat. Entwickl. Gesch. 79, 228–262.

    Article  Google Scholar 

  4. Glücksmann, A. (1951) Cell deaths in normal vertebrate ontogeny. Biol. Rev. 26, 59–86.

    Article  Google Scholar 

  5. Clarke, P. G. (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.) 181, 195–213.

    Article  CAS  Google Scholar 

  6. Kerr, J. F., Wyllie, A. H., and Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239–257.

    PubMed  CAS  Google Scholar 

  7. Hacker, G. (2000) The morphology of apoptosis. Cell Tissue Res. 301, 5–17.

    Article  PubMed  CAS  Google Scholar 

  8. Roth, K. A. (2002) In situ detection of apoptotic neurons. In Neuromethods, Vol. 37: Apoptosis Techniques and Protocols (LeBlanc, A. C., ed.), Humana Press, Totowa, NJ, pp. 205–224.

    Google Scholar 

  9. Ellis, H. M. and Horvitz, H. R. (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817–829.

    Article  PubMed  CAS  Google Scholar 

  10. Yuan, J., Shaham, S., Ledoux, S., Ellis, H. M., and Horvitz, H. R. (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75, 641–652.

    Article  PubMed  CAS  Google Scholar 

  11. Cerretti, D. P., Kozlosky, C. J., Mosley, B., et al. (1992) Molecular cloning of the interleukin-1 beta converting enzyme. Science 256, 97–100.

    Article  PubMed  CAS  Google Scholar 

  12. Thornberry, N. A., Bull, H. G., Calaycay, J. R., et al. (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356, 768–774.

    Article  PubMed  CAS  Google Scholar 

  13. Degterev, A., Boyce, M., and Yuan, J. (2003) A decade of caspases. Oncogene 22, 8543–8567.

    Article  PubMed  CAS  Google Scholar 

  14. Boatright, K. M., Renatus, M., Scott, F. L., et al. (2003) A unified model for apical caspase activation. Mol. Cell 11, 529–541.

    Article  PubMed  CAS  Google Scholar 

  15. Tsujimoto, Y., Finger, L. R., Yunis, J., Nowell, P. C., and Croce, C. M. (1984) Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226, 1097–1099.

    Article  PubMed  CAS  Google Scholar 

  16. Bakhshi, A., Jensen, J. P., Goldman, P., et al. (1985) Cloning the chromosomal breakpoint of t(14; 18) human lymphomas: clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell 41, 899–906.

    Article  PubMed  CAS  Google Scholar 

  17. Cory, S., Huang, D. C., and Adams, J. M. (2003) The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22, 8590–8607.

    Article  PubMed  CAS  Google Scholar 

  18. Akhtar, R. S., Ness, J. M., and Roth, K. A. (2004) Bcl-2 family regulation of neuronal development and neurodegeneration. Biochim. Biophys. Acta 1644, 189–203.

    Article  PubMed  CAS  Google Scholar 

  19. Oltvai, Z. N., Milliman, C. L., and Korsmeyer, S. J. (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609–619.

    Article  PubMed  CAS  Google Scholar 

  20. Armstrong, R. C., Aja, T. J., Hoang, K. D., et al. (1997) Activation of the CED3/ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis. J. Neurosci. 17, 553–562.

    PubMed  CAS  Google Scholar 

  21. Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147–157.

    Article  PubMed  CAS  Google Scholar 

  22. Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90, 405–413.

    Article  PubMed  CAS  Google Scholar 

  23. Li, P., Nijhawan, D., Budihardjo, I., et al. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479–489.

    Article  PubMed  CAS  Google Scholar 

  24. Duan, H., Orth, K., Chinnaiyan, A. M., et al. (1996) ICE-LAP6, a novel member of the ICE/Ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B. J. Biol. Chem. 271, 16720–16724.

    Article  PubMed  CAS  Google Scholar 

  25. Srinivasula, S. M., Fernandes-Alnemri, T., Zangrilli, J., et al. (1996) The Ced-3/interleukin 1beta converting enzyme-like homolog Mch6 and the lamin-cleaving enzyme Mch2alpha are substrates for the apoptotic mediator CPP32. J. Biol. Chem. 271, 27099–27106.

    Article  PubMed  CAS  Google Scholar 

  26. Acehan, D., Jiang, X., Morgan, D. G., Heuser, J. E., Wang, X., and Akey, C. W. (2002) Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol. Cell 9, 423–432.

    Article  PubMed  CAS  Google Scholar 

  27. Scorrano, L. and Korsmeyer, S. J. (2003) Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys. Res. Commun. 304, 437–444.

    Article  PubMed  CAS  Google Scholar 

  28. Mattson, M. P. and Kroemer, G. (2003) Mitochondria in cell death: novel targets for neuroprotection and cardioprotection. Trends Mol. Med. 9, 196–205.

    Article  PubMed  CAS  Google Scholar 

  29. Yang, E., Zha, J., Jockel, J., Boise, L. H., Thompson, C. B., and Korsmeyer, S. J. (1995) Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80, 285–291.

    Article  PubMed  CAS  Google Scholar 

  30. Zha, J., Harada, H., Osipov, K., Jockel, J., Waksman, G., and Korsmeyer, S. J. (1997) BH3 domain of BAD is required for heterodimerization with BCL-XL and pro-apoptotic activity. J. Biol. Chem. 272, 24101–24104.

    Article  PubMed  CAS  Google Scholar 

  31. Kelekar, A., Chang, B. S., Harlan, J. E., Fesik, S. W., and Thompson, C. B. (1997) Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-XL. Mol. Cell Biol. 17, 7040–7046.

    PubMed  CAS  Google Scholar 

  32. Oda, E., Ohki, R., Murasawa, H., et al. (2000) Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288, 1053–1058.

    Article  PubMed  CAS  Google Scholar 

  33. Boise, L. H., Gonzalez-Garcia, M., Postema, C. E., et al. (1993) bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74, 597–608.

    Article  PubMed  CAS  Google Scholar 

  34. Gonzalez-Garcia, M., Perez-Ballestero, R., Ding, L., et al. (1994) bcl-XL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development 120, 3033–3042.

    PubMed  CAS  Google Scholar 

  35. Gonzalez-Garcia, M., Garcia, I., Ding, L., et al. (1995) bcl-x is expressed in embryonic and postnatal neural tissues and functions to prevent neuronal cell death. Proc. Natl. Acad. Sci. USA 92, 4304–4308.

    Article  PubMed  CAS  Google Scholar 

  36. Yin, X. M., Oltvai, Z. N., and Korsmeyer, S. J. (1994) BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369, 321–323.

    Article  PubMed  CAS  Google Scholar 

  37. Sato, T., Hanada, M., Bodrug, S., et al. (1994) Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system. Proc. Natl. Acad. Sci. USA 91, 9238–9242.

    Article  PubMed  CAS  Google Scholar 

  38. Sedlak, T. W., Oltvai, Z. N., Yang, E., et al. (1995) Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc. Natl. Acad. Sci. USA 92, 7834–7838.

    Article  PubMed  CAS  Google Scholar 

  39. Chittenden, T., Flemington, C., Houghton, A. B., et al. (1995) A conserved domain in Bak, distinct from BH1 and BH2, mediates cell death and protein binding functions. EMBO J. 14, 5589–5596.

    PubMed  CAS  Google Scholar 

  40. Wang, S. and El Deiry, W. S. (2003) TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 22, 8628–8633.

    Article  PubMed  CAS  Google Scholar 

  41. Barnhart, B. C., Lee, J. C., Alappat, E. C., and Peter, M. E. (2003) The death effector domain protein family. Oncogene 22, 8634–8644.

    Article  PubMed  CAS  Google Scholar 

  42. Scaffidi, C., Medema, J. P., Krammer, P. H., and Peter, M. E. (1997) FLICE is predominantly expressed as two functionally active isoforms, caspase-8/a and caspase-8/b. J. Biol. Chem. 272, 26953–26958.

    Article  PubMed  CAS  Google Scholar 

  43. Muzio, M., Stockwell, B. R., Stennicke, H. R., Salvesen, G. S., and Dixit, V. M. (1998) An induced proximity model for caspase-8 activation. J. Biol. Chem. 273, 2926–2930.

    Article  PubMed  CAS  Google Scholar 

  44. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481–490.

    Article  PubMed  CAS  Google Scholar 

  45. Kim, J. and Klionsky, D. J. (2000) Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu. Rev. Biochem. 69, 303–342.

    Article  PubMed  CAS  Google Scholar 

  46. Syntichaki, P. and Tavernarakis, N. (2003) The biochemistry of neuronal necrosis: rogue biology? Nat. Rev. Neurosci. 4, 672–684.

    Article  PubMed  CAS  Google Scholar 

  47. Hall, D. H., Gu, G., Garcia-Anoveros, J., Gong, L., Chalfie, M., and Driscoll, M. (1997) Neuropathology of degenerative cell death in Caenorhabditis elegans. J. Neurosci. 17, 1033–1045.

    PubMed  CAS  Google Scholar 

  48. Roth, K. A., Kuan, C., Haydar, T. F., et al. (2000) Epistatic and independent functions of caspase-3 and Bcl-X(L) in developmental programmed cell death. Proc. Natl. Acad. Sci. USA 97, 466–471.

    Article  PubMed  CAS  Google Scholar 

  49. Pompeiano, M., Blaschke, A. J., Flavell, R. A., Srinivasan, A., and Chun, J. (2000) Decreased apoptosis in proliferative and postmitotic regions of the caspase 3-deficient embryonic central nervous system. J. Comp Neurol. 423, 1–12.

    Article  PubMed  CAS  Google Scholar 

  50. Kuida, K., Zheng, T. S., Na, S., et al. (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384, 368–372.

    Article  PubMed  CAS  Google Scholar 

  51. Hakem, R., Hakem, A., Duncan, G. S., et al. (1998) Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94, 339–352.

    Article  PubMed  CAS  Google Scholar 

  52. Cecconi, F., Alvarez-Bolado, G., Meyer, B. I., Roth, K. A., and Gruss, P. (1998) Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94, 727–737.

    Article  PubMed  CAS  Google Scholar 

  53. Yoshida, H., Kong, Y. Y., Yoshida, R., et al. (1998) Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94, 739–750.

    Article  PubMed  CAS  Google Scholar 

  54. Leonard, J. R., Klocke, B. J., D’Sa, C., Flavell, R. A., and Roth, K. A. (2002) Strain-dependent neurodevelopmental abnormalities in caspase-3-deficient mice. J. Neuro-pathol. Exp. Neurol. 61, 673–677.

    Google Scholar 

  55. Kuida, K., Haydar, T. F., Kuan, C. Y., et al. (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94, 325–337.

    Article  PubMed  CAS  Google Scholar 

  56. Kuan, C. Y., Roth, K. A., Flavell, R. A., and Rakic, P. (2000) Mechanisms of programmed cell death in the developing brain. Trends Neurosci. 23, 291–297.

    Article  PubMed  CAS  Google Scholar 

  57. Roth, K. A. and D’Sa, C. (2001) Apoptosis and brain development. Ment. Retard. Dev. Disabil. Res. Rev. 7, 261–266.

    Article  PubMed  CAS  Google Scholar 

  58. Chinnaiyan, A. M., O’Rourke, K., Yu, G. L., et al. (1996) Signal transduction by DR3, a death domain-containing receptor related to TNFR-1 and CD95. Science 274, 990–992.

    Article  PubMed  CAS  Google Scholar 

  59. Sakamaki, K., Tsukumo, S., and Yonehara, S. (1998) Molecular cloning and characterization of mouse caspase-8. Eur. J. Biochem. 253, 399–405.

    Article  PubMed  CAS  Google Scholar 

  60. Varfolomeev, E. E., Schuchmann, M., Luria, V., et al. (1998) Targeted disruption of the mouse caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9, 267–276.

    Article  PubMed  CAS  Google Scholar 

  61. Sanchez, I., Xu, C. J., Juo, P., Kakizaka, A., Blenis, J., and Yuan, J. (1999) Caspase-8 is required for cell death induced by expanded polyglutamine repeats. Neuron 22, 623–633.

    Article  PubMed  CAS  Google Scholar 

  62. Sakamaki, K., Inoue, T., Asano, M., et al. (2002) Ex vivo whole-embryo culture of caspase-8-deficient embryos normalize their aberrant phenotypes in the developing neural tube and heart. Cell Death. Differ. 9, 1196–1206.

    Article  PubMed  CAS  Google Scholar 

  63. Watanabe-Fukunaga, R., Brannan, C. I., Itoh, N., et al. (1992) The cDNA structure, expression, and chromosomal assignment of the mouse Fas antigen. J. Immunol. 148, 1274–1279.

    PubMed  CAS  Google Scholar 

  64. Takahashi, T., Tanaka, M., Brannan, C. I., et al. (1994) Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76, 969–976.

    Article  PubMed  CAS  Google Scholar 

  65. Adachi, M., Suematsu, S., Kondo, T., et al. (1995) Targeted mutation in the Fas gene causes hyperplasia in peripheral lymphoid organs and liver. Nat. Genet. 11, 294–300.

    Article  PubMed  CAS  Google Scholar 

  66. Veis, D. J., Sorenson, C. M., Shutter, J. R., and Korsmeyer, S. J. (1993) Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75, 229–240.

    Article  PubMed  CAS  Google Scholar 

  67. Nakayama, K., Nakayama, K., Negishi, I., Kuida, K., Sawa, H., and Loh, D. Y. (1994) Targeted disruption of Bcl-2 alpha beta in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc. Natl. Acad. Sci. USA 91, 3700–3704.

    Article  PubMed  CAS  Google Scholar 

  68. Motoyama, N., Wang, F., Roth, K. A., et al. (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267, 1506–1510.

    Article  PubMed  CAS  Google Scholar 

  69. Zaidi, A. U., D’Sa-Eipper, C., Brenner, J., et al. (2001) Bcl-X(L)-caspase-9 interactions in the developing nervous system: evidence for multiple death pathways. J. Neurosci. 21, 169–175.

    PubMed  CAS  Google Scholar 

  70. Krajewski, S., Krajewska, M., Shabaik, A., Miyashita, T., Wang, H. G., and Reed, J. C. (1994) Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145, 1323–1336.

    PubMed  CAS  Google Scholar 

  71. Farrow, S. N., White, J. H., Martinou, I., et al. (1995) Cloning of a bcl-2 homologue by interaction with adenovirus E1B 19K. Nature 374, 731–733.

    Article  PubMed  CAS  Google Scholar 

  72. Chittenden, T., Harrington, E. A., O’Connor, R., et al. (1995) Induction of apoptosis by the Bcl-2 homologue Bak. Nature 374, 733–736.

    Article  PubMed  CAS  Google Scholar 

  73. Kiefer, M. C., Brauer, M. J., Powers, V. C., et al. (1995) Modulation of apoptosis by the widely distributed Bcl-2 homologue Bak. Nature 374, 736–739.

    Article  PubMed  CAS  Google Scholar 

  74. Krajewska, M., Mai, J. K., Zapata, J. M., et al. (2002) Dynamics of expression of apoptosis-regulatory proteins Bid, Bcl-2, Bcl-X, Bax and Bak during development of murine nervous system. Cell Death. Differ. 9, 145–157.

    Article  PubMed  CAS  Google Scholar 

  75. Lindsten, T., Ross, A. J., King, A., et al. (2000) The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell 6, 1389–1399.

    Article  PubMed  CAS  Google Scholar 

  76. Lindsten, T., Golden, J. A., Zong, W. X., Minarcik, J., Harris, M. H., and Thompson, C. B. (2003) The proapoptotic activities of Bax and Bak limit the size of the neural stem cell pool. J. Neurosci. 23, 11112–11119.

    PubMed  CAS  Google Scholar 

  77. Roth, K. A., Motoyama, N., and Loh, D. Y. (1996) Apoptosis of bcl-x-deficient telencephalic cells in vitro. J. Neurosci. 16, 1753–1758.

    PubMed  CAS  Google Scholar 

  78. Srinivasan, A., Roth, K. A., Sayers, R. O., et al. (1998) In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death. Differ. 5, 1004–1016.

    Article  PubMed  CAS  Google Scholar 

  79. Yoshida, H., Okada, Y., Kinoshita, N., et al. (2002) Differential requirement for Apaf1 and Bcl-X(L) in the regulation of programmed cell death during development. Cell Death. Differ. 9, 1273–1276.

    Article  PubMed  CAS  Google Scholar 

  80. Cecconi, F., Roth, K. A., Dolgov, O., et al. (2004) Apaf1-dependent programmed cell death is required for inner ear morphogenesis and growth. Development 131, 2125–2135.

    Article  PubMed  CAS  Google Scholar 

  81. Shindler, K. S., Latham, C. B., and Roth, K. A. (1997) Bax deficiency prevents the increased cell death of immature neurons in bcl-x-deficient mice. J. Neurosci. 17, 3112–3119.

    PubMed  CAS  Google Scholar 

  82. D’Sa-Eipper, C. and Roth, K. A. (2000) Caspase regulation of neuronal progenitor cell apoptosis. Dev. Neurosci. 22, 116–124.

    Article  PubMed  CAS  Google Scholar 

  83. D’Sa-Eipper, C., Leonard, J. R., Putcha, G., et al. (2001) DNA damage-induced neural precursor cell apoptosis requires p53 and caspase 9 but neither Bax nor caspase 3. Development 128, 137–146.

    PubMed  CAS  Google Scholar 

  84. D’Sa, C., Klocke, B. J., Cecconi, F., et al. (2003) Caspase regulation of genotoxin-induced neural precursor cell death. J. Neurosci. Res. 74, 435–445.

    Article  PubMed  CAS  Google Scholar 

  85. Zheng, T. S., Hunot, S., Kuida, K., et al. (2000) Deficiency in caspase-9 or caspase-3 induces compensatory caspase activation. Nat. Med. 6, 1241–1247.

    Article  PubMed  CAS  Google Scholar 

  86. Honarpour, N., Du, C., Richardson, J. A., Hammer, R. E., Wang, X., and Herz, J. (2000) Adult Apaf-1-deficient mice exhibit male infertility. Dev. Biol. 218, 248–258.

    Article  PubMed  CAS  Google Scholar 

  87. Vousden, K. H. and Lu, X. (2002) Live or let die: the cell’s response to p53. Nat. Rev. Cancer 2, 594–604.

    Article  PubMed  CAS  Google Scholar 

  88. Fei, P. and El Deiry, W. S. (2003) P53 and radiation responses. Oncogene 22, 5774–5783.

    Article  PubMed  CAS  Google Scholar 

  89. Fridman, J. S. and Lowe, S. W. (2003) Control of apoptosis by p53. Oncogene 22, 9030–9040.

    Article  PubMed  CAS  Google Scholar 

  90. Schmid, P., Lorenz, A., Hameister, H., and Montenarh, M. (1991) Expression of p53 during mouse embryogenesis. Development 113, 857–865.

    PubMed  CAS  Google Scholar 

  91. Sah, V. P., Attardi, L. D., Mulligan, G. J., Williams, B. O., Bronson, R. T., and Jacks, T. (1995) A subset of p5 3-deficient embryos exhibit exencephaly. Nat. Genet. 10, 175–180.

    Article  PubMed  CAS  Google Scholar 

  92. Armstrong, J. F., Kaufman, M. H., Harrison, D. J., and Clarke, A. R. (1995) High-frequency developmental abnormalities in p53-deficient mice. Curr. Biol. 5, 931–936.

    Article  PubMed  CAS  Google Scholar 

  93. Komarova, E. A., Chernov, M. V., Franks, R., et al. (1997) Transgenic mice with p53-responsive lacZ: p53 activity varies dramatically during normal development and determines radiation and drug sensitivity in vivo. EMBO J. 16, 1391–1400.

    Article  PubMed  CAS  Google Scholar 

  94. Shindler, K. S., Yunker, A. M., Cahn, R., Zha, J., Korsmeyer, S. J., and Roth, K. A. (1998) Trophic support promotes survival of bcl-x-deficient telencephalic cells in vitro. Cell Death. Differ. 5, 901–910.

    Article  PubMed  CAS  Google Scholar 

  95. Zaidi, A. U., McDonough, J. S., Klocke, B. J., et al. (2001) Chloroquine-induced neuronal cell death is p53 and Bcl-2 family-dependent but caspase-independent. J. Neuropathol. Exp. Neurol. 60, 937–945.

    PubMed  CAS  Google Scholar 

  96. Klocke, B. J., Latham, C. B., D’Sa, C., and Roth, K. A. (2002) p53 deficiency fails to prevent increased programmed cell death in the Bcl-X(L)-deficient nervous system. Cell Death. Differ. 9, 1063–1068.

    Article  PubMed  CAS  Google Scholar 

  97. Lee, E. Y., Chang, C. Y., Hu, N., et al. (1992) Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359, 288–294.

    Article  PubMed  CAS  Google Scholar 

  98. Jacks, T., Fazeli, A., Schmitt, E. M., Bronson, R. T., Goodell, M. A., and Weinberg, R. A. (1992) Effects of an Rb mutation in the mouse. Nature 359, 295–300.

    Article  PubMed  CAS  Google Scholar 

  99. Clarke, A. R., Maandag, E. R., van Roon, M., et al. (1992) Requirement for a functional Rb-1 gene in murine development. Nature 359, 328–330.

    Article  PubMed  CAS  Google Scholar 

  100. Slack, R. S., El Bizri, H., Wong, J., Belliveau, D. J., and Miller, F. D. (1998) A critical temporal requirement for the retinoblastoma protein family during neuronal determination. J. Cell Biol. 140, 1497–1509.

    Article  PubMed  CAS  Google Scholar 

  101. Macleod, K. F., Hu, Y., and Jacks, T. (1996) Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J. 15, 6178–6188.

    PubMed  CAS  Google Scholar 

  102. Simpson, M. T., MacLaurin, J. G., Xu, D., et al. (2001) Caspase 3 deficiency rescues peripheral nervous system defect in retinoblastoma nullizygous mice. J. Neurosci. 21, 7089–7098.

    PubMed  CAS  Google Scholar 

  103. Frank, K. M., Sekiguchi, J. M., Seidl, K. J., et al. (1998) Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature 396, 173–177.

    Article  PubMed  CAS  Google Scholar 

  104. Barnes, D. E., Stamp, G., Rosewell, I., Denzel, A., and Lindahl, T. (1998) Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice. Curr. Biol. 8, 1395–1398.

    Article  PubMed  CAS  Google Scholar 

  105. Gao, Y., Sun, Y., Frank, K. M., et al. (1998) A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 95, 891–902.

    Article  PubMed  CAS  Google Scholar 

  106. Gao, Y., Ferguson, D. O., Xie, W., et al. (2000) Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature 404, 897–900.

    Article  PubMed  CAS  Google Scholar 

  107. Frank, K. M., Sharpless, N. E., Gao, Y., et al. (2000) DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell 5, 993–1002.

    Article  PubMed  CAS  Google Scholar 

  108. Fadok, V. A., Bratton, D. L., Rose, D. M., Pearson, A., Ezekewitz, R. A., and Henson, P. M. (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405, 85–90.

    Article  PubMed  CAS  Google Scholar 

  109. Savill, J. and Fadok, V. (2000) Corpse clearance defines the meaning of cell death. Nature 407, 784–788.

    Article  PubMed  CAS  Google Scholar 

  110. Li, M. O., Sarkisian, M. R., Mehal, W. Z., Rakic, P., and Flavell, R. A. (2003) Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 302, 1560–1563.

    Article  PubMed  CAS  Google Scholar 

  111. van den Eijnde, S. M., Lips, J., Boshart, L., et al. (1999) Spatiotemporal distribution of dying neurons during early mouse development. Eur. J. Neurosci. 11, 712–724.

    Article  PubMed  Google Scholar 

  112. Thomaidou, D., Mione, M. C., Cavanagh, J. F., and Parnavelas, J. G. (1997) Apoptosis and its relation to the cell cycle in the developing cerebral cortex. J. Neurosci. 17, 1075–1085.

    PubMed  CAS  Google Scholar 

  113. Chun, J. (2000) Cell death, DNA breaks and possible rearrangements: an alternative view. Trends Neurosci. 23, 407–409.

    Article  PubMed  CAS  Google Scholar 

  114. Blaschke, A. J., Staley, K., and Chun, J. (1996) Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development 122, 1165–1174.

    PubMed  CAS  Google Scholar 

  115. Blaschke, A. J., Weiner, J. A., and Chun, J. (1998) Programmed cell death is a universal feature of embryonic and postnatal neuroproliferative regions throughout the central nervous system. J. Comp Neurol. 396, 39–50.

    Article  PubMed  CAS  Google Scholar 

  116. Schatz, D. G. (1997) V(D)J recombination moves in vitro. Semin. Immunol. 9, 149–159.

    Article  PubMed  CAS  Google Scholar 

  117. Chun, J. and Schatz, D. G. (1999) Rearranging views on neurogenesis: neuronal death in the absence of DNA end-joining proteins. Neuron 22, 7–10.

    Article  PubMed  CAS  Google Scholar 

  118. Gilmore, E. C., Nowakowski, R. S., Caviness, V. S., Jr., and Herrup, K. (2000) Cell birth, cell death, cell diversity and DNA breaks: how do they all fit together? Trends Neurosci. 23, 100–105.

    Article  PubMed  CAS  Google Scholar 

  119. Alvarez-Buylla, A. and Garcia-Verdugo, J. M. (2002) Neurogenesis in adult sub-ventricular zone. J. Neurosci. 22, 629–634.

    PubMed  CAS  Google Scholar 

  120. Kempermann, G. (2002) Why new neurons? Possible functions for adult hippocampal neurogenesis. J. Neurosci. 22, 635–638.

    PubMed  CAS  Google Scholar 

  121. Taupin, P. and Gage, F. H. (2002) Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69, 745–749.

    Article  PubMed  CAS  Google Scholar 

  122. Gould, E., Beylin, A., Tanapat, P., Reeves, A., and Shors, T. J. (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260–265.

    Article  PubMed  CAS  Google Scholar 

  123. Rakic, P. (2002) Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat. Rev. Neurosci. 3, 65–71.

    Article  PubMed  CAS  Google Scholar 

  124. Cameron, H. A., Woolley, C. S., McEwen, B. S., and Gould, E. (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56, 337–344.

    Article  PubMed  CAS  Google Scholar 

  125. Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., et al. (1998) Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313–1317.

    Article  PubMed  CAS  Google Scholar 

  126. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997) Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc. Natl. Acad. Sci. USA 94, 10409–10414.

    Article  PubMed  CAS  Google Scholar 

  127. Kempermann, G., Brandon, E. P., and Gage, F. H. (1998) Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr. Biol. 8, 939–942.

    Article  PubMed  CAS  Google Scholar 

  128. Gould, E., Vail, N., Wagers, M., and Gross, C. G. (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc. Natl. Acad. Sci. USA 98, 10910–10917.

    Article  PubMed  CAS  Google Scholar 

  129. Jang, M. H., Shin, M. C., Jung, S. B., et al. (2002) Alcohol and nicotine reduce cell proliferation and enhance apoptosis in dentate gyrus. NeuroReport 13, 1509–1513.

    Article  PubMed  CAS  Google Scholar 

  130. Morshead, C. M. and van der Kooy, D. (1992) Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J. Neurosci. 12, 249–256.

    PubMed  CAS  Google Scholar 

  131. Morshead, C. M., Craig, C. G., and van der Kooy, D. (1998) In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 125, 2251–2261.

    PubMed  CAS  Google Scholar 

  132. Brunjes, P. C. and Armstrong, A. M. (1996) Apoptosis in the rostral migratory stream of the developing rat. Brain Res. Dev. Brain Res. 92, 219–222.

    Article  PubMed  CAS  Google Scholar 

  133. Fiske, B. K. and Brunjes, P. C. (2001) Cell death in the developing and sensory-deprived rat olfactory bulb. J. Comp Neurol. 431, 311–319.

    Article  PubMed  CAS  Google Scholar 

  134. Biebl, M., Cooper, C. M., Winkler, J., and Kuhn, H. G. (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett. 291, 17–20.

    Article  PubMed  CAS  Google Scholar 

  135. Moreno-Lopez, B., Romero-Grimaldi, C., Noval, J. A., Murillo-Carretero, M., Matarredona, E. R., and Estrada, C. (2004) Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J. Neurosci. 24, 85–95.

    Article  PubMed  CAS  Google Scholar 

  136. Brunjes, P. C. (1994) Unilateral naris closure and olfactory system development. Brain Res. Brain Res. Rev. 19, 146–160.

    Article  PubMed  CAS  Google Scholar 

  137. Corotto, F. S., Henegar, J. R., and Maruniak, J. A. (1994) Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience 61, 739–744.

    Article  PubMed  CAS  Google Scholar 

  138. Najbauer, J. and Leon, M. (1995) Olfactory experience modulated apoptosis in the developing olfactory bulb. Brain Res. 674, 245–251.

    Article  PubMed  CAS  Google Scholar 

  139. Mandairon, N., Jourdan, F., and Didier, A. (2003) Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 119, 507–516.

    Article  PubMed  CAS  Google Scholar 

  140. Brunet, L. J., Gold, G. H., and Ngai, J. (1996) General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17, 681–693.

    Article  PubMed  CAS  Google Scholar 

  141. Zhao, H. and Reed, R. R. (2001) X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104, 651–660.

    Article  PubMed  CAS  Google Scholar 

  142. Petreanu, L. and Alvarez-Buylla, A. (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci. 22, 6106–6113.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Humana Press Inc., Totowa, NJ

About this chapter

Cite this chapter

Akhtar, R.S., Roth, K.A. (2006). Regulation of Neural Stem Cell Death. In: Rao, M.S. (eds) Neural Development and Stem Cells. Contemporary Neuroscience. Humana Press. https://doi.org/10.1385/1-59259-914-1:097

Download citation

Publish with us

Policies and ethics