Bax promotes neuronal cell death and is downregulated during the development of the nervous system

Development

Volumn 124, Issue 6, 1997, Pages 1239-1249

  Vekrellis, Konstantinos ^a   McCarthy, Mary Jane ^a   Watson, Andrea ^a   Whitfield, Jonathan ^a   Rubin, Lee L ^a   Ham, Jonathan ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Apoptosis; Bax; Bcl x; Cell death; Nervous system; Neuronal development; Rat

Indexed keywords

PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACULOVIRUS; BRAIN CORTEX; CEREBELLUM; DEVELOPMENTAL GENETICS; DOWN REGULATION; EXPRESSION VECTOR; HEART MUSCLE; MICROINJECTION; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; RAT; SYMPATHETIC NERVE CELL;

AGING; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; BRAIN; CELL DIFFERENTIATION; CELL SURVIVAL; CEREBELLUM; CEREBRAL CORTEX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MOLECULAR SEQUENCE DATA; NERVE GROWTH FACTORS; NEURONS; ORGAN SPECIFICITY; PC12 CELLS; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA; UNIDENTIFIED BACULOVIRUS;

EID: 0031001244     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Allsopp, T. E., Wyatt, S., Paterson, H. F. and Davies, A. M. (1993). The proto-oncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis. Cell 73, 295-307.
2. Alnemri, E. S., Livingston, D. J., Nicholson, D. W., Salvesen, G., Thornberry, N. A., Wong, W. W. and Yuan, J. (1996). Human ICE/CED-3 protease nomenclature. Cell 87, 171.
3. Barde, Y.-A. (1989). Trophic factors and neuronal survival. Neuron 2, 1525-1534.
4. 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.
5. Boise, L. H., González-Garcia, M., Postema, C. E., Ding, L., Lindsten, T., Turka, L. A., Mao, X., Nuñez, G. and Thompson, C. B. (1993). bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74, 597-608.
6. Bump, N. J., Hackett, M., Hugunin, M., Seshagiri, S., Brady, K., Chen, P., Ferenz, C., Franklin, S., Ghayur, T., Li, P., Licari, P., Mankovich, J., Shi, L., Greenberg, A. H., Miller, L. K. and Wong, W. W. (1995). Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269, 1885-1888.
7. Cheng, E. H.-Y., Levine, B., Boise, L. H., Thompson, C. B. and Hardwick, J. M. (1996). Bax-independent inhibition of apoptosis by Bcl-xL. Nature 379, 554-556.
8. Chinnaiyan, A. M., Orth, K., O'Rourke, K., Duan, H., Poirer, G. G. and Dixit, V. M. (1996). Molecular ordering of the cell death pathway. J. Biol. Chem. 271, 4573-4576.
9. Cleary, M. L. and Sklar, J. (1985). Nucleotide sequence of a t(14;18) chromosomal breakpoint in follicular lymphoma and demonstration of a breakpoint-cluster region near a transcriptionally active locus on chromosome 18. Proc. Natl. Acad. Sci. USA 82, 7439-7443.
10. Davies, A. M. (1995). The Bcl-2 family of proteins, and the regulation of neuronal survival. Trends Neurosci. 18, 355-358.
11. Deckwerth, T. L., Elliott, J. L., Knudson, C. M., Johnson, E. M., Snider, W. D. and Korsmeyer, S. J. (1996). Bax is required for neuronal death after trophic factor deprivation and during development. Neuron 17, 401-411.
12. Doherty, P., Mann, D. A. and Walsh, F. S. (1988). Comparison of the effects of NGF, activators of protein kinase C, and a calcium ionophore on the expression of Thy-1 and N-CAM in PC12 cell cultures. J. Cell. Biol. 107, 333-340.
13. Ellis, R. E., Yuan, J. and Horvitz, H. R. (1991). Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7, 663-698.
14. Farrow, S. N., White, J. H. M., Martinou, I., Raven, T., Pun, K.-T., Grinham, C. J., Martinou, J. C. and Brown, R. (1995). Cloning of a bcl-2 homologue by interaction with adenovirus E1B19K. Nature 374, 731-733.
15. Gagliardini, V., Fernandez, P.-A., Lee, R. K. K., Drexler, H. C. A., Rotello, R. J., Fishman, M. C. and Yuan, J. (1994). Prevention of vertebrate neuronal death by the crmA gene. Science 263, 826-828.
16. Garcia, I., Martinou, I., Tsujimoto, Y. and Martinou, J.-C. (1992). Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. Science 258, 302-304.
17. Gonzalez-Garcia, M., Pérez-Ballestero, R., Ding, L., Duan, L., Boise, L. H., Thompson, C. B. and Nuñez, G. (1994). bcl-xL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development 120, 3033-3042.
18. Gonzalez-Garcia, M., Garcia, I., Ding, L., O'Shea, S., Boise, L.H., Thompson, C. B. and Nunez, G. (1995). bcl-x is expressed in embryonic and postnatal tissues and functions to prevent neuronal cell death. Proc. Natl. Acad. Sci. USA 92, 4304-4308.
19. Greene, L. A. and Tischler, A. S. (1976). Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 73, 2424-2428.
20. Greenlund, L. J. S., Korsmeyer, S. J. and Johnson, E. M. (1995). Role of Bcl-2 in the survival and function of developing and mature sympathetic neurons. Neuron 15, 649-661.
21. Ham, J., Babij, C., Whitfield, J., Pfarr, C. M., Lallemand, D., Yaniv, M. and Rubin, L. L. (1995). A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14, 927-939.
22. Harlow, E. and Lane, D. (1988). Antibodies: A Laboratory Manual. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
23. Hatten, M. E. and Heintz, N. (1995). Mechanisms of neural patterning and specification in the developing cerebellum. Annu. Rev. Neurosci. 18, 385-408.
24. Hayes, T. E., Valtz, N. L. M. and McKay, R. D. G. (1991). Downregulation of CDC2 upon terminal differentiation of neurons. New Biol. 3, 259-269.
25. Hockenbery, D. M., Zutter, M., Hickey, W., Nahm, M. and Korsmeyer, S. J. (1991). Bcl-2 protein is topographically restricted in tissues characterised by apoptotic cell death. Proc. Natl. Acad. Sci. USA 88, 6961-6965.
26. Korsmeyer, S. J. (1995). Regulators of cell death. Trends Genet. 11, 101-105.
27. Korsmeyer, S. J., Shutter, J. R., Veis, D. J., Merry, D. E. and Oltvai, Z. N. (1993). Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Cancer Biol. 4, 327-332.
28. 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. Amer. J. Pathol. 145, 1323-1336.
29. Krajewski, S., Mai, J. K., Krajewska, M., Sikorska, M., Mossakowski, M. J. and Reed, J. C. (1995). Upregulation of Bax protein levels in neurons following cerebral ischemia. J. Neurosci. 15, 6364-6376.
30. Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science 237, 1154-1162.
31. Martinou, I., Fernandez, P.-A., Missotten, M., White, E., Allet, B., Sadout, R. and Martinou, J.-C. (1995). Viral proteins E1B19K and p35 protect sympathetic neurons from cell death induced by NGF deprivation. J. Cell. Biol. 128, 201-208.
32. Mason, C.A., Christakos, S. and Catalano, S.M. (1990). Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J. Comp. Neurol. 297, 77-90.
33. Merry, D. E., Veis, D. J., Hickey, W. F. and Korsmeyer, S. J. (1994). Bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development 120, 301-311.
34. Michaelidis, T.M., Sendtner, M., Cooper, J.D., Airaksinen, M.S., Holtmann, B., Meyer, M. and Thoenen, H. (1996). Inactivation of bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development. Neuron 17, 75-89.
35. Middleton, G., Nuñez, G. and Davies, A. M. (1996). Bax promotes neuronal survival and antagonizes the survival effects of neurotrophic factors. Development 122, 695-701.
36. Milligan, C. E., Prevette, D., Yaginuma, H., Homma, S., Cardwell, C., Fritz, L. C., Tomaselli, K. J., Oppenheim, R. W. and Schwartz, L. M. (1995). Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro. Neuron 15, 385-393.
37. Miyashita, T. and Reed, J. C. (1995). Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293-299.
38. Miyashita, T., Krajewski, S., Krajewska, M., Wang, H. G., Lin, H. K., Liebermann, D. A., Hoffman, B. and Reed, J. C. (1994). Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9, 1799-1805.
39. Motoyama, N., Wang, F., Roth, K. A., Sawa, H., Nakayama, K.-I., Nakayama, K., Negishi, I., Senju, S., Zhang, Q., Fuji, S. and Loh, D. Y. (1995). Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267, 1506-1510.
40. Nakayama, K.-I., Nakayama, K., Negishi, I., Kuida, K., Shinkai, Y., Louie, M. C., Fields, L. E., Lucas, P. J., Stewart, V., Alt, F. W. and Loh, D. Y. (1993). Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science 261, 1584-1588.
41. Nuñez, G. and Clarke, M. F. (1994). The Bcl-2 family of proteins: regulators of cell death and survival. Trends Cell. Biol. 4, 399-403.
42. Oltvai, Z. N., Milliman, C. L. and Korsmeyer, S. J. (1993). Bcl-2 heterodimerizes with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609-619.
43. Oppenheim, R. W. (1991). Cell death during development of the nervous system. Annu. Rev. Neorosci. 14, 453-501.
44. Raff, M. C. (1992). Social controls on cell survival and cell death. Nature 356, 397-400.
45. Raff, M. C., Barres, B. A., Burne, J. F., Coles, H. S., Ishizaki, Y. and Jacobson, M. D. (1993). Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262, 695-700.
46. Rubin, L. L., Gatchalian, C. L., Rimon, G. and Brooks, S. F. (1994). The molecular mechanisms of neuronal apoptosis. Curr. Op. Neurobiol. 4, 696-702.
47. Slee, E. A., Zhu, H., Chow, S. C., MacFarlane, M., Nicholson, D. W. and Cohen, G.M. (1996). Benzyloxycarbonyl-Val-Ala-Asp (OMe) fluoromethylketone (Z-VAD.FMK) inhibits apoptosis by blocking the processing of CPP32. Biochem. J. 315, 21-24.
48. Thompson, C. L. and Stephenson, F. A. (1994). GABAA receptor subtypes expressed in cerebellar granule cells: a devlopmental study. J. Neurochem. 62, 2037-2044.
49. Tsujimoto, Y., Gorham, J., Cossman, J., Jaffe, E. and Croce, C. M. (1985). The t(14;18) chromosome translocations involved in B-cell neoplasms result from mistakes in VDJ joining. Science 229, 1390-1393.
50. Vaux, D. L., Weissman, I. L. and Kim, S. K. (1992). Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 258, 1955-1957.
51. Veis Novack, D. and Korsmeyer, S. J. (1994). Bcl-2 protein expression during murine development. Amer. J. Pathol. 145, 61-73.
52. 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.
53. White, E. (1996). Life, death and the pursuit of apoptosis. Genes Dev. 10, 1-15.
54. Wood, K. A., Dipasquale, B. and Youle, R. J. (1993). In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum. Neuron 11, 621-632.
55. Wyllie, A. H., Kerr, J. F. R. and Currie, A. R. (1980). Cell death, the significance of apoptosis. Int. Rev. Cytol. 68, 251-306.
56. Xue, D. and Horvitz, H. R. (1995). Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377, 248-251.
57. 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.
58. 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.