Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate

FASEB Journal

Volumn 14, Issue 5, 2000, Pages 779-790

  Almeida, O F X ^a   Conde G L ^a   Crochemore, C ^a   Demeneix, B A ^b   Fischer, D ^a   Hassan, A H S ^a   Meyer, M ^c   Holsboer, F ^a   Michaelidis, T M ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Apoptosis; Bax; Bax knockout mouse; Bcl 2; Corticosterone; Dexamethasone; Glucocorticoid receptor; Mineralocorticoid receptor

Indexed keywords

GLUCOCORTICOID RECEPTOR; MINERALOCORTICOID RECEPTOR; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN P53;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; GENE EXPRESSION; HIPPOCAMPUS; KNOCKOUT MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0034117178     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.14.5.779     Document Type: Article

References (75)

1. de Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., and Joëls, M. (1998) Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19, 269-301
2. Gould, E., and Cameron, H. A. (1996) Regulation of neuronal birth, migration and death in the rat dentate gyrus. Dev. Neurosci. 18, 22-35
3. Hassan, A. H. S., von Rosenstiel, P., Patchev, V. K., Holsboer, F., and Almeida, O. F. X. (1996) Exacerbation of apoptosis in the dentate gyrus of the aged rat by dexamethasone and the protective role of corticosterone. Exp. Neurol. 140, 43-54
4. Reagan, L. P., and McEwen, B. S. (1997) Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. J. Chem. Neuroanat. 13, 149-167
5. Hassan, A. H. S., Patchev, V. K., von Rosenstiel, P., Holsboer, F., and Almeida, O. F. X. (1999) Plasticity of hippocampal corticosteroid receptors during aging in the rat. FASEB J. 13, 115-122
6. Gould, E., Tanapat, P., McEwen, B. S., Flügge, G., and Fuchs, E. (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. USA 95, 3168-3171
7. Sloviter, R. S., Sollas, A. L., Dean, E., and Neubort, S. (1993) Adrenalectomy-induced granule cell degeneration in the rat hippocampal dentate gyrus: Characterization of an in vivo model of controlled neuronal death. J. Comp. Neurol. 330, 324-336
8. Sousa, N., Almeida, O. F. X., Holsboer, F., Paula-Barbosa, M. M., and Madeira, M. D. (1998) Maintenance of hippocampal cell numbers in young and aged rats submitted to chronic unpredictable stress. Comparison with the effects of corticosterone treatment. Stress 24, 237-249
9. Woolley, C. S., Gould, E., Sakai, R. R., Spencer, R. L., and McEwen, B. S. (1991) Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res. 554, 312-315
10. Farrow, S. N., and Brown, R. (1996) New members of the Bcl-2 family and their protein partners. Curr. Opin. Genet. Dev. 6, 45-49
11. Merry, D. E., and Korsmeyer, S. J. (1997) Bcl-2 gene family in the nervous system. Annu. Rev. Neurosci. 20, 245-267
12. Knudson, M. C., and Korsmeyer, S. J. (1997) Bcl-2 and Bax function independently to regulate cell death. Nat. Genet. 16, 358-363
13. Hengartner, M. O. (1998) Apoptosis - death cycle and Swiss army knives. Nature (London) 391, 441-442
14. Reed, J. C. (1997) Double identity for proteins of the Bcl-2 family. Nature (London) 387, 773-776
15. Wyllie, A. (1997) Apoptosis - clues in the p53 murder mystery. Nature (London) 389, 237-238
16. Kroemer, G. (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med. 3, 614-620
17. Williams, G. T., and Smith, C. A. (1993) Molecular regulation of apoptosis: genetic controls on cell death. Cell 74, 777-779
18. Oltvai, Z. N., and Korsmeyer, S. J. (1994) Checkpoints of dueling dimers foil death wishes. Cell 79, 189-192
19. Bayer, S. A., and Altman, J. (1974) Hippocampal development in the rat: cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J. Comp. Neurol. 158, 55-80
20. Cameron, H. A., Tanapat, P., and Gould, E. (1998) Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 82, 349-354
21. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18, 3206-3212
22. Castrén, E., Ohga, Y., Berzaghi, M. P., Tzimagiorgis, G., Thoenen, H., and Lindholm, D. (1994) bcl-2 messenger RNA is localized in neurons of the developing and adult rat brain. Neuroscience 61, 165-177
23. Bernier, P. J., and Parent, A. (1998) The anti-apoptosis bcl-2 proto-oncogene is preferentially expressed in limbic structures of the primate brain. Neuroscience 82, 635-640
24. Chen, J., Zhu, R. L., Nakayama, M., Kawaguchi, K., Jin, K. L., Stetler, R. A., Simon, R. P., and Graham, S. H. (1996) Expression of the apoptosis-effector gene. bax, is up-regulated in vulnerable hippocampal CA 1 neurons following global ischemia, J. Neurochem. 67, 64-71
25. Krajewski, S., Krajewska, M., Shabaik, A., Wang, H.-G., Irie, S., Fong, L., and Reed, J. C. (1994) Immunohistochemical analysis of in vivo patterns of Bcl-X expression. Cancer Res. 54, 5501-5507
26. Boise, L. H., González-García, 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
27. Frankowski, H., Missotten, M., Fernandez, P.-A., Martinou, I., Michel, P., Sadoul, R., and Martinou, J.-C. (1995) Function and expression of the bcl-x gene in the developing and adult nervous system. NeuroReport 6, 1917-1921
28. González-García, M., García, I., Ding, L., O'Shea, S., Boise, L. H., Thompson, C. B., and Núñez, G. (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
29. Vekrellis, K., McCarthy, M. J., Watson, A., Whitfield, J., Rubin, L. L., and Ham, J. (1997) Bax promotes neuronal cell death and is downregulated during the development of the nervous system. Development 124, 1239-1249
30. L is an antiapoptotic regulator for postnatal CNS neurons. J. Neurosci. 18, 1009-1019
31. 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
32. 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
33. Krajewski, S., Krajewski, M., Shabaik, A., Toshiyuki, M., 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
34. MacGibbon, G. A., Lawlor, P. A., Sirimanne, E. S., Walton, M. R., Connor, B., Young, D., Williams, C., Gluckman, P., Faull, R. L. M., Hughes, P., and Dragunow, M. (1997) Bax expression in mammalian neurons undergoing apoptosis, and in Alzheimer's disease hippocampus. Brain Res. 750, 223-234
35. Maiyar, A. C., Phu, P. T., Huang, A. J., and Firestone, G. L. (1997) Repression of glucocorticoid receptor transactivation and DNA binding of a glucocorticoid response element within the serum/glucocorticoid-inducible protein kinase (sgk) gene promoter by the p53 tumor suppressor protein. Mol. Endocrinol. 11, 312-29
36. Miyashita, T., Krajewski, S., Krajewska, M., Wang, H. G., Lin, H. K., Lieberman, 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
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. Spencer, R. L., Miller, A. H., Moday, H., Stein, M., and McEwen, B. S. (1993) Diurnal differences in basal and acute stress levels of type I and type II adrenal steroid receptor activation in neural and immune tissues. Endocrinology 133, 1941-1950
39. Paxinos, G., and Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, Academic Press, San Diego, California
40. Le Mouellic, H., Lallemand, Y., and Brûlet, P. (1992) Homeosis in the mouse induced by a null mutation in the Hox-3.1 gene. Cell 69, 251-264
41. Tzimagiorgis, G., Michaelidis, T. M., Lindholm, D., and Thoenen, H. (1996) Introduction of the negative selective marker into replacement vectors by a single ligation step. Nucleic Acids Res. 24, 3467-3477
42. Mansour, S. L., Thomas, K. R., and Capecchi, M. R. (1988) Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to nonselectable genes. Nature (London) 336, 348-352
43. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W., and Roder, J. C. (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424-8428
44. 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
45. Gavrieli, Y., Sherman, Y., and Ben-Sassan, S. A. (1992) Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501
46. Tilly, J. L., Tilly, K. I., Kenton, M. L., and Johnson, A. L. (1995) Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology 136, 232-241
47. 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
48. Sousa, N., Paula-Barbosa, M. M., and Almeida, O. F. X. (1998) Ligand and subfield specificity of corticoid-induced neuronal loss in the rat hippocampal formation. Neuroscience 89, 1079-1087
49. Kaplan, M. S., and Bell, D. H. (1984) Mitotic neuroblasts in the 9 day old and 11 month old rodent hippocampus. J. Neurosci. 4, 1429-1441
50. Hu, Z. T., Yuri, K., Ozawa, H., Lu, H. P., and Kawata, M. (1997) The in vivo time course for elimination of adrenalectomy-induced apoptotic profiles from the granule cell layer of the rat hippocampus. J. Neurosci. 17, 3981-3989
51. Deckwerth, T. L., Elliott, J. L., Knudson, C. M., Johnson, E. M., Jr., 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
52. White, F. A., Keller-Peck, C.R., Knudson, C. M., Korsmeyer, S. J., and Snider, W. D. (1998) Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J. Neurosci. 18, 1428-1439
53. Sedlak, T. W., Oltvai, Z. N., Yang, E., Wang, K., Boise, L. H., Thompson, C. B., and Korsmeyer, S. J. (1995) Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc. Natl. Acad. Sci. USA 92, 7834-7838
54. 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 (London) 369, 321-323
55. Gillardon, F., Lenz, C., Waschke, K. F., Krajewski, S., Reed, J. C., Zimmermann, M., and Kuschinsky, W. (1996) Altered expression of bcl-2, bcl-X, bax, and c-fos colocalizes with DNA fragmentation and ischemic cell damage following middle cerebral artery occlusion in rats. Mol. Brain Res. 40, 254-260
56. Shimazaki, K., Ishida, A., and Kawai, N. (1994) Increase in Bcl-2 oncoprotein and the tolerance to ischemia-induced neuronal death in the gerbil hippocampus. Neurosci. Res. 20, 95-99
57. Clark, R. S. B., Chen, J., Watkins, S. C., Kochanek, P. M., Chen, M. Z., Stetler, R. A., Loeffert, J. E., and Graham, S. H. (1997) Apoptosis-suppressor gene bcl-2 expression after traumatic brain injury in rats. J. Neurosci. 17, 9172-9182
58. Marshall, K. A., Daniel, S. E., Cairns, N., Jenner, P., and Halliwell, B. (1997) Upregulation of the anti-apoptotic protein Bcl-2 may be an early event in neurodegeneration: studies on Parkinson's and incidental Lewy Body disease. Biochem. Biophys. Res. Commun. 240, 84-87
59. O'Connor, L., Strasser, A., O'Reilly, L. A., Hausmann, G., Adams, J. M., Cory, S., and Huang, D. C. S. (1998) Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17, 384-395
60. Antonsson, B., Conti, F., Ciavatta, A., Montessuit, S., Lewis, S., Martinou, I., Bernasconi, L., Bernard, A., Mermod, J. J., Mazzei, G., Maundrell, K., Gambale, F., Sadoul, R., and Martinou, J. C. (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277, 370-372
61. Keller, J. N., Kindy, M. S., Holtsberg, F. W., St Clair, D. K., Yen, H. C., Germeyer, A., Steiner, S. M., Bruce-Keller, A. J., Hutchins, J. B., and Mattson, M. P. (1998) Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J. Neurosci. 18, 687-697
62. Yu, C., Yap, N., Chen, D., and Cheng, S. (1997) Modulation of hormone-dependent transcriptional activity of the glucocorticoid receptor by the tumor suppressor p53. Cancer Lett. 116, 191-196
63. Zuo, Z., Urban, G., Scammell, J. G., Dean, N. M., McLean, T. K., Aragon, I., and Honkanen, R. E. (1999) Ser/Thr protein phosphatase type 5 (PP5) is a negative regulator of glucocorticoid receptor-mediated growth arrest. Biochemistry 13, 8849-8857
64. Han, J., Sabbatini, P., Perez, D., Rao, L., Modha, D., and White, E. (1996) The E1B 19K protein blocks apoptosis by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes Dev. 10, 461-477
65. Selvakumaran, M., Lin, H.K., Miyashita, T., Wang, H., Karjewski, S., Reed, J. C., Hoffman, B., and Liebermann, D. (1994) Immediate early up-regulation of bax expression by p53 but not TGF beta 1: a paradigm for distinct apoptotic pathways. Oncogene 9, 1791-1798
66. Beato, M., Herrlich, P., and Schütz, G. (1995) Steroid hormone receptors: many actors in search of a plot. Cell 83, 851-857
67. Heck, S., Bender, K., Kullmann, M., Göttlicher, M., Herrlich, P., and Cato, A. C. B. (1997) IκBα-independent downregulation of NF-κB activity by glucocorticoid receptor. EMBO J. 16, 4698-4707
68. McKay, L. I., and Cidlowski, J. A. (1998) Cross-talk between nuclear factor-kappa B and the steroid hormone receptors: mechanisms of mutual antagonism. Mol. Endocrinol. 12, 45-56
69. Xiang, H., Kinoshita, Y., Knudson, M., Korsmeyer, S. J., Schwartzkroin, P. A., and Morrison, R. S. (1998) Bax involvement in p53-mediated neuronal cell death. J. Neurosci. 18, 1363-1373
70. Zeiner, M., and Gehring, U. (1995) A protein that interacts with members of the nuclear hormone receptor family: Identification and cDNA cloning. Proc. Natl. Acad. Sci. USA 92, 11465-11469
71. Takayama, S., Bimston, D. N., Matsuzawa, S., Freeman, B. C., Aime-Sempe, C., Xie, Z. H., Morimoto, R. I., and Reed, J. C. (1997) BAG-1 modulates the chaperone activity of Hsp70/ Hsc70. EMBO J. 16 4887-4896
72. Trapp, T., and Holsboer, F. (1996) Heterodimerization between mineralocorticoid and glucocorticoid receptors increases the functional diversity of corticosteroid action. Trends Pharmacol. Sci. 17, 145-149
73. Lupien, S. J., de Leon, M., de Santi, S., Convit, A., Tarshish, C., Nair, N. P. V., Thakar, M., McEwen, B. S., Hauger, R. L., and Meaney, M. J. (1998) Cortisol levels during human ageing predict hippocampal atrophy and memory deficits. Nat. Neurosci. 1, 69-73
74. Sapolsky, R. M. (1996) Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress 1, 1-19
75. Porter, N. M., and Landfield, P. W. (1998) Stress hormones and brain aging: adding injury to insult? Nature (London) Neurosci. 1, 3-4