Up-regulation of Bax protein in degenerating retinal ganglion cells precedes apoptotic cell death after optic nerve lesion in the rat

European Journal of Neuroscience

Volumn 9, Issue 8, 1997, Pages 1763-1772

  Isenmann, Stefan ^a   Wahl, Claudia ^a   Krajewski, Stanislaw ^b   Reed, John C ^b   Bähr, Mathias ^a,c  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b BURNHAM INSTITUTE   (United States)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Bcl 2; Bcl X; Crush lesion; Neurodegeneration; TUNEL

Indexed keywords

PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL X; TRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DNA STRAND BREAKAGE; ETIOLOGY; FEMALE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; NERVE DEGENERATION; NONHUMAN; OPTIC NERVE LESION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RETINA GANGLION CELL;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; DNA FRAGMENTATION; FEMALE; NERVE TISSUE PROTEINS; OPTIC NERVE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; RETINAL DEGENERATION; RETINAL GANGLION CELLS; TIME FACTORS; UP-REGULATION; URIDINE TRIPHOSPHATE;

EID: 0030851891     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.1997.tb01534.x     Document Type: Article

References (55)

1. Allsopp, T. E., Kiselev, S., Wyatt, S. and Davies, A. M. (1995) Role Of Bcl-2 In the brain-derived neurotrophic factor survival response. Eur. J. Neurosci., 7, 1266-1272.
2. Bähr, M. (1991) Adult rat retinal glia in vitro: effects of in vivo crush-activation on glia proliferation and permissiveness for regenerating retinal ganglion cell axons. Exp. Neurol., 111, 65-73.
3. Bähr, M. and Bonhoeffer, F. (1994) Perspectives on axonal regeneration in the mammalian CNS. Trends Neurosci., 17, 473-479.
4. Barron, K. D., Detinger, M. P., Grohel, G., Easton, S. K. and Mankes, R. (1986) Qualitative and quantitative ultrastructural observations on retinal ganglion cell layer of rat after intraorbital optic nerve crush. J. Neurocytol., 15, 345-362.
5. Berkelaar, M., Clarke, D. B., Wang, Y. C., Bray, G. M. and Aguayo, A. J. (1994) Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci., 14, 4368-4374.
6. Boise, L. H., Gonzalez-Garcia, M., Postema, C. E., Ding, L., Lindsten, T., Turka, L. A., Mao, X., Nunez, 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.
7. Bredesen, D. E. (1994) Neuronal apoptosis: genetic and biochemical modulation. In Apoptosis II: The Molecular Basis of Apoptosis in Disease. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 397-421.
8. Bredesen, D. E. (1995) Neural apoptosis. Ann. Neurol., 38, 839-851.
9. Brousset, P., Benharroch, D., Krajewski, S., Laurent, G., Meggetto, F., Rigalhuguet, F., Gopas, J., Prinsloo, I., Pris, J., Delsol., G., Reed, J. C. and Schlaifer, D. (1996) Frequent expression of the cell death-inducing gene bax in Reed-Sternberg cells of Hodgkin's disease. Blood, 87, 2470-2475.
10. Bursch, W., Kleine, L. and Tenniswood, M. (1990) The biochemistry of cell death by apoptosis. Biochem. Cell Biol., 68, 1071-1074.
11. Cellerino, A., Michaelidis, T., Meyer, M., Bähr, M. and Thoenen, H. (1996) Protracted loss of retinal ganglion cells following the period of naturally occurring cell death in mice lacking the bcl2 gene. Soc. Neurosci. Abtsr., 22, 1977.
12. Cenni, M. C., Bonfanti, L., Martinou, J. C., Ratio, G. M., Streotti, E. and Maffei, L. (1996) Long-term survival of retinal ganglion cells following optic nerve section in adult bcl-2 transgenic mice. Eur. J. Neurosci., 8, 1735-1745.
13. 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 CA1 neurons following global ischemia. J. Neurochem., 67, 64-71.
14. Chen, S. T., Garey, L. J. and Jen, L. S. (1994) Bcl-2 proto-oncogene protein immunoreactivity in normally developing and axotomised rat retinas. Neurosci. Lett., 172, 11-14.
15. 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.
16. Dubois-Dauphin, M., Frankowski, H., Tsujimoto, Y., Huarte, J. and Martinou, J. C. (1994) Neonatal motoneurons overexpressing the bcl-2 protooncogene in transgenic mice are protected from axotomy-induced cell death. Proc. Natl Acad. Sci. USA, 91, 3309-3313.
17. Garcia, I., Martinou, I., Tsujimoto, Y. and Martinou, J. C. (1992) Prevention of programmed cell death of sympathetic neurons by the bcl-2 protooncogene. Science, 258, 302-304.
18. Garcia-Valenzuela, E., Gorczyca, W., Darzynkiewicz, Z. and Sharma, S. C. (1994) Apoptosis in adult retinal ganglion cells after axotomy. J. Neurobiol., 25, 431-438.
19. Gavrieli, Y, Sherman, Y and Ben-Sasson, S. A. (1992) Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J. Cell Biol., 119, 493-501.
20. Gillardon, F., Zimmermann, M., Uhlmann, E., Krajewski, S., Reed, J. C. and Klimaschewski, L. (1996) Antisense oligodeoxynucleotides to Bax mRNA promote survival of rat sympathetic neurons in culture. J. Neurosci. Res., 43, 726-734.
21. Gonzalez-Garcia, M., Garcia, I., Ding, L. Y., Oshea, S., Boise, L. H., Thompson, C. B. and Nunez, 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.
22. Grafstein, B. and Ingoglia, N. A. (1982) Intracranial transection of the optic nerve in adult mice: preliminary observations. Exp. Neurol., 76, 318-330.
23. Hara, A., Iwai, T., Niwa, M., Uematsu, T., Yoshimi, N., Tanaka, T. and Mori, H. (1996) Immunohistochemical detection of bax and Bcl-2 proteins in gerbil hippocampus following transient forebrain ischemia. Brain Res., 711, 249-253.
24. Hüll, M. and Bähr, M. (1994) Regulation of immediate-early gene expression in rat retinal ganglion cells after axotomy and during regeneration through a peripheral nerve graft. J. Neurobiol., 25, 92-105.
25. Isenmann, S., Brandner, S., Sure, U. and Aguzzi, A. (1996a) Telencephalic transplants in mice - characterization of growth and differentiation patterns. Neuropathol. Appl. Neurobiol., 22, 108-117.
26. Isenmann, S., Wahl, C., Krajewski, S., Reed, J. C. and Bahr, M. (1996b) Up-regulation of Bax protein in retinal ganglion cells after optic nerve lesion. Soc. Neurosci. Abstr., 22, 569.
27. Isenmann, S. and Bähr, M. (1997) Expression of c-Jun protein in degenerating retinal ganglion cells after optic nerve lesion in the rat. Exp Neurol., in press.
28. Kitada, S., Krajewski, S., Miyashita, T., Krajewska, M. and Reed, J. C. (1996) Gamma-radiation induces up-regulation of Bax protein and apoptosis in radiosensitive cells in vivo. Oncogene, 12, 187-192.
29. Krajewski, S., Tanaka, S., Takayama, S., Schibler, M. J., Fenton, W. and Reed, J. C. (1993) Investigations of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmatic reticulum, and outer mitochondrial membranes. Cancer Res., 53, 4701-4714.
30. Krajewski, S., Krajewska, M., Shabaik, A., Miyashita, T., Wang, H. G. and Reed, J. C. (1994a) Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol., 145, 1323-1336.
31. Krajewski, S., Krajewska, M., Shabaik, A., Wang, H. G., Irie, S., Fong, L. and Reed, J. C. (1994b) Immunohistochemical analysis of in vivo patterns of Bcl-X expression. Cancer Res., 54, 5501-5507.
32. Krajewski, S., Mai, J. K., Krajewska, M., Sikorska, M., Mossakowski, M. J. and Reed, J. C. (1995) Up-regulation of Bax protein levels in neurons following cerebral ischemia. J. Neurosci., 15, 6364-6376.
33. Mansour-Robaey, S., Clarke, D. B., Wang, Y. C., Bray, G. M., Aguayo, A. M. (1994) Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc. Natl Acad. Sci. USA, 91, 1932-1636.
34. Martinou, J. C., Dubois-Dauphin, M., Staple, J. K., Rodriguez, I., Frankowski, H., Missotten, M., Albertini, P., Talabot, D., Catsicas, S., Pietra, C. and Huarte, J. (1994) Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron, 13, 1017-1030.
35. 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.
36. 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.
37. Motoyama, N., Wang, F., Roth, K. A., Sawa, H., Nakayama, K., Nakayama, K., Negishi, I., Senju, S., Zhang, Q., Fujii, S. and Loh, Y. L. (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science, 267, 1506-1510.
38. Myers, K. M., Fiskum, G., Liu, Y., Simmens, S. J., Bredesen, D. E. and Murphy, A. N. (1995) Bcl-2 protects neural cells from cyanide/aglycemia-induced lipid oxidation, mitochondrial injury, and loss of viability. J. Neurochem., 65, 2432-2440.
39. 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.
40. Peinado-Ramón, P., Salvador, M., Villegas-Pérez, M. P., Vidal-Sanz, M. (1996) Effects of axotomy and intraocular administration of NT-4, NT-3, and brain-derived neurotrophic factor on the survival of adult rat retinal ganglion cells. Invest. Ophthalmol. Vis. Sci., 37, 489-500.
41. Perry, V. H. (1981) Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience, 6, 931-944.
42. Rabacchi, S. A., Bonfanti, L., Liu, X. H. and Maffei, L. (1994) Apoptotic cell death induced by optic nerve lesion in the neonatal rat. J. Neurosci., 14, 5292-5301.
43. Reed, J. C. (1994) Bcl-2 and the regulation of programmed cell death. J. Cell Biol., 124, 1-6.
44. Reed, J. C., Cuddy, M., Haldar, S., Croce, C., Nowell, P., Makover, D. and Bradley, K. (1990) BCL2-mediated tumorigenicity of a human T-lymphoid cell line: synergy with MYC and inhibition by BCL2 antisense. Proc. Natl Acad. Sci. USA, 87, 3660-3664.
45. Schaden, H., Stuermer, C. A. O. and Bähr, M. (1994) GAP-43 immunoreactivity and axon regeneration in retinal ganglion cells of the rat. J. Neurobiol., 25, 1570-1578.
46. Shimizu, S., Eguchi, Y., Kamiike, W., Itoh, Y., Hasegawa, J., Yamabe, K., Otsuki, Y., Matsuda, H. and Tsujimoto, Y. (1996) Induction of apoptosis as well as necrosis by hypoxia and predominant prevention of apoptosis by Bcl-2 and Bcl-X(L). Cancer Res., 56, 2161-2166.
47. Subramanian, T., Tarodi, B. and Chinnadurai, G. (1995) p53-independent apoptotic and necrotic cell deaths induced by adenovirus infection: suppression by E1B 19K and Bcl-2 proteins. Cell Growth Diff., 6, 131-137.
48. Takayama, S., Sato, T., Krajewski, S., Kochel, K., Irie, S., Millan, J. A. and Reed, J. C. (1995) Cloning and functional analysis of BAG-1 - a novel Bcl-2-binding protein with anti-cell death activity. Cell, 80, 279-284.
49. Thanos, S. (1988) Alterations in the morphology of ganglion cell dendrites in the adult rat retina after optic nerve transection and grafting of peripheral nerve segments. Cell Tissue Res., 254, 599-609.
50. Thompson, C. B. (1995) Apoptosis in the pathogenesis and treatment of disease. Science, 267, 1456-1462.
51. 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.
52. Villegas-Perez, M. P., Vidal-Sanz, M. P., Rasminsky, M., Bray, G. M. and Aguayo, A. J. (1993) Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats. J. Neurobiol., 24, 23-36.
53. Wyllie, A., Kerr, J. and Currie, A. (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol., 68, 251-306.
54. Yang, E., Zha, J. P., Jockel, J., Boise, L. H., Thompson, C. B. and Korsmeyer, S. J. (1995) Bad, a heterodimeric partner for Bcl-X(L) and Bcl-2, displaces Bax and promotes cell death. Cell, 80, 285-291.
55. Yin, X. M., Oltval, 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.