Motor neuron degeneration is attenuated in bax-deficient neurons in vitro

Journal of Neuroscience Research

Volumn 55, Issue 5, 1999, Pages 542-556

  Bar Peled, O ^a   Knudson, M ^b   Korsmeyer, S J ^b   Rothstein, J D ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

Amyotrophic lateral sclerosis; Apoptosis; Degeneration; In vitro; Kainate; Motor neurons

Indexed keywords

KAINIC ACID; PROTEIN BAX;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; GENOTYPE; MOTONEURON; MOTOR NEURON DISEASE; MOUSE; NERVE CELL CULTURE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; ASPARTIC ACID; ASTROCYTES; BCL-2-ASSOCIATED X PROTEIN; CELL DEATH; CELL DIVISION; CELL NUCLEUS; CELL SIZE; CELL SURVIVAL; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; FEMALE; GENOTYPE; KAINIC ACID; MALE; MICE; MOTOR NEURONS; NERVE DEGENERATION; PARAQUAT; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; SPINAL CORD; SUPEROXIDES;

EID: 0033104429     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19990301)55:5<542::AID-JNR2>3.0.CO;2-7     Document Type: Article

References (61)

1. Bar-Peled O, Korkotian E, Segal M, Groner Y. 1996. Constitutive overexpression of Cu/Zn superoxide dismutase exacerbates kainic acid-induced apoptosis of transgenic-Cu/Zn superoxide dismutase neurons. Proc Natl Acad Sci USA 93:8530-8535.
2. Blum D, Wu Y, Nissou MF, Arnaud S, Alim-Louis-Benabid, Verna JM. 1997. p53 and Bax activation in 6-hydroxydopamine-induced apoptosis in PC12 cells. Brain Res 751:139-142.
3. Brady HJ, Gil-Gomez G, Kirberg J, Berns AJ. 1996. Bax alpha perturbs T cell development and affects cell cycle entry of T cells. EMBO J 15:6991-7001.
4. -2 dependent. NeuroReport 6:945-948.
5. Carriedo SG, Yin HZ, Weiss JH. 1996. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 16:4069-4079.
6. Cleary ML, 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.
7. Comella JX, Sanz-Rodriguez C, Aldea M, Esquerda JE. 1994. Skeletal muscle-derived trophic factors prevent motor neurons from entering an active cell death program in vitro. J Neurosci 14:2674-2686.
8. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM, Snider WD, Korsmeyer SJ. 1996. Bax is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
9. Gillardon F, Klimaschewski L, Wickert H, Krajewski S, Reed JC, Zimmermann M. 1996. Expression pattern of candidate cell death effector proteins Bax, Bcl-2, Bcl-X, and c-Jun in sensory and motor neurons after sciatic nerve transection in the rat. Brain Res 739:244-250.
10. Gonzalez-Garcia M, Garcia I, Ding L, O'Shea S, Boise LH, Thompson CB, 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.
11. Gotow T, Tanaka J. 1994. Phosphorylation of neurofilament H subunit as related to arrangement of neurofilaments. J Neurosci Res 37:691-713.
12. Gottron FJ, Ying HS, Choi DW. 1997. Caspase inhibition selectively reduces the apoptotic component of oxygen-glucose deprivation-induced cortical neuronal cell death. Mol Cell Neurosci 9:159-169.
13. Hara H, Friedlander RM, Gagliardini V, Ayata C, Fink K, Huang Z, Shimizu-Sasamata M, Yuan J, Moskowitz MA. 1997. Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc Natl Acad Sci USA 94:2007-2012.
14. Haviv R, Lindenboim L, Li H, Yuan J, Stein R. 1997. Need for caspases in apoptosis of trophic factor-deprived PC12 cells. J Neurosci Res 50:69-80.
15. Houenou LJ, Li L, Lo AC, Yan Q, Oppenheim RW. 1994. Naturally occurring and axotomy-induced motor neuron death and its prevention by neurotrophic agents: a comparison between chick and mouse. Prog Brain Res 102:217-225.
16. Knudson CM, Korsmeyer SJ. 1997. Bcl-2 and Bax function independently to regulate cell death. Nat Genet 16:358-363.
17. Knudson CM, Tung KSK, Tourtelotte WG, Brown GAJ, Korsmeyer SJ. 1995. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99.
18. Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN. 1993. Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Cancer Biol 4:327-332.
19. Kostic V, Jackson-Lewis V, de Bilbao F, Duhois-Dauphin M, Przedborski S. 1997. Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 277:559-562.
20. Krajewski S, Mai JK, Krajewska M, Sikorska M, Mossakowski MJ, Reed JC. 1995. Upregulation of bax protein levels in neurons following cerebral ischemia. J Neurosci 15:6364-6376.
21. Liu D, Yang J, Li L, McAdoo DJ. 1995. Paraquat - a superoxide generator - kills neurons in the rat spinal cord. Free Rad Biol Med 18:861-867.
22. Loeb J, Fischbach GD. 1997. Neurotrophic factors increase neuregulin expression in embryonic ventral spinal cord neurons. J Neurosci 17:1416-1424.
23. MacGibbon GA, Lawlor PA, Sirimanne ES, Walton MR, Connor B, Young D, Williams C, Gluckman P, Faull RL, Hughes P, Dragunow M. 1997. Bax expression in mammalian neurons undergoing apoptosis, and in Alzheimer's disease hippocampus. Brain Res 750:223-234.
24. McCurrach ME, Connor TM, Knudson CM, Korsmeyer SJ, Lowe SW. 1997. bax-deficiency promotes drug resistance and oncogenic transformation by attenuating p53-dcpendent apoptosis. Proc Natl Acad Sci USA 94:2345-2349.
25. Merry DE, Korsmeyer SJ. 1997. Bcl-2 gene family in the nervous system. Annu Rev Neurosci 20:245-267.
26. Miller TM, Moulder KL, Knudson CM, Creedon DJ, Deshmukh M, Korsmeyer SJ, Johnson EM. 1997. Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway to cell death. J Cell Biol 139:205-217.
27. Milligan CE, Prevette D, Yaginuma H, Homma S, Cardwell C, Fritz LC, Tomaselli KJ, Oppenheim RW, Schwartz LM. 1995. Peptide inhibitors of the ICE protease family arrest programmed cell death of motor neurons in vivo and in vitro. Neuron 15:385-393.
28. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Nakayama K, Negishi I, Senju S, Zhang Q, Fujii S, Loh DY. 1995. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267:1506-1510.
29. Oh JH, O'Malley KL, Krajewski S, Reed JC, Oh YJ. 1997. Bax accelerates staurosporine-induced but suppresses nigericin-induced neuronal cell death. NeuroReport 8:1851-1856.
30. Ohga Y, Zirrgiebel U, Hamner S, Michaelidis TM, Cooper J, Thoenen H, Lindholm D. 1996. Cell density increases Bcl-2 and Bcl-x expression in addition to survival of cultured cerebellar granule neurons. Neuroscience 73:913-917.
31. Oltvai ZN, Korsmeyer SJ. 1994. Checkpoints of dueling dimers foil death wishes. Cell 79:189-192.
32. Oltvai ZN, Milliman CL, Korsmeyer S J. 1993. Bcl-2 heterodimerizes with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619.
33. Oppenheim RW. 1991. Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
34. O'Reilly LA, Huang DC, Strasser A. 1996. The cell death inhibitor Bcl-2 and its homologues influence control of cell cycle entry. EMBO J 15:6979-6990.
35. Paradis E, Douillard H. Koutroumanis M, Goodyer C, LeBlanc A. 1996. Amyloid beta peptide of Alzheimer's disease downregulates Bcl-2 and upregulatcs bax expression in human neurons. J Neurosci 16:7533-7539.
36. Patel M, Day BJ, Crapo JD, Fridovich I, McNamara JO. 1996. Requirement for superoxide in excitotoxic cell death. Neuron 16:345-355.
37. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM. 1996. Requirement for LIM hogene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84:309-320.
38. Phelps PE, Barber RP, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE. 1984. Postnatal development of neurons containing choline acetyltransferase in rat spinal cord: an immunocytochemical study. J Comp Neurol 229:347-361.
39. Pollard H, Charriaut-Marlangue C, Cantagrel S, Represa A, Robain O, Moreau J, Ben-Ari Y. 1994. Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience 63:7-18.
40. Posmantur R, McGinnis K, Nadimpalli R, Gilbertsen RB, Wang KK. 1997. Characterization of CPP32-like protease activity following apoptotic challenge in SH-SY5Y neuroblastoma cells. J Neurochem 68:2328-2337.
41. Reed JC. 1997. Double identity for proteins of the Bcl-2 family. Nature 387:773-776.
42. Roth KA, Motoyama N, Loh DY. 1996. Apoptosis of bcl-x-deficient telencephalic cells in vitro. J Neurosci 16:1753-1758.
43. Rothstein JD. 1995. Excitotoxic mechanisms in the pathogenesis of amyotrophic lateral sclerosis. Adv Neurol 68:7-20.
44. Rothstein JD, Kuncl RW. 1995. Neuroprotective strategies in a model of chronic glutamate-mediated motor neuron toxicity. J Neurochem 65:643-651.
45. Rothstein JD, Jin L, Dykes-Hoberg M, Kuncl RW. 1993. Chronic glutamate uptake inhibition produces a model of slow neurotoxicity. Proc Natl Acad Sci USA 90:6591-6595.
46. Rothstein JD, Bristol LA, Hosler B, Brown RH, Kuncl RW. 1994. Chronic inhibition of superoxide dismutase produces apoptotic death of spinal neurons. Proc Natl Acad Sci USA 91:4155-5159.
47. Roy N, Mahadevan MS, McLean M, Shutler G, Yaraghi Z, Farahani R, Baird S, Besner-Johnston A, Lefebvre C, Kang X, Salih M, Aubry H, Tamai K, Guan X, Ioannou P, Crawford TO, de Jong PJ, Surh L, Ikeda JE, Korneluk RG, MacKenzie A. 1995. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80:167-178.
48. Shindler KS, Latham CB, Roth KA. 1997. Bax deficiency prevents the increased cell death of immature neurons in bcl-x-deficient mice. J Neurosci 17:3112-3119.
49. Simonian NA, Getz RL, Leveque JC, Konradi C, Coyle JT. 1996. Kainate induces apoptosis in neurons. Neuroscience 74:675-683.
50. Su JH, Deng G, Cotman CW. 1997. Bax protein expression is increased in Alzheimer's brain: correlations with DNA damage. Bcl-2 expression, and brain pathology. J Neuropathol Exp Neurol 56:86-93.
51. Tortosa A, Lopez E, Ferrer I. 1998. Bcl-2 and Bax protein expression in Alzheimer's disease. Acta Neuropathol 95:407-412.
52. Troost D, Aten J, Morsink F, De Jong JMBV. 1995. Apoptosis in amyotrophic lateral sclerosis is not restricted to motor neurons. Bcl-2 expression is increased in unaffected post-central gyrus. Neuropathol Appl Neurobiol 21:498-504.
53. Troy CM, Stefanis L, Greene LA, Shelanski ML. 1997. Nedd2 is required for apoptosis after trophic factor withdrawal, but not superoxide dismutase (SOD1) downregulation, in sympathetic neurons and PC12 cells. J Neurosci 17:1911-1918.
54. Tsujimoto Y, Gorham J, Cossman J, Jaffe E, Croce C. 1985. The t(14:18) chromosome translocations involved in B-cell neoplasms result from mistakes in VDJ joining. Science 229:1390-1393.
55. Uz T, Giusti P, Franceschini D, Kharlamov A, Manev H. 1996. Protective effect of melatonin against hippocampal DNA damage induced by intraperitoneal administration of kainate to rats. Neuroscience 73:631-636.
56. Vekrellis K, McCarthy MJ, Watson A, Whitfield J, Rubin LL, Ham J. 1997. Bax promotes neuronal cell death and is downregulated during the development of the nervous system. Development 124:1239-1249.
57. White FA, Keller-Peck CR, Knudson CM, Korsmeyer SJ, Snider WD. 1998. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci 18:1428-1439.
58. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA, Morrison RS. 1998. Bax involvement in p53-mediated neuronal cell death. J Neurosci 18:1363-1373.
59. Yamada T, Pfaff SL, Edlund T, Jessell TM. 1993. Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 73:673-686.
60. Yin C, Knudson CM, Korsmeyer SJ, Van Dyke T. 1997. Bax suppresses tumorigenesis and stimulates apoptosis in vivo. Nature 385:637-640.
61. Yoshiyama Y, Yamada T, Asanuma K, Asahi T. 1994. Apoptosis related antigen, Le(Y) and nick-end labeling are positive in spinal motor neurons in amyotrophic lateral sclerosis. Acta Neuropathol 88:207-211.