Ras regulates sympathetic neuron survival by suppressing the p53- mediated cell death pathway

Journal of Neuroscience

Volumn 19, Issue 22, 1999, Pages 9716-9727

  Mazzoni, Irene E ^a,c   Said, Farid A ^b   Aloyz, Raquel ^a   Miller, Freda D ^a   Kaplan, David ^a  

^a MCGILL UNIVERSITY   (Canada)

^b Exogen Neurosciences   (Canada)

^c Caprion Pharmaceuticals   (Canada)

Author keywords

Adenovirus; Apoptosis; Bax; Nerve growth factor; p53; PI3 kinase; Raf; Ras; Ras effectors; Survival; Sympathetic neurons; Trk

Indexed keywords

NERVE GROWTH FACTOR; PROTEIN P53; RAS PROTEIN;

ADENOVIRUS; ADRENERGIC SYSTEM; ANIMAL CELL; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SYMPATHETIC NERVE CELL;

EID: 0033571906     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-22-09716.1999     Document Type: Article

References (67)

1. Aloyz RS, Bamji SX, Pozniak CD, Toma JG, Atwal J, Kaplan DR, Miller FD (1998) p53 is essential for developmental neuron death as regulated by the TrkA and p75 neurotrophin receptors. J Cell Biol 143:1691-1703.
2. Bamji SX, Majdan M, Pozniak CD, Belliveau DJ, Aloyz R, Kohn J, Causing CG, Miller FD (1998) The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuronal death. J Cell Biol 140:911-923.
3. Belliveau DJ, Krivko I, Kohn J, Lachance C, Pozniak C, Rusakov D, Kaplan D, Miller FD (1997) NGF and neurotrophin-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J Cell Biol 136:375-388.
4. Borasio GD, Markus A, Wittinghofer A, Barde Y-A, Heumann R (1993) Involvement of ras p21 in neurotrophin-induced response of sensory, but not sympathetic neurons. J Cell Biol 121:665-672.
5. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
6. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV (1996) Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383:716-719.
7. Chun LY, Patterson PH (1977) Role of NGF in the development of rat sympathetic neurons in vitro. I. Survival, growth and differentiation of catecholamine production. J Cell Biol 75:694-704.
8. Coughlin MD, Collins MB (1985) Nerve growth factor-independent development of embryonic mouse sympathetic neurons in dissociated cell culture. Dev Biol 110:392-401.
9. Cowley S, Paterson H, Kemp P, Marshall CJ (1994) Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841-852.
10. Cox AD, Solski PA, Jordan JD, Der CJ (1995) Analysis of Ras protein expression in mammalian cells. Methods Enzymol 255:195-221.
11. Creedon DJ, Johnson Jr EM, Lawrence Jr JC (1996) Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J Biol Chem 271:20713-20718.
12. Crowder RJ, Freeman RS (1998) Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J Neurosci 18:2933-2943.
13. Darzynkiewicz Z, Bruno S, Del Bino G, Gorczyca W, Hotz MA, Lassota P, Traganos F (1992) Features of apoptotic cells measured by flow cytometry. Cytometry 13:795-808.
14. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
15. Deckwerth TL, Johnson Jr EM (1993) Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor (NGF). J Cell Biol 123:1207-1222.
16. Deckwerth TL, Elliott JL, Knudson CM, Johnson Jr EM, Snider WD, Korsmeyer SJ (1996) Bax is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
17. Dudek H, Datta SD, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DK, Greenberg ME (1997) Regulation of neuronal survival by the serine-threonine kinase Akt. Science 275:661-665.
18. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci USA 92:7686-7689.
19. Edwards SN, Tolkovsky AM (1994) Characterization of apoptosis in cultured rat sympathetic neurons after nerve growth factor withdrawal. J Cell Biol 124:537-546.
20. Eilers A, Whitfield J, Babij C, Rubin LL, Ham J (1998) Role of the jun kinase pathway in the regulation of c-jun expression and apoptosis in sympathetic neurons. J Neurosci 18:1713-1724.
21. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson Jr EM (1994) Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 127:1717-1727.
22. Eves EM, Xiong W, Bellacosa A, Kennedy SG, Tsichlis PN, Rosner MR, Hay N (1998) Akt, a target for phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol Cell Biol 18:2143-2152.
23. Fukuda M, Gotoh Y, Tachibana T, Dell K, Hattori S, Yoneda Y, Nishida E (1995) Induction of neurite outgrowth by MAP kinase in PC12 cells. Oncogene 20:239-244.
24. Ham J, Babij C, Whitfield J, Pfarr CM, Lallemand D, Yaniv M, Rubin LL (1995) A c-jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14:927-939.
25. Holgado-Madruga M, Moscatello DK, Emlet DR, Dieterich R, Wong AJ (1997) Grb2-associated binder-1 mediates phosphatidylinositol 3-kinase activation and the promotion of cell survival by nerve growth factor. Proc Natl Acad Sci USA 94:12419-12424.
26. Joneson T, White MA, Wigler MH, Bar-Sagi D (1996) Stimulation of membrane ruffling and MAP kinase activation by distinct effectors of Ras. Science 271:810-812.
27. Kaplan DR, Miller FD (1997) Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol 9:213-221.
28. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF (1991a) The trk proto-oncogene product: a signal transducing receptor for the nerve growth factor. Science 252:554-558.
29. Kaplan DR, Martin-Zanca D, Parada LF (1991b) Tyrosine phosphorylation and tyrosine kinase activity of the trk proto-oncogene product induced by NGF. Nature 350:158-160.
30. Khosravi-Far R, White MA, Westwick JK, Solski PA, Chrzanowska-Wodnicka M, Van Aelst L, Wigler MH, Der CJ (1996) Oncogenic Ras activation of Raf/mitogen-activated protein kinase-independent pathways is sufficient to cause tumorigenic transformation. Mol Cell Biol 16:3923-3933.
31. Klein R, Jing SQ, Nanduri V, O'Rourke E, Barbacid M (1991) The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65:189-197.
32. Klesse LJ, Parada LF (1998) p21 Ras and phosphatidylinositol-3 kinase are required for survival of wild-type and NF-1 mutant sensory neurons. J Neurosci 18:10420-10428.
33. Knusel B, Rabin SJ, Hefti F, Kaplan DR (1994) Regulated neurotrophin receptor responsiveness during neuronal migration and early differentiation. J Neurosci 14:1542-1554.
34. Kouhara H, Hadari YR, Spivak-Kroizman T, Schilling J, Bar-Sagi D, Lax I, Schlessinger J (1997) A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89:693-702.
35. Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237:1154-1162.
36. Levi-Montalcini R, Angeletti PU (1963) Essential role for nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic embryonic nerve cells in vitro. Dev Biol 7:653-657.
37. Levi-Montalcini R, Brooker B (1960) Destruction of sympathetic ganglia in mammals by an antiserum to the nerve growth factor protein. Proc Natl Acad Sci USA 46:384-391.
38. Ma Y, Campenot RB, Miller FD (1992) Concentration-dependent regulation of neuronal gene expression by nerve growth factor. J Cell Biol 117:135-141.
39. Manthorpe M, Fagnani R, Skaper SD, Varon S (1986) An automated colorimetric assay for neurotrophic factors. Dev Brain Res 25:191-198.
40. Markus A, von Holst A, Rohrer H, Heumann R (1997) NGF-mediated survival depends on p21ras in chick sympathetic neurons from the superior cervical ganglia but not from lumbosacral ganglia. Dev Biol 191:306-310.
41. Marshall CJ (1996) Ras effectors. Curr Opin Cell Biol 8:197-204.
42. Martin DP, Schmidt RE, Distefano PS, Lowry OH, Carter JG, Johnson EM (1988) Inhibitors of protein synthesis and mRNA synthesis prevent neuronal cell death caused by NGF deprivation. J Cell Biol 106:829-844.
43. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA, Schwartzkroin PA (1996) Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 16:1337-1345.
44. Nobes CD, Tolkovsky AM (1995) Neutralising anti-p21ras Fabs suppress rat sympathetic neuron survival induced by NGF, LIF, CNTF and cAMP. Eur J Neurosci 7:344-350.
45. Nobes CD, Reppas JB, Markus A, Tolkovsky AM (1996) Active p21Ras is sufficient for rescue of NGF-dependent rat sympathetic neurons. Neuroscience 70:1067-1079.
46. Pang L, Sawada T, Decker SJ, Saltiel AR (1995) Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J Biol Chem 270:13585-13588.
47. Philpott KL, McCarthy MJ, Klippel A, Rubin LL (1997) Activated phosphatidylinositol 3-kinase and Akt kinase promote survival of superior cervical neurons. J Cell Biol 139:809-815.
48. Qian X, Riccio A, Zhang Y, Ginty DD (1998) Identification and characterization of novel substrates of Trk receptors in developing neurons. Neuron 21:1017-1029.
49. Querido E, Marcellus RC, Lai A, Charbonneau R, Teodoro JG, Ketner G, Branton PE (1997) Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J Virol 71:3788-3798.
50. Quilliam LA, Khosravi-Far R, Huff SY, Der CJ (1995) Guanine nucleotide exchange factors: activators of the Ras superfamily of proteins. Bioessays 17:395-404.
51. Rodriguez-Viciana P, Warne PH, Dhand R, Vanhaesebroeck B, Gout I, Fry MJ, Waterfield MD, Downward J (1994) Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370:527-532.
52. Rodriguez-Viciana P, Warne PH, Khwaja A, Marte BM, Pappin D, Das P, Waterfield MD, Ridley A, Downward J (1997) Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell 89:457-467.
53. Seeburg PH, Colby WW, Capon DJ, Goeddel DV, Levinson AD (1984) Biological properties of human c-Ha-ras1 genes mutated at codon 12. Nature 312:71-75.
54. Segal RA, Greenberg ME (1996) Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 19:463-489.
55. Sigal IS, Gibbs JB, D'Alonzo JS, Temeles GL, Wolanski BS, Socher SH, Scolnick EM (1986) Mutant ras-encoded proteins with altered nucleotide binding exert dominant biological effects. Proc Natl Acad Sci USA 83:952-956.
56. Slack RS, Belliveau DJ, Rosenberg M, Atwal J, Aloyz R, Lochmuller H, Hagighi A, Lach B, Seth P, Cooper E, Miller FD (1996) Adenovirus-mediated gene transfer of the tumor suppressor p53 induces apoptosis in postmitotic neurons. J Cell Biol 135:1085-1096.
57. Teodoro JG, Branton PE (1997) Regulation of p53-dependent apoptosis, transcriptional repression, and cell transformation by phosphorylation of the 55-kilodalton E1B protein of human adenovirus type 5. J Virol 71:3620-3627.
58. Virdee K, Tolkovsky AM (1995a) Activation of p44 and p42 MAP kinases is not essential for the survival of rat sympathetic neurons. Eur J Neurosci 7:2159-2169.
59. Virdee K, Tolkovsky AM (1995b) Inhibition of p42 and p44 mitogenactivated protein kinase activity by PD98059 does not suppress nerve growth factor-induced survival of sympathetic neurones. J Neurochem 67:1801-1805.
60. Vlahos CJ, Matter WF, Hui KY, Brown RF (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-1 (LY 294002). J Biol Chem 269:5241-5248.
61. Vogel KS, Brannan CI, Jenkins NA, Copeland NG, Parada LF (1995) Loss of neurofibromin results in neurotrophin-independent survival of embryonic sensory and sympathetic neurons. Cell 82:733-742.
62. Vojtek AB, Der CJ (1998) Increasing complexity of the Ras signaling pathway. J Biol Chem 273:19925-19928.
63. Xiang H, Hochman DW, Saya H, Fujiwara T, Schwartzkroin PA, Morrison RS (1996) Evidence for p53-mediated modulation of neuronal viability. J Neurosci 16:6753-6765.
64. 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.
65. Yao RI, Cooper GM (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 275:665-668.
66. Yew PR, Berk AJ (1992) Inhibition of p53 transactivation required for transformation by adenovirus early IB protein. Nature 337:82-85.
67. Yoon SO, Casaccia-Bonnefil P, Carter B, Chao MV (1998) Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J Neurosci 18:3273-3281.