p21 Ras and phosphatidylinositol-3 kinase are required for survival of wild-type and NF1 mutant sensory neurons

Journal of Neuroscience

Volumn 18, Issue 24, 1998, Pages 10420-10428

  Klesse, Laura J ^a   Parada, Luis F ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Neurotrophin signaling; NGF; p21 ras; PI 3 kinase; Recombinant adenovirus; Sensory neuron survival

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; DIMETHYL SULFOXIDE; NEUROFIBROMIN; PHOSPHATIDYLINOSITOL; WORTMANNIN;

ADENOVIRUS; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN; CELL SURVIVAL; ENZYME ACTIVITY; GENE MUTATION; MOLECULAR CLONING; ONCOGENE RAS; PRIORITY JOURNAL; SENSORY NERVE CELL;

EID: 0032535276     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-24-10420.1998     Document Type: Article

References (59)

1. Ballester R, Marchuk D, Boguski M, Saulino A, Letcher R, Wigler M, Collins F (1990) The NF1 locus encodes a protein functionally related to mammalian GAP and yeast IRA proteins. Cell 63851-859.
2. Bar-Sagi D, Feramisco JR (1985) Microinjection of the ras oncogene protein into PC12 cells induces morphological differentiation. Cell 42841-848.
3. Bernards A (1995) Neurofibromatosis type 1 and Ras-mediated signaling filling in the GAPs. Biochim Biophys Acta 124243-59.
4. Borasio GD, John J, Wittinghofer A, Barde YA, Sendtner M, Heumann R (1989) ras p21 protein promotes survival and fiber outgrowth of cultured embryonic neurons. Neuron 21087-1096.
5. Borasio GD, Markus A, Wittinghofer A, Barde YA, Heumann R (1993) Involvement of ras p21 in neurotrophin-induced response of sensory, but not sympathetic, neurons. J Cell Biol 121665-672.
6. Borasio GD, Markus A. Heumann R, Ghezzi C, Sampietro A, Wittinghofer A, Silani V (1996) Ras p21 protein promotes survival and differentiation of human embryonic neural crest-derived cells. Neuroscience 731121-1127.
7. Brannan CI, Perkins AS, Vogel KS, Ratner N, Nordlund ML, Rcid SW, Buchberg AM, Jenkins NA, Parada LF, Copeland NG (1994) Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev [Erratum (1994) 82792] 81019-1029.
8. Bredesen DE, Rabizadeh S (1997) p75NTR and apoptosis Trkdependent and Trk-independent effects. Trends Neurosci 20287-290.
9. Brader JT, Heidecker G, Rapp UR (1992) Serum-, TPA-, and Rasinduced expression from Ap-1/Ets-driven promoters requires Raf-1 kinase. Genes Dev 6545-556.
10. 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 383716-719.
11. Conover JC, Yancopoulos GD (1997) Neurotrophin regulation of the developing nervous system analyses of knockout mice. Rev Neurosci 813-27.
12. 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 77841-852.
13. Creedon DJ, Johnson EM, Lawrence JC (1996) Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J Biol Chem 27120713-20718.
14. 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 182933-2943.
15. Datta K, Bellacosa A, Chan TO, Tsichlis PN (1996) Akt is a direct target of the phosphatidylinositol 3-kinase. Activation by growth factors, v-src and v-Ha-ras, in Sf9 and mammalian cells. J Biol Chem 27130835-30839.
16. 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 91231-241.
17. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nunez G (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278687-689.
18. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal R A, Kaplan DR, Greenberg M E (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275661-665.
19. Edwards SN, Tolkovsky AM (1994) Characterization of apoptosis in cultured rat sympathetic neurons after nerve growth factor withdrawal. J Cell Biol 124537-546.
20. Ernsberger U, Rohrer H (1988) Neuronal precursor cells in chick dorsal root ganglia differentiation and survival in vitro. Dev Biol 126420-432.
21. Feig LA, Cooper GM (1988) Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol Cell Biol 83235-3243.
22. FradeJM, Rodriguez-Tebar A, Barde YA (1996) Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 383166-168.
23. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, Kaplan DR, Tsichlis PN (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activatcd phosphatidylinositol 3-kinase. Cell 81727-736.
24. Garcia 1, Martinou I, Tsujimoto Y, Martinou J-C (1997) Prevention of programmed cell death of sympathetic neurons by the bd-2 protooncogene. Science 258302-304.
25. Gomez-Foix AM, Coats WS, Baquc S, Alam T, Gérard RD, Ncwgard CB (1992) Adenovirus-mediated transfer of the muscle glycogen phosphorylasc gene into hepatocytes confers altered regulation of glycogen metabolism. J Biol Chem 26725129-25134.
26. Greene LA (1978) Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PCI 2 pheochromocytoma cells in serum-free medium. J Cell Biol 78747-755.
27. Guo HF, The I, Hannan F, Bernards A, Zhong Y (1997) Requirement of Drosophila NF1 for activation of adenylyl cyclase by PACAP38-like neuropeptides. Science 276795-798.
28. Hagag N, Halegoua S, Viola M (1986) Inhibition of growth factorinduced differentiation of PC12 cells by microinjection of antibody to ras p21. Nature 319680-682.
29. 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 14927-939.
30. Heidecker G, Huleihel M, Cleveland JL, Kolch W, Beck TW, Lloyd P, Pawson T, Rapp UR (1990) Mutational activation of c-raf-1 and definition of the minimal transforming sequence. Mol Cell Biol 102503-2512.
31. Jackson TR, Blader IJ, Hammonds-Odie LP, Burga CR, Cooke F, Hawkins PT, Wolf AG, Heldman KA, Theibert AB (1996) Initiation and maintenance of NGF-stimulated neurite outgrowth requires activation of a phosphoinositide 3-kinase. J Cell Sei 109289-300.
32. Johnson MR, DeClue JE, Felzmann S, Vass WC, Xu G, White R, Lowy DR (1994) Neurofibromin can inhibit Ras-dependent growth by a mechanism independent of its GTPase-accelerating function. Mol Cell Biol 14641-645.
33. Kaplan DR, Miller FD (1997) Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol 9213-221.
34. Kaplan DR, Stephens RM (1994) Neurotrophin signal transduction by the Trk receptor. J Neurobiol 251404-1417.
35. Kimura K, Hattori S, Kabuyama Y, Shizawa Y, Takayanagi J, Nakamura S, Toki S, Matsuda Y, Onodera K, Fukui Y (1994) Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J Biol Chem 26918961-18967.
36. Klesse LJ, Meyers KA, Marshall CJ, Parada LF (1998) Nerve growth factor induces survival and differentiation through two distinct signaling cascades in PC12 cells. Oncogene, in press.
37. KorsmeyerSJ (1995) Regulators of cell death. Trends Genet 11101-105.
38. Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN (1993) Bcl2/Bax a rheostat that regulates an anti-oxidant pathway and cell death. Semin Cancer Biol 4327-332.
39. Nobes CD, Tolkovsky AM (1995) Neutralizing anti-p21ras Fabs suppress rat sympathetic neuron survival induced by NGF, LIF, CNTF and cAMP. Eur J Neurosci 7344-350.
40. Nobes CD, Reppas JB, Markus A, Tolkovsky AM (1996) Active p21 Ras is sufficient for rescue of NGF-dependent rat sympathetic neurons. Neuroscience 701067-1079.
41. Robbins DJ, Zhen E, Owaki H, Vanderbilt CA, Ebert D, Geppert TD, Cobb MH (1993) Regulation and properties of extracellular signalregulated protein kinases 1 and 2 in vitro. 3 Biol Chem 2685097-5106.
42. Rodriguez-Viciana P, Warne PH, Dhand R, Vanhaesebroeck B, Gout I, Fry MJ, Waterfield MD, Downward J (1994) Phosphatidylinositol3-OH kinase as a direct target of Ras. Nature 370527-532.
43. Rodriguez-Viciana P, Warne PH, Vanhaesebroeck B, Waterfield MD, Downward J (1996) Activation of phosphoinositide 3-kinase by interaction with Ras and by point mutation. EMBO J 152442-2451.
44. Segal RA, Greenberg ME (1996) Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 19463-489.
45. Snider WD, Silos-Santiago I (1996) Dorsal root ganglion neurons require functional neurotrophin receptors for survival during development. Philos Trans R Soc Lond B Biol Sei 351395-403.
46. Szeberenyi J, Cai H, Cooper GM (1990) Effect of a dominant inhibitory Ha-ras mutation on neuronal differentiation of PC12 cells. Mol Cell Biol 105324-5332.
47. Tabin CJ, Bradley SM, Bargmann CI, Weinberg RA, Papageorge AG, Scolnick EM, Dhar R, Lowy DR, Chang EH (1982) Mechanism of activation of a human oncogene. Nature 300143-149.
48. The I, Hannigan GE, Cowley GS, Reginald S, Zhong Y, Gusella if, Hariharan IK, Bernards A (1997) Rescue of a Drosophlla NF1 mutant phenotype by protein kinase A. Science 276791-794.
49. Tischler AS, Greene LA (1975) Nerve growth factor-induced process formation by cultured rat pheochromocytoma cells. Nature 258341-342.
50. Virdee K, Tolkovsky AM (1996) Inhibition of p42 and p44 mitogenactivated protein kinase activity by PD98059 does not suppress nerve growth factor-induced survival of sympathetic neurones. J Neurochem 671801-1805.
51. 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 82733-742.
52. Wood KW, Qi H, D'Arcangelo G, Armstrong RC, Roberts TM, Halegoua S (1993) The cytoplasmic raf oncogene induces a neuronal phenotype in PC12 cells a potential role for cellular raf kinases in neuronal growth factor signal transduction. Proc Natl Acad Sei USA 905016-5020.
53. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 2701326-1331.
54. Xu GF, Lin B, Tanaka K, Dünn D, Wood D, Gesteland R, White R, Weiss R, Tamanoi F (1990) The catalytic domain of the neurofibromatosis type 1 gene product stimulates ras GTPase and complements ira mutants of S. cerevisiae. Cell 63835-841.
55. Yang E, Zha J, Jockei J, Boise LH, Thompson CB, Korsmeyer SJ (1995) Bad, a heterodimeric partner for Bel-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80285-291.
56. Yao R, Cooper GM (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 2672003-2006.
57. York RD, Yao H, Dillon T, Ellig CL, Eckert SP, McCleskey EW, Stork PJS (1998) Rapl mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392622-626.
58. Zha J, Harada H, Yang E, Jockei J, Korsmeyer SJ (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87619-628.
59. Zhang XF, Settleman J, Kyriakis JM, Takeuchi-Suzuki E, Elledge SJ, Marshall MS, Bruder JT, Rapp UR, Avruch J (1993) Normal and oncogenic p21ras proteins bind to the amino-terminal regulatory domain of c-Raf-1. Nature 364308-313.