Activated phosphatidylinositol 3-kinase and Akt kinase promote survival of superior cervical neurons

Journal of Cell Biology

Volumn 139, Issue 3, 1997, Pages 809-815

  Philpott, Karen L ^a   McCarthy, Mary Jane ^a   Klippel, Anke ^b   Rubin, Lee L ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CELL DEATH; CELL STIMULATION; CELL SURVIVAL; DIMERIZATION; EFFECTOR CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; SUPERIOR CERVICAL GANGLION; SYMPATHETIC NERVE CELL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL DEATH; CELL SURVIVAL; ENZYME ACTIVATION; NERVE GROWTH FACTORS; NEURONS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-JUN; RATS; SUPERIOR CERVICAL GANGLION;

EID: 0030694175     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.3.809     Document Type: Article

References (65)

1. Ahmed, N.N., T.F. Franke, A. Bellacosa, K. Datta, M.E. Gonzalez-Portal, T. Taguchi, J.R. Testa, and P.N. Tsichlis. 1993. The proteins encoded by c-akt and v-akt differ in post-translational modification, subcellular localization and oncogenic potential. Oncogene. 8:1957-1963.
2. Bellacosa, A., J.R. Testa, S.P. Staal, and P.N. Tsichlis. 1991. A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science (Wash. DC). 254:274-277.
3. Borasio, G.D., J. John, A. Wittinghofer, Y.A. Barde, M. Sendtner, and R. Heumann. 1989. ras p21 protein promotes survival and fiber outgrowth of cultured embryonic neurons. Neuron. 2:1087-1096.
4. Borasio, G.D., A. Markus, A. Wittinghofer, Y.A. Barde, and R. Heumann. 1993. Involvement of ras p21 in neurotrophin-induced response of sensory, but not sympathetic neurons. J. Cell Biol. 121:665-672.
5. Burgering, B.M., and P.J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature (Lond.). 376:599-602.
6. Carpenter, C.L., and L.C. Cantley. 1996. Phosphoinositide kinases. Curr. Opin. Cell Biol. 8:153-158.
7. Carter, A.N., and C.P. Downes. 1995. Molecular mechanisms of regulation of phosphoinositide 3-kinase by insulin, insulin-like growth factor I and nerve growth factor in PC12 cells. Biochem. Soc. Trans. 23:148-152.
8. Choi, D.W. 1996. Ischemia-induced neuronal apoptosis. Curr. Opin. Neurobiol. 6:667-672.
9. Chou, M.M., and J. Blenis. 1995. The 70-kD S6 kinase: regulation of a kinase with multiple roles in mitogenic signalling. Curr. Opin. Cell Biol. 7:806-814.
10. Chung, J., C.J. Kuo, G.R. Crabtree, and J. Blenis. 1992. Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kd S6 protein kinases. Cell. 69:1227-1236.
11. Coffer, P.J., and J.R. Woodgett. 1991. Molecular cloning and characterisation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families. Eur. J. Biochem. 201:475-481.
12. Deckwerth, T.L., and E.M. Johnson. 1993. Neurotrophic factor deprivation-induced death. Ann. NY Acad. Sci. 679:121-131.
13. Downward, J. 1994. Signal transduction. Regulating S6 kinase. Nature (Lond.). 371:378-379.
14. Dudek, H., S.R. Datta, T.F. Franke, M.J. Birnbaum, R. Yao, G.M. Cooper, R.A. Segal, D.R. Kaplan, and M.E. Greenberg. 1997. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science (Wash. DC). 275:661-665.
15. L. J. Biol. Chem. 271:17601-17604.
16. Estus, S., W.J. Zaks, R.S. Freeman, M. Gruda, R. Bravo, and E.M. Johnson. 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.
17. Fantl, W.J., D.E. Johnson, and L.T. Williams. 1993. Signaling by receptor tyrosine kinases. Annu. Rev. Biochem. 62:453-481.
18. Franke, T.F., S.I. Yang, T.O. Chan, K. Datta, A. Kazlauskas, D.K. Morrison, D.R. Kaplan, and P.N. Tsichlis. 1995. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell. 81:727-736.
19. Franke, T.F., D.R. Kaplan, L.C. Cantley, and A. Toker. 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-biphosphate. Science (Wash. DC). 275:665-668.
20. Garcia, I., I. Martinou, Y. Tsujimoto, and J.C. Martinou. 1992. Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. Science (Wash. DC). 258:302-304.
21. Ham, J., C. Babij, J. Whitfield, C.M. Pfarr, D. Lallemand, M. Yaniv, and L.L. Rubin. 1995. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron. 14:927-939.
22. Hara, K., K. Yonezawa, H. Sakaue, A. Ando, K. Kotani, T. Kitamura, Y. Kitamura, H. Ueda, L. Stephens, T.R. Jackson et al., 1994. 1-Phosphatidylinositol 3-kinase activity is required for insulin-stimulated glucose transport but not for RAS activation in CHO cells. Proc. Natl. Acad. Sci. USA. 91:7415-7419.
23. Hawrot, E., and P.H. Patterson. 1979. Long-term culture of dissociated sympathetic neurons. Methods Enzymol. 58:574-584.
24. Hu, Q., A. Klippel, A.J. Muslin, W.J. Fantl, and L.T. Williams. 1995. Ras-dependent induction of cellular responses by constitutively active phosphatidvlinositol-3 kinase. Science (Wash. DC). 268:100-102.
25. Jackson, T.R., I.J. Blader, L.P. Hammonds-Odie, C.R. Burga, F. Cooke, P.T. Hawkins, A.G. Wolf, K.A. Heldman, and A.B. Theibert. 1996. Initiation and maintenance of NGF-stimulated neurite outgrowth requires activation of a phosphoinositide 3-kinase. J. Cell Sci. 109:289-300.
26. Jing, S., P. Tapley, and M. Barbacid. 1992. Nerve growth factor mediates signal transduction through trk homodimer receptors. Neuron. 9:1067-1079.
27. Jones, P.F., T. Jakubowicz, F.J. Pitossi, F. Maurer, and B.A. Hemmings. 1991. Molecular cloning and identification of a serine/threonine protein kinase of the second-messenger subfamily. Proc. Natl. Acad. Sci. USA. 88:4171-4175.
28. Kaplan, D.R., and R.M. Stephens. 1994. Neurotrophin signal transduction by the Trk receptor. J. Neurobiol. 25:1404-1417.
29. Kauffmann-Zeh, A., P. Rodriguez-Viciana, E. Ulrich, C. Gilbert, P. Coffer, J. Downward, and G. Evan. 1997. Suppression of c-Myc-induced apoptosis by Ras signaling through PI(3)K and PKB. Nature (Lond.). 385:544-548.
30. Kido, Y., Y. Okabayashi, T. Okutani, Y. Sugimoto, K. Sakaguchi, and M. Kasuga. 1995. EGF-induced activation of 70-kDa S6 kinase in CHO cells expressing human EGF receptors. Biochem. Biophys. Res. Commun. 209:131-138.
31. Kimura, K., S. Hattori, Y. Kabuyama, Y. Shizawa, J. Takayanagi, S. Nakamura, S. Toki, Y. Matsuda, K. Onodera, and Y. Fukui. 1994. Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J. Biol. Chem. 269:18961-18967.
32. Klippel, A., J.A. Escobedo, Q.Hu, and L.T. Williams. 1993. A region of the 85-kilodalton (kDa) subunit of phosphatidylinositol 3-kinase binds the 110-kDa catalytic subunit in vivo. Mol. Cell. Biol. 13:5560-5566.
33. Klippel, A., W.M. Kavanaugh, D. Pot, and L.T. Williams. 1997. A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17:338-344.
34. Koch, C.A., D. Anderson, M.F. Moran, C. Ellis, and T. Pawson. 1991. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science (Wash. DC). 252:668-674.
35. Kulik, G., Klippel, A., and Weber, M.J. 1997. Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol. Cell. Biol. 17:1595-1606.
36. Miller, T.M., Tansey, M.G., Johnson, E.M., and Creedon, D.J. 1997. Inhibition of phosphatidylinositol 3-kinase activity blocks depolarization and insulin-like growth factor I-mediated survival of cerebellar granule cells. J. Biol. Chem. 272:9847-9853.
37. Minshall, C., S. Arkins, G.G. Freund, and K.W. Kelley. 1996. Requirement for phosphatidylinositol 3′-kinase to protect hemopoietic progenitors against apoptosis depends upon the extracellular survival factor. J. Immunol. 156: 939-947.
38. Nicholson, D.W. 1996. ICE/CED3-like proteases as therapeutic targets for the control of inappropriate apoptosis. Nat. Biol. 14:297-301.
39. Nobes, C.D., and A.M. Tolkovsky. 1995. Neutralizing anti-p21ras Fabs suppress rat sympathetic neuron survival induced by NGF, LIF, CNTF and cAMP. Eur. J. Neurosci. 7:344-350.
40. Nobes, C.D., J.B. Reppas, A. Markus, and A.M. Tolkovsky. 1996. Active p21Ras is sufficient for rescue of NGF-dependent rat sympathetic neurons. Neuroscience. 70:1067-1079.
41. Obermeier, A., R. Lammers, K.H. Wiesmuller, G. Jung, J. Schlessinger, and A. Ullrich. 1993. Identification of Trk binding sites for SHC and phosphatidylinositol 3′-kinase and formation of a multimeric signaling complex. J. Biol. Chem. 268:22963-22966.
42. Obermeier, A., R.A. Bradshaw, K. Seedorf, A. Choidas, J. Schlessinger, and A. Ullrich. 1994. Neuronal differentiation signals are controlled by nerve growth factor receptor/Trk binding sites for SHC and PLC γ. EMBO (Eur. Mol. Biol. Organ.) J. 13:1585-1590.
43. Okada, T., L. Sakuma, Y. Fukui, O. Hazeki, and M. Ui. 1994. Blockage of chemotactic peptide-induced stimulation of neutrophils by wortmannin as a result of selective inhibition of phosphatidylinositol 3-kinase. J. Biol. Chem. 269:3563-3567.
44. Oppenheim, R.W. 1991. Cell death during development of the nervous system. Annu. Rev. Neurosci. 14:453-501.
45. Park, E.K., S.I. Yang, and S.S. Kang. 1996. Activation of Akt by nerve growth factor via phosphatidylinositol-3 kinase in PC12 pheochromocytoma cells. Mol. Cells. 6:494-498.
46. Price, D.J., J.R. Grove, V. Calvo, J. Avruch, and B.E. Bierer. 1992. Rapamycin-induced inhibition of the 70-kilodalton S6 protein kinase. Science (Wash. DC). 257:973-977.
47. Rukenstein, A., R.E. Rydel, and L.A. Greene. 1991. Multiple agents rescue PC12 cells from serum-free cell death by translation- and transcription-independent mechanisms. J. Neurosci. 11:2552-2563.
48. Scheid, M.P., R.W. Lauener, and V. Duronio. 1995. Role of phosphatidylinositol 3-OH-kinase activity in the inhibition of apoptosis in haemopoietic cells: phosphatidylinositol 3-OH-kinase inhibitors reveal a difference in signalling between interleukin-3 and granulocyte-macrophage colony stimulating factor. Biochem. J. 312:159-162.
49. Segal, R.A., and M.E. Greenberg. 1996. Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19:463-489.
50. Serve, H., N.S. Yee, G. Stella, L. Sepp-Lorenzino, J.C. Tan, and P. Besmer. 1995. Differential roles of PI3-kinase and Kit tyrosine 821 in Kit receptor-mediated proliferation, survival and cell adhesion in mast cells. EMBO (Eur. Mol. Biol. Organ.) J. 14:473-483.
51. Smeal, T., B. Binetruy, D.A. Mercola, M. Birrer, and M. Karin. 1991. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature (Lond.). 354:494-496.
52. Soltoff, S.P., S.L. Rabin, L.C. Cantley, and D.R. Kaplan. 1992. Nerve growth factor promotes the activation of phosphatidylinositol 3-kinase and its association with the trk tyrosine kinase. J. Biol. Chem. 267:17472-17477.
53. Stephens, R.M., D.M. Loeb, T.D. Copeland, T. Pawson, L.A. Greene, and D.R. Kaplan. 1994. Trk receptors use redundant signal transduction pathways involving SHC and PLC-γ 1 to mediate NGF responses. Neuron. 12:691-705.
54. Thompson, C.B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science (Lond.). 267:1456-1462.
55. Vemuri, G.S., and F.A. McMorris. 1996. Oligodendrocytes and their precursors require phosphatidylinositol 3-kinase signaling for survival. Development. 122:2529-2537.
56. Virdee, K., and A.M. Tolkovsky. 1996. Inhibition of p42 and p44 mitogen-activated protein kinase activity by PD98059 does not suppress nerve growth factor-induced survival of sympathetic neurones. J. Neurochem. 67:1801-1805.
57. Vlahos, C.J., W.F. Matter, K.Y. Hui, and R.F. Brown. 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-1 (LY294002). J. Biol. Chem. 269:5241-5248.
58. Welsh, G.I., C. Wilson, and C.G. Proud. 1996. GSK3: a SHAGGY frog story. Trends Cell Biol. 6:274-279.
59. Weng, Q.P., K. Andrabi, M.T. Kozlowski, J.R. Grove, and J. Avruch. 1995. Multiple independent inputs are required for activation of the p70 S6 kinase. Mol. Cell. Biol. 15:2333-2340.
60. Weng, G., M.A. Markus, A. Markus, A. Winkler, and G.D. Borasio. 1996. p21ras supports the survival of chick embryonic motor neurones. Neuroreport. 7:1077-1081.
61. Wood, K.W., and T.M. Roberts. 1993. Oncogenes and protein kinases in neuronal growth-factor action. Biochim. Biophys. Acta. 1155:133-150.
62. Yano, H., S. Nakanishi, K. Kimura, N. Hanai, Y. Saitoh, Y. Fukui, Y. Nonomura, and Y. Matsuda. 1993. Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268:25846-25856.
63. Yao, R., and G.M. Cooper. 1995. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science (Wash. DC). 267:2003-2006.
64. Yao, R., and G.M. Cooper. 1996. Growth factor-dependent survival of rodent fibroblasts requires phosphatidylinositol 3-kinase but is independent of pp70S6K activity. Oncogene. 13:343-351.
65. Xia, Z., M. Dickens, J. Raingeaud, R.J. Davis, and M.E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science (Wash. DC). 270:1326-1331.