Involvement of phosphatidylinositol-3 kinase in prevention of low K+- induced apoptosis of cerebellar granule neurons

Developmental Brain Research

Volumn 101, Issue 1-2, 1997, Pages 197-206

  Shimoke, Koji ^a   Kubo, Takekazu ^a   Numakawa, Tadahiro ^a   Abiru, Yasuhiro ^a   Enokido, Yasushi ^a   Takei, Nobuyuki ^b   Ikeuchi, Toshihiko ^a   Hatanaka, Hiroshi ^a  

^a BIOMOL ENG RESEARCH INSTITUTE   (Japan)

^b KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Apoptosis; Brain derived neurotrophic factor (BDNF); Ca2+ influx; High potassium; TrkB; Wortmannin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; POTASSIUM ION; WORTMANNIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CEREBELLUM; CONTROLLED STUDY; ENZYME ACTIVITY; ETIOLOGY; GRANULE CELL; NERVE CELL DEGENERATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; APOPTOSIS; BISBENZIMIDE; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; COLORING AGENTS; IMMUNOHISTOCHEMISTRY; NEURONS; PHOSPHODIESTERASE INHIBITORS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); POTASSIUM; RATS;

ANIMALIA;

EID: 0030753359     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-3806(97)00065-5     Document Type: Article

References (56)

1. Backer J.M., Myers M.G. Jr., Shoelson S.E., Chin D.J., Sun X.J., Miralpeix M., Hu P., Margolis B., Skolnik E.Y., Schlessinger J., White M.F. Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11:1992;3469-3479.
2. Barde Y.-A. Trophic factors and neuronal survival. Neuron. 2:1989;1525-1534.
3. Berkemeier L.R., Winslow J.W., Kaplan D.R., Nikolics K., Goeddel D.V., Rosenthal A. Neurotrophin-5: a novel neurotrophic factor that activates Trk and TrkB. Neuron. 7:1991;857-866.
4. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature. 361:1993;315-325.
5. Chao M.V. Growth factors signaling: where is the specificity? Cell. 68:1992;995-997.
6. S6K activation mediated by phosphatidylinositol-3-OH kinase. Nature. 370:1994;71-75.
7. Di Stefano P.S., Friedman B., Radziejewski C., Alexander C., Boland P., Schick C.M., Lindsay R.M., Wiegand S.J. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron. 8:1992;983-993.
8. D'Mello S.R., Galli C., Ciotti T., Calissano P. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc. Natl. Acad. Sci. (USA). 90:1993;10989-10993.
9. Fandl J.P., Tobkes N.J., McDonald N.Q., Hendrickson W.A., Ryan T.E., Nigam S., Acheson A., Cudny H., Panayotatos N. Characterization and crystallization of recombinant human neurotrophin-4. J. Biol. Chem. 269:1994;755-759.
10. Franke T.F., Yang S., Chan T.O., Datta K., Kazlauskas A., Morrison D.K., Kaplan D.R., Tsichlis P.N. The protein kinase encoded by the Akt protooncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell. 81:1995;727-736.
11. Franklin J.L., Johnson E.M. Jr. Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. Trends Neurosci. 15:1992;501-508.
12. Gallo V., Kinsbury A., Balazs R., Jorgensen R.O. The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci. 7:1987;2203-2213.
13. Ghosh A., Carnahan J., Greenberg M.E. Requirement for BDNF in activity-dependent survival of cortical neurons. Science. 263:1994;1618-1623.
14. Glass D.J., Yancopoulos G.D. The neurotrophins and their receptors. Trends Cell Biol. 3:1993;262-268.
15. Gotz R., Koster R., Winkler C., Raulf F., Lottspeich F., Schartl M., Thoenen H. Neurotrophin-6 is a new member of the nerve growth factor family. Nature. 372:1994;266-269.
16. Hallbook F., Ibanez C.F., Persson H. Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron. 6:1991;845-858.
17. Hansen M.B., Nielsen S.E., Berg K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Meth. 119:1989;203-210.
18. E. Harlow, D. Lane, Antibodies, Cold Spring Harbor Laboratory, Cold Spring Habor, NY, 1988, pp. 310.
19. Hatanaka H., Tsukui H., Nihonmatsu I. Developmental change in the nerve growth factor action from induction of choline acetyltransferase to promotion of cell survival in cultured basal forebrain cholinergic neurons from postnatal rats. Dev. Brain Res. 39:1988;85-95.
20. Hohn A., Leibrock J., Bailey K., Barde Y.-A. Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature. 344:1990;339-341.
21. Hu P., Margolis B., Skolnik E.Y., Lammers R., Ullrich A., Schlessinger J. Interaction of phosphatidylinositol 3-kinase-associated p85 with epidermal growth factor and platelet-derived growth factor receptors. Mol. Cell. Biol. 12:1992;981-990.
22. Ip N.Y., Ibanez C.F., Nye S.H., McClain J., Jones P.F., Gies D.R., Belluscio L., Beau M.M., Espinoza R., Squinto S.P., Persson H., Yancopoulos G.D. Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution and receptor specificity. Proc. Natl. Acad. Sci. (USA). 89:1992;3060-3064.
23. Kim U.-H., Fink D., Kim H.S., Park D.J., Contreras M.L., Guroff G., Rhee S.G. Nerve growth factor stimulates phosphorylation of phospholipase C-γ in PC12 cells. J. Biol. Chem. 266:1991;1359-1362.
24. Kimura K., Hattori S., Kabuyama Y., Shizawa Y., Takayanagi J., Nakamura S., Toki S., Matsuda Y., Onodera K., Fukui Y. Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J. Biol. Chem. 269:1994;18961-18967.
25. 2+ determine nerve growth factor dependence of sympathetic ganglion cells. Proc. Natl. Acad. Sci. (USA). 86:1989;6421-6425.
26. Kubo T., Nonomura T., Enokido Y., Hatanaka H. Brain-derived neurotrophic factor (BDNF) can prevent apoptosis of rat cerebellar granule neurons in culture. Dev. Brain Res. 85:1995;249-258.
27. Lasher R.S., Zagon I.S. The effect of potassium on neuronal differentiation in cultures of dissociated newborn rat cerebellum. Brain Res. 41:1972;482-488.
28. 2+-induced regulation of ion channel and MAP kinase functions. Nature. 376:1995;737-745.
29. Levi G., Aloisi F., Ciotti M.T., Gallo V. Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating cerebellar granule cell cultures. Brain Res. 290:1984;77-86.
30. Levi-Montalcini R. The nerve growth factor: thirty-five years later. EMBO J. 6:1987;1145-1154.
31. Lindholm D., Dechant G., Heisenberg C.-P., Thoenen H. Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. Eur. J. Neurosci. 5:1993;1455-1464.
32. R.M. Lindsay, Brain-derived neurotrophic factor: an NGF-related neurotrophin, in: J.A. Fallon, S.E. Loughlin (Eds.), Neurotrophic Factors, Academic Press, New York, pp. 257-284.
33. Lindsay R.M., Wiegand S.J., Altar C.A., Di Stefano P.S. Neurotrophic factors: from molecule to man. Trends Neurosci. 17:1994;182-190.
34. Maisonpierre P.C., Belluscio L., Squinto S., Ip N.Y., Furth M.E., Lindsay R.M., Yancopoulos G.D. Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science. 247:1990;1446-1451.
35. Merlio J.P., Ernfors P., Jaber M., Persson H. Molecular cloning of rat TrkC and distribution of cells expressing messenger RNAs for members of the Trk family in the rat central nervous system. Neuroscience. 51:1992;513-532.
36. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Meth. 65:1983;55-63.
37. Nakanishi H., Brewer A.K., Exton H.J. Activation of the isozyme of protein kinase C by phosphatidylinositol 3,4,5-triphosphate. J. Biol. Chem. 268:1993;13-16.
38. Carter N.A., Downes P.C. Phosphatidylinositol 3-kinase is activated by nerve growth factor and epidermal growth factor in PC12 cells. J. Biol. Chem. 267:1992;14563-14567.
39. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature. 334:1988;661-665.
40. Nonomura T., Kubo T., Oka T., Shimoke K., Yamada M., Enokido Y., Hatanaka H. Signaling pathway and survival effects of BDNF and NT-3 on cultured cerebellar granule cells. Dev. Brain Res. 97:1996;43-50.
41. Ohmichi M., Decker S.J., Saltiel A.R. Activation of phosphatidylinositol-3 kinase by nerve growth factor involves indirect coupling of the Trk proto-oncogene with src homology 2 domain. Neuron. 9:1992;769-777.
42. Okada T., Sakuma L., Fukui Y., Hazeki O., Ui M. Blockage of chemotactic peptide-induced stimulation of neutrophils by wortmannin as a result of selective inhibition of phosphatidylinositol 3-kinase. J. Biol. Chem. 269:1994;3563-3567.
43. Oppenheim R.W. Cell death during development of the nervous system. Annu. Rev. Neurosci. 14:1991;453-501.
44. 3 interacts with SH2 domains and modulates PI 3-kinase association with tyrosine-phosphorylated proteins. Cell. 83:1995;821-830.
45. Rodriguez-Viciana P., Warne P.H., Dhand R., Vanhaesebroeck B., Gout I., Fry M.J., Waterfield M.D., Downward J. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature. 370:1994;527-532.
46. Rosen L.B., Ginty D.D., Weber M.J., Greenberg M.E. Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron. 12:1994;1207-1221.
47. Rosenthal A., Goeddel D.V., Nguyen T., Lewis M., Shih A., Laramee G.R., Nikolics K., Winslow J.W. Primary structure and biological activity of a novel human neurotrophic factor. Neuron. 4:1990;767-773.
48. Rozakis-Adcock K., McGlade J., Mbamalu G., Pelicci G., Daly R., Li W., Batzer A., Thomas S., Brugge J., Pelicci P.G., Schlessinger J., Pawson T. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature. 360:1992;689-692.
49. Soltoff S.P., Rabin S.L., Cantley L.C., Kaplan D.R. Nerve growth factor promotes the activation of phosphatidylinositol 3-kinase and its association with the Trk tyrosine kinase. J. Biol. Chem. 267:1992;17472-17477.
50. Thoenen H., Barde Y.-A. Physiology of nerve growth factor. Physiol. Rev. 60:1980;1284-1335.
51. Thoenen H. The changing scene of neurotrophic factors. Trends Neurosci. 14:1991;165-170.
52. 3. J. Biol. Chem. 269:1994;32358-32367.
53. Vetter M.L., Martin-Zanca D., Parada L.F., Bishop J.M., Kaplan D.R. NGF rapidly stimulates tyrosine phosphorylation of phospholipase C-γ 1 by a kinase activity associated with the product of the trk proto-oncogene. Proc. Natl. Acad. Sci. (USA). 88:1991;5650-5654.
54. Yano H., Nakanishi S., Kimura K., Hanai N., Saitoh Y., Fukui Y., Nonomura Y., Matsuda Y. Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268:1993;25846-25856.
55. Yao R., Cooper G.M. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science. 267:1995;2003-2006.
56. Zirrgiebel U., Ohga Y., Carter B., Berninger B., Inagaki N., Thoenen H., Lindholm D. Characterization of TrkB receptor-mediated signaling pathways in rat cerebellar granule neurons: involvement of protein kinase C in neuronal survival. J. Neurochem. 65:1995;2241-2250.