Comparative signaling pathways of insulin-like growth factor-1 and brain-derived neurotrophic factor in hippocampal neurons and the role of the PI3 kinase pathway in cell survival

Journal of Neurochemistry

Volumn 89, Issue 4, 2004, Pages 844-852

  Zheng, Wen Hua ^a   Quirion, Rémi ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Akt; BDNF; Hippocampal neurons; IGF 1; MAPK

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; BRAIN DERIVED NEUROTROPHIC FACTOR; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; PROTEIN SHC; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHR; AKT1 PROTEIN, RAT; ENZYME INHIBITOR; INSULIN RECEPTOR SUBSTRATE 1 PROTEIN; INSULIN RECEPTOR SUBSTRATE-1 PROTEIN; ONCOPROTEIN; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SRC HOMOLOGY 2 DOMAIN CONTAINING, TRANSFORMING PROTEIN 1; SRC HOMOLOGY 2 DOMAIN-CONTAINING, TRANSFORMING PROTEIN 1; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL ASSAY; CELL DEATH; CELL FUNCTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DEPLETION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SERUM; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECT; METABOLISM; NERVE CELL; PHOSPHORYLATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; ENZYME INHIBITORS; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR I; NEURONS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 2542473205     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02350.x     Document Type: Article

References (44)

1. Alessi D. R., Andjelkovic M., Caudwell B., Cron P., Morrice N., Cohen P. and Hemmings B. A. (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15, 6541-6551.
2. Arsenijevic Y. and Weiss S. (1998) Insulin-like growth factor-I is a differentiation factor for post-mitotic CNS stem cell-derived neuronal precursors: distinct actions from those of brain-derived neurotrophic factor. J. Neurosci. 18, 2118-2128.
3. Balendran A., Casamayor A., Deak M., Paterson A., Gaffney P., Currie R., Downes C. P. and Alessi D. R. (1999) PDK1 acquires PDK2 activity in the presence of a synthetic peptide derived from the carboxyl terminus of PRK2. Curr. Biol. 9, 393-404.
4. Barbacid M. (1995) Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 7, 148-155.
5. Bonfini L., Migliaccio E., Pelicci G., Lanfrancone L. and Pelicci P. G. (1996) Not all Shc's roads lead to Ras. Trends Biochem. Sci. 21, 257-261.
6. Bonni A., Brunet A., West A. E., Datta S. R., Takasu M. A. and Greenberg M. E. (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286, 1358-1362.
7. Brunet A., Bonni A., Zigmond M. J. et al. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868.
8. Bruning J. C., Winnay J., Cheatham B. and Kahn C. R. (1997) Differential signaling by insulin receptor substrate 1 (IRS-1) and IRS-2 in IRS-1-deficient cells. Mol. Cell. Biol. 17, 1513-1521.
9. Butler A. A., Yakar S., Gewolb I. H., Karas M., Okubo Y. and LeRoith D. (1998) Insulin-like growth factor-I receptor signal transduction: at the interface between physiology and cell biology. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 121, 19-26.
10. Cardone M. H., Roy N., Stennicke H. R., Salvesen G. S., Franke T. F., Stanbridge E., Frisch S. and Reed J. C. (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282, 1318-1321.
11. Connor B. and Dragunow M. (1998) The role of neuronal growth factors in neurodegenerative disorders of the human brain. Brain Res. Brain Res. Rev. 27, 1-39.
12. Crowder R. and Freeman R. (1999) The survival of sympathetic neurons promoted by potassium depolarization, but not by cyclic AMP, requires phosphatidylinositol 3-kinase and Akt. J. Neurochem. 73, 466-475.
13. Datta S. R., Brunet A. and Greenberg M. E. (1999) Cellular survival: a play in three Akts. Genes Dev. 13, 2905-2927.
14. Delcommenne M., Tan C., Gray V., Rue L., Woodgett J. and Dedhar S. (1998) Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc. Natl Acad. Sci. USA 95, 11211-11216.
15. Dolcet X., Egea J., Soler R., Martn-Zanca D. and Comella J. (1999) Activation of phosphatidylinositol 3-kinase, but not extracellular-regulated kinases, is necessary to mediate brain-derived neurotrophic factor-induced motoneuron survival. J. Neurochem. 73, 521-531.
16. Dore S., Kar S. and Quirion R. (1997) Insulin-like growth factor I protects and rescues hippocampal neurons against β-amyloid- and human amylin-induced toxicity. Proc. Natl Acad. Sci. USA 94, 4772-4777.
17. Dudek H., Datta S. R., Franke T. F., Birnbaum M. J., Yao R., Cooper G. M., Segal R. A., Kaplan D. R. and Greenberg M. E. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275, 661-665.
18. Fernandez-Sanchez M. T., Garcia-Rodriguez A., Diaz-Trelles R. and Novelli A. (1996) Inhibition of protein phosphatases induces IGF-1-blocked neurotrophin-insensitive neuronal apoptosis. FEBS Lett. 398, 106-112.
19. Guo S., Rena G., Cichy S., He X., Cohen P. and Unterman T. (1999) Phosphorylation of serine 256 by protein kinase B disrupts trans-activation by FKHR and mediates effects of insulin on insulin-like growth factor-binding protein-1 promoter activity through a conserved insulin response sequence. J. Biol. Chem. 274, 17184-17192.
20. Jones D., Tucker B. A., Rahimtula M. and Mearow K. M. (2003) The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: convergence on the PI 3-kinase signaling pathway. J. Neurochem. 86, 1116-1128.
21. Kaplan D. R. and Miller F. D. (2000) Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391.
22. Kim A. H., Khursigara G., Sun X., Franke T. F. and Chao M. V. (2001) Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol. Cell Biol. 21, 893-901.
23. Kitamura T., Ogawa W., Sakaue H. et al. (1998) Requirement for activation of the serine-threonine kinase Akt (protein kinase B) in insulin stimulation of protein synthesis but not of glucose transport. Mol. Cell Biol. 18, 3708-3717.
24. Klein R., Parada L. F., Coulier F. and Barbacid M. (1989) trkB, a novel tyrosine protein kinase receptor expressed during mouse neural development. EMBO J. 8, 3701-3709.
25. Kops G. J., de Ruiter N. D., Vries-Smits A. M., Powell D. R., Bos J. L. and Burgering B. M. (1999) Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398, 630-634.
26. LeRoith D., Werner H., Beitner-Johnson D. and Roberts C. T. Jr (1995) Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr. Rev. 16, 143-163.
27. Lindholm D., Carroll P., Tzimagiogis G. and Thoenen H. (1996) Autocrine-paracrine regulation of hippocampal neuron survival by IGF-1 and the neurotrophins BDNF, NT-3 and NT-4. Eur. J. Neurosci. 8, 1452-1460.
28. Myers M. G., Sun X. J., Cheatham B., Jachna B. R., Glasheen E. M., Backer J. M. and White M. F. (1993) IRS-1 is a common element in insulin and insulin-like growth factor-I signaling to the phosphatidylinositol 3′-kinase. Endocrinology 132, 1421-1430.
29. del Peso L., Gonzalez-Garcia M., Page C., Herrera R. and Nunez G. (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278, 687-689.
30. Ricketts W. A., Rose D. W., Shoelson S. and Olefsky J. M. (1996) Functional roles of the Shc phosphotyrosine binding and Src homology 2 domains in insulin and epidermal growth factor signaling. J. Biol. Chem. 27, 26165-261659.
31. Sasaoka T., Rose D. W., Jhun B. H., Saltiel A. R., Draznin B. and Olefsky J. M. (1994) Evidence for a functional role of Shc proteins in mitogenic signaling induced by insulin, insulin-like growth factor-1, and epidermal growth factor. J. Biol. Chem. 269, 13689-13694.
32. Sasaoka T., Ishiki M., Sawa T., Ishihara H., Takata Y., Imamura T., Usui I., Olefsky J. M. and Kobayashi M. (1996) Comparison of the insulin and insulin-like growth factor 1 mitogenic intracellular signaling pathways. Endocrinology 137, 4427-4434.
33. Su B. and Karin M. (1996) Mitogen-activated protein kinase cascades and regulation of gene expression. Curr. Opin. Immunol. 8, 402-411.
34. Tagami M., Ikeda K., Nara Y., Fujino H., Kubota A., Numano F. and Yamori Y. (1997) Insulin-like growth factor-1 attenuates apoptosis in hippocampal neurons caused by cerebral ischemia and reperfusion in stroke-prone spontaneously hypertensive rats. Lab. Invest. 76, 613-617.
35. Trejo J. L., Carro E. and Torres-Aleman I. (2001) Circulating insulin-like growth factor I mediates exercise induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 21, 1628-1634.
36. Vivanco I. and Sawyers C. L. (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer. 2, 489-501.
37. Yamada M., Tanabe K., Wada K., Shimoke K., Ishikawa Y., Ikeuchi T., Koizumi S. and Hatanaka H. (2001) Differences in survival-promoting effects and intracellular signaling properties of BDNF and IGF-1 in cultured cerebral cortical neurons. J. Neurochem, 78, 940-951.
38. Yamaguchi A., Tamatani M., Matsuzaki H., Namikawa K., Kiyama H., Vitek M. P., Mitsuda N. and Tohyama M. (2001) Akt activation protects hippocampal neurons from apoptosis by inhibiting transcriptional activity of p53. J. Biol. Chem. 276, 5256-2564.
39. Zheng W. H., Fink D. W. Jr and Guroff G. (1996) Role of protein kinase C alpha in nerve growth factor-induced arachidonic acid release from PC12 cells. J. Neurochem. 66, 1868-1875.
40. Zheng W. H., Kar S., Dore S. and Quirion R. (2000a) Insulin-like growth factor-1 (IGF-1): a neuroprotective trophic factor acting via the Akt kinase pathway. J. Neural. Transm. Suppl. 60, 261-272.
41. Zheng W. H., Kar S. and Quirion R. (2000b) Insulin-like growth factor-1-induced phosphorylation of the forkhead family transcription factor FKHPL1 is mediated by akt kinase in PC12 cells. J. Biol. Chem. 275, 39152-39158.
42. Zheng W. H., Kar S. and Quirion R. (2000c) Stimulation of protein kinase C modulates insulin-like growth factor-1-induced akt activation in PC12 cells. J. Biol. Chem. 275, 13377-13385.
43. Zheng W. H., Kar S. and Quirion R. (2002a) Insulin-like growth factor-1-induced phosphorylation of transcription factor FKHRL1 is mediated by phosphatidylinositol 3-kinase/Akt kinase and role of this pathway in insulin-like growth factor-1-induced survival of cultured hippocampal neurons. Mol. Pharmacol. 62, 225-233.
44. Zheng W. H., Kar S. and Quirion R. (2002b) FKHRL1 and its homologs are new targets of nerve growth factor Trk receptor signaling. J. Neurochem. 80, 1049-1061.