Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt

Molecular and Cellular Biology

Volumn 17, Issue 3, 1997, Pages 1595-1606

  Kulik, George ^a   Klippel, Anke ^b   Weber, Michael J ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; SOMATOMEDIN C; SOMATOMEDIN RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; ENZYME ACTIVATION; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0031034574     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.3.1595     Document Type: Article

References (72)

1. Aaronson, S. A. 1991. Growth factors and cancer. Science 254:1146-1153.
2. Alessi, D. R., A. Cuenda, P. Cohen, D. T. Dudley, and A. R. Saltiel. 1995. PD98059 is a specific inhibitor of the activation of mitogen-activated protein kinase-kinase in vitro and in vivo. J. Biol. Chem. 270:27489-27494.
3. Andjelkovic, M., T. Jakubowicz, P. Cron, X.-F. Ming, J.-W. Han, and B. A. Hemmings. 1996. Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (Rac-PK/PKB) promoted by serum and protein phosphatase inhibitors. Proc. Natl. Acad. Sci. USA 93:5699-5704.
4. Barres, B. A., I. K. Hart, H. S. R. Coles, J. F. Burne, J. T. Voyvodic, W. D. Richardson, and M. C. Raff. 1992. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70:31-46.
5. Bhatavdekar, J. M., D. D. Patel, N. G. Shah, N. H. Karelia, H. H. Vora, N. Ghosh, T. P. Suthar, and D. B. Balar. 1995. Prognostic value of insulin-like growth factor-I receptors in patients with colon/rectal cancer: correlation with plasma prolactin. Eur. J. Surg. Oncol. 21:23-26.
6. Boldin, M. P., T. M. Goncharov, Y. V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO1- and TNF receptor-induced cell death. Cell 85:803-816.
7. Burgering, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376:599-602.
8. Bursch, W., L. Kleine, and M. Tenniswood. 1990. The biochemistry of cell death by apoptosis. Biochem. Cell Biol. 68:1071-1074.
9. Carpenter, C. L., and L. C. Cantley. 1996. Phosphoinositide kinases. Curr. Opin. Cell Biol. 8:153-158.
10. Chinnaiyan, A. M., K. Orth, K. O'Rourke, H. Duan, G. G. Poirier, and V. M. Dixit. 1996. Molecular ordering of the cell death pathway. J. Biol. Chem. 271:4573-4576.
11. Chou, M. M., and J. Blenis. 1995. The 70 kDa S6 kinase: regulation of a kinase with multiple roles in mitogenic signaling. Curr. Opin. Cell Biol. 7:806-814.
12. Creedon, D. J., E. M. Johnson, and J. C. Lawrence. 1996. Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor on neuronal survival. J. Biol. Chem. 271:20713-20718.
13. 2 activity in Swiss 3T3 cells. J. Biol. Chem. 270: 25352-25355.
14. Cuvillier, O., G. Pirianov, B. Kleuser, P. G. Vanek, O. A. Coso, J. S. Gutkind, and S. Spiegel. 1996. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 381:800-803.
15. De Meyts, B. Wallach, C. T. Cristoffersen, B. Urso, K. Gronskov, L.-J. Latus, F. Yakushiji, M. M. Ilondo, and R. M. Shymko. 1994. Insulin-like growth factor-I receptor. Structure, ligand binding mechanism and signal transduction. Horm. Res. 42:152-159.
16. Duffy, M. J. 1993. Cellular oncogenes and growth suppressor genes as prognostic markers in cancer. Clin. Biochem. 26:439-447.
17. L. J. Biol. Chem. 271:17601-17604.
18. Fisher, D. E. 1994. Apoptosis in cancer therapy: crossing the threshold. Cell 78:539-542.
19. 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 protooncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
20. src protein. Mol. Cell. Biol. 9:1651-1658.
21. Hale, A. J., C. A. Smith, L. C. Sutherland, V. A. Stoneman, V. L. Longthorne, A. C. Culhane, and G. T. Williams. 1996. Apoptosis: molecular regulation of cell death. Eur. J. Biochem. 236:1-26.
22. Harrington, E. A., M. R. Bennett, A. Fanidi, and G. I. Evan. 1994. c-Myc-induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 13:3286-3295.
23. Hartley, K. O., D. Gell, G. C. M. Smith, H. Zhang, N. Divecha, M. A. Connelly, A. Admon, S. P. Lees-Miller, C. W. Anderson, and S. P. Jackson. 1995. DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82:849-856.
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 phosphatidylinositol-3 kinase. Science 268:100-102.
25. Johnson, N. L., A. M. Gardner, K. M. Diener, C. A. Lange-Carter, J. Gleavy, M. B. Jarpe, A. Minden, M. Karin, L. I. Zon, and G. L. Johnson. 1996. Signal transduction pathways regulated by mitogen-activated/extracellular response kinase kinase kinase induce cell death. J. Biol. Chem. 271:3229-3237.
26. Jung, Y. K., M. Miura, and J. Yuan. 1996. Suppression of interleukin-1β-converting enzyme-mediated cell death by insulin-like growth factor. J. Biol. Chem. 271:5112-5117.
27. Kaiser, U., C. Schardt, D. Brandscheidt, E. Wollmer, and K. Havemann. 1993. Expression of insulin-like growth factor receptors I and II in normal human lung and in lung cancer. J. Cancer Res. Clin. Oncol. 119:665-668.
28. Kalebic, T., M. Tsokos, and L. J. Helman. 1994. In vivo treatment with antibody against IGF-I receptor suppresses growth of human rhabdomyosarcoma and downregulates p34cdc2. Cancer 54:5531-5534.
29. Kapeller, R., and L. C. Cantley. 1994. Phosphatidylinositol 3-kinase. Bioessays 16:565-576.
30. Kerr, J. F. R., C. M. Winterford, and B. V. Harmon. 1994. Apoptosis. Its significance in cancer and cancer therapy. Cancer 73:2013-2026.
31. 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.
32. Klippel, A., C. Reinhard, W. M. Kavanaugh, G. Apell, M. A. Escobedo, and L. T. Williams. 1996. Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol. Cell. Biol. 16:4117-4127.
33. Liu, Z.-G., H. Hsu, D. V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell 87:565-576.
34. Martin, S. J., and T. G. Cotter. 1991. Ultraviolet B irradiation of human leukemia HL-60 cells in vitro induce apoptosis. Int J. Radiat. Biol. 59:1001-1016.
35. McConkey, D. J., and S. Orrenius. 1994. Signal transduction pathways to apoptosis. Trends Cell Biol. 4:370-375.
36. Mendez, R., M. G. Myers, Jr., M. F. White, and R. E. Rhoads. 1996. Stimulation of protein synthesis, eukaryotic translation initiation factor 4E phosphorylation, and PHAS-I phosphorylation by insulin requires insulin receptor substrate I and phosphatidylinositol 3-kinase. Mol. Cell. Biol. 16:2857-2864.
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. Muta, K., and S. B. Krantz. 1993. Apoptosis of human erythroid colony-forming cells is decreased by stem cell factor and insulin-like growth factor I as well as erythropoietin. J. Cell. Physiol. 156:264-271.
39. Muzio, M., A. M. Chinnaiyan, F. C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J. D. Bretz, M. Zhang, R. Gentz, M. Mann, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/Apo-1) death-inducing signaling complex. Cell 85:817-828.
40. Myers, M. G., Jr., and M. F. White. 1996. Insulin signal transduction and the IRS proteins. Annu. Rev. Pharmacol. Toxicol. 36:615-658.
41. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science 267:1449-1456.
42. Nakanishi, S., K. J. Catt, and T. Balla. 1995. A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositolphospholipids. Proc. Natl. Acad. Sci. USA 92:5317-5321.
43. Nakanishi, Y., J. L. Mulshine, P. G. Kasprzyk, R. B. Natale, R. Maneckjee, I. Avis, A. M. Treston, A. F. Gazdar, J. D. Minna, and F. Cuttitta. 1988. Insulin-like growth factor-I can mediate autocrine proliferation of human small cell lung cancer cell lines in vitro. J. Clin. Invest. 82:354-359.
44. Obeid, L. M., C. M. Linardic, L. A. Karolak, and Y. A. Hannun. 1993. Programmed cell death induced by ceramide. Science 259:1769-1771.
45. Owen-Lynch, P. J., A. K. Y. Wong, and A. D. Whetton. 1995. v-Abl mediated apoptotic suppression is associated with SHC phosphorylation without concomitant mitogen-activated protein kinase activation. J. Biol. Chem. 270: 5956-5962.
46. Parsons, J. T., and M. J. Weber. 1989. Genetics of src: structure and functional organization of a protein tyrosine kinase. Curr. Top. Microbiol. Immunol. 147:79-127.
47. Peterson, J. E., T. Jelinek, M. Kaleko, K. Siddle, and M. J. Weber. 1994. Phosphorylation and activation of the IGF-I receptor in src-transformed cells. J. Biol. Chem. 269:27315-27321.
48. Peterson, J. E., G. A. Kulik, T. Jelinek, C. M. W. Reuter, J. A. Shannon, and M. J. Weber. Phosphorylation sites on the IGF-I receptor due to autophosphorylation or the Src kinase. Submitted for publication.
49. Pleiman, C. M., W. M. Hertz, and J. C. Cambier. 1994. Activation of phosphatidylinositol-3′ kinase by Src-family kinase SH3 binding to the p85 subunit. Science 263:1609-1612.
50. Railo, M. J., K. von Smitten, and F. Pekonen. 1994. The prognostic value of insulin-like growth factor-I in breast cancer patients. Results of a follow-up study on 126 patients. Eur. J. Cancer 30A:307-311.
51. Resnicoff M., D. Abraham, Y. Wiboonchai, H. R. Rotman, J. Kajstura, R. Rubin, P. Zoltick, and R. Baserga. 1995. The insulin-like growth factor I receptor protects tumor cells from apoptosis in vivo. Cancer Res. 55:2463-2469.
52. Reuter, C. W. M., A. D. Catling, and M. J. Weber. 1995. Immune complex kinase assays for mitogen-activated protein kinase. Methods Enzymol. 225: 245-256.
53. Rodriguez-Tarduchy, G., M. K. L. Collins, I. Garcia, and A. Lopez-Rivas. 1992. Insulin-like growth factor-I inhibits apoptosis in IL-3-dependent hemopoietic cells. J. Immunol. 149:535-540.
54. Santana, P., L. A. Pena, A. Haimovitz-Freidman, S. M. Martin, D. Green, M. McLoughlin, C. Cordon-Cardo, E. H. Schuchman, Z. Fuks, and R. Kolesnick. 1996. Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell 86:189-199.
55. Scheid, M. P., R. W. Lauener, and V. Duroni. 1995. Role of phosphatidylinositol 3-OH-kinase activity in the inhibition of apoptosis in hematopoietic 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.
56. Sell, C., R. Baserga, and R. Rubin. 1995. Insulin-like growth factor (IGF-I) and the IGF-I receptor prevent etoposide-induced apoptosis. Cancer Res. 55:303-306.
57. Smith, C. A., T. Farrah, and R. G. Goodwin. 1994. The TNF receptor superfamily of cellular and viral proteins: activation, costimulation and death. Cell 76:959-962.
58. cbl is a cytosolic adapter protein that associates with phosphoinositide 3-kinase in response to epidermal growth factor in PC12 and other cells. J. Biol. Chem. 271:5633-5637.
59. Soltoff, S. P., K. L. Carraway III, S. A. Prigent, W. G. Gullick, and L. C. Cantley. 1994. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol. Cell. Biol. 14:3550-3558.
60. Shi, Y., A. Frankel, G. Radvanyi, L. Z. Penn, R. G. Miller, and G. B. Mills. 1995. Rapamycin enhances apoptosis and increases sensitivity to cisplatin in vitro. Cancer Res. 55:1982-1988.
61. Steller, M. A., C. H. Delgado, C. J. Bartels, C. D. Woodworth, and Z. Q. Zou. 1996. Overexpression of the insulin-like growth factor-I receptor and autocrine stimulation in human cervical cancer cells. Cancer 56:1761-1765.
62. Szumel, I. 1994. Ionizing radiation-induced cell death. Int. J. Radiat. Biol. 66:329-331.
63. Takebe, Y., M. Seiki, J. Fujisawa, P. Hoy, K. Yokota, K. Arai, M. Yoshida, and N. Arai. 1988. SR alpha promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T-cell leukemia type I long terminal repeat. Mol. Cell. Biol. 8:466-472.
64. Tavaré, J. M., and K. Siddle. 1993. Mutational analysis of insulin receptor function: consensus and controversy. Biochim. Biophys. Acta 1178:21-39.
65. Thompson, C. B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267:1456-1462.
66. Ui, M., T. Okada, K. Hazeki, and O. Hazeki. 1995. Wortmannin as a unique probe for an intracellular signaling protein, phosphoinositide 3-kinase. Trends Biochem. Sci. 20:303-307.
67. Ullrich, A., and J. Schlessinger. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 70:313-322.
68. Verheij, M., R. Bose, X. H. Lin, B. Yao, W. D. Jarvis, S. Grant, M. J. Birrer, E. Szabo, L. I. Zon, J. M. Kyriakis, A. Haimovitz-Friedman, Z. Fuks, R. N. Kolesnick. 1996. Requirement for ceramide-initiated SAPK/JNK signaling in stress-induced apoptosis. Nature 380:75-79.
69. 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 270:1326-1331.
70. Yao, R., and G. M. Cooper. 1995. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267: 2003-2006.
71. S6K activity. Oncogene 13:343-351.
72. Zvelebil, M. J., L. Macdougall, S. Leevers, S. Volinia, B. Vanhaesebroeck, I. Gout, G. Panayotou, J. Domin, R. Stein, F. Pages, H. Koga, K. Salim, J. Linacre, P. Das, C. Panaretou, R. Wetzker, and M. Waterfield. 1996. Structural and functional diversity of phosphoinositide 3-kinases. Philos. Trans. R. Soc. Lond. 351:217-223.