IRS-4 Mediates Protein Kinase B Signaling during Insulin Stimulation without Promoting Antiapoptosis

REFERENCES

• 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
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., and Cohen, P.. 1998. Mechanism of activation and function of protein kinase B. Curr. Opin. Gene 8:55–62
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., James, S. R., Downes, C. P., Holmes, A. B., Gaffney, P. R. J., Reese, C. B., and Cohen, P.. 1997. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr. Biol. 7:261–269
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., Kozlowski, M. T., Weng, Q. P., Morrice, N., and Avruch, J.. 1998. 3-Phosphoinositide-dependent protein kinase 1 (PDK1) phosphorylates and activates the p70 S6 kinase in vivo and in vitro. Curr. Biol. 8:69–81
   PubMed Web of Science ®Google Scholar
• Araki, E., Lipes, M. A., Patti, M. E., Brüning, J. C., Haag, B. L.III, Johnson, R. S., and Kahn, C. R.. 1994. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature 372:186–190
   PubMed Web of Science ®Google Scholar
• 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. et al. 1992. Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11:3469–3479
   PubMed Web of Science ®Google Scholar
• Baffy, G., Miyashita, T., Williamson, J. R., and Reed, J. C.. 1993. Apoptosis induced by withdrawal of IL-3 from an IL-3 dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J. Biol. Chem. 268:6511–6519
   PubMed Web of Science ®Google Scholar
• Bernal, D., Almind, K., Yenush, L., Ayoub, M., Zhang, Y., Rosshani, L., Larsson, C., Pedersen, O., and White, M. F.. 1998. IRS-2 Amino acid polymorphisms are not associated with random type 2 diabetes among caucasians. Diabetes 47:976–979
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Burks, D. J., Pons, S., Towery, H., Smith-Hall, J., Myers, M. G.Jr., Yenush, L., and White, M. F.. 1997. Heterologous PH domains do not mediate coupling of IRS-1 to the insulin receptor. J. Biol. Chem. 272:27716–27721
   PubMedGoogle Scholar
• Chung, J., Grammer, T. C., Lemon, K. P., Kazlauskas, A., and Blenis, J.. 1994. PDGF- and insulin-dependent pp70S6k activation mediated by phosphatidylinositol-3-OH kinase. Nature 370:71–75
   PubMed Web of Science ®Google Scholar
• Collins, M. K., Perkins, G. R., Rodriguez Tarduchy, G., Nieto, M. A., and Lopez-Rivas, A.. 1994. Growth factors as survival factors: regulation of apoptosis. Bioessays 16:133–138
   PubMed Web of Science ®Google Scholar
• Datta, S. R., Dudek, H., Tao, X., Masters, S., Fu, H., Gotoh, Y., and Greenberg, M. E.. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231–241
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Dennis, P. B., Pullen, N., Pearson, R. B., Kozma, S. C., and Thomas, G.. 1998. Phosphorylation sites in the autoinhibitory domain participate in p70(s6k) activation loop phosphorylation. J. Biol. Chem. 273:14845–14852
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Fantin, V. R., Sparling, J. D., Slot, J. W., Keller, S. R., Lienhard, G. E., and Lavan, B. E.. 1998. Characterization of insulin receptor substrate 4 in human embryonic kidney 293 cells. J. Biol. Chem. 273:10726–10732
   PubMedGoogle Scholar
• Feinstein, R., Kanety, H., Papa, M. Z., Lunenfeld, B., and Karasik, A.. 1993. Tumor necrosis factor-alpha suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. J. Biol. Chem. 268:26055–26058
   PubMed Web of Science ®Google Scholar
• Guilherme, A., and Czech, M. P.. 1998. Stimulation of IRS-1-associated phosphatidylinositol 3-kinase and Akt/protein kinase B but not glucose transport by β1-integrin signaling in rat adipocytes. J. Biol. Chem. 273:33119–33122
   PubMed Web of Science ®Google Scholar
• Hemmings, B. A.. 1997. Akt signaling linked membrane events to life and death decisions. Science 275:628–630
   PubMed Web of Science ®Google Scholar
• Hotamisligil, G. S., Peraldi, P., Budvari, A., Ellis, R. W., White, M. F., and Spiegelman, B. M.. 1996. IRS-1 mediated inhibition of insulin receptor tyrosine kinase activity in TNF-α- and obesity-induced insulin resistance. Science 271:665–668
   PubMed Web of Science ®Google Scholar
• Kapeller, R., Cantley, L. C.Jr.. 1994. Phosphatidylinositol 3-kinase. Bioessays 16:565–576
   PubMed Web of Science ®Google Scholar
• Lane, H. A., Fernandez, A., Lamb, N. J. C., and Thomas, G.. 1993. p70s6k function is essential for G1 progression. Nature 363:170–172
   PubMed Web of Science ®Google Scholar
• Lavan, B. E., Fantin, V. R., Chang, E. T., Lane, W. S., Keller, S. R., and Lienhard, G. E.. 1997. A novel 160 kDa phosphotyrosine protein in insulin-treated embryonic kidney cells is a new member of the insulin receptor substrate family. J. Biol. Chem. 272:21403–21407
   PubMed Web of Science ®Google Scholar
• Lavan, B. E., Lane, W. S., and Lienhard, G. E.. 1997. The 60-kDa phosphotyrosine protein in insulin-treated adipocytes is a new member of the insulin receptor substrate family. J. Biol. Chem. 272:11439–11443
   PubMed Web of Science ®Google Scholar
• Lemmon, M. A., Ferguson, K. M., and Schlessinger, J.. 1996. PH domains: diverse sequences with a common fold recruit signaling molecules to the cell surface. Cell 85:621–624
   PubMed Web of Science ®Google Scholar
• Liu, S. C., Wang, Q., Lienhard, G. E., and Keller, S. R.. 1999. Insulin receptor substrate 3 is not essential for growth or glucose homeostasis. J. Biol. Chem. 274:18093–18099
   PubMed Web of Science ®Google Scholar
• Magnelli, L., Cinelli, M., Turchetti, A., and Chiarugi, V. P.. 1993. Apoptosis induction in 32D cells by IL-3 withdrawal is preceded by a drop in the intracellular calcium level. Biochem. Biophys. Res. Commun. 194:1394–1397
   PubMedGoogle Scholar
• Mendez, R., Kollmorgen, G., White, M. F., and Rhoads, R. E.. 1997. Requirement of protein kinase C zeta for stimulation of protein synthesis by insulin. Mol. Cell. Biol. 17:5184–5192
   PubMedGoogle Scholar
• Mendez, R., Myers, M. G.Jr., White, M. F., and Rhoads, R. E.. 1996. Stimulation of protein synthesis, eukaryotic translation initiation factor 4E phosphorylation, and PHAS-1 phosphorylation by insulin requires insulin receptor substrate-1 and phosphotidylinositol-3-kinase. Mol. Cell. Biol. 16:2857–2864
   PubMed Web of Science ®Google Scholar
• Myers, M. G. J., Mendez, R., Shi, P., Pierce, J. H., Rhoads, R., and White, M. F.. 1998. The COOH-terminal tyrosine phosphorylation sites on IRS-1 bind SHP-2 and negatively regulate insulin signaling. J. Biol. Chem. 273:26908–26914
   PubMed Web of Science ®Google Scholar
• Myers, M. G.Jr., Grammer, T. C., Wang, L. M., Sun, X. J., Pierce, J. H., Blenis, J., and White, M. F.. 1994. IRS-1 mediates PI 3′-kinase and p70s6k signaling during insulin, IGF-1 and IL-4 stimulation. J. Biol. Chem. 269:28783–28789
   PubMed Web of Science ®Google Scholar
• Myers, M. G.Jr., Wang, L. M., Sun, X. J., Zhang, Y., Yenush, L., Schlessinger, J., Pierce, J. H., and White, M. F.. 1994. The role of IRS-1/GRB2 complexes in insulin signaling. Mol. Cell. Biol. 14:3577–3587
   PubMed Web of Science ®Google Scholar
• Myers, M. G.Jr., and White, M. F.. 1993. The new elements in insulin signaling. Insulin receptor substrate-1 and proteins with SH2 domains. Diabetes 42:643–650
   PubMed Web of Science ®Google Scholar
• Myers, M. G.Jr., Zhang, Y., Aldaz, G. A. I., Grammer, T. C., Glasheen, E. M., Yenush, L., Wang, L. M., Sun, X. J., Blenis, J., Pierce, J. H., and White, M. F.. 1996. YMXM motifs and signaling by an insulin receptor substrate 1 molecule without tyrosine phosphorylation sites. Mol. Cell. Biol. 16:4147–4155
   PubMed Web of Science ®Google Scholar
• Pruett, W., Yuan, Y., Rose, E., Batzer, A. G., Harada, N., and Skolnik, E. Y.. 1995. Association between GRB2/Sos and insulin receptor substrate 1 is not sufficient for activation of extracellular signal-regulated kinases by interleukin-4: Implications for ras activation by insulin. Mol. Cell. Biol. 15:1778–1785
   PubMedGoogle Scholar
• Pullen, N., Dennis, P. B., Andjelkovic, M., Dufner, A., Kozma, S. C., Hemmings, B. A., and Thomas, G.. 1998. Phosphorylation and activation of p70s6k by PDK1. Science 279:707–710
   PubMed Web of Science ®Google Scholar
• Reiss, K., Porcu, P., Sell, C., Pietrzkowski, Z., and Baserga, R.. 1992. The insulin-like growth factor 1 receptor is required for the proliferation of hemopoietic cells. Oncogene 7:2243–2248
   PubMed Web of Science ®Google Scholar
• Rodriguez-Viciana, P., Warne, P. H., Dhand, R., Vanhaesebroeck, B., Gout, I., Fry, M. J., Waterfield, M. D., and Downward, J.. 1994. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370:527–532
   PubMed Web of Science ®Google Scholar
• Rordorf-Nikolic, T., Van Horn, D. J., Chen, D., White, M. F., and Backer, J. M.. 1995. Regulation of phosphatidylinositol 3-kinase by tyrosyl phosphoproteins. Full activation requires occupancy of both SH2 domains in the 85 kDa regulatory subunit. J. Biol. Chem. 270:3662–3666
   PubMed Web of Science ®Google Scholar
• Shepherd, P. R., Withers, D. J., and Siddle, K.. 1998. Phosphoinositide 3-kinase: the key switch mechanism in insulin signalling. Biochem. J. 333:471–490
   PubMed Web of Science ®Google Scholar
• Shima, H., Pende, M., Chen, Y., Fumagalli, S., Thomas, G., and Kozma, S. C.. 1998. Disruption of the p70(s6k)/p85(s6k) gene reveals a small mouse phenotype and a new functional S6 kinase. EMBO J. 17:6649–6659
   PubMed Web of Science ®Google Scholar
• Skolnik, E. Y., Batzer, A. G., Li, N., Lee, C. H., Lowenstein, E. J., Mohammadi, M., Margolis, B., and Schlessinger, J.. 1993. The function of GRB2 in linking the insulin receptor to ras signaling pathways. Science 260:1953–1955
   PubMed Web of Science ®Google Scholar
• Songyang, Z., and Cantley, L. C.. 1995. Recognition and specificity in protein tyrosine kinase-mediated signaling. Trends Biochem. Sci. 20:470–475
   PubMed Web of Science ®Google Scholar
• Songyang, Z., Carraway, K. L.III, Eck, M. J., Harrison, S. C., Feldman, R. A., Mohammadi, M., Schlessinger, J., Hubbard, S. R., Lorenzo, M. J., Ponder, B. A. J., Mayer, B. J., and Cantley, L. C.. 1995. Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature 373:536–539
   PubMed Web of Science ®Google Scholar
• Sun, X. J., Pons, S., Wang, L. M., Zhang, Y., Yenush, L., Burks, D., Myers, M. G.Jr., Glasheen, E., Copeland, N. G., Jenkins, N. A., Pierce, J. H., and White, M. F.. 1997. The IRS-2 gene on murine chromosome 8 encodes a unique signaling adapter for insulin and cytokine action. Mol. Endocrinol. 11:251–262
   PubMed Web of Science ®Google Scholar
• Sun, X. J., Rothenberg, P. L., Kahn, C. R., Backer, J. M., Araki, E., Wilden, P. A., Cahill, D. A., Goldstein, B. J., and White, M. F.. 1991. The structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 352:73–77
   PubMed Web of Science ®Google Scholar
• Sun, X. J., Wang, L. M., Zhang, Y., Yenush, L., Myers, M. G.Jr., Glasheen, E. M., Lane, W. S., Pierce, J. H., and White, M. F.. 1995. Role of IRS-2 in insulin and cytokine signalling. Nature 377:173–177
   PubMed Web of Science ®Google Scholar
• Toker, A., and Cantley, L. C.. 1997. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387:673–676
   PubMed Web of Science ®Google Scholar
• Walker, K. S., Deak, M., Paterson, A., Hudson, K., Cohen, P., and Alessi, D. R.. 1998. Activation of protein kinase B β and γ isoforms by insulin in vivo and by 3-phosphoinositide-dependent protein kinase-1 in vitro: comparison with protein kinase B α. Biochem. J. 331:299–308
   PubMedGoogle Scholar
• Wang, L. M., Myers, M. G.Jr., Sun, X. J., Aaronson, S. A., White, M. F., and Pierce, J. H.. 1993. IRS-1: essential for insulin and IL-4-stimulated mitogenesis in hematopoietic cells. Science 261:1591–1594
   PubMedGoogle Scholar
• Weng, Q. P., Andrabi, K., Klippel, A., Kozlowski, M. T., Williams, L. T., and Avruch, J.. 1995. Phosphatidylinositiol 3-kinase signals activation of p70 S6 kinase in situ through site-specific p70 phosphorylation. Proc. Natl. Acad. Sci. USA 92:5744–5748
   PubMedGoogle Scholar
• Weng, Q. P., Kozlowski, M., Belham, C., Zhang, A., Comb, M. J., and Avruch, J.. 1998. Regulation of the p70 S6 kinase by phosphorylation in vivo. Analysis using site-specific anti-phosphopeptide antibodies. J. Biol. Chem. 273:16621–16629
   PubMedGoogle Scholar
• Withers, D. J., Gutierrez, J. S., Towery, H., Burks, D. J., Ren, J. M., Previs, S., Zhang, Y., Bernal, D., Pons, S., Shulman, G. I., Bonner-Weir, S., and White, M. F.. 1998. Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391:900–903
   PubMed Web of Science ®Google Scholar
• Wyllie, A. H., Kerr, J. F., and Currie, A. R.. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251–306
   PubMedGoogle Scholar
• Yenush, L., Fernandez, R., Myers, M. G.Jr., Grammer, T. C., Sun, X. J., Blenis, J., Pierce, J. H., Schlessinger, J., and White, M. F.. 1996. The Drosophila insulin receptor activates multiple signaling pathways but requires insulin receptor substrate proteins for DNA synthesis. Mol. Cell. Biol. 16:2509–2517
   PubMed Web of Science ®Google Scholar
• Yenush, L., Makati, K. J., Smith-Hall, J., Ishibashi, O., Myers, M. G.Jr., and White, M. F.. 1996. The pleckstrin homology domain is the principle link between the insulin receptor and IRS-1. J. Biol. Chem. 271:24300–24306
   PubMed Web of Science ®Google Scholar
• Yenush, L., and White, M. F.. 1997. The IRS-signaling system during insulin and cytokine action. Bioessays 19:491–500
   PubMed Web of Science ®Google Scholar
• Yenush, L., Zanella, C., Uchida, T., Bernal, D., and White, M. F.. 1998. The pleckstrin homology and phosphotyrosine binding domains of insulin receptor substrate 1 mediate inhibition of apoptosis by insulin. Mol. Cell. Biol. 18:6784–6794
   PubMed Web of Science ®Google Scholar