Molecular Balance between the Regulatory and Catalytic Subunits of Phosphoinositide 3-Kinase Regulates Cell Signaling and Survival

REFERENCES

• Antonetti, D. A., P. Algenstaedt, and C. R. Kahn. 1996. Insulin receptor substrate 1 binds two novel splice variants of the regulatory subunit of phosphatidylinositol 3-kinase in muscle and brain. Mol. Cell. Biol. 16: 2195–2203.
   PubMedGoogle Scholar
• Backer, J. M., M. G. Myers, Jr., S. E. Shoelson, D. J. Chin, X. J. Sun, M. Miralpeix, P. Hu, B. Margolis, E. Y. Skolnik, J. Schlessinger, and M. F. White. 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
• Baltensperger, K., L. M. Kozma, S. R. Jaspers, and M. P. Czech. 1994. Regulation by insulin of phosphatidylinositol 3′-kinase bound to alpha- and beta-isoforms of p85 regulatory subunit. J. Biol. Chem. 269: 28937–28946.
   PubMed Web of Science ®Google Scholar
• Bonni, A., A. Brunet, A. E. West, S. R. Datta, M. A. Takasu, and M. E. Greenberg. 1999. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286: 1358–1362.
   PubMed Web of Science ®Google Scholar
• Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857–868.
   PubMed Web of Science ®Google Scholar
• Bruning, J. C., J. Winnay, S. Bonner-Weir, S. I. Taylor, D. Accili, and C. R. Kahn. 1997. Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell 88: 561–572.
   PubMed Web of Science ®Google Scholar
• Bruning, J. C., J. Winnay, B. Cheatham, and C. R. Kahn. 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
• Cantley, L. C., and B. G. Neel. 1999. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc. Natl. Acad. Sci. USA 96: 4240–4245.
   PubMed Web of Science ®Google Scholar
• Cheatham, B., C. J. Vlahos, L. Cheatham, L. Wang, J. Blenis, and C. R. Kahn. 1994. Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis, and glucose transporter translocation. Mol. Cell. Biol. 14: 4902–4911.
   PubMed Web of Science ®Google Scholar
• Coffer, P. J., J. Jin, and J. R. Woodgett. 1998. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem. J. 335: 1–13.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13: 2905–2927.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M. E. Greenberg. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231–241.
   PubMed Web of Science ®Google Scholar
• Du, K., and M. Montminy. 1998. CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273: 32377–32379.
   PubMed Web of Science ®Google Scholar
• Franke, T. F., D. R. Kaplan, and L. C. Cantley. 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88: 435–437.
   PubMed Web of Science ®Google Scholar
• Fruman, D. A., L. C. Cantley, and C. L. Carpenter. 1996. Structural organization and alternative splicing of the murine phosphoinositide 3-kinase p85α gene. Genomics 37: 113–121.
   PubMedGoogle Scholar
• Fruman, D. A., F. Mauvais-Jarvis, D. A. Pollard, C. M. Yballe, D. Brazil, R. T. Bronson, C. R. Kahn, and L. C. Cantley. 2000. Hypoglycaemia, liver necrosis and perinatal death in mice lacking all isoforms of phosphoinositide 3-kinase p85α. Nat. Genet. 26: 379–382.
   PubMed Web of Science ®Google Scholar
• Fruman, D. A., R. E. Meyers, and L. C. Cantley. 1998. Phosphoinositide kinases. Annu. Rev. Biochem. 67: 481–507.
   PubMed Web of Science ®Google Scholar
• Fruman, D. A., S. B. Snapper, C. M. Yballe, L. Davidson, J. Y. Yu, F. W. Alt, and L. C. Cantley. 1999. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85α. Science 283: 393–397.
   PubMed Web of Science ®Google Scholar
• Gonzalez, G. A., and M. R. Montminy. 1989. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59: 675–680.
   PubMed Web of Science ®Google Scholar
• Hara, K., K. Yonezawa, H. Sakaue, A. Ando, K. Kotani, T. Kitamura, Y. Kitamura, H. Ueda, L. Stephens, T. R. Jackson, P. T. Hawkins, R. Dahnd, A. E. Clark, G. D. Holman, M. D. Waterfield, and M. Kasuga. 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.
   PubMed Web of Science ®Google Scholar
• Harada, H., B. Becknell, M. Wilm, M. Mann, L. J. Huang, S. S. Taylor, J. D. Scott, and S. J. Korsmeyer. 1999. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell 3: 413–422.
   PubMed Web of Science ®Google Scholar
• Hemmings, B. A. 1997. Akt signaling: linking membrane events to life and death decisions. Science 275: 628–630.
   PubMed Web of Science ®Google Scholar
• Inukai, K., M. Anai, E. Van Breda, T. Hosaka, H. Katagiri, M. Funaki, Y. Fukushima, T. Ogihara, Y. Yazaki, M. Kikuchi, Y. Oka, and T. Asano. 1996. A novel 55-kDa regulatory subunit for phosphatidylinositol 3-kinase structurally similar to p55PIK is generated by alternative splicing of the p85α gene. J. Biol. Chem. 271: 5317–5320.
   PubMedGoogle Scholar
• Inukai, K., M. Funaki, T. Ogihara, H. Katagiri, A. Kanda, M. Anai, Y. Fukushima, T. Hosaka, M. Suzuki, B. C. Shin, K. Takata, Y. Yazaki, M. Kikuchi, Y. Oka, and T. Asano. 1997. p85α gene generates three isoforms of regulatory subunit for phosphatidylinositol 3-kinase (PI 3-kinase), p50α, p55α, and p85α, with different PI 3-kinase activity elevating responses to insulin. J. Biol. Chem. 272: 7873–7882.
   PubMed Web of Science ®Google Scholar
• Jensen, C. J., M. B. Buch, T. O. Krag, B. A. Hemmings, S. Gammeltoft, and M. Frodin. 1999. 90-kDa ribosomal S6 kinase is phosphorylated and activated by 3-phosphoinositide-dependent protein kinase-1. J. Biol. Chem. 274: 27168–27176.
   PubMed Web of Science ®Google Scholar
• Kerouz, N. J., D. Horsch, S. Pons, and C. R. Kahn. 1997. Differential regulation of insulin receptor substrates-1 and -2 (IRS-1 and IRS-2) and phosphatidylinositol 3-kinase isoforms in liver and muscle of the obese diabetic (ob/ob) mouse. J. Clin. Investig. 100: 3164–3172.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kimura, K. D., H. A. Tissenbaum, Y. Liu, and G. Ruvkun. 1997. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277: 942–946.
   PubMed Web of Science ®Google Scholar
• Kops, G. J., N. D. de Ruiter, A. M. De Vries-Smits, D. R. Powell, J. L. Bos, and B. M. Burgering. 1999. Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398: 630–634.
   PubMed Web of Science ®Google Scholar
• Korsmeyer, S. J. 1999. BCL-2 gene family and the regulation of programmed cell death. Cancer Res. 59: 1693s–1700s.
   PubMed Web of Science ®Google Scholar
• Lin, K., J. B. Dorman, A. Rodan, and C. Kenyon. 1997. daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319–1322.
   PubMed Web of Science ®Google Scholar
• Mauvais-Jarvis, F., K. Ueki, D. A. Fruman, M. F. Hirshman, K. Sakamoto, L. J. Goodyear, M. Iannacone, D. Accili, L. C. Cantley, and C. R. Kahn. Reduction in the p85α subunit of phosphoinositide 3-kinase improves insulin signaling and ameliorates diabetes in mice. J Clin. Investig., in press.
   Google Scholar
• Ogg, S., S. Paradis, S. Gottlieb, G. I. Patterson, L. Lee, H. A. Tissenbaum, and G. Ruvkun. 1997. The Forkhead transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389: 994–999.
   PubMed Web of Science ®Google Scholar
• Okada, T., Y. Kawano, T. Sakakibara, O. Hazeki, and M. Ui. 1994. Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J. Biol. Chem. 269: 3568–3573.
   PubMed Web of Science ®Google Scholar
• Otsu, M., I. Hiles, I. Gout, M. J. Fry, F. Ruiz-Larrea, G. Panayotou, A. Thompson, R. Dhand, J. Hsuan, and N. Totty. 1991. Characterization of two 85 kd proteins that associate with receptor tyrosine kinases, middle-T/pp60c-src complexes, and PI3-kinase. Cell 65: 91–104.
   PubMed Web of Science ®Google Scholar
• Pons, S., T. Asano, E. Glasheen, M. Miralpeix, Y. Zhang, T. L. Fisher, M. G. Myers, Jr., X. J. Sun, and M. F. White. 1995. The structure and function of p55PIK reveal a new regulatory subunit for phosphatidylinositol 3-kinase. Mol. Cell. Biol. 15: 4453–4465.
   PubMed Web of Science ®Google Scholar
• Pugazhenthi, S., T. Boras, D. O’Connor, M. K. Meintzer, K. A. Heidenreich, and J. E. Reusch. 1999. Insulin-like growth factor I-mediated activation of the transcription factor cAMP response element-binding protein in PC12 cells. Involvement of p38 mitogen-activated protein kinase-mediated pathway. J. Biol. Chem. 274: 2829–2837.
   PubMedGoogle Scholar
• Pullen, N., P. B. Dennis, M. Andjelkovic, A. Dufner, S. C. Kozma, B. A. Hemmings, and G. Thomas. 1998. Phosphorylation and activation of p70s6k by PDK1. Science 279: 707–710.
   PubMed Web of Science ®Google Scholar
• Rameh, L. E., C. S. Chen, and L. C. Cantley. 1995. Phosphatidylinositol (3,4,5)P3 interacts with SH2 domains and modulates PI 3-kinase association with tyrosine-phosphorylated proteins. Cell 83: 821–830.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Viciana, P., P. H. Warne, R. Dhand, B. Vanhaesebroeck, I. Gout, M. J. Fry, M. D. Waterfield, and J. Downward. 1994. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370: 527–532.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Viciana, P., P. H. Warne, B. Vanhaesebroeck, M. D. Waterfield, and J. Downward. 1996. Activation of phosphoinositide 3-kinase by interaction with Ras and by point mutation. EMBO J. 15: 2442–2451.
   PubMed Web of Science ®Google Scholar
• Rohrschneider, L. R., J. F. Fuller, I. Wolf, Y. Liu, and D. M. Lucas. 2000. Structure, function, and biology of SHIP proteins. Genes Dev. 14: 505–520.
   PubMed Web of Science ®Google Scholar
• Shepherd, P. R., D. J. Withers, and K. Siddle. 1998. Phosphoinositide 3-kinase: the key switch mechanism in insulin signalling. Biochem. J. 333: 471–490.
   PubMed Web of Science ®Google Scholar
• Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, B. G. Neel, R. B. Birge, J. E. Fajardo, M. M. Chou, H. Hanafusa, B. Schaffhausen, and L. C. Cantley. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72: 767–778.
   PubMed Web of Science ®Google Scholar
• Sun, X. J., P. Rothenberg, C. R. Kahn, J. M. Backer, E. Araki, P. A. Wilden, D. A. Cahill, B. J. Goldstein, and M. F. White. 1991. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 352: 73–77.
   PubMed Web of Science ®Google Scholar
• Suzuki, H., Y. Terauchi, M. Fujiwara, S. Aizawa, Y. Yazaki, T. Kadowaki, and S. Koyasu. 1999. Xid-like immunodeficiency in mice with disruption of the p85α subunit of phosphoinositide 3-kinase. Science 283: 390–392.
   PubMed Web of Science ®Google Scholar
• Tang, E. D., G. Nunez, F. G. Barr, and K. L. Guan. 1999. Negative regulation of the forkhead transcription factor FKHR by Akt. J. Biol. Chem. 274: 16741–16746.
   PubMed Web of Science ®Google Scholar
• Terauchi, Y., Y. Tsuji, S. Satoh, H. Minoura, K. Murakami, A. Okuno, K. Inukai, T. Asano, Y. Kaburagi, K. Ueki, H. Nakajima, T. Hanafusa, Y. Matsuzawa, H. Sekihara, Y. Yin, J. C. Barrett, H. Oda, T. Ishikawa, Y. Akanuma, I. Komuro, M. Suzuki, K. Yamamura, T. Kodama, H. Suzuki, and T. Kadowaki. 1999. Increased insulin sensitivity and hypoglycaemia in mice lacking the p85α subunit of phosphoinositide 3-kinase. Nat. Genet. 21: 230–235.
   PubMed Web of Science ®Google Scholar
• Toker, A., and L. C. Cantley. 1997. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387: 673–676.
   PubMed Web of Science ®Google Scholar
• Ueki, K., P. Algenstaedt, F. Mauvais-Jarvis, and C. R. Kahn. 2000. Positive and negative regulation of phosphoinositide 3-kinase-dependent signaling pathways by three different gene products of the p85α regulatory subunit. Mol. Cell. Biol. 20: 8035–8046.
   PubMed Web of Science ®Google Scholar
• Ueki, K., R. Yamamoto-Honda, Y. Kaburagi, T. Yamauchi, K. Tobe, B. M. Burgering, P. J. Coffer, I. Komuro, Y. Akanuma, Y. Yazaki, and T. Kadowaki. 1998. Potential role of protein kinase B in insulin-induced glucose transport, glycogen synthesis, and protein synthesis. J. Biol. Chem. 273: 5315–5322.
   PubMed Web of Science ®Google Scholar
• White, M. F., and C. R. Kahn. 1994. The insulin signaling system. J. Biol. Chem. 269: 1–4.
   PubMed Web of Science ®Google Scholar
• Wilson, B. E., E. Mochon, and L. M. Boxer. 1996. Induction of bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Mol. Cell. Biol. 16: 5546–5556.
   PubMed Web of Science ®Google Scholar
• Winnay, J. N., J. C. Bruning, D. J. Burks, and C. R. Kahn. 2000. Gab-1-mediated IGF-1 signaling in IRS-1-deficient 3T3 fibroblasts. J. Biol. Chem. 275: 10545–10550.
   PubMedGoogle Scholar
• Xing, J., D. D. Ginty, and M. E. Greenberg. 1996. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273: 959–963.
   PubMed Web of Science ®Google Scholar
• Yu, J., Y. Zhang, J. McIlroy, T. Rordorf-Nikolic, G. A. Orr, and J. M. Backer. 1998. Regulation of the p85/p110 phosphatidylinositol 3′-kinase: stabilization and inhibition of the p110α catalytic subunit by the p85 regulatory subunit. Mol. Cell. Biol. 18: 1379–1387.
   PubMed Web of Science ®Google Scholar