Ceramide Disables 3-Phosphoinositide Binding to the Pleckstrin Homology Domain of Protein Kinase B (PKB)/Akt by a PKCζ-Dependent Mechanism

REFERENCES

• Akimoto, K., R. Takahashi, S. Moriya, N. Nishioka, J. Takayanagi, K. Kimura, Y. Fukui, S. Osada, K. Mizuno, S. Hirai, A. Kazlauskas, and S. Ohno. 1996. EGF or PDGF receptors activate atypical PKCλ through phosphatidylinositol 3-kinase. EMBO J. 15: 788–798.
   PubMedGoogle Scholar
• Alessi, D. R. 1997. The protein kinase C inhibitors RO318220 and GF109203X are equally potent inhibitors of MAPKAP kinase-1β (Rsk-2) and p70 s6 kinase. FEBS Lett. 402: 121–123.
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., and P. Cohen. 1998. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8: 55–62.
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., S. R. James, C. P. Downes, A. B. Holmes, P. R. Gaffney, C. B. Reese, and P. Cohen. 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
• Andjelkovic, M., D. R. Alessi, R. Meier, A. Fernandez, N. J. C. Lamb, M. Frech, P. Cron, P. Cohen, J. M. Lucocq, and B. A. Hemmings. 1997. Role of translocation in the activation and function of protein kinase B. J. Biol. Chem. 272: 31515–31524.
   PubMed Web of Science ®Google Scholar
• Balendran, A., G. R. Hare, A. Kieloch, M. R. Williams, and D. R. Alessi. 2000. Further evidence that 3-phosphoinositide-dependent protein kinase-1 (PDK1) is required for the stability and phosphorylation of protein kinase C (PKC) isoforms. FEBS Lett. 484: 217–223.
   PubMed Web of Science ®Google Scholar
• Bandyopadhyay, G., M. L. Standaert, M. P. Sajan, L. M. Karnitz, L. Cong, M. J. Quon, and R. V. Farese. 1999. Dependence of insulin-stimulated glucose transporter 4 translocation on 3-phosphoinositide-dependent protein kinase-1 and its target threonine-410 in the activation loop of protein kinase Cζ. Mol. Endocrinol. 13: 1766–1772.
   PubMed Web of Science ®Google Scholar
• Bieberich, E., T. Kawaguchi, and R. K. Yu. 2000. N-acylated serinol is a novel ceramide mimic inducing apoptosis in neuroblastoma cells. J. Biol. Chem. 275: 177–181.
   PubMed Web of Science ®Google Scholar
• Bourbon, N. A., L. Sandirasegarane, and M. Kester. 2002. Ceramide-induced inhibition of Akt is mediated through protein kinase Cζ: implications for growth arrest. J. Biol. Chem. 277: 3286–3292.
   PubMed Web of Science ®Google Scholar
• Bourbon, N. A., J. Yun, and M. Kester. 2000. Ceramide directly activates protein kinase C ζ to regulate a stress-activated protein kinase signaling complex. J. Biol. Chem. 275: 35617–35623.
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.
   PubMed Web of Science ®Google Scholar
• Braiman, L., A. Alt, T. Kuroki, M. Ohba, A. Bak, T. Tennenbaum, and S. R. Sampson. 2001. Activation of protein kinase C ζ induces serine phosphorylation of VAMP2 in the GLUT4 compartment and increases glucose transport in skeletal muscle. Mol. Cell. Biol. 21: 7852–7861.
   PubMedGoogle Scholar
• Brazil, D. P., J. Park, and B. A. Hemmings. 2002. PKB binding proteins: getting in on the Akt. Cell 111: 293–303.
   PubMed Web of Science ®Google Scholar
• Cazzolli, R., L. Carpenter, T. J. Biden, and C. Schmitz-Peiffer. 2001. A role for protein phosphatase 2A-like activity, but not atypical protein kinase Cζ, in the inhibition of protein kinase B/Akt and glycogen synthesis by palmitate. Diabetes 50: 2210–2218.
   PubMedGoogle Scholar
• Chan, T. O., and P. N. Tsichlis. 2001. PDK2: a complex tail in one Akt. Science STKE 2001: E1.
   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
• Cross, D. A. E., D. R. Alessi, P. Cohen, M. Andjelkovic, and B. A. Hemmings. 1995. Inhibition of glycogen synthase kinase-3 by insulin-mediated protein kinase B. Nature 378: 785–789.
   PubMed Web of Science ®Google Scholar
• Das, M., K. R. Stenmark, L. J. Ruff, and E. C. Dempsey. 1997. Selected isozymes of PKC contribute to augmented growth of fetal and neonatal bovine PA adventitial fibroblasts. Am. J. Physiol. 273: L1276–L1284.
   PubMedGoogle Scholar
• Datta, K., T. F. Franke, T. O. Chan, A. Makris, S. I. Yang, D. R. Kaplan, D. K. Morrison, E. A. Golemis, and P. N. Tsichlis. 1995. AH/PH domain-mediated interaction between Akt molecules and its potential role in Akt regulation. Mol. Cell. Biol. 15: 2304–2310.
   PubMedGoogle Scholar
• Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351: 95–105.
   PubMed Web of Science ®Google Scholar
• Dobrowsky, R. T. 2000. Sphingolipid signalling domains floating on rafts or buried in caves? Cell Signal 12: 81–90.
   PubMed Web of Science ®Google Scholar
• Doornbos, R. P., M. Theelen, P. C. van der Hoeven, W. J. van Blitterswijk, A. J. Verkleij, and van Bergen en Henegouwen PM. 1999. Protein kinase Cζ is a negative regulator of protein kinase B activity. J. Biol. Chem. 274: 8589–8596.
   PubMedGoogle Scholar
• Dowler, S., G. Kular, and D. R. Alessi. 2002. Protein lipid overlay assay. Science STKE 2002: L6.
   Google Scholar
• Gray, A., H. Olsson, I. H. Batty, L. Priganica, and C. P. Downes. 2003. Nonradioactive methods for the assay of phosphoinositide 3-kinases and phosphoinositide phosphatases and selective detection of signaling lipids in cell and tissue extracts. Anal. Biochem. 313: 234–245.
   PubMed Web of Science ®Google Scholar
• Hajduch, E., D. R. Alessi, B. A. Hemmings, and H. S. Hundal. 1998. Constitutive activation of protein kinase Bα (PKBα) by membrane targeting promotes glucose and system A amino acid transport, protein synthesis and GSK3 inactivation in L6 muscle cells. Diabetes 47: 1006–1013.
   PubMed Web of Science ®Google Scholar
• Hajduch, E., A. Balendran, I. H. Batty, G. J. Litherland, A. S. Blair, C. P. Downes, and H. S. Hundal. 2001. Ceramide impairs the insulin-dependent membrane recruitment of protein kinase B leading to a loss in downstream signalling in L6 skeletal muscle cells. Diabetologia 44: 173–183.
   PubMedGoogle Scholar
• Hajduch, E., G. J. Litherland, and H. S. Hundal. 2001. Protein kinase B: a key regulator of glucose transport? FEBS Lett. 492: 199–203.
   PubMed Web of Science ®Google Scholar
• Hannun, Y. A., and L. M. Obeid. 2002. The Ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind. J. Biol. Chem. 277: 25847–25850.
   PubMed Web of Science ®Google Scholar
• Hodgkinson, C. P., E. M. Sale, and G. J. Sale. 2002. Characterization of PDK2 activity against protein kinase B gamma. Biochemistry 41: 10351–10359.
   PubMed Web of Science ®Google Scholar
• Ko, Y. G., J. S. Lee, Y. S. Kang, J. H. Ahn, and J. S. Seo. 1999. TNF-alpha-mediated apoptosis is initiated in caveolae-like domains. J. Immunol. 162: 7217–7223.
   PubMed Web of Science ®Google Scholar
• Kolesnick, R. 2002. The therapeutic potential of modulating the ceramide/sphingomyelin pathway. J. Clin. Investig. 110: 3–8.
   PubMed Web of Science ®Google Scholar
• Kolesnick, R. N., and M. Kronke. 1998. Regulation of ceramide production and apoptosis. Annu. Rev. Physiol. 60: 643–665.
   PubMed Web of Science ®Google Scholar
• Konishi, H., S. Kuroda, and U. Kikkawa. 1994. The pleckstrin homology domain of RAC protein kinase associates with the regulatory domain of protein kinase C ζ. Biochem. Biophys. Res. Commun. 205: 1770–1775.
   PubMedGoogle Scholar
• Lawlor, M. A., and D. R. Alessi. 2001. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J. Cell Sci. 114: 2903–2910.
   PubMed Web of Science ®Google Scholar
• Mao, M., X. Fang, Y. Lu, R. Lapushin, J. R. Bast, and G. B. Mills. 2000. Inhibition of growth-factor-induced phosphorylation and activation of protein kinase B/Akt by atypical protein kinase C in breast cancer cells. Biochem. J. 352: 475–482.
   PubMedGoogle Scholar
• Mathias, S., L. A. Pena, and R. N. Kolesnick. 1998. Signal transduction of stress via ceramide. Biochem. J. 335: 465–480.
   PubMed Web of Science ®Google Scholar
• Muller, G., M. Ayoub, P. Storz, J. Rennecke, D. Fabbro, and K. Pfizenmaier. 1995. PKCζ is a molecular switch in signal transduction of TNF-α, bifunctionally regulated by ceramide and arachidonic acid. EMBO J. 14: 1961–1969.
   PubMedGoogle Scholar
• Oka, N., M. Yamamoto, C. Schwencke, J. Kawabe, T. Ebina, S. Ohno, J. Couet, M. P. Lisanti, and Y. Ishikawa. 1997. Caveolin interaction with protein kinase C: isoenzyme-dependent regulation of kinase activity by the caveolin scaffolding domain peptide. J. Biol. Chem. 272: 33416–33421.
   PubMed Web of Science ®Google Scholar
• Puceat, M., R. Hilal-Dandan, B. Strulovici, L. L. Brunton, and J. H. Brown. 1994. Differential regulation of protein kinase C isoforms in isolated neonatal and adult rat cardiomyocytes. J. Biol. Chem. 269: 16938–16944.
   PubMed Web of Science ®Google Scholar
• Salinas, M., R. Lopez-Valdaliso, D. Martin, A. Alvarez, and A. Cuadrado. 2000. Inhibition of PKB/Akt1 by C2-ceramide involves activation of ceramide-activated protein phosphatase in PC12 cells. Mol. Cell. Neurosci. 15: 156–169.
   PubMedGoogle Scholar
• Schmitz-Peiffer, C., D. L. Craig, and T. J. Biden. 1999. Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J. Biol. Chem. 274: 24202–24210.
   PubMed Web of Science ®Google Scholar
• Standaert, M. L., G. Bandyopadhyay, Y. Kanoh, M. P. Sajan, and R. V. Farese. 2001. Insulin and PIP3 activate PKC-ζ by mechanisms that are both dependent and independent of phosphorylation of activation loop (T410) and autophosphorylation (T560) sites. Biochemistry 40: 249–255.
   PubMedGoogle Scholar
• Standaert, M. L., L. Galloway, P. Karnam, G. Bandyopadhyay, J. Moscat, and R. V. Farese. 1997. Protein kinase C-ζ as a downstream effector of phosphatidylinositol 3-kinase during insulin stimulation in rat adipocytes: potential role in glucose transport. J. Biol. Chem. 272: 30075–30082.
   PubMed Web of Science ®Google Scholar
• Stokoe, D., L. R. Stephens, T. Copeland, P. R. J. Gaffney, C. B. Reese, G. F. Painter, A. B. Holmes, F. McCormick, and P. T. Hawkins. 1997. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277: 567–570.
   PubMed Web of Science ®Google Scholar
• Stratford, S., D. B. Dewald, and S. A. Summers. 2001. Ceramide dissociates 3′-phosphoinositide production from pleckstrin homology domain translocation. Biochem. J. 354: 359–368.
   PubMed Web of Science ®Google Scholar
• Summers, S. A., L. A. Garza, H. Zhou, and M. J. Birnbaum. 1998. Regulation of insulin-stimulated glucose transporter GLUT4 translocation and Akt kinase activity by ceramide. Mol. Cell. Biol. 18: 5457–5464.
   PubMed Web of Science ®Google Scholar
• Thomas, C. C., M. Deak, D. R. Alessi, and D. M. van Aalten. 2002. High-resolution structure of the pleckstrin homology domain of protein kinase B/akt bound to phosphatidylinositol-(3,4,5)-trisphosphate. Curr. Biol. 12: 1256–1262.
   PubMedGoogle Scholar
• Whiteman, E. L., H. Cho, and M. J. Birnbaum. 2002. Role of Akt/protein kinase B in metabolism. Trends Endocrinol. Metab. 13: 444–451.
   PubMed Web of Science ®Google Scholar
• Yaffe, M. B., G. G. Leparc, J. Lai, T. Obata, S. Volinia, and L. C. Cantley. 2001. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat. Biotechnol. 19: 348–353.
   PubMed Web of Science ®Google Scholar
• Zhou, H., S. A. Summers, M. J. Birnbaum, and R. N. Pittman. 1998. Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J. Biol. Chem. 273: 16568–16575.
   PubMed Web of Science ®Google Scholar
• Zundel, W., and A. Giaccia. 1998. Inhibition of the anti-apoptotic PI(3)K/Akt/Bad pathway by stress. Genes Dev. 12: 1941–1946.
   PubMed Web of Science ®Google Scholar