14
Views
60
CrossRef citations to date
0
Altmetric
Cell and Organelle Structure and Assembly

Intracellular Segregation of Phosphatidylinositol-3,4,5-Trisphosphate by Insulin-Dependent Actin Remodeling in L6 Skeletal Muscle Cells

, , , &
Pages 4611-4626 | Received 20 Aug 2002, Accepted 16 Apr 2003, Published online: 27 Mar 2023

REFERENCES

  • Asano, T., A. Kanda, H. Katagiri, M. Nawano, T. Ogihara, K. Inukai, M. Anai, Y. Fukushima, Y. Yazaki, M. Kikuchi, R. Hooshmand-Rad, C. H. Heldin, Y. Oka, and M. Funaki. 2000. p110beta is up-regulated during differentiation of 3T3-L1 cells and contributes to the highly insulin-responsive glucose transport activity. J. Biol. Chem. 275: 17671–17676.
  • Bandyopadhyay, G., M. L. Standaert, L. Galloway, J. Moscat, and R. V. Farese. 1997. Evidence for involvement of protein kinase C (PKC)-zeta and noninvolvement of diacylglycerol-sensitive PKCs in insulin-stimulated glucose transport in L6 myotubes. Endocrinology 138: 4721–4731.
  • Braiman, L., A. Alt, T. Kuroki, M. Ohba, A. Bak, T. Tennenbaum, and S. R. Sampson. 2001. Activation of protein kinase Cζ induces serine phosphorylation of VAMP2 in the GLUT4 compartment and increases glucose transport in skeletal muscle. Mol. Cell. Biol. 21: 7852–7861.
  • Brozinick, J. T., Jr., and M. J. Birnbaum. 1998. Insulin, but not contraction, activates Akt/PKB in isolated rat skeletal muscle. J. Biol. Chem. 273: 14679–14682.
  • 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.
  • Chiang, S. H., C. A. Baumann, M. Kanzaki, D. C. Thurmond, R. T. Watson, C. L. Neudauer, I. G. Macara, J. E. Pessin, and A. R. Saltiel. 2001. Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 410: 944–948.
  • Clark, S. F., S. Martin, A. J. Carozzi, M. M. Hill, and D. E. James. 1998. Intracellular localization of phosphatidylinositide 3-kinase and insulin receptor substrate-1 in adipocytes: potential involvement of a membrane skeleton. J. Cell Biol. 140: 1211–1225.
  • Clark, S. F., J. C. Molero, and D. E. James. 2000. Release of insulin receptor substrate proteins from an intracellular complex coincides with the development of insulin resistance. J. Biol. Chem. 275: 3819–3826.
  • Clarke, J. F., P. W. Young, K. Yonezawa, M. Kasuga, and G. D. Holman. 1994. Inhibition of the translocation of GLUT1 and GLUT4 in 3T3-L1 cells by the phosphatidylinositol 3-kinase inhibitor, wortmannin. Biochem. J. 300: 631–635.
  • Douen, A. G., T. Ramlal, S. Rastogi, P. J. Bilan, G. D. Cartee, M. Vranic, J. O. Holloszy, and A. Klip. 1990. Exercise induces recruitment of the “insulin-responsive glucose transporter.” Evidence for distinct intracellular insulin- and exercise-recruitable transporter pools in skeletal muscle. J. Biol. Chem. 265: 13427–13430.
  • Ducluzeau, P. H., L. M. Fletcher, G. I. Welsh, and J. M. Tavare. 2002. Functional consequence of targeting protein kinase B/Akt to GLUT4 vesicles. J. Cell Sci. 115: 2857–2866.
  • Egawa, K., H. Maegawa, K. Shi, T. Nakamura, T. Obata, T. Yoshizaki, K. Morino, S. Shimizu, Y. Nishio, E. Suzuki, and A. Kashiwagi. 2002. Membrane localization of 3-phosphoinositide-dependent protein kinase-1 stimulates activities of Akt and atypical PKC, but does not stimulate glucose transport and glycogen synthesis in 3T3-L1 adipocytes. J. Biol. Chem. 277: 38863-38869.
  • Foster, L. J., D. Li, V. K. Randhawa, and A. Klip. 2001. Insulin accelerates inter-endosomal GLUT4 traffic via phosphatidylinositol 3-kinase and protein kinase B. J. Biol. Chem. 276: 44212–44221.
  • Franke, T. F., D. R. Kaplan, L. C. Cantley, and A. Toker. 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275: 665–668.
  • Frech, M., M. Andjelkovic, E. Ingley, K. K. Reddy, J. R. Falck, and B. A. Hemmings. 1997. High affinity binding of inositol phosphates and phosphoinositides to the pleckstrin homology domain of RAC/protein kinase B and their influence on kinase activity. J. Biol. Chem. 272: 8474–8481.
  • Goodyear, L. J., M. F. Hirshman, R. Napoli, J. Calles, J. F. Markuns, O. Ljungqvist, and E. S. Horton. 1996. Glucose ingestion causes GLUT4 translocation in human skeletal muscle. Diabetes 45: 1051–1056.
  • Gray, A., J. Van Der Kaay, and C. P. Downes. 1999. The pleckstrin homology domains of protein kinase B and GRP1 (general receptor for phosphoinositides-1) are sensitive and selective probes for the cellular detection of phosphatidylinositol 3,4-bisphosphate and/or phosphatidylinositol 3,4,5-trisphosphate in vivo. Biochem. J. 344(Pt 3): 929–936.
  • Heart, E., W. S. Choi, and C. K. Sung. 2000. Glucosamine-induced insulin resistance in 3T3-L1 adipocytes. Am. J. Physiol. 278: E103–E112.
  • Heller-Harrison, R. A., M. Morin, A. Guilherme, and M. P. Czech. 1996. Insulin-mediated targeting of phosphatidylinositol 3-kinase to GLUT4-containing vesicles. J. Biol. Chem. 271: 10200–10204.
  • Hill, M. M., S. F. Clark, D. F. Tucker, M. J. Birnbaum, D. E. James, and S. L. Macaulay. 1999. A role for protein kinase Bbeta/Akt2 in insulin-stimulated GLUT4 translocation in adipocytes. Mol. Cell. Biol. 19: 7771–7781.
  • Hooshmand-Rad, R., L. Hajkova, P. Klint, R. Karlsson, B. Vanhaesebroeck, L. Claesson-Welsh, and C. H. Heldin. 2000. The PI 3-kinase isoforms p110(alpha) and p110(beta) have differential roles in PDGF- and insulin-mediated signaling. J. Cell Sci. 113(Pt. 2): 207–214.
  • Huang, C., R. Somwar, N. Patel, W. Niu, D. Torok, and A. Klip. 2002. Sustained exposure of L6 myotubes to high glucose and insulin decreases insulin-stimulated GLUT4 translocation but upregulates GLUT4 activity. Diabetes 51: 2090–2098.
  • Inoue, G., B. Cheatham, R. Emkey, and C. R. Kahn. 1998. Dynamics of insulin signaling in 3T3-L1 adipocytes. Differential compartmentalization and trafficking of insulin receptor substrate (IRS)-1 and IRS-2. J. Biol. Chem. 273: 11548–11555.
  • Jiang, Z. Y., A. Chawla, A. Bose, M. Way, and M. P. Czech. 2002. A phosphatidylinositol 3-kinase-independent insulin signaling pathway to N-WASP/Arp2/3/F-actin required for GLUT4 glucose transporter recycling. J. Biol. Chem. 277: 509–515.
  • Kanzaki, M., and J. E. Pessin. 2001. Insulin-stimulated GLUT4 translocation in adipocytes is dependent upon cortical actin remodeling. J. Biol. Chem. 276: 42436–42444.
  • Kanzaki, M., R. T. Watson, A. H. Khan, and J. E. Pessin. 2001. Insulin stimulates actin comet tails on intracellular GLUT4-containing compartments in differentiated 3T3L1 adipocytes. J. Biol. Chem. 276: 49331–49336.
  • Katagiri, H., T. Asano, H. Ishihara, K. Inukai, Y. Shibasaki, M. Kikuchi, Y. Yazaki, and Y. Oka. 1996. Overexpression of catalytic subunit p110alpha of phosphatidylinositol 3- kinase increases glucose transport activity with translocation of glucose transporters in 3T3-L1 adipocytes. J. Biol. Chem. 271: 16987–16990.
  • Kelly, K. L., and N. B. Ruderman. 1993. Insulin-stimulated phosphatidylinositol 3-kinase. Association with a 185-kDa tyrosine-phosphorylated protein (IRS-1) and localization in a low density membrane vesicle. J. Biol. Chem. 268: 4391–4398.
  • Khayat, Z. A., P. Tong, K. Yaworsky, R. J. Bloch, and A. Klip. 2000. Insulin-induced actin filament remodeling colocalizes actin with phosphatidylinositol 3-kinase and GLUT4 in L6 myotubes. J. Cell Sci. 113(Pt. 2): 279–290.
  • Klarlund, J. K., W. Tsiaras, J. J. Holik, A. Chawla, and M. P. Czech. 2000. Distinct polyphosphoinositide binding selectivities for pleckstrin homology domains of GRP1-like proteins based on diglycine versus triglycine motifs. J. Biol. Chem. 275: 32816–32821.
  • 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.
  • Kupriyanova, T. A., and K. V. Kandror. 1999. Akt-2 binds to Glut4-containing vesicles and phosphorylates their component proteins in response to insulin. J. Biol. Chem. 274: 1458–1464.
  • Marette, A., E. Burdett, A. Douen, M. Vranic, and A. Klip. 1992. Insulin induces the translocation of GLUT4 from a unique intracellular organelle to transverse tubules in rat skeletal muscle. Diabetes 41: 1562–1569.
  • Martelli, A. M., P. Borgatti, R. Bortul, M. Manfredini, L. Massari, S. Capitani, and L. M. Neri. 2000. Phosphatidylinositol 3-kinase translocates to the nucleus of osteoblast-like MC3T3-E1 cells in response to insulin-like growth factor I and platelet-derived growth factor but not to the proapoptotic cytokine tumor necrosis factor alpha. J. Bone Miner. Res. 15: 1716–1730.
  • Mosser, V. A., Y. Li, and M. J. Quon. 2001. PTEN does not modulate GLUT4 translocation in rat adipose cells under physiological conditions. Biochem. Biophys. Res. Commun. 288: 1011–1017.
  • Nakanishi, H., K. A. Brewer, and J. H. Exton. 1993. Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 268: 13–16.
  • Nakashima, N., P. M. Sharma, T. Imamura, R. Bookstein, and J. M. Olefsky. 2000. The tumor suppressor PTEN negatively regulates insulin signaling in 3T3-L1 adipocytes. J. Biol. Chem. 275: 12889–12895.
  • Nave, B. T., R. J. Haigh, A. C. Hayward, K. Siddle, and P. R. Shepherd. 1996. Compartment-specific regulation of phosphoinositide 3-kinase by platelet-derived growth factor and insulin in 3T3-L1 adipocytes. Biochem. J. 318: 55–60.
  • Nawano, M., K. Ueta, A. Oku, K. Arakawa, A. Saito, M. Funaki, M. Anai, M. Kikuchi, Y. Oka, and T. Asano. 1999. Hyperglycemia impairs the insulin signaling step between PI 3-kinase and Akt/PKB activations in ZDF rat liver. Biochem. Biophys. Res. Commun. 266: 252–256.
  • Oatey, P. B., K. Venkateswarlu, A. G. Williams, L. M. Fletcher, E. J. Foulstone, P. J. Cullen, and J. M. Tavare. 1999. Confocal imaging of the subcellular distribution of phosphatidylinositol 3,4,5-trisphosphate in insulin- and PDGF-stimulated 3T3-L1 adipocytes. Biochem. J. 344(Pt. 2): 511–518.
  • Omata, W., H. Shibata, L. Li, K. Takata, and I. Kojima. 2000. Actin filaments play a critical role in insulin-induced exocytotic recruitment but not in endocytosis of GLUT4 in isolated rat adipocytes. Biochem. J. 346(Pt. 2): 321–328.
  • Patki, V., J. Buxton, A. Chawla, L. Lifshitz, K. Fogarty, W. Carrington, R. Tuft, and S. Corvera. 2001. Insulin action on GLUT4 traffic visualized in single 3T3-l1 adipocytes by using ultra-fast microscopy. Mol. Biol. Cell 12: 129–141.
  • Peyrollier, K., E. Hajduch, A. Gray, G. J. Litherland, A. R. Prescott, N. R. Leslie, and H. S. Hundal. 2000. A role for the actin cytoskeleton in the hormonal and growth-factor-mediated activation of protein kinase B. Biochem. J. 352(Pt. 3): 617–622.
  • Rameh, L. E., A. Arvidsson, K. L. Carraway III, A. D. Couvillon, G. Rathbun, A. Crompton, B. VanRenterghem, M. P. Czech, K. S. Ravichandran, S. J. Burakoff, D. S. Wang, C. S. Chen, and L. C. Cantley. 1997. A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem. 272: 22059–22066.
  • Randhawa, V. K., P. J. Bilan, Z. A. Khayat, N. Daneman, Z. Liu, T. Ramlal, A. Volchuk, X. R. Peng, T. Coppola, R. Regazzi, W. S. Trimble, and A. Klip. 2000. VAMP2, but not VAMP3/cellubrevin, mediates insulin-dependent incorporation of GLUT4 into the plasma membrane of L6 myoblasts. Mol. Biol. Cell 11: 2403–2417.
  • Ricort, J. M., J. F. Tanti, E. Van Obberghen, and Y. Le Marchand-Brustel. 1996. Different effects of insulin and platelet-derived growth factor on phosphatidylinositol 3-kinase at the subcellular level in 3T3-L1 adipocytes. A possible explanation for their specific effects on glucose transport. Eur. J. Biochem. 239: 17–22.
  • Ryder, J. W., J. Yang, D. Galuska, J. Rincon, M. Bjornholm, A. Krook, S. Lund, O. Pedersen, H. Wallberg-Henriksson, J. R. Zierath, and G. D. Holman. 2000. Use of a novel impermeable biotinylated photolabeling reagent to assess insulin- and hypoxia-stimulated cell surface GLUT4 content in skeletal muscle from type 2 diabetic patients. Diabetes 49: 647–654.
  • Shepherd, P. R., D. J. Withers, and K. Siddle. 1998. Phosphoinositide 3-kinase: the key switch mechanism in insulin signaling. Biochem. J. 333: 471–490.
  • Siddhanta, U., J. McIlroy, A. Shah, Y. Zhang, and J. M. Backer. 1998. Distinct roles for the p110alpha and hVPS34 phosphatidylinositol 3′-kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J. Cell Biol. 143: 1647–1659.
  • Somwar, R., W. Niu, D. Y. Kim, G. Sweeney, V. K. Randhawa, C. Huang, T. Ramlal, and A. Klip. 2001. Differential effects of phosphatidylinositol 3-kinase inhibition on intracellular signals regulating GLUT4 translocation and glucose transport. J. Biol. Chem. 276: 46079–46087.
  • Standaert, M. L., L. Galloway, P. Karnam, G. Bandyopadhyay, J. Moscat, and R. V. Farese. 1997. Protein kinase C-zeta 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.
  • Tengholm, A., and T. Meyer. 2002. A PI3-kinase signaling code for insulin-triggered insertion of glucose transporters into the plasma membrane. Curr. Biol. 12: 1871–1876.
  • Tirosh, A., R. Potashnik, N. Bashan, and A. Rudich. 1999. Oxidative stress disrupts insulin-induced cellular redistribution of insulin receptor substrate-1 and phosphatidylinositol 3-kinase in 3T3-L1 adipocytes. A putative cellular mechanism for impaired protein kinase B activation and GLUT4 translocation. J. Biol. Chem. 274: 10595–10602.
  • Tong, P., Z. A. Khayat, C. S. Chan, and A. Klip. 2001. A mechanism for the impairment of insulin action by high levels of insulin and glucose in L6 rat skeletal muscle cells. Diabetes 50(Suppl. 2): A507.
  • Tong, P., Z. A. Khayat, C. Huang, N. Patel, A. Ueyama, and A. Klip. 2001. Insulin-induced cortical actin remodeling promotes GLUT4 insertion at muscle cell membrane ruffles. J. Clin. Investig. 108: 371–381.
  • Tsakiridis, T., A. Bergman, R. Somwar, C. Taha, K. Aktories, T. F. Cruz, A. Klip, and G. P. Downey. 1998. Actin filaments facilitate insulin activation of the src and collagen homologous/mitogen-activated protein kinase pathway leading to DNA synthesis and c-fos expression. J. Biol. Chem. 273: 28322–28331.
  • Tsakiridis, T., H. E. McDowell, T. Walker, C. P. Downes, H. S. Hundal, M. Vranic, and A. Klip. 1995. Multiple roles of phosphatidylinositol 3-kinase in regulation of glucose transport, amino acid transport, and glucose transporters in L6 skeletal muscle cells. Endocrinology 136: 4315–4322.
  • Tsakiridis, T., P. Tong, B. Matthews, E. Tsiani, P. J. Bilan, A. Klip, and G. P. Downey. 1999. Role of the actin cytoskeleton in insulin action. Microsc. Res. Tech. 47: 79–92.
  • Tsakiridis, T., M. Vranic, and A. Klip. 1994. Disassembly of the actin network inhibits insulin-dependent stimulation of glucose transport and prevents recruitment of glucose transporters to the plasma membrane. J. Biol. Chem. 269: 29934–29942.
  • Tsakiridis, T., M. Vranic, and A. Klip. 1995. Phosphatidylinositol 3-kinase and the actin network are not required for the stimulation of glucose transport caused by mitochondrial uncoupling: comparison with insulin action. Biochem. J. 309: 1–5.
  • Tsuji, Y., Y. Kaburagi, Y. Terauchi, S. Satoh, N. Kubota, H. Tamemoto, F. B. Kraemer, H. Sekihara, S. Aizawa, Y. Akanuma, K. Tobe, S. Kimura, and T. Kadowaki. 2001. Subcellular localization of insulin receptor substrate family proteins associated with phosphatidylinositol 3-kinase activity and alterations in lipolysis in primary mouse adipocytes from IRS-1 null mice. Diabetes 50: 1455–1463.
  • Turinsky, J., and A. Damrau-Abney. 1999. Akt kinases and 2-deoxyglucose uptake in rat skeletal muscles in vivo: study with insulin and exercise. Am. J. Physiol. 276: R277–R282.
  • Ueyama, A., K. L. Yaworsky, Q. Wang, Y. Ebina, and A. Klip. 1999. GLUT-4myc ectopic expression in L6 myoblasts generates a GLUT-4-specific pool conferring insulin sensitivity. Am. J. Physiol. 277: E572–E578.
  • Venkateswarlu, K., P. B. Oatey, J. M. Tavare, and P. J. Cullen. 1998. Insulin-dependent translocation of ARNO to the plasma membrane of adipocytes requires phosphatidylinositol 3-kinase. Curr. Biol. 8: 463–466.
  • Wada, T., T. Sasaoka, M. Funaki, H. Hori, S. Murakami, M. Ishiki, T. Haruta, T. Asano, W. Ogawa, H. Ishihara, and M. Kobayashi. 2001. Overexpression of SH2-containing inositol phosphatase 2 results in negative regulation of insulin-induced metabolic actions in 3T3-L1 adipocytes via its 5′-phosphatase catalytic activity. Mol. Cell. Biol. 21: 1633–1646.
  • Wang, F., P. Herzmark, O. D. Weiner, S. Srinivasan, G. Servant, and H. R. Bourne. 2002. Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat. Cell Biol. 4: 513–518.
  • Wang, Q., P. J. Bilan, T. Tsakiridis, A. Hinek, and A. Klip. 1998. Actin filaments participate in the relocalization of phosphatidylinositol 3-kinase to glucose transporter-containing compartments and in the stimulation of glucose uptake in 3T3-L1 adipocytes. Biochem. J. 331: 917–928.
  • Wang, Q., Z. Khayat, K. Kishi, Y. Ebina, and A. Klip. 1998. GLUT4 translocation by insulin in intact muscle cells: detection by a fast and quantitative assay. FEBS Lett. 427: 193–197.
  • Wang, Q., R. Somwar, P. J. Bilan, Z. Liu, J. Jin, J. R. Woodgett, and A. Klip. 1999. Protein kinase B/Akt participates in GLUT4 translocation by insulin in L6 myoblasts. Mol. Cell. Biol. 19: 4008–4018.
  • Weiner, O. D., P. O. Neilsen, G. D. Prestwich, M. W. Kirschner, L. C. Cantley, and H. R. Bourne. 2002. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 4: 509–513.
  • White, M. F., and C. R. Kahn. 1994. The insulin signaling system. J. Biol. Chem. 269: 1–4.
  • Zierath, J. R., L. He, A. Guma, E. Odegoard Wahlstrom, A. Klip, and H. Wallberg-Henriksson. 1996. Insulin action on glucose transport and plasma membrane GLUT4 content in skeletal muscle from patients with NIDDM. Diabetologia 39: 1180–1189.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.