Loss of cortical actin filaments in insulin-resistant skeletal muscle cells impairs GLUT4 vesicle trafficking and glucose transport

American Journal of Physiology - Cell Physiology

Volumn 291, Issue 5, 2006, Pages

  McCarthy, Alicia M ^a   Spisak, Kristen O ^a   Brozinick, Joseph T ^a,b   Elmendorf, Jeffrey S ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ELI LILLY AND COMPANY   (United States)

Author keywords

Hyperinsulinemia; Phosphatidylinositol 4,5 bisphosphate

Indexed keywords

F ACTIN; GLUCOSE TRANSPORTER 4; INSULIN; MYC PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FEMALE; GLUCOSE TRANSPORT; HYPERINSULINEMIA; INSULIN RESISTANCE; MUSCLE CELL; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELLS, CULTURED; CYTOSKELETON; FEMALE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; INSULIN; INSULIN RESISTANCE; MICROFILAMENTS; MUSCLE FIBERS; MUSCLE, SKELETAL; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PREDIABETIC STATE; RATS; SIGNAL TRANSDUCTION; TRANSPORT VESICLES;

EID: 33751076023     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00107.2006     Document Type: Article

References (49)

1. Advani A, Marshall SM, and Thomas TH. Impaired neutrophil actin assembly causes persistent CD11b expression and reduced primary granule exocytosis in Type II diabetes. Diabetologia 45: 719-727, 2002.
2. Advani A, Marshall SM, and Thomas TH. Increasing neutrophil F-actin corrects CD11b exposure in Type 2 diabetes. Eur J Clin Invest 34: 358-364, 2004.
3. Asahi Y, Hayashi H, Wang L, and Ebina Y. Fluoromicroscopic detection of myc-tagged GLUT4 on the cell surface. Co-localization of the translocated GLUT4 with rearranged actin by insulin treatment in CHO cells and L6 myotubes. J Med Invest 46: 192-199, 1999.
4. Bae SS, Cho H, Mu J, and Birnbaum MJ. Isoform-specific regulation of insulin-dependent glucose uptake by Akt/protein kinase B. J Biol Chem 278: 49530-49536, 2003.
5. Baron AD, Brechtel G, Wallace P, and Edelman SV. Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. Am J Physiol Endocrinol Metab 255: E769-E774, 1988.
6. Bose A, Cherniack AD, Langille SE, Nicoloro SM, Buxton JM, Park JG, Chawla A, and Czech MP. G(alpha)11 signaling through ARF6 regulates F-actin mobilization and GLUT4 glucose transporter translocation to the plasma membrane. Mol Cell Biol 21: 5262-5275, 2001.
7. Brozinick JT Jr, Hawkins ED, Strawbridge AB, and Elmendorf JS. Disruption of cortical actin in skeletal muscle demonstrates an essential role of the cytoskeleton in glucose transporter 4 translocation in insulin-sensitive tissues. J Biol Chem 279: 40699-40706, 2004.
8. Brozinick JT Jr, Roberts BR, and Dohm GL. Defective signaling through Akt-2 and -3 but not Akt-1 in insulin-resistant human skeletal muscle: potential role in insulin resistance. Diabetes 52: 935-941, 2003.
9. Candiloros H, Zeghari N, Ziegler O, Donner M, and Drouin P. Hyperinsulinemia is related to erythrocyte phospholipid composition and membrane fluidity changes in obese nondiabetic women. J Clin Endocrinol Metab 81: 2912-2918, 1996.
10. Chen F, Ma L, Parrini MC, Mao X, Lopez M, Wu C, Marks PW, Davidson L, Kwiatkowski DJ, Kirchhausen T, Orkin SH, Rosen FS, Mayer BJ, Kirschner MW, and Alt FW. Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability. Curr Biol 10: 758-765, 2000.
11. Chen G, Raman P, Bhonagiri P, Strawbridge AB, Pattar GR, and Elmendorf JS. Protective effect of phosphatidylinositol 4,5-bisphosphate against cortical filamentous actin loss and insulin resistance induced by sustained exposure of 3T3-L1 adipocytes to insulin. J Biol Chem 279: 39705-39709, 2004.
12. DeFronzo RA, Gunnarsson R, Bjorkman O, Olsson M, and Wahren J. Effects of insulin on peripheral and splanchnic glucose metabolism in noninsulin-dependent (type II) diabetes mellitus. J Clin Invest 76: 149-155, 1985.
13. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, and Felber JP. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30: 1000-1007, 1981.
14. Emoto M, Langille SE, and Czech MP. A role for kinesin in insulin-stimulated GLUT4 glucose transporter translocation in 3T3-L1 adipocytes. J Biol Chem 276: 10677-10682, 2001.
15. Ferrannini E, Haffner SM, Mitchell BD, and Stern MP. Hyperinsulinaemia: the key feature of a cardiovascular and metabolic syndrome. Diabetologia 34: 416-422, 1991.
16. Ferrannini E, Smith JD, Cobelli C, Toffolo G, Pilo A, and DeFronzo RA. Effect of insulin on the distribution and disposition of glucose in man. J Clin Invest 76: 357-364, 1985.
17. Gabella G. Inpocketings of the cell membrane (caveolae) in the rat myocardium. J Ultrastruct Res 65: 135-147, 1978.
18. Guilherme A, Emoto M, Buxton JM, Bose S, Sabini R, Theurkauf WE, Leszyk J, and Czech MP. Perinuclear localization and insulin responsiveness of GLUT4 requires cytoskeletal integrity in 3T3-L1 adipocytes. J Biol Chem 275: 38151-38159, 2000.
19. Hilpela P, Vartiainen MK, and Lappalainen P. Regulation of the actin cytoskeleton by PI(4,5)P2 and PI(3,4,5)P3. Curr Top Microbiol Immunol 282: 117-163, 2004.
20. Huang C, Somwar R, Patel N, Niu W, Torok D, and Klip A. Sustained exposure of L6 myotubes to high glucose and insulin decreases insulin-stimulated GLUT4 translocation but upregulates GLUT4 activity. Diabetes 51: 2090-2098, 2002.
21. Imamura T, Ishibashi K, Dalle S, Ugi S, and Olefsky JM. Endothelin-1-induced GLUT4 translocation is mediated via Gα(q/11) protein and phosphatidylinositol 3-kinase in 3T3-L1 adipocytes. J Biol Chem 274: 33691-33695, 1999.
22. Kanai F, Nishioka Y, Hayashi H, Kamohara S, Todaka M, and Ebina Y. Direct demonstration of insulin-induced GLUT4 translocation to the surface of intact cells by insertion of a c-myc epitope into an exofacial GLUT4 domain. J Biol Chem 268: 14523-14526, 1993.
23. Kane S, Sano H, Liu SC, Asara JM, Lane WS, Garner CC, and Lienhard GE. A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J Biol Chem 277: 22115-22118, 2002.
24. Kanzaki M, Watson RT, Hou JC, Stamnes M, Saltiel AR, and Pessin JE. Small GTP-binding protein TC10 differentially regulates two distinct populations of filamentous actin in 3T3L1 adipocytes. Mol Biol Cell 13: 2334-2346, 2002.
25. 2+ and cPKC. Am J Physiol Cell Physiol 275: C1487-C1497, 1998.
26. Koopmans SJ, Ohman L, Haywood JR, Mandarino LJ, and DeFronzo RA. Seven days of euglycemic hyperinsulinemia induces insulin resistance for glucose metabolism but not hypertension, elevated catecholamine levels, or increased sodium retention in conscious normal rats. Diabetes 46: 1572-1578, 1997.
27. Kralik SF, Liu P, Leffler BJ, and Elmendorf JS. Ceramide and glucosamine antagonism of alternate signaling pathways regulating insulin- and osmotic shock-induced glucose transporter 4 translocation. Endocrinology 143: 37-46, 2002.
28. Krook A, Bjornholm M, Galuska D, Jiang XJ, Fahlman R, Myers MG Jr, Wallberg-Henriksson H, and Zierath JR. Characterization of signal transduction and glucose transport in skeletal muscle from type 2 diabetic patients. Diabetes 49: 284-292, 2000.
29. Mulvey C, Harno E, Keenan A, and Ohlendieck K. Expression of the skeletal muscle dystrophin-dystroglycan complex and syntrophin-nitric oxide synthase complex is severely affected in the type 2 diabetic Goto-Kakizaki rat. Eur J Cell Biol 84: 867-883, 2005.
30. Nelson BA, Robinson KA, and Buse MG. High glucose and glucosamine induce insulin resistance via different mechanisms in 3T3-L1 adipocytes. Diabetes 49: 981-991, 2000.
31. Omata W, Shibata H, Li L, Takata K, and Kojima I. Actin filaments play a critical role in insulin-induced exocytotic recruitment but not in endocytosis of GLUT4 in isolated rat adipocytes. Biochem J 346: 321-328, 2000.
32. Ozaki S, DeWald DB, Shope JC, Chen J, and Prestwich GD. Intracellular delivery of phosphoinositides and inositol phosphates using polyamine carriers. Proc Natl Acad Sci USA 97: 11286-11291, 2000.
33. Phillips MS, Liu Q, Hammond HA, Dugan V, Hey PJ, Caskey CJ, and Hess JF. Leptin receptor missense mutation in the fatty Zucker rat. Nat Genet 13: 18-19, 1996.
34. Pirola L, Bonnafous S, Johnston AM, Chaussade C, Portis F, and Van Obberghen E. Phosphoinositide 3-kinase-mediated reduction of insulin receptor substrate-1/2 protein expression via different mechanisms contributes to the insulin-induced desensitization of its signaling pathways in L6 muscle cells. J Biol Chem 278: 15641-15651, 2003.
35. Razidlo GL, Kortum RL, Haferbier JL, and Lewis RE. Phosphorylation regulates KSR1 stability, ERK activation, and cell proliferation. J Biol Chem 279: 47808-47814, 2004.
36. Ricort JM, Tanti JF, Van Obberghen E, and Le Marchand-Brustel Y. Alterations in insulin signalling pathway induced by prolonged insulin treatment of 3T3-L1 adipocytes. Diabetologia 38: 1148-1156, 1995.
37. Ross SA, Chen X, Hope HR, Sun S, McMahon EG, Broschat K, and Gulve EA. Development and comparison of two 3T3-L1 adipocyte models of insulin resistance: increased glucose flux vs glucosamine treatment. Biochem Biophys Res Commun 273: 1033-1041, 2000.
38. Sano H, Kane S, Sano E, Miinea CP, Asara JM, Lane WS, Garner CW, and Lienhard GE. Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 278: 14599-14602, 2003.
39. Strawbridge AB and Elmendorf JS. Phosphatidylinositol 4,5-bisphosphate reverses endothelin-1-induced insulin resistance via an actin-dependent mechanism. Diabetes 54: 1698-1705, 2005.
40. Tong P, Khayat ZA, Huang C, Patel N, Ueyama A, and Klip A. Insulin-induced cortical actin remodeling promotes GLUT4 insertion at muscle cell membrane ruffles. J Clin Invest 108: 371-381, 2001.
41. Torok D, Patel N, Jebailey L, Thong FS, Randhawa VK, Klip A, and Rudich A. Insulin but not PDGF relies on actin remodeling and on VAMP2 for GLUT4 translocation in myoblasts. J Cell Sci 117: 5447-5455, 2004.
42. Tsakiridis T, Bergman A, Somwar R, Taha C, Aktories K, Cruz TF, Klip A, and Downey GP. 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, 1998.
43. Tsakiridis T, Vranic M, and Klip A. 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, 1994.
44. Ueyama A, Yaworsky KL, Wang Q, Ebina Y, and Klip A. GLUT-4myc ectopic expression in L6 myoblasts generates a GLUT-4-specific pool conferring insulin sensitivity. Am J Physiol Endocrinol Metab 277: E572-E578, 1999.
45. Walker PS, Ramlal T, Sarabia V, Koivisto UM, Bilan PJ, Pessin JE, and Klip A. Glucose transport activity in L6 muscle cells is regulated by the coordinate control of subcellular glucose transporter distribution, biosynthesis, and mRNA transcription. J Biol Chem 265: 1516-1523, 1990.
46. Wang Q, Bilan PJ, Tsakiridis T, Hinek A, and Klip A. 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, 1998.
47. Wong SK. A 384-well cell-based phospho-ERK assay for dopamine D2 and D3 receptors. Anal Biochem 333: 265-272, 2004.
48. Wu-Wong JR, Berg CE, Wang J, Chiou WJ, and Fissel B. Endothelin stimulates glucose uptake and GLUT4 translocation via activation of endothelin ETA receptor in 3T3-L1 adipocytes. J Biol Chem 274: 8103-8110, 1999.
49. Younsi M, Quilliot D, Al-Makdissy N, Delbachian I, Drouin P, Donner M, and Ziegler O. Erythrocyte membrane phospholipid composition is related to hyperinsulinemia in obese nondiabetic women: effects of weight loss. Metabolism 51: 1261-1268, 2002.