Regulation of glucose transporter 4 translocation by the rab guanosine triphosphatase-activating protein AS160/TBC1D4: Role of phosphorylation and membrane association

Molecular Endocrinology

Volumn 22, Issue 12, 2008, Pages 2703-2715

  Stöckli, Jacqueline ^a   Davey, Jonathan R ^a   Hohnen Behrens, Cordula ^a   Xu, Aimin ^b   James, David E ^a   Ramm, Georg ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 4; GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN; PROTEIN KINASE B; RAB PROTEIN;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL FUNCTION; CYTOSOL; DISSOCIATION; GENE OVEREXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION;

3T3-L1 CELLS; ANDROSTADIENES; ANIMALS; CELL MEMBRANE; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; CYTOSOL; GLUCOSE TRANSPORTER TYPE 4; GTPASE-ACTIVATING PROTEINS; INSULIN; MICE; MUSCLE FIBERS, SKELETAL; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; TRANSPORT VESICLES;

EID: 56749173518     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2008-0111     Document Type: Article

References (43)

1. Bryant NJ, Govers R, James DE 2002 Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol 3:267-277
2. Eguez L, Lee A, Chavez JA, Miinea CP, Kane S, Lienhard GE, McGraw TE 2005 Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein. Cell Metab 2:263-272
3. Zeigerer A, McBrayer MK, McGraw TE 2004 Insulin stimulation of GLUT4 exocytosis, but not its inhibition of endocytosis, is dependent on RabGAP AS160. Mol Biol Cell 15:4406-4415
4. Sano H, Kane S, Sano E, Miinea CP, Asara JM, Lane WS, Garner CW, Lienhard GE 2003 Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 278:14599-14602
5. Kane S, Sano H, Liu SC, Asara JM, Lane WS, Garner CC, Lienhard GE 2002 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
6. Deshmukh A, Coffey VG, Zhong Z, Chibalin AV, Hawley JA, Zierath JR 2006 Exercise-induced phosphorylation of the novel Akt substrates AS160 and filamin A in human skeletal muscle. Diabetes 55:1776-1782
7. Bruss MD, Arias EB, Lienhard GE, Cartee GD 2005 Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes 54:41-50
8. Kramer HF, Witczak CA, Taylor EB, Fujii N, Hirshman MF, Goodyear LJ 2006 AS160 regulates insulin- and contraction-stimulated glucose uptake in mouse skeletal muscle. J Biol Chem 281:31478-31485
9. Thong FS, Bilan PJ, Klip A 2007 The Rab GTPase-activating protein AS160 integrates Akt, protein kinase C, and AMP-activated protein kinase signals regulating GLUT4 traffic. Diabetes 56:414-423
10. Treebak JT, Glund S, Deshmukh A, Klein DK, Long YC, Jensen TE, Jorgensen SB, Viollet B, Andersson L, Neumann D, Wallimann T, Richter EA, Chibalin AV, Zierath JR, Wojtaszewski JF 2006 AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits. Diabetes 55:2051-2058
11. Cartee GD, Wojtaszewski JF 2007 Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport. Appl Physiol Nutr Metab 32:557-566
12. Kramer HF, Witczak CA, Fujii N, Jessen N, Taylor EB, Arnolds DE, Sakamoto K, Hirshman MF, Goodyear LJ 2006 Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes 55:2067-2076
13. Ramm G, Larance M, Guilhaus M, James DE 2006 A role for 14-3-3 in insulin-stimulated GLUT4 translocation through its interaction with the RabGAP AS160. J Biol Chem 281:29174-29180
14. Larance M, Ramm G, Stöckli J, van Dam EM, Winata S, Wasinger V, Simpson F, Graham M, Junutula JR, Guilhaus M, James DE 2005 Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J Biol Chem 280:37803-37813
15. Miinea CP, Sano H, Kane S, Sano E, Fukuda M, Peranen J, Lane WS, Lienhard GE 2005 AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem J 391:87-93
16. Ishikura S, Bilan PJ, Klip A 2007 Rabs 8A and 14 are targets of the insulin-regulated Rab-GAP AS160 regulating GLUT4 traffic in muscle cells. Biochem Biophys Res Commun 353:1074-1079
17. Sano H, Eguez L, Teruel MN, Fukuda M, Chuang TD, Chavez JA, Lienhard GE, McGraw TE 2007 Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab 5:293-303
18. Sano H, Roach WG, Peck GR, Fukuda M, Lienhard GE 2008 Rab10 in insulin-stimulated GLUT4 translocation. Biochem J 411:89-95
19. Peck GR, Ye S, Pham V, Fernando RN, Macaulay SL, Chai SY, Albiston AL 2006 Interaction of the Akt substrate, AS160, with the glucose transporter 4 vesicle marker protein, insulin-regulated aminopeptidase. Mol Endocrinol 20:2576-2583
20. Cai SL, Tee AR, Short JD, Bergeron JM, Kim J, Shen J, Guo R, Johnson CL, Kiguchi K, Walker CL 2006 Activity of TSC2 is inhibited by AKT-mediated phosphorylation and membrane partitioning. J Cell Biol 173:279-289
21. Clark SF, Martin S, Carozzi AJ, Hill MM, James DE 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
22. Kane S, Lienhard GE 2005 Calmodulin binds to the Rab GTPase activating protein required for insulin-stimulated GLUT4 translocation. Biochem Biophys Res Commun 335:175-180
23. Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y, Ye JM, Lee CH, Oh WK, Kim CT, Hohnen-Behrens C, Gosby A, Kraegen EW, James DE, Kim JB 2006 Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55:2256-2264
24. Imamura T, Ishibashi K, Dalle S, Ugi S, Olefsky JM 1999 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
25. Wu-Wong JR, Berg CE, Wang J, Chiou WJ, Fissel B 1999 Endothelin stimulates glucose uptake and GLUT4 translocation via activation of endothelin ETA receptor in 3T3-L1 adipocytes. J Biol Chem 274:8103-8110
26. Carey AL, Steinberg GR, Macaulay SL, Thomas WG, Holmes AG, Ramm G, Prelovsek O, Hohnen-Behrens C, Watt MJ, James DE, Kemp BE, Pedersen BK, Febbraio MA 2006 Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes 55:2688-2697
27. Ceddia RB, Somwar R, Maida A, Fang X, Bikopoulos G, Sweeney G 2005 Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells. Diabetologia 48:132-139
28. Mao X, Kikani CK, Riojas RA, Langlais P, Wang L, Ramos FJ, Fang Q, Christ-Roberts CY, Hong JY, Kim RY, Liu F, Dong LQ 2006 APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat Cell Biol 8:516-523
29. Somwar R, Niu W, Kim DY, Sweeney G, Randhawa VK, Huang C, Ramlal T, Klip A 2001 Differential effects of phosphatidylinositol 3-kinase inhibition on intracellular signals regulating GLUT4 translocation and glucose transport. J Biol Chem 276:46079-46087
30. Govers R, Coster AC, James DE 2004 Insulin increases cell surface GLUT4 levels by dose dependently discharging GLUT4 into a cell surface recycling pathway. Mol Cell Biol 24:6456-6466
31. Slot JW, Geuze HJ, Gigengack S, Lienhard GE, James DE 1991 Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol 113:123-135
32. Martin S, Millar CA, Lyttle CT, Meerloo T, Marsh BJ, Gould GW, James DE 2000 Effects of insulin on intracellular GLUT4 vesicles in adipocytes: evidence for a secretory mode of regulation. J Cell Sci 113:3427-3438
33. Ramm G, Slot JW, James DE, Stoorvogel W 2000 Insulin recruits GLUT4 from specialized VAMP2-carrying vesicles as well as from the dynamic endosomal/trans-Golgi network in rat adipocytes. Mol Biol Cell 11:4079-4091
34. Larance M, Ramm G, James DE 2008 The GLUT4 code. Mol Endocrinol 22:226-233
35. Roach WG, Chavez JA, Miinea CP, Lienhard GE 2007 Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1. Biochem J 403:353-358
36. Chen S, Murphy J, Toth R, Campbell DG, Morrice NA, Mackintosh C 2008 Complementary regulation of TBC1D1 and AS160 by growth factors, insulin and AMPK activators. Biochem J 409:449-459
37. Chavez JA, Roach WG, Keller SR, Lane WS, Lienhard GE 2008 Inhibition of GLUT4 translocation by Tbc1d1, a Rab GTPase-activating protein abundant in skeletal muscle, is partially relieved by AMP-activated protein kinase activation. J Biol Chem 283:9187-9195
38. Wang Y, Xu A, Knight C, Xu LY, Cooper GJ 2002 Hydroxylation and glycosylation of the four conserved lysine residues in the collagenous domain of adiponectin. Potential role in the modulation of its insulin-sensitizing activity. J Biol Chem 277:19521-19529
39. James DE, Brown R, Navarro J, Pilch PF 1988 Insulin-regulatable tissues express a unique insulin-sensitive glucose-transport protein. Nature 333:183-185
40. Malide D, Yewdell JW, Bennink JR, Cushman SW 2001 The export of major histocompatibility complex class I molecules from the endoplasmic reticulum of rat brown adipose cells is acutely stimulated by insulin. Mol Biol Cell 12:101-114
41. Shewan AM, van Dam EM, Martin S, Luen TB, Hong W, Bryant NJ, James DE 2003 GLUT4 recycles via a trans-Golgi network (TGN) subdomain enriched in Syntaxins 6 and 16 but not TGN38: involvement of an acidic targeting motif. Mol Biol Cell 14:973-986
42. Van Parijs L, Refaeli Y, Lord JD, Nelson BH, Abbas AK, Baltimore D 1999 Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation-induced cell death. Immunity 11:281-288
43. Wei ML, Bonzelius F, Scully RM, Kelly RB, Herman GA 1998 GLUT4 and transferrin receptor are differentially sorted along the endocytic pathway in CHO cells. J Cell Biol 140:565-575