2,055
Views
21
CrossRef citations to date
0
Altmetric
Review

Rho GTPases in insulin-stimulated glucose uptake

Article: e28102 | Received 02 Oct 2013, Accepted 04 Feb 2014, Published online: 10 Mar 2014

References

  • Rorsman P, Braun M. Regulation of insulin secretion in human pancreatic islets. Annu Rev Physiol 2013; 75:155 - 79; http://dx.doi.org/10.1146/annurev-physiol-030212-183754; PMID: 22974438
  • Seino S, Shibasaki T. PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 2005; 85:1303 - 42; http://dx.doi.org/10.1152/physrev.00001.2005; PMID: 16183914
  • Wollheim CB, Sharp GW. Regulation of insulin release by calcium. Physiol Rev 1981; 61:914 - 73; PMID: 6117094
  • Kahn CR. The molecular mechanism of insulin action. Annu Rev Med 1985; 36:429 - 51; http://dx.doi.org/10.1146/annurev.me.36.020185.002241; PMID: 2986528
  • Bogan JS. Regulation of glucose transporter translocation in health and diabetes. Annu Rev Biochem 2012; 81:507 - 32; http://dx.doi.org/10.1146/annurev-biochem-060109-094246; PMID: 22482906
  • Huang S, Czech MP. The GLUT4 glucose transporter. Cell Metab 2007; 5:237 - 52; http://dx.doi.org/10.1016/j.cmet.2007.03.006; PMID: 17403369
  • Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001; 414:799 - 806; http://dx.doi.org/10.1038/414799a; PMID: 11742412
  • Li J, Malaby AW, Famulok M, Sabe H, Lambright DG, Hsu VW. Grp1 plays a key role in linking insulin signaling to glut4 recycling. Dev Cell 2012; 22:1286 - 98; http://dx.doi.org/10.1016/j.devcel.2012.03.004; PMID: 22609160
  • Abel ED, Peroni O, Kim JK, Kim YB, Boss O, Hadro E, Minnemann T, Shulman GI, Kahn BB. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 2001; 409:729 - 33; http://dx.doi.org/10.1038/35055575; PMID: 11217863
  • Zisman A, Peroni OD, Abel ED, Michael MD, Mauvais-Jarvis F, Lowell BB, Wojtaszewski JF, Hirshman MF, Virkamaki A, Goodyear LJ, et al. Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat Med 2000; 6:924 - 8; http://dx.doi.org/10.1038/78693; PMID: 10932232
  • Shepherd PR, Gnudi L, Tozzo E, Yang H, Leach F, Kahn BB. Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J Biol Chem 1993; 268:22243 - 6; PMID: 8226728
  • Tozzo E, Shepherd PR, Gnudi L, Kahn BB. Transgenic GLUT-4 overexpression in fat enhances glucose metabolism: preferential effect on fatty acid synthesis. Am J Physiol 1995; 268:E956 - 64; PMID: 7762651
  • Tsao TS, Burcelin R, Katz EB, Huang L, Charron MJ. Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle. Diabetes 1996; 45:28 - 36; http://dx.doi.org/10.2337/diab.45.1.28; PMID: 8522056
  • Franke TF. PI3K/Akt: getting it right matters. Oncogene 2008; 27:6473 - 88; http://dx.doi.org/10.1038/onc.2008.313; PMID: 18955974
  • Vanhaesebroeck B, Stephens L, Hawkins P. PI3K signalling: the path to discovery and understanding. Nat Rev Mol Cell Biol 2012; 13:195 - 203; http://dx.doi.org/10.1038/nrm3290; PMID: 22358332
  • Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 2011; 12:21 - 35; http://dx.doi.org/10.1038/nrm3025; PMID: 21157483
  • Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, Crenshaw EB 3rd, Kaestner KH, Bartolomei MS, Shulman GI, Birnbaum MJ. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB β). Science 2001; 292:1728 - 31; http://dx.doi.org/10.1126/science.292.5522.1728; PMID: 11387480
  • Garofalo RS, Orena SJ, Rafidi K, Torchia AJ, Stock JL, Hildebrandt AL, Coskran T, Black SC, Brees DJ, Wicks JR, et al. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB β. J Clin Invest 2003; 112:197 - 208; http://dx.doi.org/10.1172/JCI16885; PMID: 12843127
  • Kane S, Sano H, Liu SC, Asara JM, Lane WS, Garner CC, 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 2002; 277:22115 - 8; http://dx.doi.org/10.1074/jbc.C200198200; PMID: 11994271
  • Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 2006; 103:11821 - 7; http://dx.doi.org/10.1073/pnas.0601617103; PMID: 16882731
  • Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001; 2:107 - 17; http://dx.doi.org/10.1038/35052055; PMID: 11252952
  • Sano H, Eguez L, Teruel MN, Fukuda M, Chuang TD, Chavez JA, Lienhard GE, McGraw TE. Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab 2007; 5:293 - 303; http://dx.doi.org/10.1016/j.cmet.2007.03.001; PMID: 17403373
  • Sun Y, Bilan PJ, Liu Z, Klip A. Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells. Proc Natl Acad Sci U S A 2010; 107:19909 - 14; http://dx.doi.org/10.1073/pnas.1009523107; PMID: 21041651
  • Kramer HF, Witczak CA, Taylor EB, Fujii N, Hirshman MF, Goodyear LJ. AS160 regulates insulin- and contraction-stimulated glucose uptake in mouse skeletal muscle. J Biol Chem 2006; 281:31478 - 85; http://dx.doi.org/10.1074/jbc.M605461200; PMID: 16935857
  • Larance M, Ramm G, Stöckli J, van Dam EM, Winata S, Wasinger V, Simpson F, Graham M, Junutula JR, Guilhaus M, et al. Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J Biol Chem 2005; 280:37803 - 13; http://dx.doi.org/10.1074/jbc.M503897200; PMID: 16154996
  • Sano H, Kane S, Sano E, Mîinea CP, Asara JM, Lane WS, Garner CW, Lienhard GE. Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 2003; 278:14599 - 602; http://dx.doi.org/10.1074/jbc.C300063200; PMID: 12637568
  • Ramm G, Larance M, Guilhaus M, James DE. A role for 14-3-3 in insulin-stimulated GLUT4 translocation through its interaction with the RabGAP AS160. J Biol Chem 2006; 281:29174 - 80; http://dx.doi.org/10.1074/jbc.M603274200; PMID: 16880201
  • Roach WG, Chavez JA, Mîinea CP, Lienhard GE. Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1. Biochem J 2007; 403:353 - 8; http://dx.doi.org/10.1042/BJ20061798; PMID: 17274760
  • Xie X, Gong Z, Mansuy-Aubert V, Zhou QL, Tatulian SA, Sehrt D, Gnad F, Brill LM, Motamedchaboki K, Chen Y, et al. C2 domain-containing phosphoprotein CDP138 regulates GLUT4 insertion into the plasma membrane. Cell Metab 2011; 14:378 - 89; http://dx.doi.org/10.1016/j.cmet.2011.06.015; PMID: 21907143
  • JeBailey L, Rudich A, Huang X, Di Ciano-Oliveira C, Kapus A, Klip A. Skeletal muscle cells and adipocytes differ in their reliance on TC10 and Rac for insulin-induced actin remodeling. Mol Endocrinol 2004; 18:359 - 72; http://dx.doi.org/10.1210/me.2003-0294; PMID: 14615606
  • Chiu TT, Jensen TE, Sylow L, Richter EA, Klip A. Rac1 signalling towards GLUT4/glucose uptake in skeletal muscle. Cell Signal 2011; 23:1546 - 54; http://dx.doi.org/10.1016/j.cellsig.2011.05.022; PMID: 21683139
  • JeBailey L, Wanono O, Niu W, Roessler J, Rudich A, Klip A. Ceramide- and oxidant-induced insulin resistance involve loss of insulin-dependent Rac-activation and actin remodeling in muscle cells. Diabetes 2007; 56:394 - 403; http://dx.doi.org/10.2337/db06-0823; PMID: 17259384
  • Khayat ZA, Tong P, Yaworsky K, Bloch RJ, Klip A. Insulin-induced actin filament remodeling colocalizes actin with phosphatidylinositol 3-kinase and GLUT4 in L6 myotubes. J Cell Sci 2000; 113:279 - 90; PMID: 10633079
  • Ueda S, Kataoka T, Satoh T. Activation of the small GTPase Rac1 by a specific guanine-nucleotide-exchange factor suffices to induce glucose uptake into skeletal-muscle cells. Biol Cell 2008; 100:645 - 57; http://dx.doi.org/10.1042/BC20070160; PMID: 18482007
  • Marcusohn J, Isakoff SJ, Rose E, Symons M, Skolnik EY. The GTP-binding protein Rac does not couple PI 3-kinase to insulin-stimulated glucose transport in adipocytes. Curr Biol 1995; 5:1296 - 302; http://dx.doi.org/10.1016/S0960-9822(95)00256-9; PMID: 8574587
  • Balamatsias D, Kong AM, Waters JE, Sriratana A, Gurung R, Bailey CG, Rasko JE, Tiganis T, Macaulay SL, Mitchell CA. Identification of P-Rex1 as a novel Rac1-guanine nucleotide exchange factor (GEF) that promotes actin remodeling and GLUT4 protein trafficking in adipocytes. J Biol Chem 2011; 286:43229 - 40; http://dx.doi.org/10.1074/jbc.M111.306621; PMID: 22002247
  • Chiu TT, Sun Y, Koshkina A, Klip A. Rac-1 superactivation triggers insulin-independent glucose transporter 4 (GLUT4) translocation that bypasses signaling defects exerted by c-Jun N-terminal kinase (JNK)- and ceramide-induced insulin resistance. J Biol Chem 2013; 288:17520 - 31; http://dx.doi.org/10.1074/jbc.M113.467647; PMID: 23640896
  • Ueda S, Kitazawa S, Ishida K, Nishikawa Y, Matsui M, Matsumoto H, Aoki T, Nozaki S, Takeda T, Tamori Y, et al. Crucial role of the small GTPase Rac1 in insulin-stimulated translocation of glucose transporter 4 to the mouse skeletal muscle sarcolemma. FASEB J 2010; 24:2254 - 61; http://dx.doi.org/10.1096/fj.09-137380; PMID: 20203090
  • Sylow L, Jensen TE, Kleinert M, Højlund K, Kiens B, Wojtaszewski J, Prats C, Schjerling P, Richter EA. Rac1 signaling is required for insulin-stimulated glucose uptake and is dysregulated in insulin-resistant murine and human skeletal muscle. Diabetes 2013; 62:1865 - 75; http://dx.doi.org/10.2337/db12-1148; PMID: 23423567
  • Bogan JS, McKee AE, Lodish HF. Insulin-responsive compartments containing GLUT4 in 3T3-L1 and CHO cells: regulation by amino acid concentrations. Mol Cell Biol 2001; 21:4785 - 806; http://dx.doi.org/10.1128/MCB.21.14.4785-4806.2001; PMID: 11416153
  • Hou JC, Shigematsu S, Crawford HC, Anastasiadis PZ, Pessin JE. Dual regulation of Rho and Rac by p120 catenin controls adipocyte plasma membrane trafficking. J Biol Chem 2006; 281:23307 - 12; http://dx.doi.org/10.1074/jbc.M603127200; PMID: 16754687
  • Lewis JP, Palmer ND, Ellington JB, Divers J, Ng MC, Lu L, Langefeld CD, Freedman BI, Bowden DW. Analysis of candidate genes on chromosome 20q12-13.1 reveals evidence for BMI mediated association of PREX1 with type 2 diabetes in European Americans. Genomics 2010; 96:211 - 9; http://dx.doi.org/10.1016/j.ygeno.2010.07.006; PMID: 20650312
  • Nozaki S, Takeda T, Kitaura T, Takenaka N, Kataoka T, Satoh T. Akt2 regulates Rac1 activity in the insulin-dependent signaling pathway leading to GLUT4 translocation to the plasma membrane in skeletal muscle cells. Cell Signal 2013; 25:1361 - 71; http://dx.doi.org/10.1016/j.cellsig.2013.02.023; PMID: 23499910
  • Takenaka N, Izawa R, Wu J, Kitagawa K, Nihata Y, Hosooka T, Noguchi T, Ogawa W, Aiba A, Satoh T. A critical role of the small GTPase Rac1 in Akt2-mediated GLUT4 translocation in mouse skeletal muscle. FEBS J 2014; 281:1493 - 504; http://dx.doi.org/10.1111/febs.12719; PMID: 24438685
  • Sylow L, Kleinert M, Pehmøller C, Prats C, Chiu TT, Klip A, Richter EA, Jensen TE. Akt and Rac1 signaling are jointly required for insulin-stimulated glucose uptake in skeletal muscle and downregulated in insulin resistance. Cell Signal 2014; 26:323 - 31; http://dx.doi.org/10.1016/j.cellsig.2013.11.007; PMID: 24216610
  • Brozinick JT Jr., Hawkins ED, Strawbridge AB, 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 2004; 279:40699 - 706; http://dx.doi.org/10.1074/jbc.M402697200; PMID: 15247264
  • Kanzaki M, Pessin JE. Insulin-stimulated GLUT4 translocation in adipocytes is dependent upon cortical actin remodeling. J Biol Chem 2001; 276:42436 - 44; http://dx.doi.org/10.1074/jbc.M108297200; PMID: 11546823
  • Tsakiridis T, Vranic M, 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 1994; 269:29934 - 42; PMID: 7961991
  • Bose A, Guilherme A, Robida SI, Nicoloro SM, Zhou QL, Jiang ZY, Pomerleau DP, Czech MP. Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 2002; 420:821 - 4; http://dx.doi.org/10.1038/nature01246; PMID: 12490950
  • Imamura T, Huang J, Usui I, Satoh H, Bever J, Olefsky JM. Insulin-induced GLUT4 translocation involves protein kinase C-λ-mediated functional coupling between Rab4 and the motor protein kinesin. Mol Cell Biol 2003; 23:4892 - 900; http://dx.doi.org/10.1128/MCB.23.14.4892-4900.2003; PMID: 12832475
  • Ishikura S, Klip A. Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation. Am J Physiol Cell Physiol 2008; 295:C1016 - 25; http://dx.doi.org/10.1152/ajpcell.00277.2008; PMID: 18701652
  • Semiz S, Park JG, Nicoloro SM, Furcinitti P, Zhang C, Chawla A, Leszyk J, Czech MP. Conventional kinesin KIF5B mediates insulin-stimulated GLUT4 movements on microtubules. EMBO J 2003; 22:2387 - 99; http://dx.doi.org/10.1093/emboj/cdg237; PMID: 12743033
  • Yip MF, Ramm G, Larance M, Hoehn KL, Wagner MC, Guilhaus M, James DE. CaMKII-mediated phosphorylation of the myosin motor Myo1c is required for insulin-stimulated GLUT4 translocation in adipocytes. Cell Metab 2008; 8:384 - 98; http://dx.doi.org/10.1016/j.cmet.2008.09.011; PMID: 19046570
  • Yoshizaki T, Imamura T, Babendure JL, Lu JC, Sonoda N, Olefsky JM. Myosin 5a is an insulin-stimulated Akt2 (protein kinase Bbeta) substrate modulating GLUT4 vesicle translocation. Mol Cell Biol 2007; 27:5172 - 83; http://dx.doi.org/10.1128/MCB.02298-06; PMID: 17515613
  • Fukata M, Nakagawa M, Kaibuchi K. Roles of Rho-family GTPases in cell polarisation and directional migration. Curr Opin Cell Biol 2003; 15:590 - 7; http://dx.doi.org/10.1016/S0955-0674(03)00097-8; PMID: 14519394
  • Raftopoulou M, Hall A. Cell migration: Rho GTPases lead the way. Dev Biol 2004; 265:23 - 32; http://dx.doi.org/10.1016/j.ydbio.2003.06.003; PMID: 14697350
  • Loubéry S, Coudrier E. Myosins in the secretory pathway: tethers or transporters?. Cell Mol Life Sci 2008; 65:2790 - 800; PMID: 18726179
  • Randhawa VK, Ishikura S, Talior-Volodarsky I, Cheng AW, Patel N, Hartwig JH, Klip A. GLUT4 vesicle recruitment and fusion are differentially regulated by Rac, AS160, and Rab8A in muscle cells. J Biol Chem 2008; 283:27208 - 19; http://dx.doi.org/10.1074/jbc.M804282200; PMID: 18650435
  • Chen XW, Leto D, Chiang SH, Wang Q, Saltiel AR. Activation of RalA is required for insulin-stimulated Glut4 trafficking to the plasma membrane via the exocyst and the motor protein Myo1c. Dev Cell 2007; 13:391 - 404; http://dx.doi.org/10.1016/j.devcel.2007.07.007; PMID: 17765682
  • Feig LA. Ral-GTPases: approaching their 15 minutes of fame. Trends Cell Biol 2003; 13:419 - 25; http://dx.doi.org/10.1016/S0962-8924(03)00152-1; PMID: 12888294
  • Chen XW, Leto D, Xiao J, Goss J, Wang Q, Shavit JA, Xiong T, Yu G, Ginsburg D, Toomre D, et al. Exocyst function is regulated by effector phosphorylation. Nat Cell Biol 2011; 13:580 - 8; http://dx.doi.org/10.1038/ncb2226; PMID: 21516108
  • Moskalenko S, Henry DO, Rosse C, Mirey G, Camonis JH, White MA. The exocyst is a Ral effector complex. Nat Cell Biol 2002; 4:66 - 72; http://dx.doi.org/10.1038/ncb728; PMID: 11740492
  • Sugihara K, Asano S, Tanaka K, Iwamatsu A, Okawa K, Ohta Y. The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat Cell Biol 2002; 4:73 - 8; http://dx.doi.org/10.1038/ncb720; PMID: 11744922
  • Nozaki S, Ueda S, Takenaka N, Kataoka T, Satoh T. Role of RalA downstream of Rac1 in insulin-dependent glucose uptake in muscle cells. Cell Signal 2012; 24:2111 - 7; http://dx.doi.org/10.1016/j.cellsig.2012.07.013; PMID: 22820503
  • Tsakiridis T, Taha C, Grinstein S, Klip A. Insulin activates a p21-activated kinase in muscle cells via phosphatidylinositol 3-kinase. J Biol Chem 1996; 271:19664 - 7; http://dx.doi.org/10.1074/jbc.271.33.19664; PMID: 8702668
  • Wang Z, Oh E, Clapp DW, Chernoff J, Thurmond DC. Inhibition or ablation of p21-activated kinase (PAK1) disrupts glucose homeostatic mechanisms in vivo. J Biol Chem 2011; 286:41359 - 67; http://dx.doi.org/10.1074/jbc.M111.291500; PMID: 21969371
  • You GY, Lee JO, Kim JH, Kim N, Lee SK, Moon JW, Jie S, Lee HJ, Kim SJ, Park SH, et al. Tiam-1, a GEF for Rac1, plays a critical role in metformin-mediated glucose uptake in C2C12 cells. Cell Signal 2013; 25:2558 - 65; http://dx.doi.org/10.1016/j.cellsig.2013.08.018; PMID: 23993965
  • Hardie DG. AMP-activated protein kinase as a drug target. Annu Rev Pharmacol Toxicol 2007; 47:185 - 210; http://dx.doi.org/10.1146/annurev.pharmtox.47.120505.105304; PMID: 16879084
  • Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, Cantley LC. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci U S A 2004; 101:3329 - 35; http://dx.doi.org/10.1073/pnas.0308061100; PMID: 14985505
  • Sakamoto K, McCarthy A, Smith D, Green KA, Grahame Hardie D, Ashworth A, Alessi DR. Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction. EMBO J 2005; 24:1810 - 20; http://dx.doi.org/10.1038/sj.emboj.7600667; PMID: 15889149
  • Sylow L, Jensen TE, Kleinert M, Mouatt JR, Maarbjerg SJ, Jeppesen J, Prats C, Chiu TT, Boguslavsky S, Klip A, et al. Rac1 is a novel regulator of contraction-stimulated glucose uptake in skeletal muscle. Diabetes 2013; 62:1139 - 51; http://dx.doi.org/10.2337/db12-0491; PMID: 23274900
  • Kanzaki M, Pessin JE. Insulin signaling: GLUT4 vesicles exit via the exocyst. Curr Biol 2003; 13:R574 - 6; http://dx.doi.org/10.1016/S0960-9822(03)00478-0; PMID: 12867054
  • Chiang SH, Baumann CA, Kanzaki M, Thurmond DC, Watson RT, Neudauer CL, Macara IG, Pessin JE, Saltiel AR. Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 2001; 410:944 - 8; http://dx.doi.org/10.1038/35073608; PMID: 11309621
  • Inoue M, Chang L, Hwang J, Chiang SH, Saltiel AR. The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 2003; 422:629 - 33; http://dx.doi.org/10.1038/nature01533; PMID: 12687004
  • Lodhi IJ, Chiang SH, Chang L, Vollenweider D, Watson RT, Inoue M, Pessin JE, Saltiel AR. Gapex-5, a Rab31 guanine nucleotide exchange factor that regulates Glut4 trafficking in adipocytes. Cell Metab 2007; 5:59 - 72; http://dx.doi.org/10.1016/j.cmet.2006.12.006; PMID: 17189207
  • Kanzaki M, Watson RT, Hou JC, Stamnes M, Saltiel AR, Pessin JE. Small GTP-binding protein TC10 differentially regulates two distinct populations of filamentous actin in 3T3L1 adipocytes. Mol Biol Cell 2002; 13:2334 - 46; http://dx.doi.org/10.1091/mbc.01-10-0490; PMID: 12134073