Rab10 and myosin-va mediate insulin-stimulated GLUT4 storage vesicle translocation in adipocytes

Journal of Cell Biology

Volumn 198, Issue 4, 2012, Pages 545-560

  Chen, Yu ^b   Wang, Yan ^a,d   Zhang, Jinzhong ^a   Deng, Yongqiang ^a   Jiang, Li ^a   Song, Eli ^a   Wu, Xufeng S ^c   Hammer, John A ^c   Xu, Tao ^a   Lippincott Schwartz, Jennifer ^b  

^a INSTITUTE OF BIOPHYSICS   (China)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE; GLUCOSE TRANSPORTER 4; INSULIN; INSULIN RESPONSIVE AMINOPEPTIDASE; MYOSIN VA; PROTEIN RAB10; PROTEIN RAB4A; PROTEIN RAB4B; PROTEIN RAB8A; RAB PROTEIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; ENDOSOME; FLUORESCENCE MICROSCOPY; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CELL MEMBRANE; CYTOPLASMIC VESICLES; GLUCOSE TRANSPORTER TYPE 4; INSULIN; MICE; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS;

EID: 84866347107     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201111091     Document Type: Article

References (42)

1. Babbey, C.M., N. Ahktar, E. Wang, C.C. Chen, B.D. Grant, and K.W. Dunn. 2006. Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol. Biol. Cell. 17: 3156-3175. http://dx.doi.org/10.1091/mbc.E05-08-0799
2. Bai, L., Y. Wang, J. Fan, Y. Chen, W. Ji, A. Qu, P. Xu, D.E. James, and T. Xu. 2007. Dissecting multiple steps of GLUT4 trafficking and identifying the sites of insulin action. Cell Metab. 5: 47-57. http://dx.doi .org/10.1016/j.cmet.2006.11.013
3. Bose, A., A. Guilherme, S.I. Robida, S.M. Nicoloro, Q.L. Zhou, Z.Y. Jiang, D.P. Pomerleau, and M.P. Czech. 2002. Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature. 420: 821-824. http://dx.doi.org/10.1038/nature01246
4. Bryant, N.J., R. Govers, and D.E. James. 2002. Regulated transport of the glucose transporter GLUT4. Nat. Rev. Mol. Cell Biol. 3: 267-277. http://dx.doi.org/10.1038/nrm782
5. Chen, Y., Y. Wang, W. Ji, P. Xu, and T. Xu. 2008. A pre-docking role for micro-tubules in insulin-stimulated glucose transporter 4 translocation. FEBS J. 275: 705-712. http://dx.doi.org/10.1111/j.1742-4658.2007.06232.x
6. Cormont, M., J.F. Tanti, A. Zahraoui, E. Van Obberghen, A. Tavitian, and Y. Le Marchand-Brustel. 1993. Insulin and okadaic acid induce Rab4 redistribution in adipocytes. J. Biol. Chem. 268:19491-19497.
7. Eguez, L., A. Lee, J.A. Chavez, C.P. Miinea, S. Kane, G.E. Lienhard, and T.E. McGraw. 2005. Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein. Cell Metab. 2: 263-272. http://dx.doi .org/10.1016/j.cmet.2005.09.005
8. Foley, K., S. Boguslavsky, and A. Klip. 2011. Endocytosis, recycling, and regulated exocytosis of glucose transporter 4. Biochemistry. 50: 3048-3061. http://dx.doi.org/10.1021/bi2000356
9. Fulcher, F.K., B.T. Smith, M. Russ, and Y.M. Patel. 2008. Dual role for myosin II in GLUT4-mediated glucose uptake in 3T3-L1 adipocytes. Exp. Cell Res. 314: 3264-3274. http://dx.doi.org/10.1016/j.yexcr.2008.08.007
10. Huang, S., L.M. Lifshitz, C. Jones, K.D. Bellve, C. Standley, S. Fonseca, S. Corvera, K.E. Fogarty, and M.P. Czech. 2007. Insulin stimulates membrane fusion and GLUT4 accumulation in clathrin coats on adipocyte plasma membranes. Mol. Cell. Biol. 27: 3456-3469. http://dx.doi.org/ 10.1128/MCB.01719-06
11. Hutagalung, A.H., and P.J. Novick. 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91: 119-149. http://dx.doi.org/10.1152/physrev.00059.2009
12. Jiang, L., J. Fan, L. Bai, Y. Wang, Y. Chen, L. Yang, L. Chen, and T. Xu. 2008. Direct quantification of fusion rate reveals a distal role for AS160 in insulin-stimulated fusion of GLUT4 storage vesicles. J. Biol. Chem. 283: 8508-8516. http://dx.doi.org/10.1074/jbc.M708688200
13. Kaddai, V., T. Gonzalez, F. Keslair, T. Grémeaux, S. Bonnafous, J. Gugenheim, A. Tran, P. Gual, Y. Le Marchand-Brustel, and M. Cormont. 2009. Rab4b is a small GTPase involved in the control of the glucose transporter GLUT4 localization in adipocyte. PLoS ONE. 4:e5257. http://dx.doi.org/ 10.1371/journal.pone.0005257
14. Kandror, K.V., and P.F. Pilch. 1994. gp160, a tissue-specific marker for insulin-activated glucose transport. Proc. Natl. Acad. Sci. USA. 91: 8017-8021. http://dx.doi.org/10.1073/pnas.91.17.8017
15. Kane, S., H. Sano, S.C. Liu, J.M. Asara, W.S. Lane, C.C. Garner, and G.E. Lienhard. 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. http://dx.doi .org/10.1074/jbc.C200198200
16. 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. http://dx.doi.org/10.1074/jbc.M108297200
17. Larance, M., G. Ramm, J. Stöckli, E.M. van Dam, S. Winata, V. Wasinger, F. Simpson, M. Graham, J.R. Junutula, M. Guilhaus, and D.E. James. 2005. Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J. Biol. Chem. 280: 37803-37813. http://dx.doi.org/10.1074/jbc.M503897200
18. Lizunov, V.A., H. Matsumoto, J. Zimmerberg, S.W. Cushman, and V.A. Frolov. 2005. Insulin stimulates the halting, tethering, and fusion of mobile GLUT4 vesicles in rat adipose cells. J. Cell Biol. 169: 481-489. http://dx.doi.org/10.1083/jcb.200412069
19. Lopez, J.A., J.G. Burchfield, D.H. Blair, K. Mele, Y. Ng, P. Vallotton, D.E. James, and W.E. Hughes. 2009. Identification of a distal GLUT4 trafficking event controlled by actin polymerization. Mol. Biol. Cell. 20: 3918-3929. http://dx.doi.org/10.1091/mbc.E09-03-0187
20. Maxfield, F.R., and T.E. McGraw. 2004. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5: 121-132. http://dx.doi.org/10.1038/nrm1315
21. Miesenböck, G., D.A. De Angelis, and J.E. Rothman. 1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature. 394: 192-195. http://dx.doi.org/10.1038/28190
22. Mîinea, C.P., H. Sano, S. Kane, E. Sano, M. Fukuda, J. Peränen, W.S. Lane, and G.E. Lienhard. 2005. AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem. J. 391: 87-93. http://dx.doi.org/10.1042/BJ20050887
23. Muretta, J.M., I. Romenskaia, and C.C. Mastick. 2008. Insulin releases Glut4 from static storage compartments into cycling endosomes and increases the rate constant for Glut4 exocytosis. J. Biol. Chem. 283: 311-323. http://dx.doi.org/10.1074/jbc.M705756200
24. 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: 321-328. http://dx.doi.org/10.1042/0264-6021:3460321
25. Ross, S.A., H.M. Scott, N.J. Morris, W.Y. Leung, F. Mao, G.E. Lienhard, and S.R. Keller. 1996. Characterization of the insulin-regulated membrane aminopeptidase in 3T3-L1 adipocytes. J. Biol. Chem. 271: 3328-3332. http://dx.doi.org/10.1074/jbc.271.6.3328
26. Sakamoto, K., and G.D. Holman. 2008. Emerging role for AS160/TBC1D4 and TBC1D1 in the regulation of GLUT4 traffic. Am. J. Physiol. Endocrinol. Metab. 295:E29-E37. http://dx.doi.org/10.1152/ajpendo.90331.2008
27. Sano, H., S. Kane, E. Sano, C.P. Mîinea, J.M. Asara, W.S. Lane, C.W. Garner, and G.E. Lienhard. 2003. Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J. Biol. Chem. 278: 14599-14602. http://dx.doi.org/10.1074/jbc.C300063200
28. Sano, H., L. Eguez, M.N. Teruel, M. Fukuda, T.D. Chuang, J.A. Chavez, G.E. Lienhard, and T.E. McGraw. 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. http://dx.doi.org/ 10.1016/j.cmet.2007.03.001
29. Sano, H., W.G. Roach, G.R. Peck, M. Fukuda, and G.E. Lienhard. 2008. Rab10 in insulin-stimulated GLUT4 translocation. Biochem. J. 411: 89-95. http://dx.doi.org/10.1042/BJ20071318
30. Sano, H., G.R. Peck, A.N. Kettenbach, S.A. Gerber, and G.E. Lienhard. 2011. Insulin-stimulated GLUT4 protein translocation in adipocytes requires the Rab10 guanine nucleotide exchange factor Dennd4C. J. Biol. Chem. 286: 16541-16545. http://dx.doi.org/10.1074/jbc.C111.228908
31. Schwartz, S.L., C. Cao, O. Pylypenko, A. Rak, and A. Wandinger-Ness. 2007. Rab GTPases at a glance. J. Cell Sci. 120: 3905-3910. http://dx.doi.org/10.1242/jcs.015909
32. Seabra, M.C., and E. Coudrier. 2004. Rab GTPases and myosin motors in organelle motility. Traffic. 5: 393-399. http://dx.doi.org/10.1111/j.1398-9219.2004.00190.x
33. Seperack, P.K., J.A. Mercer, M.C. Strobel, N.G. Copeland, and N.A. Jenkins. 1995. Retroviral sequences located within an intron of the dilute gene alter dilute expression in a tissue-specific manner. EMBO J. 14:2326-2332.
34. Stenmark, H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10: 513-525. http://dx.doi.org/10.1038/nrm2728
35. Sun, Y., P.J. Bilan, Z. Liu, and A. Klip. 2010. Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells. Proc. Natl. Acad. Sci. USA. 107: 19909-19914. http://dx.doi.org/10.1073/pnas .1009523107
36. Watson, R.T., M. Kanzaki, and J.E. Pessin. 2004. Regulated membrane traf- ficking of the insulin-responsive glucose transporter 4 in adipocytes. Endocr. Rev. 25: 177-204. http://dx.doi.org/10.1210/er.2003-0011
37. Wu, X., B. Bowers, Q. Wei, B. Kocher, and J.A. Hammer III. 1997. Myosin V associates with melanosomes in mouse melanocytes: evidence that myosin V is an organelle motor. J. Cell Sci. 110:847-859.
38. Wu, X., B. Bowers, K. Rao, Q. Wei, and Hammer JA III. 1998. Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function In vivo. J. Cell Biol. 143: 1899-1918. http://dx.doi.org/10.1083/jcb.143.7.1899
39. Wu, X., F. Wang, K. Rao, J.R. Sellers, and J.A. Hammer III. 2002. Rab27a is an essential component of melanosome receptor for myosin Va. Mol. Biol. Cell. 13: 1735-1749. http://dx.doi.org/10.1091/mbc.01-12-0595
40. Xu, Y., B.R. Rubin, C.M. Orme, A. Karpikov, C. Yu, J.S. Bogan, and D.K. Toomre. 2011. Dual-mode of insulin action controls GLUT4 vesicle exocytosis. J. Cell Biol. 193: 643-653. http://dx.doi.org/10.1083/jcb.201008135
41. Yoshizaki, T., T. Imamura, J.L. Babendure, J.C. Lu, N. Sonoda, and J.M. Olefsky. 2007. Myosin 5a is an insulin-stimulated Akt2 (protein kinase Bbeta) substrate modulating GLUT4 vesicle translocation. Mol. Cell. Biol. 27: 5172-5183. http://dx.doi.org/10.1128/MCB.02298-06
42. Zeigerer, A., M.A. Lampson, O. Karylowski, D.D. Sabatini, M. Adesnik, M. Ren, and T.E. McGraw. 2002. GLUT4 retention in adipocytes requires two intracellular insulin-regulated transport steps. Mol. Biol. Cell. 13: 2421-2435. http://dx.doi.org/10.1091/mbc.E02-02-0071