SEC16A is a RAB10 effector required for insulinstimulated GLUT4 trafficking in adipocytes

Journal of Cell Biology

Volumn 214, Issue 1, 2016, Pages 61-76

  Bruno, Joanne ^a,b   Brumfield, Alexandria ^a   Chaudhary, Natasha ^a   Iaea, David ^a   McGraw, Timothy E ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN COMPLEX II; GLUCOSE TRANSPORTER 4; INSULIN; PROTEIN DERIVATIVE; PROTEIN RAB10; PROTEIN SEC16A; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN BINDING; RAB PROTEIN; RAB10 PROTEIN, MOUSE; SEC16A PROTEIN, MOUSE; TBC1D4 PROTEIN, MOUSE; VESICULAR TRANSPORT PROTEIN;

ADIPOCYTE; ANIMAL CELL; ARTICLE; BIOGENESIS; COMPLEX FORMATION; CONTROLLED STUDY; EFFECTOR CELL; ENDOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TRANSPORT VESICLE; 3T3-L1 CELL LINE; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE; DRUG EFFECTS; ENDOPLASMIC RETICULUM; GENE SILENCING; GOLGI COMPLEX; MASS SPECTROMETRY; METABOLISM; MOUSE; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CELL MEMBRANE; ENDOPLASMIC RETICULUM; ENDOSOMES; GENE KNOCKDOWN TECHNIQUES; GLUCOSE TRANSPORTER TYPE 4; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; GTPASE-ACTIVATING PROTEINS; INSULIN; MASS SPECTROMETRY; MICE; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; VESICULAR TRANSPORT PROTEINS;

EID: 84979966869     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201509052     Document Type: Article

References (60)

1. Abel, E.D., O. Peroni, J.K. Kim, Y.B. Kim, O. Boss, E. Hadro, T. Minnemann, G.I. Shulman, and B.B. Kahn. 2001. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature. 409:729-733. http ://dx.doi.org/10.1038/35055575
2. 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
3. Babbey, C.M., R.L. Bacallao, and K.W. Dunn. 2010. Rab10 associates with primary cilia and the exocyst complex in renal epithelial cells. Am. J. Physiol. Renal Physiol. 299:F495-F506. http ://dx.doi.org/10.1152/ajprenal.00198.2010
4. 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
5. Bhattacharyya, D., and B.S. Glick. 2007. Two mammalian Sec16 homologues have nonredundant functions in endoplasmic reticulum (ER) export and transitional ER organization. Mol. Biol. Cell. 18:839-849. http ://dx.doi.org/10.1091/mbc.E06-08-0707
6. Budnik, A., and D.J. Stephens. 2009. ER exit sites-localization and control of COP II vesicle formation. FEBS Lett. 583:3796-3803. http ://dx.doi.org/10.1016/j.febslet.2009.10.038
7. Chen, S., D.H. Wasserman, C. MacKintosh, and K. Sakamoto. 2011. Mice with AS160/TBC1D4-Thr649Ala knockin mutation are glucose intolerant with reduced insulin sensitivity and altered GLUT4 trafficking. Cell Metab. 13:68-79. http ://dx.doi.org/10.1016/j.cmet.2010.12.005
8. Chen, Y., Y. Wang, J. Zhang, Y. Deng, L. Jiang, E. Song, X.S. Wu, J.A. Hammer, T. Xu, and J. Lippincott-Schwartz. 2012. Rab10 and myosin-Va mediate insulin-stimulated GLUT4 storage vesicle translocation in adipocytes. J. Cell Biol. 198:545-560. http ://dx.doi.org/10.1083/jcb.201111091
9. Cho, H.J., J. Yu, C. Xie, P. Rudrabhatla, X. Chen, J. Wu, L. Parisiadou, G. Liu, L. Sun, B. Ma, et al. 2014. Leucine-rich repeat kinase 2 regulates Sec16A at ER exit sites to allow ER-Golgi export. EMBO J. 33:2314-2331. http ://dx.doi.org/10.15252/embj.201487807
10. Connerly, P.L., M. Esaki, E.A. Montegna, D.E. Strongin, S. Levi, J. Soderholm, and B.S. Glick. 2005. Sec16 is a determinant of transitional ER organization. Curr. Biol. 15:1439-1447. http ://dx.doi.org/10.1016/j.cub.2005.06.065
11. D'Arcangelo, J.G., K.R. Stahmer, and E.A. Miller. 2013. Vesicle-mediated export from the ER: COP II coat function and regulation. Biochim. Biophys. Acta. 1833:2464-2472. http ://dx.doi.org/10.1016/j.bbamcr.2013.02.003
12. Deen, A.J., K. Rilla, S. Oikari, R. Kärnä, G. Bart, J. Häyrinen, A.R. Bathina, A. Ropponen, K. Makkonen, R.H. Tammi, and M.I. Tammi. 2014. Rab10-mediated endocytosis of the hyaluronan synthase HAS3 regulates hyaluronan synthesis and cell adhesion to collagen. J. Biol. Chem. 289:8375-8389. http ://dx.doi.org/10.1074/jbc.M114.552133
13. 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
14. English, A.R., and G.K. Voeltz. 2013. Rab10 GTPase regulates ER dynamics and morphology. Nat. Cell Biol. 15:169-178. http ://dx.doi.org/10.1038/ncb2647
15. Foley, K.P., and A. Klip. 2014. Dynamic GLUT4 sorting through a syntaxin-6 compartment in muscle cells is derailed by insulin resistance-causing ceramide. Biol. Open. 3:314-325. http ://dx.doi.org/10.1242/bio.20147898
16. Friedman, J.R., B.M. Webster, D.N. Mastronarde, K.J. Verhey, and G.K. Voeltz. 2010. ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules. J. Cell Biol. 190:363-375. http ://dx.doi.org/10.1083/jcb.200911024
17. Giordano, F., Y. Saheki, O. Idevall-Hagren, S.F. Colombo, M. Pirruccello, I. Milosevic, E.O. Gracheva, S.N. Bagriantsev, N. Borgese, and P. De Camilli. 2013. PI(4, 5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell. 153:1494-1509. http ://dx.doi.org/10.1016/j.cell.2013.05.026
18. Gonzalez, E., and T.E. McGraw. 2006. Insulin signaling diverges into Aktdependent and-independent signals to regulate the recruitment/docking and the fusion of GLUT4 vesicles to the plasma membrane. Mol. Biol. Cell. 17:4484-4493. http ://dx.doi.org/10.1091/mbc.E06-07-0585
19. Habraken, J.B., J. Booij, P. Slomka, E.B. Sokole, and E.A. van Royen. 1999. Quantification and visualization of defects of the functional dopaminergic system using an automatic algorithm. J. Nucl. Med. 40:1091-1097.
20. Huang, S., and M.P. Czech. 2007. The GLUT4 glucose transporter. Cell Metab. 5:237-252. http ://dx.doi.org/10.1016/j.cmet.2007.03.006.
21. Huang, G., D. Buckler-Pena, T. Nauta, M. Singh, A. Asmar, J. Shi, J.Y. Kim, and K.V. Kandror. 2013. Insulin responsiveness of glucose transporter 4 in 3T3-L1 cells depends on the presence of sortilin. Mol. Biol. Cell. 24:3115-3122. http ://dx.doi.org/10.1091/mbc.E12-10-0765
22. Hughes, H., A. Budnik, K. Schmidt, K.J. Palmer, J. Mantell, C. Noakes, A. Johnson, D.A. Carter, P. Verkade, P. Watson, and D.J. Stephens. 2009. Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER. J. Cell Sci. 122:2924-2934. http ://dx.doi.org/10.1242/jcs.044032
23. Iinuma, T., A. Shiga, K. Nakamoto, M.B. O'Brien, M. Aridor, N. Arimitsu, M. Tagaya, and K. Tani. 2007. Mammalian Sec16/p250 plays a role in membrane traffic from the endoplasmic reticulum. J. Biol. Chem. 282:17632-17639. http ://dx.doi.org/10.1074/jbc.M611237200
24. Jedrychowski, M.P., C.A. Gartner, S.P. Gygi, L. Zhou, J. Herz, K.V. Kandror, and P.F. Pilch. 2010. Proteomic analysis of GLUT4 storage vesicles reveals LRP1 to be an important vesicle component and target of insulin signaling. J. Biol. Chem. 285:104-114. http ://dx.doi.org/10.1074/jbc.M109.040428
25. Jordens, I., D. Molle, W. Xiong, S.R. Keller, and T.E. McGraw. 2010. Insulinregulated aminopeptidase is a key regulator of GLUT4 trafficking by controlling the sorting of GLUT4 from endosomes to specialized insulinregulated vesicles. Mol. Biol. Cell. 21:2034-2044. http ://dx.doi.org/10.1091/mbc.E10-02-0158
26. Karunanithi, S., T. Xiong, M. Uhm, D. Leto, J. Sun, X.W. Chen, and A.R. Saltiel. 2014. A Rab10 :RalA G protein cascade regulates insulin-stimulated glucose uptake in adipocytes. Mol. Biol. Cell. 25:3059-3069. http ://dx.doi.org/10.1091/mbc.E14-06-1060
27. Karylowski, O., A. Zeigerer, A. Cohen, and T.E. McGraw. 2004. GLUT4 is retained by an intracellular cycle of vesicle formation and fusion with endosomes. Mol. Biol. Cell. 15:870-882. http ://dx.doi.org/10.1091/mbc.E03-07-0517
28. Kasprzak, J.D., W.B. Vletter, J.R. Roelandt, J.R. van Meegen, R. Johnson, and F.J. Ten Cate. 1998. Visualization and quantification of myocardial mass at risk using three-dimensional contrast echocardiography. Cardiovasc. Res. 40:314-321. http ://dx.doi.org/10.1016/S0008-6363(98)00178-3
29. Khoriaty, R., M.P. Vasievich, and D. Ginsburg. 2012. The COP II pathway and hematologic disease. Blood. 120:31-38. http ://dx.doi.org/10.1182/blood-2012-01-292086
30. Lampson, M.A., A. Racz, S.W. Cushman, and T.E. McGraw. 2000. Demonstration of insulin-responsive trafficking of GLUT4 and vpTR in fibroblasts. J. Cell Sci. 113:4065-4076.
31. Lampson, M.A., J. Schmoranzer, A. Zeigerer, S.M. Simon, and T.E. McGraw. 2001. Insulin-regulated release from the endosomal recycling compartment is regulated by budding of specialized vesicles. Mol. Biol. Cell. 12:3489-3501. http ://dx.doi.org/10.1091/mbc.12.11.3489
32. 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
33. Lerner, D.W., D. McCoy, A.J. Isabella, A.P. Mahowald, G.F. Gerlach, T.A. Chaudhry, and S. Horne-Badovinac. 2013. A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev. Cell. 24:159-168. http ://dx.doi.org/10.1016/j.devcel.2012.12.005
34. Leto, D., and A.R. Saltiel. 2012. Regulation of glucose transport by insulin: traffic control of GLUT4. Nat. Rev. Mol. Cell Biol. 13:383-396. http ://dx.doi.org/10.1038/nrm3351
35. Lizunov, V.A., J.P. Lee, M.C. Skarulis, J. Zimmerberg, S.W. Cushman, and K.G. Stenkula. 2013. Impaired tethering and fusion of GLUT4 vesicles in insulin-resistant human adipose cells. Diabetes. 62:3114-3119. http ://dx.doi.org/10.2337/db12-1741
36. Martin, O.J., A. Lee, and T.E. McGraw. 2006. GLUT4 distribution between the plasma membrane and the intracellular compartments is maintained by an insulin-modulated bipartite dynamic mechanism. J. Biol. Chem. 281:484-490. http ://dx.doi.org/10.1074/jbc.M505944200
37. Martin, S., C.A. Millar, C.T. Lyttle, T. Meerloo, B.J. Marsh, G.W. Gould, and D.E. James. 2000a. Effects of insulin on intracellular GLUT4 vesicles in adipocytes: evidence for a secretory mode of regulation. J. Cell Sci. 113:3427-3438.
38. Martin, S., G. Ramm, C.T. Lyttle, T. Meerloo, W. Stoorvogel, and D.E. James. 2000b. Biogenesis of insulin-responsive GLUT4 vesicles is independent of brefeldin A-sensitive trafficking. Traffic. 1:652-660. http ://dx.doi.org/10.1034/j.1600-0854.2000.010809.x
39. Millar, C.A., T. Meerloo, S. Martin, G.R. Hickson, N.J. Shimwell, M.J. Wakelam, D.E. James, and G.W. Gould. 2000. Adipsin and the glucose transporter GLUT4 traffic to the cell surface via independent pathways in adipocytes. Traffic. 1:141-151. http ://dx.doi.org/10.1034/j.1600-0854.2000.010206.x
40. Miller, E.A., and C. Barlowe. 2010. Regulation of coat assembly-sorting things out at the ER. Curr. Opin. Cell Biol. 22:447-453. http ://dx.doi.org/10.1016/j.ceb.2010.04.003
41. Penn, M.S., M.R. Koelle, S.M. Schwartz, and G.M. Chisolm. 1990. Visualization and quantification of transmural concentration profiles of macromolecules across the arterial wall. Circ. Res. 67:11-22. http ://dx.doi.org/10.1161/01.RES.67.1.11
42. Perera, H.K., M. Clarke, N.J. Morris, W. Hong, L.H. Chamberlain, and G.W. Gould. 2003. Syntaxin 6 regulates Glut4 trafficking in 3T3-L1 adipocytes. Mol. Biol. Cell. 14:2946-2958. http ://dx.doi.org/10.1091/mbc.E02-11-0722
43. Rowland, A.A., P.J. Chitwood, M.J. Phillips, and G.K. Voeltz. 2014. ER contact sites define the position and timing of endosome fission. Cell. 159:1027-1041. http ://dx.doi.org/10.1016/j.cell.2014.10.023
44. Sadacca, L.A., J. Bruno, J. Wen, W. Xiong, and T.E. McGraw. 2013. Specialized sorting of GLUT4 and its recruitment to the cell surface are independently regulated by distinct Rabs. Mol. Biol. Cell. 24:2544-2557. http ://dx.doi.org/10.1091/mbc.E13-02-0103
45. 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
46. 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.
47. Sano, H., G.R. Peck, S. Blachon, and G.E. Lienhard. 2015. A potential link between insulin signaling and GLUT4 translocation: Association of Rab10-GTP with the exocyst subunit Exoc6/6b. Biochem. Biophys. Res. Commun. 465:601-605. http ://dx.doi.org/10.1016/j.bbrc.2015.08.069
48. Shewan, A.M., E.M. van Dam, S. Martin, T.B. Luen, W. Hong, N.J. Bryant, and D.E. James. 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. http ://dx.doi.org/10.1091/mbc.E02-06-0315
49. Shi, J., and K.V. Kandror. 2005. Sortilin is essential and sufficient for the formation of Glut4 storage vesicles in 3T3-L1 adipocytes. Dev. Cell. 9:99-108. http ://dx.doi.org/10.1016/j.devcel.2005.04.004
50. Söderberg, O., M. Gullberg, M. Jarvius, K. Ridderstråle, K.J. Leuchowius, J. Jarvius, K. Wester, P. Hydbring, F. Bahram, L.G. Larsson, and U. Landegren. 2006. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods. 3:995-1000. http ://dx.doi.org/10.1038/nmeth947
51. Sprangers, J., and C. Rabouille. 2015. SEC16 in COP II coat dynamics at ER exit sites. Biochem. Soc. Trans. 43:97-103. http ://dx.doi.org/10.1042/BST20140283
52. Stöckli, J., D.J. Fazakerley, and D.E. James. 2011. GLUT4 exocytosis. J. Cell Sci. 124:4147-4159. http ://dx.doi.org/10.1242/jcs.097063
53. Subtil, A., M.A. Lampson, S.R. Keller, and T.E. McGraw. 2000. Characterization of the insulin-regulated endocytic recycling mechanism in 3T3-L1 adipocytes using a novel reporter molecule. J. Biol. Chem. 275:4787-4795. http ://dx.doi.org/10.1074/jbc.275.7.4787
54. Tillmann, K.D., V. Reiterer, F. Baschieri, J. Hoffmann, V. Millarte, M.A. Hauser, A. Mazza, N. Atias, D.F. Legler, R. Sharan, et al. 2015. Regulation of Sec16 levels and dynamics links proliferation and secretion. J. Cell Sci. 128:670-682. http ://dx.doi.org/10.1242/jcs.157115
55. Vazirani, R.P., A. Verma, L.A. Sadacca, M.S. Buckman, B. Picatoste, M. Beg, C. Torsitano, J.H. Bruno, R.T. Patel, K. Simonyte, et al. 2016. Disruption of adipose Rab10-dependent insulin signaling causes hepatic insulin resistance. Diabetes. 65:1577-1589. http ://dx.doi.org/10.2337/db15-1128
56. Watson, P., A.K. Townley, P. Koka, K.J. Palmer, and D.J. Stephens. 2006. Sec16 defines endoplasmic reticulum exit sites and is required for secretory cargo export in mammalian cells. Traffic. 7:1678-1687. http ://dx.doi.org/10.1111/j.1600-0854.2006.00493.x
57. Whittle, J.R., and T.U. Schwartz. 2010. Structure of the Sec13-Sec16 edge element, a template for assembly of the COP II vesicle coat. J. Cell Biol. 190:347-361. http ://dx.doi.org/10.1083/jcb.201003092
58. Xiong, W., I. Jordens, E. Gonzalez, and T.E. McGraw. 2010. GLUT4 is sorted to vesicles whose accumulation beneath and insertion into the plasma membrane are differentially regulated by insulin and selectively affected by insulin resistance. Mol. Biol. Cell. 21:1375-1386. http ://dx.doi.org/10.1091/mbc.E09-08-0751
59. Xu, X.H., C.Y. Deng, Y. Liu, M. He, J. Peng, T. Wang, L. Yuan, Z.S. Zheng, P.J. Blackshear, and Z.G. Luo. 2014. MAR CKS regulates membrane targeting of Rab10 vesicles to promote axon development. Cell Res. 24:576-594. http ://dx.doi.org/10.1038/cr.2014.33
60. 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