RalA GTPase Tethers Insulin Granules to L- and R-Type Calcium Channels Through Binding α2δ-1 Subunit

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Volumn 14, Issue 4, 2013, Pages 428-439

  Xie, Li ^a   Kang, Youhou ^a   Liang, Tao ^a   Dolai, Subhankar ^a   Xie, Huanli ^a   Parsaud, Leon ^b,c   Lopez, Jamie A ^d   He, Yu ^a   Chidambaram, Subbulakshmi ^a   Lam, Patrick P ^a   James, David E ^d   Sugita, Shuzo ^b,c   Gaisano, Herbert Y ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

2 1 subunit; Calcium channels; Insulin granules; Plasma membrane; RalA GTPase

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL R TYPE; CALCIUM ION; EXOCYST; INSULIN; RALA PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMMUNOPRECIPITATION; INSULIN RELEASE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CALCIUM CHANNELS, R-TYPE; CELL MEMBRANE; EXOCYTOSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RAL GTP-BINDING PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SECRETORY VESICLES;

EID: 84874681164     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12047     Document Type: Article

References (36)

1. 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.
2. Wang L, Li G, Sugita S. RalA-exocyst interaction mediates GTP-dependent exocytosis. J Biol Chem 2004;279:19875-19881.
3. Shen Y, Xu L, Foster DA. Role for phospholipase D in receptor-mediated endocytosis. Mol Cell Biol 2001;21:595-602.
4. Ohta Y, Suzuki N, Nakamura S, Hartwig JH, Stossel TP. The small GTPase RalA targets filamin to induce filopodia. Proc Natl Acad Sci USA 1999;96:2122-2128.
5. Hamad NM, Elconin JH, Karnoub AE, Bai W, Rich JN, Abraham RT, Der CJ, Counter CM. Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev 2002;16:2045-2057.
6. 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.
7. Brymora A, Valova VA, Larsen MR, Roufogalis BD, Robinson PJ. The brain exocyst complex interacts with RalA in a GTP-dependent manner: identification of a novel mammalian Sec3 gene and a second Sec15 gene. J Biol Chem 2001;276:29792-29797.
8. Moskalenko S, Tong C, Rosse C, Mirey G, Formstecher E, Daviet L, Camonis J, White MA. Ral GTPases regulate exocyst assembly through dual subunit interactions. J Biol Chem 2003;278:51743-51748.
9. Vitale N, Mawet J, Camonis J, Regazzi R, Bader MF, Chasserot-Golaz S. The small GTPase RalA controls exocytosis of large dense core secretory granules by interacting with ARF6-dependent phospholipase D1. J Biol Chem 2005;280:29921-29928.
10. Jin R, Junutula JR, Matern HT, Ervin KE, Scheller RH, Brunger AT. Exo84 and Sec5 are competitive regulatory Sec6/8 effectors to the RalA GTPase. EMBO J 2005;24:2064-2074.
11. Munson M, Novick P. The exocyst defrocked, a framework of rods revealed. Nat Struct Mol Biol 2006;13:577-581.
12. Dolphin AC. β subunits of voltage-gated calcium channels. J Bioenerg Biomembr 2003;35:599-620.
13. Arikkath J, Campbell KP. Auxiliary subunits: essential components of the voltage-gated calcium channel complex. Curr Opin Neurobiol 2003;13:298-307.
14. Sokolov S, Weiss RG, Timin EN, Hering S. Modulation of slow inactivation in class A Ca2+ channels by beta-subunits. J Physiol 2000;527(Pt 3):445-454.
15. Canti C, Nieto-Rostro M, Foucault I, Heblich F, Wratten J, Richards MW, Hendrich J, Douglas L, Page KM, Davies A, Dolphin AC. The metal-ion-dependent adhesion site in the Von Willebrand factor-A domain of alpha2delta subunits is key to trafficking voltage-gated Ca2+ channels. Proc Natl Acad Sci USA 2005;102:11230-11235.
16. Dolphin AC. Calcium channel diversity: multiple roles of calcium channel subunits. Curr Opin Neurobiol 2009;19:237-244.
17. 2+ channel null mice. EMBO J 2003;22:3844-3854.
18. Davalli AM, Biancardi E, Pollo A, Socci C, Pontiroli AE, Pozza G, Clementi F, Sher E, Carbone E. Dihydropyridine-sensitive and -insensitive voltage-operated calcium channels participate in the control of glucose-induced insulin release from human pancreatic beta cells. J Endocrinol 1996;150:195-203.
19. Yang SN, Berggren PO. The role of voltage-gated calcium channels in pancreatic beta-cell physiology and pathophysiology. Endocr Rev 2006;27:621-676.
20. Jing X, Li DQ, Olofsson CS, Salehi A, Surve VV, Caballero J, Ivarsson R, Lundquist I, Pereverzev A, Schneider T, Rorsman P, Renström E. CaV2.3 calcium channels control second-phase insulin release. J Clin Invest 2005;115:146-154.
21. Yang SN, Berggren PO. CaV2.3 channel and PKClambda: new players in insulin secretion. J Clin Invest 2005;115:16-20.
22. Lopez JA, Kwan EP, Xie L, He Y, James DE, Gaisano HY. The RalA GTPase is a central regulator of insulin exocytosis from pancreatic islet beta cells. J Biol Chem 2008;283:17939-17945.
23. Atlas D. Functional and physical coupling of voltage-sensitive calcium channels with exocytotic proteins: ramifications for the secretion mechanism. J Neurochem 2001;77:972-985.
24. 2+ channel is functionally coupled to the exocytotic machinery. Proc Natl Acad Sci USA 1999;96:248-253.
25. Guo W, Sacher M, Barrowman J, Ferro-Novick S, Novick P. Protein complexes in transport vesicle targeting. Trends Cell Biol 2000;10:251-255.
26. Whyte JR, Munro S. Vesicle tethering complexes in membrane traffic. J Cell Sci 2002;115:2627-2637.
27. 2+ channels from secretory vesicles. Diabetes 2010;59:1192-1201.
28. 2δ subunit in current stimulation and subunit interaction. Neuron 1996;16:431-440.
29. 2δ subunit. J Neurosci 1997;17:6884-6891.
30. Kwan EP, Xie L, Sheu L, Ohtsuka T, Gaisano HY. Interaction between Munc13-1 and RIM is critical for glucagon-like peptide-1 mediated rescue of exocytotic defects in Munc13-1 deficient pancreatic beta-cells. Diabetes 2007;56:2579-2588.
31. Manders EMM, Verbeek FJ, Aten JA. Measurement of co-localization of objects in dual-colour confocal images. J Microscopy 1993;169:375-382.
32. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microscopy 2006;224:213-232.
33. Pasyk EA, Kang Y, Huang X, Cui N, Sheu L, Gaisano HY. Syntaxin-1A binds the nucleotide-binding folds of sulphonylurea receptor 1 to regulate the KATP channel. J Biol Chem 2004;279:4234-4240.
34. Dotta F, Previti M, Neerman-Arbez M, Dionisi S, Cucinotta D, Lenti L, Di Mario U, Halban PA. The GM2-1 ganglioside islet autoantigen in insulin-dependent diabetes mellitus is expressed in secretory granules and is not beta-cell specific. Endocrinology 1998;139:316-319.
35. Kang Y, Zhang Y, Liang T, Leung YM, Ng B, Xie H, Chang N, Chan J, Shyng SL, Tsushima RG, Gaisano HY. ATP modulated interaction of syntaxin-1A with sulfonylurea receptor 1 to regulate pancreatic beta-cell KATP channels. J Biol Chem 2011;286:5876-5883.
36. Chang N, Liang T, Lin X, Kang Y, Xie H, Feng ZP, Gaisano HY. Syntaxin-1A interacts with distinct domains within nucleotide-binding folds of sulfonylurea receptor 1 to inhibit beta-cell ATP-sensitive potassium channels. J Biol Chem 2011;286:23308-23318.