Arf nucleotide binding site opener [ARNO] promotes sequential activation of Arf6, Cdc42 and Rac1 and insulin secretion in INS 832/13 β-cells and rat islets

Biochemical Pharmacology

Volumn 81, Issue 8, 2011, Pages 1016-1027

  Jayaram, Bhavaani ^a   Syed, Ismail ^a   Kyathanahalli, Chandrashekara N ^a   Rhodes, Christopher J ^b   Kowluru, Anjaneyulu ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Arf6; ARNO; Insulin secretion; Pancreatic islet; Rac1; SecinH3

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ARF NUCLEOTIDE BINDING SITE OPENER; GLUCOSE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INSULIN; P21 ACTIVATED KINASE 1; PROTEIN CDC42; PROTEIN INHIBITOR; RAC1 PROTEIN; SECINH3; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTORS; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL CULTURE TECHNIQUES; CELL LINE; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE; GTPASE-ACTIVATING PROTEINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMMUNOPRECIPITATION; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MICROSCOPY, CONFOCAL; RAC1 GTP-BINDING PROTEIN; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 79952802634     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.01.006     Document Type: Article

References (48)

1. Y.T. Takai, and T. Matozaki Small GTP-binding proteins Physiol Rev 81 1 2001 153 208 (Pubitemid 32098004)
2. M.C. Galas, J.B. Helms, N. Vitale, D. Thierse, D. Aunis, and M.F. Bader Regulated exocytosis in chromaffin cells. A potential role for a secretory granule-associated ARF6 protein J Biol Chem 272 5 1997 2788 2793 (Pubitemid 27053323)
3. R. Regazzi, S. Ullrich, R.A. Kahn, and C.B. Wollheim Redistribution of ADP-ribosylation factor during stimulation of permeabilized cells with GTP analogues Biochem J 275 3 1991 639 644
4. R. Regazzi, A. Kikuchi, Y. Takai, and C.B. Wollheim The small GTP-binding proteins in the cytosol of insulin-secreting cells are complexed to GDP dissociation inhibitor proteins J Biol Chem 267 25 1992 17512 17519
5. J.T. Lawrence, and M.J. Birnbaum ADP-ribosylation factor 6 regulates insulin secretion through plasma membrane phosphatidylinositol 4,5-bisphosphate Proc Natl Acad Sci USA 100 23 2003 13320 13325 (Pubitemid 37444740)
6. M. Dunlop, and S.A. Metz A phospholipase D-like mechanism in pancreatic islet cells: stimulation by calcium ionophore, phorbol ester and sodium fluoride Biochem Biophys Res Commun 163 2 1989 922 928 (Pubitemid 19236938)
7. S.A. Metz The pancreatic islet as Rubik's cube. Is phospholipid hydrolysis a piece of the puzzle? Diabetes 40 12 1991 1565 1573
8. V. Poitout Phospholipid hydrolysis and insulin secretion: a step toward solving the Rubik's cube Am J Physiol Endocrinol Metab 294 2 2008 214 216
9. A.K. Gillingham, and S. Munro The small G proteins of the Arf family and their regulators Annu Rev Cell Dev Biol 23 2007 579 611
10. J.E. Casanova Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors Traffic 8 11 2007 1476 1485 (Pubitemid 47578354)
11. E. Macia, M. Chabre, and M. Franco Specificities for the small G proteins ARF1 and ARF6 of the guanine nucleotide exchange factors ARNO and EFA6 J Biol Chem 276 27 2001 24925 24930
12. R. Cox, R.J. Mason-Gamer, C.L. Jackson, and N. Segev Phylogenetic analysis of Sec7-domain-containing Arf nucleotide exchangers Mol Biol Cell 15 4 2004 1487 1505 (Pubitemid 38401802)
13. P. Chardin, S. Paris, B. Antonny, S. Robineau, S. Béraud-Dufour, and C.L. Jackson A human exchange factor for ARF contains Sec7- and pleckstrin-homology domains Nature 384 1996 481 484 (Pubitemid 26414668)
14. L.A. Cohen, A. Honda, P. Varnai, F.D. Brown, T. Balla, and J.G. Donaldson Active Arf6 recruits ARNO/cytohesin GEFs to the PM by binding their PH domains Mol Biol Cell 18 2007 2244 2253 (Pubitemid 46911374)
15. A. Someya, M. Sata, K. Takeda, G. Pacheco-Rodriguez, V.J. Ferrans, and J. Moss ARF-GEP(100), a guanine nucleotide-exchange protein for ADP-ribosylation factor 6 Proc Natl Acad Sci USA 98 2001 2413 2418 (Pubitemid 32209496)
16. J.L. Dunphy, R. Moravec, K. Ly, T.K. Lasell, P. Melancon, and J.E. Casanova The Arf6 GEF GEP100/BRAG2 regulates cell adhesion by controlling endocytosis of beta1 integrins Curr Biol 16 2006 315 320 (Pubitemid 43190232)
17. A.S. Caumont, N. Vitale, M. Gensse, M.C. Galas, J.E. Casanova, and M.F. Bader Identification of a plasma membrane-associated guanine nucleotide exchange factor for ARF6 in chromaffin cells. Possible role in the regulated exocytotic pathway J Biol Chem 275 2000 15637 15644 (Pubitemid 30366858)
18. S. Frank, S. Upender, S.H. Hansen, and J.E. Casanova ARNO is a guanine nucleotide exchange factor for ADP-ribosylation factor 6 J Biol Chem 273 1998 23 27 (Pubitemid 28042170)
19. M. Hafner, A. Schmitz, I. Grune, S.G. Srivatsan, B. Paul, and W. Kolanus Inhibition of cytohesins by secinH3 leads to hepatic insulin resistance Nature 444 2006 941 944 (Pubitemid 46025008)
20. J. Yamauchi, Y. Miyamoto, T. Torii, R. Mizutani, K. Nakamura, and A. Sanbe Valproic acid-inducible Arl4D and cytohesin-2/ARNO, acting through the downstream Arf6, regulate neurite outgrowth in N1E-115 cells Exp Cell Res 315 2009 2043 2052
21. T. Torii, Y. Miyamoto, A. Sanbe, K. Nishimura, J. Yamauchi, and A. Tanoue Cytohesin-2/ARNO, through its interaction with focal adhesion adaptor protein paxillin, regulates preadipocyte migration via the downstream activation of Arf6 J Biol Chem 285 2010 24270 24281
22. A. Kowluru, and R. Veluthakal Rho guanosine diphosphate-dissociation inhibitor plays a negative modulatory role in glucose-stimulated insulin secretion Diabetes 54 2005 3523 3529 (Pubitemid 43334345)
23. P. McDonald, R. Veluthakal, H. Kaur, and A. Kowluru Biologically active lipids promote trafficking and membrane association of Rac1 in insulin-secreting INS 832/13 cells Am J Physiol Cell Physiol 292 2007 C1216 C1220
24. A.K. Nevins, and D.C. Thurmond Glucose regulates the cortical actin network through modulation of Cdc42 cycling to stimulate insulin secretion Am J Physiol Cell Physiol 285 2003 698 710
25. Z. Wang, E. Oh, and D.C. Thurmond Glucose-stimulated Cdc42 signaling is essential for the second phase of insulin secretion J Biol Chem 282 2007 9536 9546 (Pubitemid 47104622)
26. V. Kamath, C.N. Kyathanahalli, B. Jayaram, I. Syed, L.K. Olson, and K. Ludwig Regulation of glucose- and mitochondrial fuel-induced insulin secretion by a cytosolic protein histidine phosphatase in pancreatic beta-cells Am J Physiol Endocrinol Metab 29 2010 E276 E286
27. H. Takatsu, K. Yoshino, K. Toda, and K. Nakayama GGA proteins associate with Golgi membranes through interaction between their GGAH domains and ADP-ribosylation factors Biochem J 365 Pt. 2 2002 369 378 (Pubitemid 36135309)
28. Z. Wang, and D.C. Thurmond Mechanisms of biphasic insulin-granule exocytosis - roles of the cytoskeleton, small GTPases and SNARE proteins J Cell Sci 122 2009 893 903
29. A. Kowluru, and Small G proteins in islet beta-cell function Endocr Rev 31 2010 52 78
30. L.C. Santy, and J.E. Casanova Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D J Cell Biol 154 2001 599 610 (Pubitemid 34286164)
31. L.C. Santy, K.S. Ravichandran, and J.E. Casanova The DOCK180/Elmo complex couples ARNO-mediated Arf6 activation to the downstream activation of Rac1 Curr Biol 15 2005 1749 1754 (Pubitemid 41415632)
32. M. Cotton, P.L. Boulay, T. Houndolo, N. Vitale, J.A. Pitcher, and A. Claing Endogenous ARF6 interacts with Rac1 upon angiotensin II stimulation to regulate membrane ruffling and cell migration Mol Biol Cell 18 2007 501 511 (Pubitemid 46213219)
33. J.S. Tushir, and C. D'Souza-Schorey ARF6-dependent activation of ERK and Rac1 modulates epithelial tubule development EMBO J 26 2007 1806 1819 (Pubitemid 46624055)
34. B. Hu, B. Shi, M.J. Jarzynka, J.J. Yiin, C. D'Souza-Schorey, and S.Y. Cheng ADP-ribosylation factor 6 regulates glioma cell invasion through the IQ-domain GTPase-activating protein 1-Rac1-mediated pathway Cancer Res 69 2009 794 801
35. V. Muralidharan-Chari, H. Hoover, J. Clancy, J. Schweitzer, M.A. Suckow, and V. Schroeder ADP-ribosylation factor 6 regulates tumorigenic and invasive properties in vivo Cancer Res 69 2009 2201 2209
36. A. Kowluru, S.E. Seavey, G. Li, R.L. Sorenson, A.J. Weinhaus, and R. Nesher Glucose- and GTP-dependent stimulation of the carboxyl methylation of CDC42 in rodent and human pancreatic islets and pure beta cells. Evidence for an essential role of GTP-binding proteins in nutrient-induced insulin secretion J Clin Invest 98 1996 540 555 (Pubitemid 26255756)
37. R. Veluthakal, S.V. Madathilparambil, P. McDonald, L.K. Olson, and A. Kowluru Regulatory roles for Tiam1, a guanine nucleotide exchange factor for Rac1, in glucose-stimulated insulin secretion in pancreatic beta-cells Biochem Pharmacol 77 1 2009 101 113
38. M. Murakami, P.I. Meneses, J.S. Knight, K. Lan, R. Kaul, and S.C. Verma Nm23-H1 modulates the activity of the guanine exchange factor Dbl-1 Int J Cancer 123 3 2008 500 510 (Pubitemid 351898406)
39. C. D'Souza-Schorey, and P. Chavrier ARF proteins: roles in membrane traffic and beyond Nat Rev Mol Cell Biol 7 2006 347 358
40. M.F. Bader, and N. Vitale Phospholipase D in calcium-regulated exocytosis: lessons from chromaffin cells Biochim Biophys Acta 1791 2009 936 941
41. A. Begle, P. Tryoen-Toth, J. de Barry, M.F. Bader, and N. Vitale ARF6 regulates the synthesis of fusogenic lipids for calcium-regulated exocytosis in neuroendocrine cells J Biol Chem 284 2009 4836 4845
42. J.A. Grodnitzky, N. Syed, M.J. Kimber, T.A. Day, J.G. Donaldson, and W.H. Hsu Somatostatin receptors signal through EFA6A-ARF6 to activate phospholipase D in clonal beta-cells J Biol Chem 282 2007 13410 13418 (Pubitemid 47100549)
43. W.N. Ma, S.Y. Park, and J.S. Han Role of phospholipase D1 in glucose-induced insulin secretion in pancreatic Beta cells Exp Mol Med 42 2010 456 464
44. S.A. Metz, and M. Dunlop Stimulation of insulin release by phospholipase D. A potential role for endogenous phosphatidic acid in pancreatic islet function Biochem J 270 1990 427 435 (Pubitemid 20273485)
45. S. Metz, M. Dunlop, and Phospholipase D in the pancreatic islet: evidence suggesting the involvement of phosphatidic acid in signal transduction Adv Prostaglandin Thromboxane Leukot Res 21A 1991 287 290
46. W.E. Hughes, Z. Elgundi, P. Huang, M.A. Frohman, and T.J. Biden Phospholipase D1 regulates secretagogue-stimulated insulin release in pancreatic beta-cells J Biol Chem 279 2004 27534 27541 (Pubitemid 38812594)
47. T. Dubois, O. Olivia Paléotti, A.A. Mironov, V. Fraisier, T.E.B. Stradal, and A. De Matteis Golgi-localized GAP for Cdc42 functions downstream of ARF1to control Arp2/3 complex and F-actin dynamics Nat Cell Biol 7 2005 353 364 (Pubitemid 40533124)
48. A. Kowluru, and S.A. Metz Regulation of guanine-nucleotide binding proteins in islet subcellular fractions by phospholipase-derived lipid mediators of insulin secretion Biochim Biophys Acta 1222 1994 360 368