Phagocytic NADPH oxidase links ARNO-Arf6 signaling pathway in glucose-stimulated insulin secretion from the pancreatic β-cell

Cellular Physiology and Biochemistry

Volumn 30, Issue 6, 2012, Pages 1351-1362

  Jayaram, Bhavaani ^a,b   Kowluru, Anjaneyulu ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

ADP ribosylation factor 6; Insulin secretion; NADPH oxidase; Pancreatic islet; Reactive oxygen species

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR NUCLEOTIDE BINDING SITE OPENER; ARF PROTEIN; COFILIN; GLUCOSE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOLIPASE D; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION;

RATTUS;

EID: 84867687387     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000343324     Document Type: Article

References (36)

1. Kowluru A: Small G proteins in islet beta-cell function. Endocr Rev 2010;31:52-78.
2. Wang Z, Thurmond DC: Mechanisms of biphasic insulin-granule exocytosis - roles of the cytoskeleton, small GTPases and SNARE proteins. J Cell Sci 2009;122:893-903.
3. Donaldson JG: Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J Biol Chem 2003;278:41573-41576. (Pubitemid 37310409)
4. Galas MC, Helms JB, Vitale N, Thierse D, Aunis D, Bader MF: Regulated exocytosis in chromaffin cells. A potential role for a secretory granule-associated ARF6 protein. J Biol Chem 1997;272:2788-2793. (Pubitemid 27053323)
5. Ma WN, Park SY, Han JS: Role of phospholipase D1 in glucose-induced insulin secretion in pancreatic Beta cells. Exp Mol Med 2010;42:456-464.
6. Jayaram B, Syed I, Kyathanahalli CN, Rhodes CJ, Kowluru A: Arf nucleotide binding site opener [ARNO] promotes sequential activation of Arf6, Cdc42 and Rac1 and insulin secretion in INS 832/13 beta-cells and rat islets. Biochem Pharmacol 2011;81:1016-1027.
7. Kolanus W: Guanine nucleotide exchange factors of the cytohesin family and their roles in signal transduction. Immunol Rev 2007;218:102-113. (Pubitemid 47052312)
8. Caumont AS, Galas MC, Vitale N, Aunis D, Bader MF: Regulated exocytosis in chromaffin cells. Translocation of ARF6 stimulates a plasma membrane-associated phospholipase D. J Biol Chem 1998;273:1373-1379. (Pubitemid 28133655)
9. Vitale N, Chasserot-Golaz S, Bader MF: Regulated secretion in chromaffin cells: an essential role for ARF6-regulated phospholipase D in the late stages of exocytosis. Ann N Y Acad Sci 2002;971:193-200. (Pubitemid 35305293)
10. McDonald P, Veluthakal R, Kaur H, Kowluru A: Biologically active lipids promote trafficking and membrane association of Rac1 in insulin-secreting INS 832/13 cells. Am J Physiol Cell Physiol 2007;292:C1216-C1220. (Pubitemid 46440411)
11. Hu B, Shi B, Jarzynka MJ, Yiin JJ, D'Souza-Schorey C, Cheng SY: ADP-ribosylation factor 6 regulates glioma cell invasion through the IQ-domain GTPase-activating protein 1-Rac1-mediated pathway. Cancer Res 2009;69:794-801.
12. Hordijk PL: Regulation of NADPH oxidases: the role of Rac proteins. Circ Res 2006;98:453-462.
13. Brown DI, Griendling KK: Nox proteins in signal transduction. Free Radic Biol Med 2009;47:1239-1253.
14. Syed I, Kyathanahalli CN, Kowluru A: Phagocyte-like NADPH oxidase generates ROS in INS 832/13 cells and rat islets: role of protein prenylation. Am J Physiol Regul Integr Comp Physiol 2011;300:R756-R762.
15. Morgan D, Rebelato E, Abdulkader F, Graciano MF, Oliveira-Emilio HR, Hirata AE, Rocha MS, Bordin S, Curi R, Carpinelli AR: Association of NAD (P) H oxidase with glucose-induced insulin secretion by pancreatic betacells. Endocrinology 2009;150:2197-2201.
16. Abe J, Berk BC: Fyn and JAK2 mediate Ras activation by reactive oxygen species. J Biol Chem 1999;274:21003-21010.
17. Bi X, Schmitz A, Hayallah AM, Song JN, Famulok M: Affinity-based labeling of cytohesins with a bifunctional SecinH3 photoaffinity probe. Angew Chem Int Ed Engl 2008;47:9565-9568.
18. Kowluru A, Veluthakal R: Rho guanosine diphosphate-dissociation inhibitor plays a negative modulatory role in glucose-stimulated insulin secretion. Diabetes 2005;54:3523-3529. (Pubitemid 43334345)
19. Kim C, Dinauer MC: Impaired NADPH oxidase activity in Rac2-deficient murine neutrophils does not result from defective translocation of p47phox and p67phox and can be rescued by exogenous arachidonic acid. J Leukoc Biol 2006;79:223-234. (Pubitemid 43054268)
20. Begle A, Tryoen-Toth P, De BJ, Bader MF, Vitale N: ARF6 regulates the synthesis of fusogenic lipids for calciumregulated exocytosis in neuroendocrine cells. J Biol Chem 2009;284:4836-4845.
21. Massenburg D, Han JS, Liyanage M, Patton WA, Rhee SG, Moss J, Vaughan M: Activation of rat brain phospholipase D by ADP-ribosylation factors 1, 5, and 6: separation of ADP-ribosylation factor-dependent and oleate-dependent enzymes. Proc Natl Acad Sci USA 1994;91:11718-11722. (Pubitemid 24356416)
22. Metz SA, Dunlop M: Stimulation of insulin release by phospholipase D. A potential role for endogenous phosphatidic acid in pancreatic islet function. Biochem J 1990;270:427-435. (Pubitemid 20273485)
23. El Azreq MA, Garceau V, Harbour D, Pivot-Pajot C, Bourgoin SG: Cytohesin-1 regulates the Arf6-phospholipase D signaling axis in human neutrophils: impact on superoxide anion production and secretion. J Immunol 2010;184:637-649.
24. Vignais PV: The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell Mol Life Sci 2002;59:1428-1459. (Pubitemid 35239301)
25. Dusi S, Della B, V, Grzeskowiak M, Rossi F: Relationship between phosphorylation and translocation to the plasma membrane of p47phox and p67phox and activation of the NADPH oxidase in normal and Ca (2+) - depleted human neutrophils. Biochem J 1993;290:173-178. (Pubitemid 23081216)
26. Kowluru A, Veluthakal R, Rhodes CJ, Kamath V, Syed I, Koch BJ: Protein farnesylation-dependent Raf/extracellular signal-related kinase signaling links to cytoskeletal remodeling to facilitate glucose-induced insulin secretion in pancreatic beta-cells. Diabetes 2010;59:967-977.
27. Matti A, Kyathanahalli C, Kowluru A: Protein farnesylation is requisite for mitochondrial fuel-induced insulin release: Further evidence to link reactive oxygen species generation to insulin secretion in pancreatic betacells. Islets 2012;4
28. Graciano MF, Valle MM, Kowluru A, Curi R, Carpinelli AR: Regulation of insulin secretion and reactive oxygen species production by free fatty acids in pancreatic islets. Islets 2011;3:213-223.
29. Rebelato E, Mares-Guia TR, Graciano MF, Labriola L, Britto LR, Garay-Malpartida HM, Curi R, Sogayar MC, Carpinelli AR: Expression of NAD (P) H oxidase in human pancreatic islets. Life Sci 2012;91:244-249.
30. Parton LE, McMillen PJ, Shen Y, Docherty E, Sharpe E, Diraison F, Briscoe CP, Rutter GA: Limited role for SREBP-1c in defective glucose-induced insulin secretion from Zucker diabetic fatty rat islets: a functional and gene profiling analysis. Am J Physiol Endocrinol Metab 2006;291:E982-E994. (Pubitemid 44794221)
31. Tushir JS, D'Souza-Schorey C: ARF6-dependent activation of ERK and Rac1 modulates epithelial tubule development. EMBO J 2007;26:1806-1819. (Pubitemid 46624055)
32. Paruch S, El-Benna J, Djerdjouri B, Marullo S, Perianin A: A role of p44/42 mitogen-activated protein kinases in formyl-peptide receptor-mediated phospholipase D activity and oxidant production. FASEB J 2006;20:142-144. (Pubitemid 43100494)
33. Tushir JS, Clancy J, Warren A, Wrobel C, Brugge JS, D'Souza-Schorey C: Unregulated ARF6 activation in epithelial cysts generates hyperactive signaling endosomes and disrupts morphogenesis. Mol Biol Cell 2010;21:2355-2366.
34. Kowluru A: Friendly, and not so friendly, roles of Rac1 in islet beta-cell function: lessons learnt from pharmacological and molecular biological approaches. Biochem Pharmacol 2011;81:965-975.
35. Pi J, Bai Y, Zhang Q, Wong V, Floering LM, Daniel K, Reece JM, Deeney JT, Andersen ME, Corkey BE, Collins S: Reactive oxygen species as a signal in glucose-stimulated insulin secretion. Diabetes 2007;56:1783-1791. (Pubitemid 47025446)
36. Ishibashi F: High glucose increases phosphocofilin via phosphorylation of LIM kinase due to Rho/Rho kinase activation in cultured pig proximal tubular epithelial cells. Diabetes Res Clin Pract 2008;80:24-33.