Protein farnesylation-dependent Raf/extracellular signal-related kinase signaling links to cytoskeletal remodeling to facilitate glucose-induced insulin secretion in pancreatic β-cells

Diabetes

Volumn 59, Issue 4, 2010, Pages 967-977

  Kowluru, Anjaneyulu ^a   Veluthakal, Rajakrishnan ^a   Rhodes, Christopher J ^b   Kamath, Vasudeva ^a   Syed, Ismail ^a   Koch, Brandon J ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b University of Chicago ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 (3,5 DIBROMO 4 HYDROXYBENZYLIDENE) 1,3 DIHYDRO 5 IODO 2 INDOLONE; GLUCOSE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; P21 ACTIVATED KINASE; PROTEIN FARNESYLTRANSFERASE INHIBITOR; RAF PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE SILENCING; GENETIC TRANSFECTION; INSULIN RELEASE; MALE; NONHUMAN; PANCREAS ISLET BETA CELL; PRENYLATION; PRIORITY JOURNAL; PROTEIN FARNESYLATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; CYTOSKELETON; ENZYME ACTIVATION; GENES, RAS; GLUCOSE; GTP-BINDING PROTEINS; INSULIN; INSULIN-SECRETING CELLS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PRENYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-RAF; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 77951159949     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-1334     Document Type: Article

References (50)

1. Prentki M, Matschinsky FM. Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol Rev 1987;67:1185-1248
2. MacDonald MJ. Elusive proximal signals of beta-cells for insulin secretion. Diabetes 1990;39:1461-1466
3. Newgard CB, McGarry JD. Metabolic coupling factors in pancreatic β-cell signal transduction. Annu Rev Biochem 1995;64:689-719
4. Poitout V. Phospholipid hydrolysis and insulin secretion: a step toward solving the Rubik's cube. Am J Physiol Endocrinol Metab 2008;294:E214-E216
5. Jones PM, Persaud SJ. Protein kinases, protein phosphorylation, and the regulation of insulin secretion from pancreatic β-cells. Endocr Rev 1998; 19:429-461
6. Khoo S, Gibson TB, Arnette D, Lawrence M, January B, McGlynn K, Vanderbilt CA, Griffen SC, German MS, Cobb MH. MAP kinases and their roles in pancreatic beta-cells. Cell Biochem Biophys 2004;40(Suppl. 3):191-200
7. Kowluru A. Identification and characterization of a novel protein histidine kinase in the islet beta cell: evidence for its regulation by mastoparan, an activator of G-proteins and insulin secretion. Biochem Pharmacol 2002;63: 2091-2100
8. 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
9. Bokoch GM. Biology of the p21-activated kinases. Annu Rev Biochem 2003;72:743-781
10. Chong H, Vikis HG, Guan KL. Mechanisms of regulating the Raf kinase family. Cell Signal 2003;15:463-469
11. Baccarini M. Second nature: biological functions of the Raf-1 "kinase." FEBS Lett 2005;579:3271-3277
12. DerMardirossian CM, Bokoch GM. Phosphorylation of RhoGDI by p21-activated kinase 1. Methods Enzymol 2006;406:80-90
13. Takai Y, Sasaki T, Matozaki T. Small GTP-binding proteins. Physiol Rev 2001;81:153-208
14. Kowluru A. Small G-proteins in islet beta-cell function. Endocr Rev 2010;31:52-78
15. Kowluru A. Protein prenylation in glucose-induced insulin secretion from the pancreatic islet beta cell: a perspective. J Cell Mol Med 2008;12:164-173
16. Casey PJ, Seabra MC. Protein prenyltransferases. J Biol Chem 1996;271: 5289-5292
17. Seabra MC, Reiss Y, Casey PJ, Brown MS, Goldstein JL. Protein farnesyltransferase and geranylgeranyltransferase share a common alpha subunit. Cell 1991;65:429-434
18. Fu HW, Casey PJ. Enzymology and biology of CaaX protein prenylation. Rec Prog Horm Res 1999;54:315-342; discussion 342-343
19. Goalstone M, Carel K, Leitner JW, Draznin B. Insulin stimulates the phosphorylation and activity of farnesyltransferase via the Ras-mitogen- activated protein kinase pathway. Endocrinology 1997;138:5119-5124
20. Li G, Regazzi R, Roche E, Wollheim CB. Blockade of mevalonate production by lovastatin attenuates bombesin and vasopressin potentiation of nutrient-induced insulin secretion in HIT-T15 cells: probable involvement of small GTP-binding proteins. Biochem J 1993;289:379-385
21. Metz SA, Rabaglia ME, Stock JB, Kowluru A. Modulation of insulin secretion from normal rat islets by inhibitors of the post-translational modifications of GTP-binding proteins. Biochem J 1993;295:31-40
22. Amin R, Chen HQ, Tannous M, Gibbs R, Kowluru A. Inhibition of glucose-and calcium-induced insulin secretion from betaTC3 cells by novel inhibitors of protein isoprenylation. J Pharmacol Exp Ther 2002;303:82-88
23. Veluthakal R, Kaur H, Goalstone M, Kowluru A. Dominant-negative alpha-subunit of farnesyl- and geranylgeranyltransferase inhibits glucose-stimulated, but not KCl-stimulated, insulin secretion in INS 832/13 cells. Diabetes 2007;56:204-210
24. Ehses JA, Pelech SL, Pederson RA, McIntosh CH. Glucose-dependent insulinotropic polypeptide activates the Raf-Mek1/2-ERK1/2 module via a cyclic AMP/cAMP-dependent protein kinase/Rap1-mediated pathway. J Biol Chem 2002;277:37088-37097
25. Briaud I, Lingohr MK, Dickson LM, Wrede CE, Rhodes CJ. Differential activation mechanisms of Erk-1/2 and p70(S6K) by glucose in pancreatic beta-cells. Diabetes 2003;52:974-983
26. Trümper J, Ross D, Jahr H, Brendel MD, Göke R, Hörsch D. The Rap-B-Raf signalling pathway is activated by glucose and glucagon-like peptide-1 in human islet cells. Diabetologia 2005;48:1534-1540
27. 2+ influx through L-type voltage-gated calcium channels mediate Rafindependent activation of extracellular regulated kinase in response to glucagon-like peptide-1 in pancreatic beta-cells. J Biol Chem 2002;277: 48146-48151
28. Raman M, Chen W, Cobb MH. Differential regulation and properties of MAPKs. Oncogene 2007;26:3100-3112
29. Veluthakal R, Madathilparambil SV, McDonald P, Olson LK, Kowluru A. Regulatory roles of Tiam1, a guanine nucleotide exchange factor for Rac1, in glucose-stimulated insulin secretion in pancreatic beta-cells. Biochem Pharmacol 2009;77:101-113
30. Kowluru A, Seavey SE, Li G, Sorenson RL, Weinhaus AJ, Nesher R, Rabaglia ME, Vadakekalam J, Metz SA. Glucose- and GTP-dependent stimulation of the carboxylmethylation of Cdc42 in rodent and human pancreatic islets and pure beta cells: evidence for an essential role for GTP-binding proteins in nutrient-induced insulin secretion. J Clin Invest 1996;98:540-555
31. Li J, Luo R, Kowluru A, Li G. Novel regulation by Rac1 of glucose- and forskolin-induced insulin secretion in INS-1 beta-cells. Am J Physiol Endocrinol Metab 2004;286:E818-E827
32. Higashijima T, Uzu S, Nakajima T, Ross EM. Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTP-binding proteins (G proteins). J Biol Chem 1988;263:6491-6494
33. Straub SG, James RF, Dunne MJ, Sharp GW. Glucose augmentation of mastoparan-stimulated insulin secretion in rat and human pancreatic islets. Diabetes 1998;47:1053-1057
34. Daniel S, Noda M, Cerione RA, Sharp GW. A link between Cdc42 and syntaxin is involved in mastoparan-stimulated insulin release. Biochemistry 2002;41:9663-9671
35. Amin RH, Chen HQ, Veluthakal R, Silver RB, Li J, Li G, Kowluru A. Mastoparan-induced insulin secretion from insulin-secreting betaTC3 and INS-1 cells: evidence for its regulation by Rho subfamily of G proteins. Endocrinology 2003;144:4508-4518
36. Jones PM, Mann FM, Persaud SJ, Wheeler-Jones CP. Mastoparan stimulates insulin secretion from pancreatic beta-cells by effects at a late stage in the secretory pathway. Mol Cell Endocrinol 1993;94:97-103
37. Lawrence M, Shao C, Duan L, McGlynn K, Cobb MH. The protein kinases ERK1/2 and their roles in pancreatic beta cells. Acta Physiol (Oxf) 2008;192:11-17
38. Khoo S, Griffen SC, Xia Y, Baer RJ, German MS, Cobb MH. Regulation of insulin gene transcription by ERK1 and ERK2 in pancreatic beta cells. J Biol Chem 2003;278:32969-32977 (Pubitemid 37055741)
39. Arnette D, Gibson TB, Lawrence MC, January B, Khoo S, McGlynn K, Vanderbilt CA, Cobb MH. Regulation of ERK1 and ERK2 by glucose and peptide hormones in pancreatic beta cells. J Biol Chem 2003;278:32517-32525 (Pubitemid 37055689)
40. Gibson TB, Lawrence MC, Gibson CJ, Vanderbilt CA, McGlynn K, Arnette D, Chen W, Collins J, Naziruddin B, Levy MF, Ehrlich BE, Cobb MH. Inhibition of glucose-stimulated activation of extracellular signal-regulated protein kinase 1 and 2 by epinephrine in pancreatic beta-cells. Diabetes 2006;55:1066-1073
41. Frödin M, Sekine N, Roche E, Filloux C, Prentki M, Wollheim CB, Van Obberghen E. Glucose, other secretagogues, and nerve growth factor stimulate mitogen-activated protein kinase in the insulin-secreting beta-cell line, INS-1. J Biol Chem 1995;270:7882-7889
42. Kowluru A, Veluthakal R. Rho guanosine diphosphate-dissociation inhibitor plays a negative modulatory role in glucose-stimulated insulin secretion. Diabetes 2005;54:3523-3529
43. Kowluru A, Li G, Metz SA. Glucose activates the carboxyl methylation of gamma subunits of trimeric GTP-binding proteins in pancreatic beta cells. Modulation in vivo by calcium, GTP, and pertussis toxin. J Clin Invest 1997;100:1596-1610
44. Khoo S, Cobb MH. Activation of mitogen-activating protein kinase by glucose is not required for insulin secretion. Proc Natl Acad Sci U S A 1997;94:5599-5604
45. Burns CJ, Howell SL, Jones PM, Persaud SJ. Glucose-stimulated insulin secretion from rat islets of Langerhans is independent of mitogen-activated protein kinase activation. Biochem Biophys Res Commun 1997;239:447-450
46. Gray E, Muller D, Squires PE, Asare-Anane H, Huang GC, Amiel S, Persaud SJ, Jones PM. Activation of the extracellular calcium-sensing receptor initiates insulin secretion from human islets of Langerhans: involvement of protein kinases. J Endocrinol 2006;190:703-710
47. Longuet C, Broca C, Costes S, Hani EH, Bataille D, Dalle S. Extracellularly regulated kinases 1/2 (p44/42 mitogen-activated protein kinases) phosphorylate synapsin I and regulate insulin secretion in the MIN6 beta-cell line and islets of Langerhans. Endocrinology 2005;146:643-654
48. Kawabata M, Imamura T, Miyazono K, Engel ME, Moses HL. Interaction of the transforming growth factor-beta type I receptor with farnesyl-protein transferase-alpha. J Biol Chem 1995;270:29628-29631
49. Wang T, Danielson PD, Li BY, Shah PC, Kim SD, Donahoe PK. The p21(RAS) farnesyltransferase alpha subunit in TGF-beta and activin signaling. Science 1996;271:1120-1122
50. Goalstone M, Kamath V, Kowluru A. Glucose activates prenyltransferases in pancreatic islet beta-cells. Biochem Biophys Res Commun 2010;391: 895-898