Novel roles for palmitoylation of Ras in IL-1β-induced nitric oxide release and caspase 3 activation in insulin-secreting β cells

Biochemical Pharmacology

Volumn 66, Issue 9, 2003, Pages 1681-1694

  Chen, Hai Qing ^a   Tannous, Marie ^a   Veluthakal, Rajakrishnan ^a   Amin, Rajesh ^a   Kowluru, Anjaneyulu ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Caspase 3; Cerulenin; IL 1 ; Insulin dependent diabetes mellitus; Nitric oxide; Palmitoylation; Ras

Indexed keywords

CASPASE 3; CAVEOLIN 1; CERULENIN; CHOLESTEROL; CYTOKINE; INTERLEUKIN 1BETA; METHYL BETA CYCLODEXTRIN; N(G) METHYLARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PALMITIC ACID; PROTEIN INHIBITOR; RAS PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL FUNCTION; CELL ISOLATION; CELL MEMBRANE; CELL STRAIN; CONTROLLED STUDY; CROSS LINKING; CYTOSOL; CYTOSOLIC FRACTION; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME RELEASE; GENE EXPRESSION; INSULIN RELEASE; MEMBRANE BINDING; MICROSCOPY; MYRISTYLATION; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE;

EID: 0141888306     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(03)00549-5     Document Type: Article

References (61)

1. Takai Y., Kaibuchi K., Kikuchi A., Kawata M. Small GTP-binding proteins. Int. Rev. cytol. 36:1992;187-230.
2. Kowluru A, Robertson RP, Metz SA. In: LeRoith D, Taylor SI, Olefsky JM, editors. Diabetes mellitus: a fundamental and clinical text. Philadelphia: Lippincott Williams and Wilkins; 2000. p. 78-94.
3. Rando R.R. Chemical biology of protein isoprenylation/methylation. Biochim. Biophys. Acta. 300:1996;5-16.
4. Philips M.R., Staud R., Pillinger M., Feoktistov A., Volker C., Stock J., Weisermann G. Activation-dependent carboxyl methylation of neutrophil G-protein gamma subunit. Proc. Natl. Acad. Sci. U.S.A. 92:1995;2283-2287.
5. Metz S.A., Rabaglia M.E., Stock J.B., Kowluru A. Modulation of insulin secretion from normal rat islets by inhibitors of the post-translational modifications of GTP-binding proteins. Biochem. J. 295:1993;31-40.
6. Li G., Regazzi R., Roche E., Wollheim C.B. Blockade of mevalonate production by lovastatin attenuates bombesin and vasopressin potentiation of nutrient-induced insulin secretion in HIT-T15 cells. Biochem. J. 289:1993;379-385.
7. Amin R., Chen H.-Q., Tannous M., Gibbs R., Kowluru A. Inhibition by novel inhibitors of protein isoprenylation of glucose- and calcium-induced insulin secretion from βTC3 cells. J. Pharmacol. Exp. Ther. 303:2002;82-88.
8. Moffett S., Brown D.A., Linder M.E. Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 275:2000;2191-2198.
9. Wedegaertner P.B., Bourne H.R. Activation and depalmitoylation of Gs alpha. Cell. 77:1994;1063-1070.
10. Bourne H.R. Do GTPases direct membrane traffic in secretion? Cell. 53:1988;669-672.
11. Camp L.A., Hofman S.L. Assay and isolation of palmitoyl-protein thioesterase from bovine brain using palmitoylated H-Ras as substrate. Methods Enzymol. 250:1995;336-347.
12. Chen C.A., Manning D.R. Regulation of G proteins by covalent modification. Oncogene. 20:2001;1643-1652.
13. Straub S.G., Yajima H., Komatsu M., Aizawa T., Sharp G.W. The effects of cerulenin, an inhibitor of protein acylation, on the two phases of glucose-stimulated insulin secretion. Diabetes. 51:2002;91-95.
14. Yajima H., Komatsu M., Yamada S., Straub S.G., Kaneko T., Sato Y., Yamauchi K., Hashizume K., Sharp G.W., Aizawa T. The effects of cerulenin, an inhibitor of protein acylation, on the two phases of glucose-stimulated insulin secretion. Diabetes. 49:2002;712-717.
15. Deeney J.T., Gromada J., Hoy M., Olson H.L., Rhodes C.J., Prentki M., Berggren P.O., Corkey B.E. Acute stimulation with long chain acyl-CoA enhances exocytosis in insulin-secreting cells (HIT T-15 and NMRI beta-cells). J. Biol. Chem. 275:2000;9363-9368.
16. Prior I.A., Harding A., Yan J., Sluimer J., Parton R.G., Hancock J.F. GTP dependent segregation of H-Ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3:2001;368-375.
17. Chen Z.Q., Ulsh L.S., DuBois G., Shih T.Y. Posttranslational processing of p21 ras proteins involves palmitoylation of the C-terminal tetrapeptide containing cysteine-186. J. Virol. 56:1985;607-612.
18. Dudler T., Gelb M.H. Palmitoylation of Ha-Ras facilitates membrane binding, activation of downstream effectors, and meiotic maturation in Xenopus oocytes. J. Biol. Chem. 271:1996;11541-11547.
19. Song K.S., Li S., Okamoto T., Quilliam L.A., Sargiacomo M., Lisanti M.P. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J. Biol. Chem. 271:1996;9690-9697.
20. Li S., Couet J., Lisanti M.P. Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J. Biol. Chem. 271:1996;29182-29190.
21. Chen C.H., Wang H.C., Chuang N.N. Interaction of shrimp ras protein with mammalian caveolin-1. J. Exp. Zool. 287:2000;432-439.
22. Tannous M., Amin R., Popoff M., Fiorentini C., Kowluru A. Positive modulation by Ras of interleukin-1beta-mediated nitric oxide generation in insulin-secreting clonal beta (HIT-T15) cells. Biochem. Pharmacol. 62:2001;1459-1468.
23. Kowluru A., Seavey S.E., Rabaglia M.E., Nesher R., Metz S.A. Carboxylmethylation of the catalytic subunit of protein phosphatase 2A in insulin-secreting cells: evidence for functional consequences on enzyme activity and insulin secretion. Endocrinology. 137:1996;2315-2323.
24. Kowluru A., Metz S.A. Characterization of nucleoside diphosphokinase activity in human and rodent pancreatic beta cells: evidence for its role in the formation of guanosine triphosphate, a permissive factor for nutrient-induced insulin secretion. Biochemistry. 41:1994;12495-12503.
25. Kowluru A., Seavey S.E., Rhodes C.J., Metz S.A. A novel regulatory mechanism for trimeric GTP-binding proteins in the membrane and secretory granule fractions of human and rodent beta cells. Biochem. J. 313:1996;97-107.
26. Kowluru A., Seavey S., Li G., Sorenson R.L., Weinhaus A.J., Nesher R., Rabaglia M.E., Vadakekalam J., Metz S.A. 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.
27. Kowluru A., Li G., Metz S.A. 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. 100:1997;596-610.
28. Kowluru A., Li G., Rabaglia M., Segu V., Hofmann F., Aktories K., Metz S. Evidence for differential roles of the Rho subfamily of GTP-binding proteins in glucose- and calcium-induced insulin secretion from pancreatic beta cells. Biochem. Pharmacol. 54:1997;1097-1108.
29. Ushio-Fukai M., Santanam H.L., Becker P.L., Ma Y., Griendling K.K., Alexander R.W. Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells: role of cholesterol-rich microdomains and focal adhesions in angiotensin II signaling. J. Biol. Chem. 276:2001;48269-48275.
30. Webb Y., Matsumoto H.L., Resh M.D. Inhibition of protein palmitoylation, raft localization, and T cell signaling by 2-bromopalmitate and polyunsaturated fatty acids. J. Biol. Chem. 275:2000;261-270.
31. Paige L.A., Zheng G.Q., DeFrees S.A., Cassady J.M., Geahlen R.L. Metabolic activation of 2-substituted derivatives of myristic acid to form potent inhibitors of myristoyl CoA:protein N-myristoyltransferase. Biochemistry. 29:1990;10566-10573.
32. Apolloni A., Prior I.A., Linseay M., Parton R.G., Hancock J.F. H-ras but not K-ras traffics to the plasma membrane through the exocytotic pathway. Mol. Cell. Biol. 20:2000;2475-2487.
33. Coats S.G., Booden M.A., Buss J.E. Transient palmitoylation supports H-Ras membrane binding but only partial biological activity. Biochemistry. 38:1999;12926-12934.
34. Willusen B.M., Cox A.D., Solski P.A., Der C.J., Buss J.E. Novel determinants of H-Ras plasma membrane localization and transformation. Oncogene. 13:1996;1901-1909.
35. Van Cott E.M., Muszbek L., Laposata M. Fatty acid acylation of platelet proteins. Prostaglandins Leukot. Essent. Fatty Acids. 57:1997;33-37.
36. Kowluru A, Metz SA. In: Draznin B, LeRoith D, editors. Molecular biology of diabetes. Tottawa, NJ: Humana Press; 1994. p. 249-83.
37. Kowluru A., Metz S.A. Subcellular distribution and posttranslational modifications of GTP-binding proteins in insulin-secreting cells. Methods Neurosci. 29:1996;298-318.
38. Leiser M., Efrat S., Fleischer N. Evidence that Rap1 carboxylmethylation is involved in regulated insulin secretion. Endocrinology. 136:1995;2521-2530.
39. Clarke S. Protein isoprenylation and methylation at carboxyl-terminal cysteine residues. Annu. Rev. Biochem. 61:1992;355-386.
40. Kumar S. Mechanisms mediating caspase activation in cell death. Cell Death Differ. 6:1999;1060-1066.
41. Earnshaw W.C., Martins L.M., Kaufmann S.H. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68:1999;383-424.
42. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
43. Cross T., Griffiths G., Deacon E., Sallis R., Gough M., Watters D., Lord J.M. PKC-delta is an apoptotic lamin kinase. Oncogene. 19:2000;2331-2337.
44. Dreja K., Voldstedlund M., Vinten J., Tranum-Jensen J., Hellstrand P., Sward K. Cholesterol depletion disrupts caveolae and differentially impairs agonist-induced arterial contraction. Arterioscler. Thromb. Vasc. Biol. 22:2002;1267-1272.
45. Bach J.F. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr. Rev. 15:1994;516-542.
46. Rabinovitch A., Suarez-Pinzon W.L. Cytokines and their roles in pancreatic islet beta-cell destruction and insulin-dependent diabetes mellitus. Biochem. Pharmacol. 55:1998;139-149.
47. Kowluru A., Amin R. Inhibitors of post-translational modifications of G-proteins as probes to study the pancreatic beta cell function: potential therapeutic implications. Curr. Drug Targets Immun. Endocr. Metab. Disord. 2:2002;129-138.
48. Carey KD, Watson RT, Pessin JE, Stork PJ. The requirement of specific membrane domains for Raf-1 phosphorylation and activation. J Biol Chem 2002; in press.
49. Roy S., Wyse B., Hancock J.F. H-Ras signaling and K-Ras signaling are differentially dependent on endocytosis. Mol. Cell. Biol. 22:2002;5128-5140.
50. Kowluru A., Morgan N.G. GTP-binding proteins in cell survival and demise: the emerging picture in the pancreatic beta-cell. Biochem. Pharmacol. 63:2002;1027-1035.
51. Baker T.L., Booden M.A., Buss J.E. S-Nitrosocysteine increases palmitate turnover on Ha-Ras in NIH 3T3 cells. J. Biol. Chem. 275:2000;22037-22047.
52. Prior I.A., Hancock J.F. Compartmentalization of Ras proteins. J. Cell Sci. 114:2001;1603-1608.
53. Jochen A.L., Hays J., Mick G. Inhibitory effects of cerulenin on protein palmitoylation and insulin internalization in rat adipocytes. Biochim. Biophys. Acta. 1259:1995;65-72.
54. Pizer E.S., Thupari J., Han W.F., Pinn M.L., Chrest F.J., Frehywot G.L., Townsend C.A., Kuhajda F.P. Malonyl-coenzyme-A is a potential mediator of cytotoxicity induced by fatty-acid synthase inhibition in human breast cancer cells and xenografts. Cancer Res. 60:2000;213-218.
55. De Vos M.L., Lawrence D.S., Smith C.D. Cellular pharmacology of cerulenin analogs that inhibit protein palmitoylation. Biochem. Pharmacol. 62:2001;985-995.
56. Cadwallader K.A., Paterson H., Macdonald S.G., Hancock J.F. N-Terminally myristoylated Ras proteins require palmitoylation or a polybasic domain for plasma membrane localization. Mol. Cell. Biol. 14:1994;4722-4730.
57. Hawash I.Y., Hu X.E., Adal A., Cassady J.M., Geahlen R.L., Harrison M.L. The oxygen-substituted palmitic acid analogue, 13-oxypalmitic acid, inhibits Lck localization to lipid rafts and T cell signaling. Biochim. Biophys. Acta. 1589:2002;140-150.
58. Parton G.P., Hancock J.F. Caveolin and Ras function. Methods Enzymol. 333:2001;172-183.
59. Sternberg P.W., Schmid S.L. Caveolin, cholesterol and Ras signalling. Nat. Cell Biol. 1:1999;E35-E37.
60. Prat M.O., Fox P.L. Palmitoylation of caveolin-1 in endothelial cells is post-translational but irreversible. J. Biol. Chem. 276:2001;15776-15782.
61. Tannous M., Veluthakal R., Amin R., Kowluru A. IL-1β-induced nitric oxide release from insulin-secreting β-cells: further evidence for the involvement of GTP-binding proteins. Diabetes Metab. 28:2002;3S0-3S7.