Role of insulin-induced reactive oxygen species in the insulin signaling pathway

Antioxidants and Redox Signaling

Volumn 7, Issue 7-8, 2005, Pages 1021-1031

  Goldstein, Barry J ^a   Mahadev, Kalyankar ^a   Wu, Xiangdong ^a   Zhu, Li ^a   Motoshima, Hiroyuki ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CATALASE; DITHIOTHREITOL; HYDROGEN PEROXIDE; INSULIN; PROTEIN TYROSINE PHOSPHATASE 1B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; THIOL; WORTMANNIN;

ANIMAL CELL; CELL STRAIN 3T3; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE TARGETING; GLUCOSE TRANSPORT; GLYCOGEN SYNTHESIS; INSULIN RELEASE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; INSULIN; OXIDATION-REDUCTION; PHOSPHOTYROSINE; REACTIVE OXYGEN SPECIES; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 17644399404     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2005.7.1021     Document Type: Review

References (78)

1. Andersen IN, Mortensen OH, Peters GH, Drake PG, Iversen LF, Olsen OH, Jansen PG, Andersen HS, Tonks NK, and Moller NP. Structural and evolutionary relationships among protein tyrosine phosphatase domains. Mol Cell Biol 21: 7117-7136, 2001.
2. Babior BM, Lambeth JD, and Nauseef W. The neutrophil NADPH oxidase. Arch Biochem Biophys 397: 342-344, 2002.
3. 2 production requires the activation of phosphatidylinositol 3-kinase. J Biol Chem 275: 10527-10531, 2000.
4. Barford D, Das AK, and Egloff MP. The structure and mechanism of protein phosphatases-insights into catalysis and regulation. Annu Rev Biophys Biomol Struct 27: 133-164, 1998.
5. Barrett WC, DeGnore JP, Keng YF, Zhang ZY, Yim MB, and Chock PB. Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B. J Biol Chem 214: 34543-34546, 1999.
6. Barrett WC, DeGnore JP, Konig S, Fales HM, Keng YF, Zhang ZY, Yim MB, and Chock PB. Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 38: 6699-6705, 1999.
7. Biteau B, Labarre J, and Toledano MB. ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425: 980-984, 2003.
8. Bleyle LA, Peng Y, Ellis C, and Mooney RA. Dissociation of PTPase levels from their modulation of insulin receptor signal transduction. Cell Signal 11: 719-725, 1999.
9. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820, 2001.
10. Chen JF, Guo JH, Moxham CM, Wang HY, and Malbon CC. Conditional, tissue-specific expression of Q205L G alpha i2 in vivo mimics insulin action. J Mol Med 75: 283-289, 1997.
11. Cheng G, Cao Z, Xu X, Van Meir EG, and Lambeth JD. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269: 131-140, 2001.
12. Cheung A, Kusari J, Jansen D, Bandyopadhyay D, Kusari A, and Bryer-Ash M. Marked impairment of protein tyrosine phosphatase 1B activity in adipose tissue of obese subjects with and without type 2 diabetes mellitus. J Lab Clin Med 134: 115-123, 1999.
13. Claiborne A, Yeh JI, Mallett TC, Luba J, Crane EJ, Charrier V, and Parsonage D. Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation. Biochemistry 38: 15407-15416, 1999.
14. ++-dependent thiol stimulation of glucose metabolism in white fat cells. J Biol Chem 247: 6218-6223, 1972.
15. 2+-dependent thiol activation of fat cell glucose utilization. J Biol Chem 249: 1001-1006, 1974.
16. Czech MP, Lawrence JC Jr, and Lynn WS. Evidence for the involvement of sulfhydryl oxidation in the regulation of fat cell hexose transport by insulin. Proc Natl Acad Sci U S A 71: 4173-4177, 1974.
17. DeGnore JP, Konig S, Barrett WC, Chock PB, and Fales HM. Identification of the oxidation states of the active site cysteine in a recombinant protein tyrosine phosphatase by electrospray mass spectrometry using on-line desalting. Rapid Commun Mass Spectrom 12: 1457-1462, 1998.
18. Denu JM and Dixon JE. Protein tyrosine phosphatases-mechanisms of catalysis and regulation. Curr Opin Chem Biol 2: 633-641, 1998.
19. Denu JM and Tanner KG. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide-evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37: 5633-5642, 1998.
20. Ebina Y, Ellis L, Jarnagin K, Edery M, Graf L, Clauser E, Ou J-H, Masiarz F, Kan YW, Goldfine ID, Roth RA, and Rutter WJ. Human insulin receptor cDNA: the structural basis for hormone activated transmembrane signalling. Cell 40: 747-758, 1985.
21. Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, Loy AL, Normandin D, Cheng A, Himms-Hagen J, Chan CC, Ramachandran C, Gresser MJ, Tremblay ML, and Kennedy BP. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283: 1544-1548, 1999.
22. Finkel T. Redox-dependent signal transduction. FEBS Lett 476: 52-54, 2000.
23. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol 15: 247-254, 2003.
24. Flores-Riveros JR, Sibley E, Kastelic T, and Lane MD. Substrate phosphorylation catalyzed by the insulin receptor tyrosine kinase. Kinetic correlation to autophosphorylation of specific sites in the beta subunit. J Biol Chem 264: 21557-21572, 1989.
25. Galic S, Klingler-Hoffmann M, Fodero-Tavoletti MT, Puryer MA, Meng TC, Tonks NK, and Tiganis T. Regulation of insulin receptor signaling by the protein tyrosine phosphatase TCPTP. Mol Cell Biol 23: 2096-2108, 2003.
26. Goldstein BJ. Protein-tyrosine phosphatase 1B (PTP1B): a novel therapeutic target for type 2 diabetes mellitus, obesity and related states of insulin resistance. Curr Drug Targets Immune Endocr Metabol Disord 1: 265-275, 2001.
27. Goldstein BJ. Protein-tyrosine phosphatases and the regulation of insulin action. In: Diabetes Mellitus: A Fundamental and Clinical Text, Vol. 3, edited by LeRoith D, Taylor SI, and Olefsky JM. Philadelphia: Lippincott, 2003, pp. 255-268.
28. Guy GR, Cairns J, Ng SB, and Tan YH. Inactivation of a redox-sensitive protein phosphatase during the early events of tumor necrosis factor/interleukin-1 signal transduction. J Biol Chem 268: 2141-2148, 1993.
29. Haring HU, Kasuga M, White MF, Crettaz M, and Kahn CR. Phosphorylation and dephosphorylation of the insulin receptor: evidence against an intrinsic phosphatase activity. Biochemistry 23: 3298-3306, 1984.
30. Hubbard SR. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J 16: 5572-5581, 1997.
31. Kasuga M, Zick Y, Blithe DL, Crettaz M, and Kahn CR. Insulin stimulates tyrosine phosphorylation of the insulin receptor in a cell-free system. Nature 298: 667-669, 1982.
32. Keyse SM. Protein phosphatases and the regulation of MAP kinase activity. Semin Cell Dev Biol 9: 143-152, 1998.
33. Klaman LD, Boss O, Peroni OD, Kim JK, Martino JL, Zabolotny JM, Moghal N, Lubkin M, Kim YB, Sharpe AH, Stricker-Krongrad A, Shulman GI, Neel BG, and Kahn BB. Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice. Mol Cell Biol 20: 5479-5489, 2000.
34. Kowalski A, Gazzano H, Fehlmann M, and Van Obberghen E. Dephosphorylation of the hepatic insulin receptor: absence of intrinsic phosphatase activity in purified receptors. Biochem Biophys Res Commun 117: 885-893, 1983.
35. 2-generating system that is activated by insulin via a mechanism bypassing the receptor kinase. J Clin Invest 89: 1006-1013, 1992.
36. 2 generation in 3T3 L1-cells. Biochem J 307: 549-556, 1995.
37. 2-generating system present in human fat-cell plasma membranes is multireceptor-linked and under antagonistic control by hormones and cytokines. Biochem J 307: 543-548, 1995.
38. 2 generation in human adipocyte plasma membranes is mediated by Galphai2. J Biol Chem 212: 10135-10143, 1997.
39. Kulas DT. Zhang WR, Goldstein BJ, Furlanetto RW, and Mooney RA. Insulin receptor signaling is augmented by antisense inhibition of the protein tyrosine phosphatase LAR. J Biol Chem 270: 2435-2438, 1995.
40. Kusari AB, Byon S, Bandyopadhyay D, Kenner KA, and Kusari J. Insulin-induced mitogen-activated protein (MAP) kinase phosphatase-1 (MKP-1) attenuates insulin-stimulated MAP kinase activity: a mechanism for the feedback inhibition of insulin signaling. Mol Endocrinol 11: 1532-1543, 1997.
41. Lambeth JD. Nox/Duox family of nicotinamide adenine dinucleotide (phosphate) oxidases. Curr Opin Hematol 9: 11-17, 2002.
42. Lassegue B and Clempus RE. Vascular NADPH oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285: R277-R297, 2003.
43. Lee SR, Kwon KS, Kim SR, and Rhee SG. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J Biol Chem 273: 15366-15372, 1998.
44. 2. J Biol Chem 277: 20336-20342, 2002.
45. 2 formation. J Biol Chem 252: 560-562, 1977.
46. Mahadev K, Wu X, Zilbering A, Zhu L, Lawrence JTR, and Goldstein BJ. Hydrogen peroxide generated during cellular insulin stimulation is integral to activation of the distal insulin signaling cascade in 3T3-L1 adipocytes. J Biol Chem 276: 48662-48669, 2001.
47. Mahadev K, Zilbering A, Zhu L, and Goldstein BJ. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1B in vivo and enhances the early insulin action cascade. J Biol Chem 276: 21938-21942, 2001.
48. 2 and plays an integral role in insulin signal transduction. Mol Cell Biol 24: 1844-1854, 2004.
49. 2. Cell Signal 16: 323-331, 2004.
50. May JM. The insulin-like effects of low molecular weight thiols: role of trace metal contamination of commercial thiols. Horm Metab Res 12: 587-590, 1980.
51. May JM and de Haen C. The insulin-like effect of hydrogen peroxide on pathways of lipid synthesis in rat adipocytes. J Biol Chem 254: 9017-9021, 1979.
52. May JM and de Haen C. Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. J Biol Chem 254: 2214-2220, 1979.
53. Meng TC, Fukada T, and Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 9: 387-399, 2002.
54. Moxham CM and Malbon CC. Insulin action impaired by deficiency of the G-protein subunit G ialpha2. Nature 379: 840-844, 1996.
55. Mukherjee SP and Lynn WS. Reduced nicotinamide adenine dinucleotide phosphate oxidase in adipocyte plasma membrane and its activation by insulin. Possible role in the hormone's effects on adenylate cyclase and the hexose monophosphate shunt. Arch Biochem Biophys 184: 69-76, 1977.
56. Mukherjee SP and Lynn WS. Role of cellular redox state and glutathione in adenylate cyclase activity in rat adipocytes. Biochim Biophys Acta 568: 224-233, 1979.
57. Mukherjee SP, Lane RH, and Lynn WS. Endogenous hydrogen peroxide and peroxidative metabolism in adipocytes in response to insulin and sulfhydryl reagents. Biochem Pharmacol 27: 2589-2594, 1978.
58. Nakashima N, Sharma PM, Imamura T, Bookstein R, and Olefsky JM. The tumor suppressor PTEN negatively regulates insulin signaling in 3T3-L1 adipocytes. J Biol Chem 275: 12889-12895, 2000.
59. Ren JM, Li PM, Zhang WR, Sweet LJ, Cline G, Shulman GI, Livingston JN, and Goldstein BJ. Transgenic mice deficient in the LAR protein-tyrosine phosphatase exhibit profound defects in glucose homeostasis. Diabetes 47: 493-497, 1998.
60. Rhee SG, Bae YS, Lee SR, and Kwon J. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE 2000: E1, 2000. www.stke.org/cgi/content/full/OC_sigtrans
61. Rhee SG, Chang TS, Bae YS, Lee SR, and Rang SW. Cellular regulation by hydrogen peroxide. J Am Soc Nephrol 14: 8211-5215, 2003.
62. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, and Barford D. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423: 769-773, 2003.
63. Saltiel AR and Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414: 799-806, 2001.
64. Schmid E, Elbenna J, Galter D, Klein G, and Droge W. Redox priming of the insulin receptor beta-chain associated with altered tyrosine kinase activity and insulin responsiveness in the absence of tyrosine autophosphorylation. FASEB J 12: 863-870, 1998.
65. Schmid E, Hotz-Wagenblatt A, Hack V, and Droge W. Phosphorylation of the insulin receptor kinase by phosphocreatine in combination with hydrogen peroxide: the structural basis of redox priming. FASEB J 13: 1491-1500, 1999.
66. 2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem J 336: 241-246, 1998.
67. Sun XJ, Rothenberg PL, Kahn CR, Backer JM, Araki E, Wilden PA, Cahill DA, Goldstein BJ, and White MF. Structure of the insulin receptor substrate IRS-I defines a unique signal transduction protein. Nature 352: 73-77, 1991.
68. Tonks NK. PTP1B: from the sidelines to the front lines! FEBS Lett 546: 140-148, 2003.
69. Tonks NK and Neel BG. Combinatorial control of the specificity of protein tyrosine phosphatases. Curr Opin Cell Biol 13: 182-195, 2001.
70. Ullrich A, Bell JR, Chen EY, Herrera R, Petruzzelli LM, Dull TJ, Gray A, Coussens L, Liao Y-C, Tsubokawa M, Mason A, Seeburg PH, Grunfeld C, Rosen OM, and Ramachandran J. Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes. Nature 313: 756-761, 1985.
71. Ushio-Fukai M, Alexander RW, Akers M, Yin QQ, Fujio Y, Walsh K, and Griendling KK. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem 274: 22699-22704, 1999.
72. van Montfort RL, Congreve M, Tisi D, Carr R, and Jhoti H. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423: 773-777, 2003.
73. White MF. IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab 283: E413-E422, 2002.
74. White MF, Shoelson SE, Keutmann H, and Kahn CR. A cascade of tyrosine autophosphorylation in the β-subunit activates the phosphotransferase of the insulin receptor. J Biol Chem 263: 2969-2980, 1988.
75. Woo HA, Chae HZ, Hwang SC, Yang KS, Kang SW, Kim K, and Rhee SG. Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300: 653-656, 2003.
76. Wu X, Hoffstedt J, Deeb W, Singh R, Sedkova N, Zilbering A, Zhu L, Park PK, Arner P, and Goldstein BJ. Depot-specific variation in protein-tyrosine phosphatase activities in human omental and subcutaneous adipose tissue: a potential contribution to differential insulin sensitivity. J Clin Endocrinol Metab 86: 5973-5980, 2001.
77. Zhang WR, Li PM, Oswald MA, and Goldstein BJ. Modulation of insulin signal transduction by eutopic overexpression of the receptor-type protein-tyrosine phosphatase LAR. Mol Endocrinol 10: 575-584, 1996.
78. Zhu L, Zilbering A, Wu X, Mahadev K, Joseph JI, Jabbour S, Deeb W, and Goldstein BJ. Use of an anaerobic environment to preserve the endogenous activity of protein-tyrosine phosphatases isolated from intact cells. FASEB J 15: 1637-1639, 2001.