Oxidative stress stimulates skeletal muscle glucose uptake through a phosphatidylinositol 3-kinase-dependent pathway

American Journal of Physiology - Endocrinology and Metabolism

Volumn 294, Issue 5, 2008, Pages

  Higaki, Yasuki ^a   Mikami, Toshio ^b   Fujii, Nobuharu ^c   Hirshman, Michael F ^c   Koyama, Katsuhiro ^d   Seino, Tetsuya ^e   Tanaka, Keitaro ^a   Goodyear, Laurie J ^c  

^a SAGA UNIVERSITY   (Japan)

^b NIPPON MEDICAL SCHOOL   (Japan)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d UNIVERSITY OF YAMANASHI   (Japan)

^e KISARAZU NATIONAL COLLEGE OF TECHNOLOGY   (Japan)

Author keywords

Adenosine monophosphate activated protein kinase; Akt phosphorylation; Hydrogen peroxide

Indexed keywords

DEOXYGLUCOSE; HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; XANTHINE OXIDASE; ANDROSTANE DERIVATIVE; ANTIMETABOLITE; CATALASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENZYME INHIBITOR; GLUCOSE; HYPOXANTHINE; OXIDIZING AGENT; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXTENSOR DIGITORUM LONGUS MUSCLE; GLUCOSE TRANSPORT; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TRANSPORT KINETICS; ACTIVE TRANSPORT; ANIMAL; DOSE RESPONSE; DRUG EFFECT; ENZYMOLOGY; IN VITRO STUDY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; ANTIMETABOLITES; BIOLOGICAL TRANSPORT, ACTIVE; CATALASE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DEOXYGLUCOSE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GLUCOSE; HYDROGEN PEROXIDE; HYPOXANTHINE; MALE; MUSCLE, SKELETAL; OXIDANTS; OXIDATIVE STRESS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; XANTHINE OXIDASE;

EID: 45549104269     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00150.2007     Document Type: Article

References (57)

1. Barnes BR, Ryder JW, Steiler TL, Fryer LG, Carling D, Zierath JR. Isoform-specific regulation of 5′ AMP-activated protein kinase in skeletal muscle from obese Zucker (fa/fa) rats in response to contraction. Diabetes 51: 2703-2708, 2002.
2. Barrett WC, DeGnore JP, Keng YF, Zhang ZY, Yim MB, Chock PB. Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B. J Biol Chem 274: 34543-34546, 1999.
3. Berti L, Gammeltoft S. Leptin stimulates glucose uptake in C2C12 muscle cells by activation of ERK2. Mol Cell Endocrinol 157: 121-130, 1999.
4. Blair AS, Hajduch E, Litherland GJ, Hundal HS. Regulation of glucose transport and glycogen synthesis in L6 muscle cells during oxidative stress. Evidence for cross-talk between the insulin and SAPK2/p38 mitogen-activated protein kinase signaling pathways. J Biol Chem 274: 36293-36299, 1999.
5. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, Accili D, Goodyear LJ, Kahn CR. A Muscle-specific insulin receptor knockout challenges the current concepts of glucose disposal and NIDDM pathogenesis. Mol Cell 2: 559-569, 1998.
6. Cartee GD, Douen AG, Ramlal T, Klip A, Holloszy JO. Stimulation of glucose transport in skeletal muscle by hypoxia. J Appl Physiol 70: 1593-1600, 1991.
7. Cartee GD, Holloszy JO. Exercise increases susceptibility of muscle glucose transport to activation by various stimuli. Am J Physiol Endocrinol Metab 258: E390-E393, 1990.
8. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605, 1979.
9. 2. Biochem Biophys Res Commun 287: 92-97, 2001.
10. Connett RJ, Sahlin K. Control of glycolysis and glycogen metabolism. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, part III, chapt. 19, p. 870-911.
11. Cross MJ, Stewart A, Hodgkin MN, Kerr DJ, Wakelam MJ. Wortmannin and its structural analogue demethoxyviridin inhibit stimulated phospholipase A2 activity in Swiss 3T3 cells. Wortmannin is not a specific inhibitor of phosphatidylinositol 3-kinase. J Biol Chem 270: 25352-25355, 1995.
12. Czech MP, Lawrence JC Jr, Lynn WS. Evidence for the involvement of sulfhydryl oxidation in the regulation of fat cell hexose transport by insulin. Proc Natl Acad Sci USA 71: 4173-4177, 1974.
13. Davies SP, Carling D, Hardie DG. Tissue distribution of the AMP-activated protein kinase, and lack of activation by cyclic-AMP-dependent protein kinase, studied using a specific and sensitive peptide assay. Eur J Biochem 186: 123-128, 1989.
14. Etgen GJ Jr, Fryburg DA, Gibbs EM. Nitric oxide stimulates skeletal muscle glucose transport through a calcium/contraction- and phosphatidylinositol-3-kinase-independent pathway. Diabetes 46: 1915-1919, 1997.
15. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 52: 1-8, 2003.
16. Fiorentini D, Hakim G, Bonsi L, Bagnara GP, Maraldi T, Landi L. Acute regulation of glucose transport in a human megakaryocytic cell line: difference between growth factors and H(2)O(2). Free Radic Biol Med 31: 923-931, 2001.
17. Ford ES, Mokdad AH, Giles WH, Brown DW. The metabolic syndrome and antioxidant concentrations: findings from the Third National Health and Nutrition Examination Survey. Diabetes 52: 2346-2352, 2003.
18. Forsayeth J, Gould MK. Effects of hyperosmolarity on basal and insulin-stimulated muscle sugar transport. Am J Physiol Endocrinol Metab 240: E263-E267, 1981.
19. Goodyear LJ, Kahn BB. Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49: 235-61: 235-261, 1998.
20. Hadari YR, Tzahar E, Nadiv O, Rothenberg P, Roberts CT Jr, LeRoith D, Yarden Y, Zick Y. Insulin and insulinomimetic agents induce activation of phosphatidylinositol 3′-kinase upon its association with pp185 (IRS-1) in intact rat livers. J Biol Chem 267: 17483-17486, 1992.
21. Hansen LL, Ikeda Y, Olsen GS, Busch AK, Mosthaf L. Insulin signaling is inhibited by micromolar concentrations of H(2)O(2). Evidence for a role of H(2)O(2) in tumor necrosis factor alpha-mediated insulin resistance. J Biol Chem 274: 25078-25084, 1999.
22. Hayashi T, Hirshman MF, Fujii N, Habinowski SA, Witters LA, Goodyear LJ. Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 49: 527-531, 2000.
23. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, Goodyear LJ. Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47: 1369-1373, 1998.
24. Hellsten Y, Frandsen U, Orthenblad N, Sjodin B, Richter EA. Xanthine oxidase in human skeletal muscle following eccentric exercise: a role in inflammation. J Physiol 498: 239-248, 1997.
25. Higaki Y, Hirshman MF, Fujii N, Goodyear LJ. Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle. Diabetes 50: 241-247, 2001.
26. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440: 944-948, 2006.
27. JeBailey L, Wanono O, Niu W, Roessler J, Rudich A, Klip A. Ceramide- and oxidant-induced insulin resistance involve loss of insulin-dependent Rac-activation and actin remodeling in muscle cells. Diabetes 56: 394-403, 2007.
28. Jorgensen SB, Viollet B, Andreelli F, Frosig C, Birk JB, Schjerling P, Vaulont S, Richter EA, Wojtaszewski JF. Knockout of the alpha2 but not alpha1 5′-AMP-activated protein kinase isoform abolishes 5-amino-imidazole-4-carboxamide-1-beta-4-ribofuranosidebut not contraction-induced glucose uptake in skeletal muscle. J Biol Chem 279: 1070-1079, 2004.
29. Kadota S, Fantus IG, Deragon G, Guyda HJ, Hersh B, Posner BI. Peroxide(s) of vanadium: a novel and potent insulin-mimetic agent which activates the insulin receptor kinase. Biochem Biophys Res Commun 147: 259-266, 1987.
30. Kishi K, Muromoto N, Nakaya Y, Miyata I, Hagi A, Hayashi H, Ebina Y. Bradykinin directly triggers GLUT4 translocation via an insulin-independent pathway. Diabetes 47: 550-558, 1998.
31. Kozlovsky N, Rudich A, Potashnik R, Bashan N. Reactive oxygen species activate glucose transport in L6 myotubes. Free Radic Biol Med 23: 859-869, 1997.
32. Kozlovsky N, Rudich A, Potashnik R, Ebina Y, Murakami T, Bashan N. Transcriptional activation of the Glut1 gene in response to oxidative stress in L6 myotubes. J Biol Chem 272: 33367-33372, 1997.
33. Lee AD, Hansen PA, Holloszy JO. Wortmannin inhibits insulin-stimulated but not contraction-stimulated glucose transport activity in skeletal muscle. FEBS Lett 361: 51-54, 1995.
34. Leon H, Atkinson LL, Sawicka J, Strynadka K, Lopaschuk GD, Schulz R. Pyruvate prevents cardiac dysfunction and AMP-activated protein kinase activation by hydrogen peroxide in isolated rat hearts. Can J Physiol Pharmacol 82: 409-416, 2004.
35. Ludvigsen C, Jarett L. Similarities between insulin, hydrogen peroxide, concanavalin A, and anti-insulin receptor antibody stimulated glucose transport: increase in the number of transport sites. Metabolism 31: 284-287, 1982.
36. Lund S, Holman GD, Schmitz O, Pedersen O. Contraction stimulates translocation of glucose transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin. Proc Natl Acad Sci USA 92: 5817-5821, 1995.
37. Mahadev K, Motoshima H, Wu X, Ruddy JM, Arnold RS, Cheng G, Lambeth JD, Goldstein BJ. The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol Cell Biol 24: 1844-1854, 2004.
38. Mahadev K, Wu X, Zilbering A, Zhu L, Lawrence JT, 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.
39. Mahadev K, Zilbering A, Zhu L, 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.
40. McClung JP, Roneker CA, Mu W, Lisk DJ, Langlais P, Liu F, Lei XG. Development of insulin resistance and obesity in mice overexpressing cellular glutathione peroxidase. Proc Natl Acad Sci USA 101: 8852-8857, 2004.
41. McCord JM, Fridovich I. The reduction of cytochrome c by milk xanthine oxidase. J Biol Chem 243: 5753-5760, 1968.
42. Merrill GF, Kurth EJ, Hardie DG, Winder WW. AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol Endocrinol Metab 273: E1107-E1112, 1997.
43. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7: 1085-1094, 2001.
44. Musi N, Goodyear LJ. AMP-activated protein kinase and muscle glucose uptake. Acta Physiol Scand 178: 337-345, 2003.
45. Musi N, Hirshman MF, Nygren J, Svanfeldt M, Bavenholm P, Rooyackers O, Zhou G, Williamson JM, Ljunqvist O, Efendic S, Moller DE, Thorell A, Goodyear LJ. Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes. Diabetes 51: 2074-2081, 2002.
46. Ponticos M, Lu QL, Morgan JE, Hardie DG, Partridge TA, Carling D. Dual regulation of the AMP-activated protein kinase provides a novel mechanism for the control of creatine kinase in skeletal muscle. EMBO J 17: 1688-1699, 1998.
47. Reid MB. Nitric oxide, reactive oxygen species, and skeletal muscle contraction. Med Sci Sports Exerc 33: 371-376, 2001.
48. Rudich A, Tirosh A, Potashnik R, Hemi R, Kanety H, Bashan N. Prolonged oxidative stress impairs insulin-induced GLUT4 translocation in 3T3-L1 adipocytes. Diabetes 47: 1562-1569, 1998.
49. Sakamoto K, Arnolds DE, Fujii N, Kramer HF, Hirshman MF, Goodyear LJ. Role of Akt2 in contraction-stimulated cell signaling and glucose uptake in skeletal muscle. Am J Physiol Endocrinol Metab 291: E1031-E1037, 2006.
50. Sandstrom ME, Zhang SJ, Bruton J, Silva JP, Reid MB, Westerblad H, Katz A. Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J Physiol 575: 251-262, 2006.
51. Seino T, Higaki Y, Koyama K, Ogasawara M. Continuous production of Hx in slow-twitch muscles contributes to exercise-induced prolonged hyperuricemia. Purine Pyrimidine Metab 22: 115-122, 1998.
52. Sen CK. Antioxidant and redox regulation of cellular signaling: introduction. Med Sci Sports Exerc 33: 368-370, 2001.
53. Toyoda T, Hayashi T, Miyamoto L, Yonemitsu S, Nakano M, Tanaka S, Ebihara K, Masuzaki H, Hosoda K, Inoue G, Otaka A, Sato K, Fushiki T, Nakao K. Possible involvement of the alpha1 isoform of 5′ AMP-activated protein kinase in oxidative stress-stimulated glucose transport in skeletal muscle. Am J Physiol Endocrinol Metab 287: E166-E173, 2004.
54. Vincent AM, Russell JW, Low P, Feldman EL. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev 25: 612-628, 2004.
55. Wojtaszewski JF, Higaki Y, Hirshman MF, Michael MD, Dufresne SD, Kahn CR, Goodyear LJ. Exercise modulates postreceptor insulin signaling and glucose transport in muscle-specific insulin receptor knockout mice. J Clin Invest 104: 1257-1264, 1999.
56. Yeh JI, Gulve EA, Rameh L, Birnbaum MJ. The effects of wortmannin on rat skeletal muscle. Dissociation of signaling pathways for insulin- and contraction-activated hexose transport. J Biol Chem 270: 2107-2111, 1995.
57. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108: 1167-1174, 2001.