Mitochondrial antioxidative capacity regulates muscle glucose uptake in the conscious mouse: Effect of exercise and diet

Journal of Applied Physiology

Volumn 113, Issue 8, 2012, Pages 1173-1183

  Kang, Li ^a,b   Lustig, Mary E ^a   Bonner, Jeffrey S ^a   Lee Young, Robert S ^a   Mayes, Wesley H ^a   James, Freyja D ^a   Lin, Chien Te ^c   Perry, Christopher G R ^c   Anderson, Ethan J ^c   Neufer, P Darrell ^c   Wasserman, David H ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Catalase; High fat diet; Hydrogen peroxide; Superoxide anion; Superoxide dismutase

Indexed keywords

3 NITROTYROSINE; 3-NITROTYROSINE; ANTIOXIDANT; CATALASE; DRUG DERIVATIVE; GLUCOSE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; NITRIC OXIDE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TYROSINE;

ACTION POTENTIAL; ANIMAL; ANIMAL EXPERIMENT; ANIMAL FOOD; ARTICLE; C57BL MOUSE; LIPID DIET; METABOLISM; MITOCHONDRION; MOUSE; PHYSIOLOGY; SKELETAL MUSCLE; TRANSGENIC MOUSE; TRANSPORT AT THE CELLULAR LEVEL;

ACTION POTENTIALS; ANIMAL FEED; ANIMALS; ANTIOXIDANTS; BIOLOGICAL TRANSPORT; CATALASE; DIET, HIGH-FAT; GLUCOSE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; MUSCLE, SKELETAL; NITRIC OXIDE; PHYSICAL CONDITIONING, ANIMAL; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; TYROSINE;

EID: 84867511291     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01344.2011     Document Type: Article

References (64)

1. Abdul-Ghani MA, DeFronzo RA. Pathogenesis of insulin resistance in skeletal muscle. J Biomed Biotechnol 2010: 476279, 2010.
2. Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, Lin CT, Price JW 3rd, Kang L, Rabinovitch PS, Szeto HH, Houmard JA, Cortright RN, Wasserman DH, Neufer PD. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119: 573-581, 2009.
3. Asha Devi S, Prathima S, Subramanyam MV. Dietary vitamin E and physical exercise: I. Altered endurance capacity and plasma lipid profile in ageing rats. Exp. Gerontol 38: 285-290, 2003.
4. Ayala JE, Bracy DP, Julien BM, Rottman JN, Fueger PT, Wasserman DH. Chronic treatment with sildenafil improves energy balance and insulin action in high fat-fed conscious mice. Diabetes 56: 1025-1033, 2007.
5. Ayala JE, Bracy DP, McGuinness OP, Wasserman DH. Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55: 390-397, 2006.
6. Berglund ED, Li CY, Poffenberger G, Ayala JE, Fueger PT, Willis SE, Jewell MM, Powers AC, Wasserman DH. Glucose metabolism in vivo in four commonly used inbred mouse strains. Diabetes 57: 1790-1799, 2008.
7. Booth FW, Laye MJ. Lack of adequate appreciation of physical exercise's complexities can pre-empt appropriate design and interpretation in scientific discovery. J Physiol 587: 5527-5539, 2009.
8. Buerk DG, Lamkin-Kennard K, Jaron D. Modeling the influence of superoxide dismutase on superoxide and nitric oxide interactions, including reversible inhibition of oxygen consumption. Free Radic Biol Med 34: 1488-1503, 2003.
9. Buettner GR, Ng CF, Wang M, Rodgers VG, Schafer FQ. A new paradigm: manganese superoxide dismutase influences the production of H2O2 in cells and thereby their biological state. Free Radic Biol Med 41: 1338-1350, 2006.
10. Davies KJ, Quintanilha AT, Brooks GA, Packer L. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107: 1198-1205, 1982.
11. de Haan JB, Cristiano F, Iannello R, Bladier C, Kelner MJ, Kola I. Elevation in the ratio of Cu/Zn-superoxide dismutase to glutathione peroxidase activity induces features of cellular senescence and this effect is mediated by hydrogen peroxide. Hum Mol Genet 5: 283-292, 1996.
12. Fueger PT, Bracy DP, Malabanan CM, Pencek RR, Granner DK, Wasserman DH. Hexokinase II overexpression improves exercise-stimulated but not insulin-stimulated muscle glucose uptake in high-fat-fed C57BL/6J mice. Diabetes 53: 306-314, 2004.
13. Fueger PT, Bracy DP, Malabanan CM, Pencek RR, Wasserman DH. Distributed control of glucose uptake by working muscles of conscious mice: roles of transport and phosphorylation. Am J Physiol Endocrinol Metab 286: E77-E84, 2004.
14. Fueger PT, Hess HS, Posey KA, Bracy DP, Pencek RR, Charron MJ, Wasserman DH. Control of exercise-stimulated muscle glucose uptake by GLUT4 is dependent on glucose phosphorylation capacity in the conscious mouse. J Biol Chem 279: 50956-50961, 2004.
15. Fueger PT, Lee-Young RS, Shearer J, Bracy DP, Heikkinen S, Laakso M, Rottman JN, Wasserman DH. Phosphorylation barriers to skeletal and cardiac muscle glucose uptakes in high-fat fed mice: studies in mice with a 50% reduction of hexokinase II. Diabetes 56: 2476-2484, 2007.
16. Fueger PT, Li CY, Ayala JE, Shearer J, Bracy DP, Charron MJ, Rottman JN, Wasserman DH. Glucose kinetics and exercise tolerance in mice lacking the GLUT4 glucose transporter. J Physiol 582: 801-812, 2007.
17. Fueger PT, Shearer J, Krueger TM, Posey KA, Bracy DP, Heikkinen S, Laakso M, Rottman JN, Wasserman DH. Hexokinase II protein content is a determinant of exercise endurance capacity in the mouse. J Physiol 566: 533-541, 2005.
18. Fujii N, Jessen N, Goodyear LJ. AMP-activated protein kinase and the regulation of glucose transport. Am J Physiol Endocrinol Metab 291: E867-E877, 2006.
19. Gardner R, Salvador A, Moradas-Ferreira P. Why does SOD overexpression sometimes enhance, sometimes decrease, hydrogen peroxide production? A minimalist explanation. Free Radic Biol Med 32: 1351-1357, 2002.
20. Gomez-Cabrera MC, Borras C, Pallardo FV, Sastre J, Ji LL, Vina J. Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J Physiol 567: 113-120, 2005.
21. Gomez-Cabrera MC, Domenech E, Romagnoli M, Arduini A, Borras C, Pallardo FV, Sastre J, Vina J. Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr 87: 142-149, 2008.
22. Halseth AE, Bracy DP, Wasserman DH. Limitations to exercise- and maximal insulin-stimulated muscle glucose uptake. J Appl Physiol 85: 2305-2313, 1998.
23. Higashida K, Kim SH, Higuchi M, Holloszy JO, Han DH. Normal adaptations to exercise despite protection against oxidative stress. Am J Physiol Endocrinol Metab 301: E779-E784, 2011.
24. Hoehn KL, Salmon AB, Hohnen-Behrens C, Turner N, Hoy AJ, Maghzal GJ, Stocker R, Van Remmen H, Kraegen EW, Cooney GJ, Richardson AR, James DE. Insulin resistance is a cellular antioxidant defense mechanism. Proc Natl Acad Sci USA 106: 17787-17792, 2009.
25. Hood DA, Irrcher I, Ljubicic V, Joseph AM. Coordination of metabolic plasticity in skeletal muscle. J Exp Biol 209: 2265-2275, 2006.
26. Jackson MJ. Control of reactive oxygen species production in contracting skeletal muscle. Antioxid Redox Signal 15: 2477-2486, 2011.
27. Jones DP. Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 295: C849-C868, 2008.
28. Kang L, Ayala JE, Lee-Young RS, Zhang Z, James FD, Neufer PD, Pozzi A, Zutter MM, Wasserman DH. Diet-induced muscle insulin resistance is associated with extracellular matrix remodeling and interaction with integrin alpha2beta1 in mice. Diabetes 60: 416-426, 2011.
29. Katz A, Sahlin K, Broberg S. Regulation of glucose utilization in human skeletal muscle during moderate dynamic exercise. Am J Physiol Endocrinol Metab 260: E411-E415, 1991.
30. Lee-Young RS, Ayala JE, Fueger PT, Mayes WH, Kang L, Wasserman DH. Obesity impairs skeletal muscle AMPK signaling during exercise: role of AMPKalpha2 in the regulation of exercise capacity in vivo. Int J Obes (Lond) 35: 982-989, 2011.
31. Lee-Young RS, Griffee SR, Lynes SE, Bracy DP, Ayala JE, McGuinness OP, Wasserman DH. Skeletal muscle AMP-activated protein kinase is essential for the metabolic response to exercise in vivo. J Biol Chem 284: 23925-23934, 2009.
32. Liochev SI, Fridovich I. The effects of superoxide dismutase on H2O2 formation. Free Radic Biol Med 42: 1465-1469, 2007.
33. Lowry OH, Passonneau JV. A flexible system of enzymatic analysis. Starch 25: 322, 1972.
34. Merry TL, Dywer RM, Bradley EA, Rattigan S, McConell GK. Local hindlimb antioxidant infusion does not affect muscle glucose uptake during in situ contractions in rat. J Appl Physiol 108: 1275-1283, 2010.
35. Merry TL, McConell GK. Do reactive oxygen species regulate skeletal muscle glucose uptake during contraction? Exerc Sport Sci Rev 40: 102-105, 2012.
36. Merry TL, Steinberg GR, Lynch GS, McConell GK. Skeletal muscle glucose uptake during contraction is regulated by nitric oxide and ROS independently of AMPK. Am J Physiol Endocrinol Metab 298: E577-E585, 2010.
37. Merry TL, Wadley GD, Stathis CG, Garnham AP, Rattigan S, Hargreaves M, McConell GK. N-acetylcysteine infusion does not affect glucose disposal during prolonged moderate-intensity exercise in humans. J Physiol 588: 1623-1634, 2010.
38. Michaelson LP, Shi G, Ward CW, Rodney GG. Mitochondrial redox potential during contraction in single intact muscle fibers. Muscle Nerve 42: 522-529, 2010.
39. Motoori S, Majima HJ, Ebara M, Kato H, Hirai F, Kakinuma S, Yamaguchi C, Ozawa T, Nagano T, Tsujii H, Saisho H. Overexpression of mitochondrial manganese superoxide dismutase protects against radiation-induced cell death in the human hepatocellular carcinoma cell line HLE. Cancer Res 61: 5382-5388, 2001.
40. Murrant CL, Reid MB. Detection of reactive oxygen and reactive nitrogen species in skeletal muscle. Microsc Res Tech 55: 236-248, 2001.
41. Raineri I, Carlson EJ, Gacayan R, Carra S, Oberley TD, Huang TT, Epstein CJ. Strain-dependent high-level expression of a transgene for manganese superoxide dismutase is associated with growth retardation and decreased fertility. Free Radic Biol Med 31: 1018-1030, 2001.
42. Ranganathan AC, Nelson KK, Rodriguez AM, Kim KH, Tower GB, Rutter JL, Brinckerhoff CE, Huang TT, Epstein CJ, Jeffrey JJ, Melendez JA. Manganese superoxide dismutase signals matrix metalloproteinase expression via H2O2-dependent ERK1/2 activation. J Biol Chem 276: 14264-14270, 2001.
43. Richter EA, Jensen P, Kiens B, Kristiansen S. Sarcolemmal glucose transport and GLUT-4 translocation during exercise are diminished by endurance training. Am J Physiol Endocrinol Metab 274: E89-E95, 1998.
44. Richter EA, Ruderman NB. AMPK and the biochemistry of exercise: implications for human health and disease. Biochem J 418: 261-275, 2009.
45. Rigoulet M, Yoboue ED, Devin A. Mitochondrial ROS generation and its regulation: mechanisms involved in H(2)O(2) signaling. Antioxid Redox Signal 14: 459-468, 2011.
46. Ristow M, Zarse K, Oberbach A, Kloting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR, Bluher M. Antioxidants prevent healthpromoting effects of physical exercise in humans. Proc Natl Acad Sci USA 106: 8665-8670, 2009.
47. Rodriguez AM, Carrico PM, Mazurkiewicz JE, Melendez JA. Mitochondrial or cytosolic catalase reverses the MnSOD-dependent inhibition of proliferation by enhancing respiratory chain activity, net ATP production, and decreasing the steady state levels of H(2)O(2). Free Radic Biol Med 29: 801-813, 2000.
48. 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.
49. Schmidt KN, Amstad P, Cerutti P, Baeuerle PA. The roles of hydrogen peroxide and superoxide as messengers in the activation of transcription factor NF-kappa B. Chem Biol 2: 13-22, 1995.
50. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabinovitch PS. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308: 1909-1911, 2005.
51. Silva JP, Shabalina IG, Dufour E, Petrovic N, Backlund EC, Hultenby K, Wibom R, Nedergaard J, Cannon B, Larsson NG. SOD2 overexpression: enhanced mitochondrial tolerance but absence of effect on UCP activity. EMBO J 24: 4061-4070, 2005.
52. Sreekumar R, Unnikrishnan J, Fu A, Nygren J, Short KR, Schimke J, Barazzoni R, Nair KS. Impact of high-fat diet and antioxidant supplement on mitochondrial functions and gene transcripts in rat muscle. Am J Physiol Endocrinol Metab 282: E1055-E1061, 2002.
53. Sriwijitkamol A, Coletta DK, Wajcberg E, Balbontin GB, Reyna SM, Barrientes J, Eagan PA, Jenkinson CP, Cersosimo E, DeFronzo RA, Sakamoto K, Musi N. Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study. Diabetes 56: 836-848, 2007.
54. Sriwijitkamol A, Ivy JL, Christ-Roberts C, DeFronzo RA, Mandarino LJ, Musi N. LKB1-AMPK signaling in muscle from obese insulinresistant Zucker rats and effects of training. Am J Physiol Endocrinol Metab 290: E925-E932, 2006.
55. Teixeira HD, Schumacher RI, Meneghini R. Lower intracellular hydrogen peroxide levels in cells overexpressing CuZn-superoxide dismutase. Proc Natl Acad Sci USA 95: 7872-7875, 1998.
56. Tiidus PM, Houston ME. Antioxidant and oxidative enzyme adaptations to vitamin E deprivation and training. Med Sci Sports Exerc 26: 354-359, 1994.
57. 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.
58. Veal EA, Day AM, Morgan BA. Hydrogen peroxide sensing and signaling. Mol Cell 26: 1-14, 2007.
59. Wadley GD, Lee-Young RS, Canny BJ, Wasuntarawat C, Chen ZP, Hargreaves M, Kemp BE, McConell GK. Effect of exercise intensity and hypoxia on skeletal muscle AMPK signaling and substrate metabolism in humans. Am J Physiol Endocrinol Metab 290: E694-E702, 2006.
60. Wasserman DH. Four grams of glucose. Am J Physiol Endocrinol Metab 296: E11-E21, 2009.
61. Wasserman DH, Kang L, Ayala JE, Fueger PT, Lee-Young RS. The physiological regulation of glucose flux into muscle in vivo. J Exp Biol 214: 254-262, 2011.
62. Wenk J, Brenneisen P, Wlaschek M, Poswig A, Briviba K, Oberley TD, Scharffetter-Kochanek K. Stable overexpression of manganese superoxide dismutase in mitochondria identifies hydrogen peroxide as a major oxidant in the AP-1-mediated induction of matrix-degrading metalloprotease-1. J Biol Chem 274: 25869-25876, 1999.
63. Winder WW, Taylor EB, Thomson DM. Role of AMP-activated protein kinase in the molecular adaptation to endurance exercise. Med Sci Sports Exerc 38: 1945-1949, 2006.
64. Yfanti C, Akerstrom T, Nielsen S, Nielsen AR, Mounier R, Mortensen OH, Lykkesfeldt J, Rose AJ, Fischer CP, Pedersen BK. Antioxidant supplementation does not alter endurance training adaptation. Med Sci Sports Exerc 42: 1388-1395, 2010.