Mice Deficient in the Respiratory Chain Gene Cox6a2 Are Protected against High-Fat Diet-Induced Obesity and Insulin Resistance

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Quintens, Roel ^a,g   Singh, Sarvjeet ^b   Lemaire, Katleen ^a   de Bock, Katrien ^a,c   Granvik, Mikaela ^a   Schraenen, Anica ^a   Vroegrijk, Irene Olga Cornelia Maria ^d   Costa, Veronica ^e   van Noten, Pieter ^a   Lambrechts, Dennis ^a   Lehnert, Stefan ^a   van Lommel, Leentje ^a   Thorrez, Lieven ^a   de Faudeur, Geoffroy ^a   Romijn, Johannes Anthonius ^d   Shelton, John Michael ^b   Scorrano, Luca ^e   Lijnen, Henri Roger ^f   Voshol, Peter Jacobus ^d   Carmeliet, Peter ^a,c   Mammen, Pradeep Puthenveetil Abraham ^b   Schuit, Frans ^a   more..

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF GENEVA   (Switzerland)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

COX6A1 PROTEIN; CYTOCHROME C OXIDASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COX6A2 GENE; ENERGY EXPENDITURE; ENERGY METABOLISM; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; HEART; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MITOCHONDRIAL GENE; MOUSE; MUSCLE FATIGUE; NONHUMAN; OBESITY; SKELETAL MUSCLE; THERMOGENESIS; WEIGHT REDUCTION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BODY WEIGHT; DIET, HIGH-FAT; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; ENERGY METABOLISM; ENZYME ACTIVATION; GLUCOSE TOLERANCE TEST; INSULIN; INSULIN RESISTANCE; ION CHANNELS; MICE; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL SIZE; MODELS, BIOLOGICAL; MUSCLE FATIGUE; MUSCLE PROTEINS; MUSCLE, SKELETAL; OBESITY; REACTIVE OXYGEN SPECIES; STARVATION; THERMOGENESIS; THINNESS;

EID: 84874511732     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056719     Document Type: Article

References (79)

1. Crawford D, Jeffery RW, French SA, (2000) Can anyone successfully control their weight? Findings of a three year community-based study of men and women. Int J Obes Relat Metab Disord 24: 1107-1110.
2. Choi CS, Fillmore JJ, Kim JK, Liu Z-X, Kim S, et al. (2007) Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J Clin Invest 117: 1995-2003.
3. Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, et al. (2000) Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406: 415-418.
4. Horvath TL, Diano S, Miyamoto S, Barry S, Gatti S, et al. (2003) Uncoupling proteins-2 and 3 influence obesity and inflammation in transgenic mice. Int J Obes Relat Metab Disord 27: 433-442.
5. Li B, Nolte LA, Ju JS, Han DH, Coleman T, et al. (2000) Skeletal muscle respiratory uncoupling prevents diet-induced obesity and insulin resistance in mice. Nat Med 6: 1115-1120.
6. Lee FY, Li Y, Zhu H, Yang S, Lin HZ, et al. (1999) Tumor necrosis factor increases mitochondrial oxidant production and induces expression of uncoupling protein-2 in the regenerating mice [correction of rat] liver. Hepatology 29: 677-687.
7. Jäger S, Handschin C, St-Pierre J, Spiegelman BM, (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci USA 104: 12017-12022.
8. Klaus S, Keipert S, Rossmeisl M, Kopecky J, (2011) Augmenting energy expenditure by mitochondrial uncoupling: a role of AMP-activated protein kinase. Genes Nutr Available at: http://www.ncbi.nlm.nih.gov/pubmed/22139637.
9. Mootha VK, Lindgren CM, Eriksson K-F, Subramanian A, Sihag S, et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273.
10. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, et al. (2003) Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100: 8466-8471.
11. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, et al. (2003) Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-1142.
12. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, et al. (2005) A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54: 1926-1933.
13. Houstis N, Rosen ED, Lander ES, (2006) Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440: 944-948.
14. Kim J-A, Wei Y, Sowers JR, (2008) Role of mitochondrial dysfunction in insulin resistance. Circ Res 102: 401-414.
15. Lowell BB, Shulman GI, (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307: 384-387.
16. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin M-A, et al. (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118: 789-800.
17. Hoeks J, Van Herpen NA, Mensink M, Moonen-Kornips E, Van Beurden D, et al. (2010) Prolonged Fasting Identifies Skeletal Muscle Mitochondrial Dysfunction as Consequence Rather Than Cause of Human Insulin Resistance. Diabetes 59: 2117-2125.
18. Sadler NC, Angel TE, Lewis MP, Pederson LM, Chauvigné-Hines LM, et al. (2012) Activity-based protein profiling reveals mitochondrial oxidative enzyme impairment and restoration in diet-induced obese mice. PLoS ONE 7: e47996.
19. Pospisilik JA, Knauf C, Joza N, Benit P, Orthofer M, et al. (2007) Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131: 476-491.
20. Wredenberg A, Freyer C, Sandström ME, Katz A, Wibom R, et al. (2006) Respiratory chain dysfunction in skeletal muscle does not cause insulin resistance. Biochem Biophys Res Commun 350: 202-207.
21. Kadenbach B, Barth J, Akgün R, Freund R, Linder D, et al. (1995) Regulation of mitochondrial energy generation in health and disease. Biochim Biophys Acta 1271: 103-109.
22. Taanman JW, Hall RE, Tang C, Marusich MF, Kennaway NG, et al. (1993) Tissue distribution of cytochrome c oxidase isoforms in mammals. Characterization with monoclonal and polyclonal antibodies. Biochim Biophys Acta 1225: 95-100.
23. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, et al. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272: 1136-1144.
24. Anthony G, Reimann A, Kadenbach B, (1993) Tissue-specific regulation of bovine heart cytochrome-c oxidase activity by ADP via interaction with subunit VIa. Proc Natl Acad Sci USA 90: 1652-1656.
25. Frank V, Kadenbach B, (1996) Regulation of the H+/e- stoichiometry of cytochrome c oxidase from bovine heart by intramitochondrial ATP/ADP ratios. FEBS Lett 382: 121-124.
26. Rohdich F, Kadenbach B, (1993) Tissue-specific regulation of cytochrome c oxidase efficiency by nucleotides. Biochemistry 32: 8499-8503.
27. Korshunov SS, Skulachev VP, Starkov AA, (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416: 15-18.
28. Papa S, Guerrieri F, Capitanio N, (1997) A possible role of slips in cytochrome C oxidase in the antioxygen defense system of the cell. Biosci Rep 17: 23-31.
29. Fornuskova D, Stiburek L, Wenchich L, Vinsova K, Hansikova H, et al. (2010) Novel insights into the assembly and function of human nuclear-encoded cytochrome c oxidase subunits 4, 5a, 6a, 7a and 7b. Biochem J 428: 363-374.
30. Radford NB, Wan B, Richman A, Szczepaniak LS, Li J-L, et al. (2002) Cardiac dysfunction in mice lacking cytochrome-c oxidase subunit VIaH. Am J Physiol Heart Circ Physiol 282: H726-733.
31. Anthony G, Stroh A, Lottspeich F, Kadenbach B, (1990) Different isozymes of cytochrome c oxidase are expressed in bovine smooth muscle and skeletal or heart muscle. FEBS Lett 277: 97-100.
32. Kadenbach B, Stroh A, Becker A, Eckerskorn C, Lottspeich F, (1990) Tissue- and species-specific expression of cytochrome c oxidase isozymes in vertebrates. Biochim Biophys Acta 1015: 368-372.
33. Zanetti M, D'Uscio LV, Peterson TE, Katusic ZS, O'Brien T, (2005) Analysis of superoxide anion production in tissue. Methods Mol Med 108: 65-72.
34. Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, et al. (2011) Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest 121: 96-105.
35. Nakai Y, Hashida H, Kadota K, Minami M, Shimizu K, et al. (2008) Up-regulation of genes related to the ubiquitin-proteasome system in the brown adipose tissue of 24-h-fasted rats. Biosci Biotechnol Biochem 72: 139-148.
36. Wamil M, Battle JH, Turban S, Kipari T, Seguret D, et al. (2011) Novel fat depot-specific mechanisms underlie resistance to visceral obesity and inflammation in 11 β-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 60: 1158-1167.
37. Sokolović M, Wehkamp D, Sokolović A, Vermeulen J, Gilhuijs-Pederson LA, et al. (2007) Fasting induces a biphasic adaptive metabolic response in murine small intestine. BMC Genomics 8: 361.
38. Surwit RS, Wang S, Petro AE, Sanchis D, Raimbault S, et al. (1998) Diet-induced changes in uncoupling proteins in obesity-prone and obesity-resistant strains of mice. Proc Natl Acad Sci USA 95: 4061-4065.
39. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, et al. (2012) A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481: 463-468.
40. Chemello F, Bean C, Cancellara P, Laveder P, Reggiani C, et al. (2011) Microgenomic analysis in skeletal muscle: expression signatures of individual fast and slow myofibers. PLoS ONE 6: e16807.
41. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
42. Lin J, Wu H, Tarr PT, Zhang C-Y, Wu Z, et al. (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418: 797-801.
43. Jheng H-F, Tsai P-J, Guo S-M, Kuo L-H, Chang C-S, et al. (2012) Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol Cell Biol 32: 309-319.
44. Bal NC, Maurya SK, Sopariwala DH, Sahoo SK, Gupta SC, et al. (2012) Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nat Med.
45. Boily G, Seifert EL, Bevilacqua L, He XH, Sabourin G, et al. (2008) SirT1 regulates energy metabolism and response to caloric restriction in mice. PLoS ONE 3: e1759.
46. Chida D, Hashimoto O, Kuwahara M, Sagara H, Osaka T, et al. (2008) Increased fat:carbohydrate oxidation ratio in Il1ra (-/-) mice on a high-fat diet is associated with increased sympathetic tone. Diabetologia 51: 1698-1706.
47. Feige JN, Lagouge M, Canto C, Strehle A, Houten SM, et al. (2008) Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab 8: 347-358.
48. Handschin C, Chin S, Li P, Liu F, Maratos-Flier E, et al. (2007) Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals. J Biol Chem 282: 30014-30021.
49. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, et al. (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127: 1109-1122.
50. Polak P, Cybulski N, Feige JN, Auwerx J, Rüegg MA, et al. (2008) Adipose-specific knockout of raptor results in lean mice with enhanced mitochondrial respiration. Cell Metab 8: 399-410.
51. Neschen S, Katterle Y, Richter J, Augustin R, Scherneck S, et al. (2008) Uncoupling protein 1 expression in murine skeletal muscle increases AMPK activation, glucose turnover, and insulin sensitivity in vivo. Physiol. Genomics 33: 333-340.
52. Kopecky J, Clarke G, Enerbäck S, Spiegelman B, Kozak LP, (1995) Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest 96: 2914-2923.
53. Wu J, Boström P, Sparks LM, Ye L, Choi JH, et al. (2012) Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150: 366-376.
54. Azzu V, Brand MD, (2010) The on-off switches of the mitochondrial uncoupling proteins. Trends Biochem Sci 35: 298-307.
55. Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, et al. (2000) Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26: 435-439.
56. Gong DW, Monemdjou S, Gavrilova O, Leon LR, Marcus-Samuels B, et al. (2000) Lack of obesity and normal response to fasting and thyroid hormone in mice lacking uncoupling protein-3. J Biol Chem 275: 16251-16257.
57. Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, et al. (2000) Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 275: 16258-16266.
58. Brand MD, Esteves TC, (2005) Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab 2: 85-93.
59. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, et al. (2002) Superoxide activates mitochondrial uncoupling proteins. Nature 415: 96-99.
60. Vernochet C, Mourier A, Bezy O, Macotela Y, Boucher J, et al. (2012) Adipose-Specific Deletion of TFAM Increases Mitochondrial Oxidation and Protects Mice against Obesity and Insulin Resistance. Cell Metab 16: 765-776.
61. Gomez-Cabrera M-C, Domenech E, Viña J, (2008) Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med 44: 126-131.
62. Ristow M, Zarse K, Oberbach A, Klöting N, Birringer M, et al. (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci USA 106: 8665-8670.
63. Ristow M, Zarse K, (2010) How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 45: 410-418.
64. Loh K, Deng H, Fukushima A, Cai X, Boivin B, et al. (2009) Reactive oxygen species enhance insulin sensitivity. Cell Metab 10: 260-272.
65. Rufini A, Niklison-Chirou MV, Inoue S, Tomasini R, Harris IS, et al. (2012) TAp73 depletion accelerates aging through metabolic dysregulation. Genes Dev 26: 2009-2014.
66. Irrcher I, Ljubicic V, Hood DA, (2009) Interactions between ROS and AMP kinase activity in the regulation of PGC-1alpha transcription in skeletal muscle cells. Am J Physiol, Cell Physiol 296: C116-123.
67. Fritah A, Steel JH, Parker N, Nikolopoulou E, Christian M, et al. (2012) Absence of RIP140 Reveals a Pathway Regulating glut4-Dependent Glucose Uptake in Oxidative Skeletal Muscle through UCP1-Mediated Activation of AMPK. PLoS ONE 7: e32520.
68. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, et al. (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127: 397-408.
69. Diaz F, Thomas CK, Garcia S, Hernandez D, Moraes CT, (2005) Mice lacking COX10 in skeletal muscle recapitulate the phenotype of progressive mitochondrial myopathies associated with cytochrome c oxidase deficiency. Hum Mol Genet 14: 2737-2748.
70. Chen W, Zhang X, Birsoy K, Roeder RG, (2010) A muscle-specific knockout implicates nuclear receptor coactivator MED1 in the regulation of glucose and energy metabolism. Proc Natl Acad Sci USA 107: 10196-10201.
71. Handschin C, Choi CS, Chin S, Kim S, Kawamori D, et al. (2007) Abnormal glucose homeostasis in skeletal muscle-specific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J Clin Invest 117: 3463-3474.
72. Pearen MA, Eriksson NA, Fitzsimmons RL, Goode JM, Martel N, et al. (2012) The Nuclear Receptor, Nor-1, Markedly Increases Type II Oxidative Muscle Fibers and Resistance to Fatigue. Mol Endocrinol 26: 372-384.
73. Wang Y-X, Zhang C-L, Yu RT, Cho HK, Nelson MC, et al. (2004) Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2: e294.
74. Hoeks J, Schrauwen P, (2012) Muscle mitochondria and insulin resistance: a human perspective. Trends Endocrinol Metab 23: 444-450.
75. Lijnen HR, Christiaens V, Scroyen I, Voros G, Tjwa M, et al. (2006) Impaired adipose tissue development in mice with inactivation of placental growth factor function. Diabetes 55: 2698-2704.
76. Netea MG, Joosten LAB, Lewis E, Jensen DR, Voshol PJ, et al. (2006) Deficiency of interleukin-18 in mice leads to hyperphagia, obesity and insulin resistance. Nat Med 12: 650-656.
77. Lee C-H, Olson P, Hevener A, Mehl I, Chong L-W, et al. (2006) PPARdelta regulates glucose metabolism and insulin sensitivity. Proc Natl Acad Sci USA 103: 3444-3449.
78. Ivarsson R, Quintens R, Dejonghe S, Tsukamoto K, In't Veld P, et al. (2005) Redox control of exocytosis: regulatory role of NADPH, thioredoxin, and glutaredoxin. Diabetes 54: 2132-2142.
79. Ogilvie RW, Feeback DL, (1990) A metachromatic dye-ATPase method for the simultaneous identification of skeletal muscle fiber types I, IIA, IIB and IIC. Stain Technol 65: 231-241.