Complete failure of insulin-transmitted signaling, but not obesity-induced insulin resistance, impairs respiratory chain function in muscle (original) (raw)

References

1. Finck BN, Bernal-Mizrachi C, Han DH, Coleman T, Sambandam N, LaRiviere LL, Holloszy JO, Semenkovich CF, Kelly DP (2005) A potential link between muscle peroxisome proliferator-activated receptor-alpha signaling and obesity-related diabetes. Cell Metab 1:133–144
   Article PubMed CAS Google Scholar
2. Lowell BB, Shulman GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307:384–387
   Article PubMed CAS Google Scholar
3. Holland WL, Summers SA (2008) Sphingolipids, insulin resistance, and metabolic disease: new insights from in vivo manipulation of sphingolipid metabolism. Endocr Rev 29:381–402
   Article PubMed CAS Google Scholar
4. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664–671
   Article PubMed CAS Google Scholar
5. Petersen KF, Dufour S, Shulman GI (2005) Decreased insulin-stimulated ATP synthesis and phosphate transport in muscle of insulin-resistant offspring of type 2 diabetic parents. PLoS Med 2:e233
   Article PubMed Google Scholar
6. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone 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
   Article PubMed CAS Google Scholar
7. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E et al (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267–273
   Article PubMed CAS Google Scholar
8. Szendroedi J, Roden M (2009) Ectopic lipids and organ function. Curr Opin Lipidol 20:50–56
   Article PubMed CAS Google Scholar
9. Schrauwen P, Schrauwen-Hinderling V, Hoeks J, Hesselink MK (2009) Mitochondrial dysfunction and lipotoxicity. Biochim Biophys Acta 1801:266–271
   PubMed Google Scholar
10. Wredenberg A, Freyer C, Sandstrom ME, Katz A, Wibom R, Westerblad H, Larsson NG (2006) Respiratory chain dysfunction in skeletal muscle does not cause insulin resistance. Biochem Biophys Res Commun 350:202–207
    Article PubMed CAS Google Scholar
11. Pospisilik JA, Knauf C, Joza N, Benit P, Orthofer M, Cani PD, Ebersberger I, Nakashima T, Sarao R, Neely G et al (2007) Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131:476–491
    Article PubMed CAS Google Scholar
12. Han DH, Hancock CR, Jung SR, Higashida K, Kim SH, Holloszy JO (2011) Deficiency of the mitochondrial electron transport chain in muscle does not cause insulin resistance. PLoS One 6:e19739
    Article PubMed CAS Google Scholar
13. Schiff M, Loublier S, Coulibaly A, Benit P, de Ogier B, Rustin P (2009) Mitochondria and diabetes mellitus: untangling a conflictive relationship? J Inherit Metab Dis 32:684–698
    Article PubMed CAS Google Scholar
14. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, Accili D, Goodyear LJ, Kahn CR (1998) A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 2:559–569
    Article PubMed CAS Google Scholar
15. Wade JM, Juneja P, MacKay AW, Graham J, Havel PJ, Tecott LH, Goulding EH (2008) Synergistic impairment of glucose homeostasis in ob/ob mice lacking functional serotonin 2C receptors. Endocrinology 149:955–961
    Article PubMed CAS Google Scholar
16. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3:965–976
    Article PubMed CAS Google Scholar
17. Franko A, Mayer S, Thiel G, Mercy L, Arnould T, Hornig-Do HT, Wiesner RJ, Goffart S (2008) CREB-1alpha is recruited to and mediates upregulation of the cytochrome c promoter during enhanced mitochondrial biogenesis accompanying skeletal muscle differentiation. Mol Cell Biol 28:2446–2459
    Article PubMed CAS Google Scholar
18. Kleist-Retzow JC, Hornig-Do HT, Schauen M, Eckertz S, Dinh TA, Stassen F, Lottmann N, Bust M, Galunska B, Wielckens K et al (2007) Impaired mitochondrial Ca2+ homeostasis in respiratory chain-deficient cells but efficient compensation of energetic disadvantage by enhanced anaerobic glycolysis due to low ATP steady state levels. Exp Cell Res 313:3076–3089
    Article Google Scholar
19. Kerner J, Parland WK, Minkler PE, Hoppel CL (2008) Rat liver mitochondrial carnitine palmitoyltransferase-I, hepatic carnitine, and malonyl-CoA: effect of starvation. Arch Physiol Biochem 114:161–170
    Article PubMed CAS Google Scholar
20. Rustin P, Chretien D, Bourgeron T, Gerard B, Rotig A, Saudubray JM, Munnich A (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 228:35–51
    Article PubMed CAS Google Scholar
21. Hornig-Do HT, von Kleist-Retzow JC, Lanz K, Wickenhauser C, Kudin AP, Kunz WS, Wiesner RJ, Schauen M (2007) Human epidermal keratinocytes accumulate superoxide due to low activity of Mn-SOD, leading to mitochondrial functional impairment. J Invest Dermatol 127:1084–1093
    Article PubMed CAS Google Scholar
22. Huang TT, Naeemuddin M, Elchuri S, Yamaguchi M, Kozy HM, Carlson EJ, Epstein CJ (2006) Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Hum Mol Genet 15:1187–1194
    Article PubMed CAS Google Scholar
23. Belgardt BF, Mauer J, Wunderlich FT, Ernst MB, Pal M, Spohn G, Bronneke HS, Brodesser S, Hampel B, Schauss AC et al (2010) Hypothalamic and pituitary c-Jun N-terminal kinase 1 signaling coordinately regulates glucose metabolism. Proc Natl Acad Sci USA 107:6028–6033
    Article PubMed CAS Google Scholar
24. Shaner RL, Allegood JC, Park H, Wang E, Kelly S, Haynes CA, Sullards MC, Merrill AH Jr (2009) Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers. J Lipid Res 50:1692–1707
    Article PubMed CAS Google Scholar
25. O’Brien PC (1984) Procedures for comparing samples with multiple endpoints. Biometrics 40:1079–1087
    Article PubMed Google Scholar
26. Lindstrom P (2007) The physiology of obese-hyperglycemic mice [ob/ob mice]. Sci World J 7:666–685
    Article Google Scholar
27. Freeman HC, Hugill A, Dear NT, Ashcroft FM, Cox RD (2006) Deletion of nicotinamide nucleotide transhydrogenase: a new quantitative trait locus accounting for glucose intolerance in C57BL/6J mice. Diabetes 55:2153–2156
    Article PubMed CAS Google Scholar
28. Turpin SM, Ryall JG, Southgate R, Darby I, Hevener AL, Febbraio MA, Kemp BE, Lynch GS, Watt MJ (2009) Examination of ‘lipotoxicity’ in skeletal muscle of high-fat fed and ob/ob mice. J Physiol 587:1593–1605
    Article PubMed CAS Google Scholar
29. Schagger H, Pfeiffer K (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19:1777–1783
    Article PubMed CAS Google Scholar
30. Acin-Perez R, Fernandez-Silva P, Peleato ML, Perez-Martos A, Enriquez JA (2008) Respiratory active mitochondrial supercomplexes. Mol Cell 32:529–539
    Article PubMed CAS Google Scholar
31. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, Vidal H, Rieusset J (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118:789–800
    PubMed CAS Google Scholar
32. Cheng Z, Guo S, Copps K, Dong X, Kollipara R, Rodgers JT, Depinho RA, Puigserver P, White MF (2009) Foxo1 integrates insulin signaling with mitochondrial function in the liver. Nat Med 15:1307–1311
    Article PubMed CAS Google Scholar
33. Canto C, Auwerx J (2009) PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr Opin Lipidol 20:98–105
    Article PubMed CAS Google Scholar
34. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132:27–42
    Article PubMed CAS Google Scholar
35. Kim I, Rodriguez-Enriquez S, Lemasters JJ (2007) Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462:245–253
    Article PubMed CAS Google Scholar
36. Tanida I, Ueno T, Kominami E (2004) LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 36:2503–2518
    Article PubMed CAS Google Scholar
37. Aerts JM, Ottenhoff R, Powlson AS, Grefhorst A, van Eijk M, Dubbelhuis PF, Aten J, Kuipers F, Serlie MJ, Wennekes T et al (2007) Pharmacological inhibition of glucosylceramide synthase enhances insulin sensitivity. Diabetes 56:1341–1349
    Article PubMed CAS Google Scholar
38. Ardail D, Popa I, Alcantara K, Pons A, Zanetta JP, Louisot P, Thomas L, Portoukalian J (2001) Occurrence of ceramides and neutral glycolipids with unusual long-chain base composition in purified rat liver mitochondria. FEBS Lett 488:160–164
    Article PubMed CAS Google Scholar
39. Strasberg P (1986) Cerebrosides and psychosine disrupt mitochondrial functions. Biochem Cell Biol 64:485–489
    Article PubMed CAS Google Scholar
40. Ljubicic V, Hood DA (2008) Kinase-specific responsiveness to incremental contractile activity in skeletal muscle with low and high mitochondrial content. Am J Physiol Endocrinol Metab 295:E195–E204
    Article PubMed CAS Google Scholar
41. Nair KS, Bigelow ML, Asmann YW, Chow LS, Coenen-Schimke JM, Klaus KA, Guo ZK, Sreekumar R, Irving BA (2008) Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance. Diabetes 57:1166–1175
    Article PubMed CAS Google Scholar
42. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsoe R, Dela F (2007) Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50:790–796
    Article PubMed CAS Google Scholar
43. Rabol R, Hojberg PM, Almdal T, Boushel R, Haugaard SB, Madsbad S, Dela F (2009) Effect of hyperglycemia on mitochondrial respiration in type 2 diabetes. J Clin Endocrinol Metab 94:1372–1378
    Article PubMed Google Scholar
44. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS, Cooney GJ (2007) Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56:2085–2092
    Article PubMed CAS Google Scholar
45. Hancock CR, Han DH, Chen M, Terada S, Yasuda T, Wright DC, Holloszy JO (2008) High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci USA 105:7815–7820
    Article PubMed CAS Google Scholar
46. Bonen A, Holloway GP, Tandon NN, Han XX, McFarlan JT, Glatz JF, Luiken JJ (2009) Cardiac and skeletal muscle fatty acid transport and transporters, triacylglycerol and fatty acid oxidation in lean and Zucker diabetic fatty (ZDF) rats. Am J Physiol 297:R1202–R1212
    Article CAS Google Scholar
47. Ogata T, Yamasaki Y (1997) Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers. Anat Rec 248:214–223
    Article PubMed CAS Google Scholar
48. Gollnick PD, Sjodin B, Karlsson J, Jansson E, Saltin B (1974) Human soleus muscle: a comparison of fiber composition and enzyme activities with other leg muscles. Pflugers Arch 348:247–255
    Article PubMed CAS Google Scholar
49. Yechoor VK, Patti ME, Ueki K, Laustsen PG, Saccone R, Rauniyar R, Kahn CR (2004) Distinct pathways of insulin-regulated versus diabetes-regulated gene expression: an in vivo analysis in MIRKO mice. Proc Natl Acad Sci USA 101:16525–16530
    Article PubMed CAS Google Scholar
50. Stump CS, Short KR, Bigelow ML, Schimke JM, Nair KS (2003) Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc Natl Acad Sci USA 100:7996–8001
    Article PubMed CAS Google Scholar
51. Karakelides H, Asmann YW, Bigelow ML, Short KR, Dhatariya K, Coenen-Schimke J, Kahl J, Mukhopadhyay D, Nair KS (2007) Effect of insulin deprivation on muscle mitochondrial ATP production and gene transcript levels in type 1 diabetic subjects. Diabetes 56:2683–2689
    Article PubMed CAS Google Scholar
52. Sleigh A, Raymond-Barker P, Thackray K, Porter D, Hatunic M, Vottero A, Burren C, Mitchell C, McIntyre M, Brage S et al (2011) Mitochondrial dysfunction in patients with primary congenital insulin resistance. J Clin Invest 121:2457–2461
    Article PubMed CAS Google Scholar

Download references