Opening of the mitochondrial permeability transition pore links mitochondrial dysfunction to insulin resistance in skeletal muscle

Molecular Metabolism

Volumn 3, Issue 2, 2014, Pages 124-134

  Taddeo, E P ^a   Laker, R C ^a   Breen, D S ^a   Akhtar, Y N ^a   Kenwood, B M ^a   Liao, J A ^a   Zhang, M ^a   Fazakerley, D J ^c   Tomsig, J L ^a   Harris, T E ^a   Keller, S R ^a   Chow, J D ^a   Lynch, K R ^a,b   Chokki, M ^f   Molkentin, J D ^e   Turner, N ^d   James, D E ^c,d   Yan, Z ^a   Hoehn, K L ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e UNIVERSITY OF CINCINNATI   (United States)

^f TEIJIN PHARMA LIMITED   (Japan)

Author keywords

Cyclophilin D; Glucose; Insulin resistance; Mitochondrial dysfunction; Mitochondrial permeability transition pore; Skeletal muscle

Indexed keywords

ANTIMYCIN A1; CALCIUM; CERAMIDE; CYCLOPHILIN D; CYCLOSPORIN A; GLUCOSE; GLUCOSE TRANSPORTER 4; GLYCEROLIPID; INSULIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PALMITIC ACID; PHOSPHOLIPID; SPHINGOLIPID;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOENERGY; CELL MEMBRANE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GLUCOSE INTOLERANCE; GLUCOSE TRANSPORT; IN VITRO STUDY; IN VIVO STUDY; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIPID STORAGE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WESTERN BLOTTING;

MUS; PYRONIA TITHONUS;

EID: 84895822623     PISSN: 22128778     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmet.2013.11.003     Document Type: Article

References (60)

1. Holland W.L., Knotts T.A., Chavez J.A., Wang L.P., Hoehn K.L., Summers S.A. Lipid mediators of insulin resistance. Nutrition Reviews 2007, 65:S39-S46.
2. Hoehn K.L., Salmon A.B., Hohnen-Behrens C., Turner N., Hoy A.J., Maghzal G.J., et al. Insulin resistance is a cellular antioxidant defense mechanism. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:17787-17792.
3. Murrow B.A., Hoehn K.L. Mitochondrial regulation of insulin action. International Journal of Biochemistry and Cell Biology 2010, 42:1936-1939.
4. Savage D.B., Petersen K.F., Shulman G.I. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiological Reviews 2007, 87:507-520.
5. Houstis N., Rosen E.D., Lander E.S. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006, 440:944-948.
6. Anderson E.J., Lustig M.E., Boyle K.E., Woodlief T.L., Kane D.A., Lin C.T., et al. Mitochondrial h2o2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. Journal of Clinical Investigation 2009, 119:573-581.
7. Holland W.L., Brozinick J.T., Wang L.P., Hawkins E.D., Sargent K.M., Liu Y., et al. Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metabolism 2007, 5:167-179.
8. Itani S.I., Ruderman N.B., Schmieder F., Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase c, and ikappab-alpha. Diabetes 2002, 51:2005-2011.
9. Storlien L.H., James D.E., Burleigh K.M., Chisholm D.J., Kraegen E.W. Fat feeding causes widespread in vivo insulin resistance, decreased energy expenditure, and obesity in rats. American Journal of Physiology 1986, 251:E576-E583.
10. Bonnard C., Durand A., Peyrol S., Chanseaume E., Chauvin M.A., Morio B., et al. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. Journal of Clinical Investigation 2008, 118:789-800.
11. Petersen K.F., Dufour S., Befroy D., Garcia R., Shulman G.I. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. New England Journal of Medicine 2004, 350:664-671.
12. Turner N., Heilbronn L.K. Is mitochondrial dysfunction a cause of insulin resistance?. Trends in Endocrinology & Metabolism 2008, 19:324-330.
13. Muoio D.M., Neufer P.D. Lipid-induced mitochondrial stress and insulin action in muscle. Cell Metabolism 2012, 15:595-605.
14. Kim J.A., Wei Y., Sowers J.R. Role of mitochondrial dysfunction in insulin resistance. Circulation Research 2008, 102:401-414.
15. Giorgi C., Agnoletto C., Bononi A., Bonora M., De Marchi E., Marchi S., et al. Mitochondrial calcium homeostasis as potential target for mitochondrial medicine. Mitochondrion 2012, 12:77-85.
16. Halestrap A.P., Woodfield K.Y., Connern C.P. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. Journal of Biological Chemistry 1997, 272:3346-3354.
17. McStay G.P., Clarke S.J., Halestrap A.P. Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore. Biochemical Journal 2002, 367:541-548.
18. Zorov D.B., Juhaszova M., Yaniv Y., Nuss H.B., Wang S., Sollott S.J. Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovascular Research 2009, 83:213-225.
19. Elrod J.W., Molkentin J.D. Physiologic functions of cyclophilin d and the mitochondrial permeability transition pore. Circulation Journal 2013, 77:1111-1122.
20. Zhivotovsky B., Galluzzi L., Kepp O., Kroemer G. Adenine nucleotide translocase: a component of the phylogenetically conserved cell death machinery. Cell Death and Differentiation 2009, 16:1419-1425.
21. Halestrap A.P. What is the mitochondrial permeability transition pore?. Journal of Molecular and Cellular Cardiology 2009, 46:821-831.
22. Hoehn K.L., Hohnen-Behrens C., Cederberg A., Wu L.E., Turner N., Yuasa T., et al. Irs1-independent defects define major nodes of insulin resistance. Cell Metabolism 2008, 7:421-433.
23. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., et al. Loss of cyclophilin d reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434:658-662.
24. Hoehn K.L., Turner N., Swarbrick M.M., Wilks D., Preston E., Phua Y., et al. Acute or chronic upregulation of mitochondrial fatty acid oxidation has no net effect on whole-body energy expenditure or adiposity. Cell Metabolism 2010, 11:70-76.
25. Patel S.A., Hoehn K.L., Lawrence R.T., Sawbridge L., Talbot N.A., Tomsig J.L., et al. Overexpression of the adiponectin receptor adipor1 in rat skeletal muscle amplifies local insulin sensitivity. Endocrinology 2012, 153:5231-5246.
26. Murphy R.C., James P.F., McAnoy A.M., Krank J., Duchoslav E., Barkley R.M. Detection of the abundance of diacylglycerol and triacylglycerol molecular species in cells using neutral loss mass spectrometry. Analytical Biochemistry 2007, 366:59-70.
27. Kim H., Ahn E., Moon M.H. Profiling of human urinary phospholipids by nanoflow liquid chromatography/tandem mass spectrometry. Analyst 2008, 133:1656-1663.
28. Pulfer M., Murphy R.C. Electrospray mass spectrometry of phospholipids. Mass Spectrometry Reviews 2003, 22:332-364.
29. Stuart C.A., McCurry M.P., Marino A., South M.A., Howell M.E., Layne A.S., et al. Slow-twitch fiber proportion in skeletal muscle correlates with insulin responsiveness. Journal of Clinical Endocrinology and Metabolism 2013, 98:2027-2036.
30. Halestrap A.P., Davidson A.M. Inhibition of Ca-2+-induced large-amplitude swelling of liver and heart-mitochondria by cyclosporine is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine-nucleotide translocase. Biochemical Journal 1990, 268:153-160.
31. Macho A., Blanco-Molina M., Spagliardi P., Appendino G., Bremner P., Heinrich M., et al. Calcium ionophoretic and apoptotic effects of ferutinin in the human jurkat t-cell line. Biochemical Pharmacology 2004, 68:875-883.
32. Abramov A.Y., Duchen M.R. Actions of ionomycin, 4-bra23187 and a novel electrogenic Ca2+ ionophore on mitochondria in intact cells. Cell Calcium 2003, 33:101-112.
33. Garcia-Ruiz C., Colell A., Mari M., Morales A., Fernandez-Checa J.C. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. Journal of Biological Chemistry 1997, 272:11369-11377.
34. Chiu T.T., Sun Y., Koshkina A., Klip A. Rac-1 superactivation triggers insulin-independent glucose transporter 4 (glut4) translocation that bypasses signaling defects exerted by c-jun n-terminal kinase (jnk)- and ceramide-induced insulin resistance. Journal of Biological Chemistry 2013, 288:17520-17531.
35. Vyssokikh M.Y., Katz A., Rueck A., Wuensch C., Dorner A., Zorov D.B., et al. Adenine nucleotide translocator isoforms 1 and 2 are differently distributed in the mitochondrial inner membrane and have distinct affinities to cyclophilin d. Biochemical Journal 2001, 358:349-358.
36. Arora K.K., Filburn C.R., Pedersen P.L. Structure/function relationships in hexokinase. Site-directed mutational analyses and characterization of overexpressed fragments implicate different functions for the n- and c-terminal halves of the enzyme. Journal of Biological Chemistry 1993, 268:18259-18266.
37. Wu R., Wyatt E., Chawla K., Tran M., Ghanefar M., Laakso M., et al. Hexokinase ii knockdown results in exaggerated cardiac hypertrophy via increased ros production. EMBO Molecular Medicine 2012, 4:633-646.
38. 2+ ions. Acta Medica (Hradec Kralove) 2009, 52:69-72.
39. Tsuchiya Y., Hatakeyama H., Emoto N., Wagatsuma F., Matsushita S., Kanzaki M. Palmitate-induced down-regulation of sortilin and impaired glut4 trafficking in c2c12 myotubes. Journal of Biological Chemistry 2010, 285:34371-34381.
40. Kim Y.B., Nikoulina S.E., Ciaraldi T.P., Henry R.R., Kahn B.B. Normal insulin-dependent activation of akt/protein kinase b, with diminished activation of phosphoinositide 3-kinase, in muscle in type 2 diabetes. Journal of Clinical Investigation 1999, 104:733-741.
41. Frojdo S., Vidal H., Pirola L. Alterations of insulin signaling in type 2 diabetes: a review of the current evidence from humans. Biochimica et Biophysica Acta 2009, 1792:83-92.
42. Patergnani S., Suski J.M., Agnoletto C., Bononi A., Bonora M., De Marchi E., et al. Calcium signaling around mitochondria associated membranes (mams). Cell Communication and Signaling 2011, 9:19.
43. Teodoro J.S., Duarte F.V., Gomes A.P., Varela A.T., Peixoto F.M., Rolo A.P., et al. Berberine reverts hepatic mitochondrial dysfunction in high-fat fed rats: a possible role for sirt3 activation. Mitochondrion 2013, 13:637-646.
44. Zemel M.B. Nutritional and endocrine modulation of intracellular calcium: implications in obesity, insulin resistance and hypertension. Molecular and Cellular Biochemistry 1998, 188:129-136.
45. Han D.H., Hancock C.R., Jung S.R., Higashida K., Kim S.H., Holloszy J.O. Deficiency of the mitochondrial electron transport chain in muscle does not cause insulin resistance. PLoS One 2011, 6:e19739.
46. Fernandez-Real J.M., Lopez-Bermejo A., Ricart W. Cross-talk between iron metabolism and diabetes. Diabetes 2002, 51:2348-2354.
47. Frizzell N., Lima M., Baynes J.W. Succination of proteins in diabetes. Free Radical Research 2011, 45:101-109.
48. Koves T.R., Ussher J.R., Noland R.C., Slentz D., Mosedale M., Ilkayeva O., et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metabolism 2008, 7:45-56.
49. Schooneman M.G., Vaz F.M., Houten S.M., Soeters M.R. Acylcarnitines: reflecting or inflicting insulin resistance?. Diabetes 2013, 62:1-8.
50. Galloway C.A., Yoon Y.S. What comes first, misshape or dysfunction? The view from metabolic excess. Journal of General Physiology 2012, 139:455-463.
51. Zhang X., Wang C., Song G., Gan K., Kong D., Nie Q., et al. Mitofusion-2-mediated alleviation of insulin resistance in rats through reduction in lipid intermediate accumulation in skeletal muscle. Journal of Biomedical Science 2013, 20:45.
52. Hansson M.J., Morota S., Chen L., Matsuyama N., Suzuki Y., Nakajima S., et al. Cyclophilin d-sensitive mitochondrial permeability transition in adult human brain and liver mitochondria. Journal of Neurotrauma 2011, 28:143-153.
53. Franko A., von Kleist-Retzow J.C., Bose M., Sanchez-Lasheras C., Brodesser S., Krut O., et al. Complete failure of insulin-transmitted signaling, but not obesity-induced insulin resistance, impairs respiratory chain function in muscle. Journal of Molecular Medicine (Berlin) 2012, 90:1145-1160.
54. Unger R.H. Lipid overload and overflow: metabolic trauma and the metabolic syndrome. Trends in Endocrinology and Metabolism 2003, 14:398-403.
55. Nunn A.V., Bell J.D., Guy G.W. Lifestyle-induced metabolic inflexibility and accelerated ageing syndrome: insulin resistance, friend or foe?. Nutrition and Metabolism (London) 2009, 6:16.
56. Harmancey R., Lam T.N., Lubrano G.M., Guthrie P.H., Vela D., Taegtmeyer H. Insulin resistance improves metabolic and contractile efficiency in stressed rat heart. FASEB Journal 2012, 26:3118-3126.
57. Barzilai N., Ferrucci L. Insulin resistance and aging: a cause or a protective response?. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 2012, 67:1329-1331.
58. Guigas B., Detaille D., Chauvin C., Batandier C., De Oliveira F., Fontaine E., et al. Metformin inhibits mitochondrial permeability transition and cell death: a pharmacological in vitro study. Biochemical Journal 2004, 382:877-884.
59. Suwa M., Egashira T., Nakano H., Sasaki H., Kumagai S. Metformin increases the pgc-1alpha protein and oxidative enzyme activities possibly via ampk phosphorylation in skeletal muscle in vivo. Journal of Applied Physiology (1985) 2006, 101:1685-1692.
60. Rossetti L., DeFronzo R.A., Gherzi R., Stein P., Andraghetti G., Falzetti G., et al. Effect of metformin treatment on insulin action in diabetic rats: in vivo and in vitro correlations. Metabolism 1990, 39:425-435.