Long-chain fatty acid combustion rate is associated with unique metabolite profiles in skeletal muscle mitochondria

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Seifert, Erin L ^a   Fiehn, Oliver ^b   Bezaire, Véronic ^a   Bickel, David R ^a   Wohlgemuth, Gert ^b   Adams, Sean H ^b   Harper, Mary Ellen ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; FATTY ACID; KETONE; OXYGEN;

ANIMAL; ARTICLE; C57BL MOUSE; FEMALE; GAS CHROMATOGRAPHY; INSULIN RESISTANCE; MASS SPECTROMETRY; METABOLISM; METABOLOMICS; METHODOLOGY; MITOCHONDRION; MOUSE; MUSCLE MITOCHONDRION; SKELETAL MUSCLE;

3-HYDROXYBUTYRIC ACID; ANIMALS; CHROMATOGRAPHY, GAS; FATTY ACIDS; FEMALE; INSULIN RESISTANCE; KETONES; MASS SPECTROMETRY; METABOLOMICS; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OXYGEN;

EID: 78650735706     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009834     Document Type: Article

References (64)

1. Randle PJ (1998) Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab Rev 14: 263-283.
2. Savage DB, Petersen KF, Shulman GI (2007) Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 87: 507-520.
3. Muoio DM, Newgard CB (2006) Obesity-related derangements in metabolic regulation. Annu Rev Biochem 75: 367-401.
4. Yu C, Chen Y, Cline GW, Zhang D, Zong H, et al. (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem 277: 50230-50236.
5. Choi CS, Fillmore JJ, Kim JK, Liu ZX, 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.
6. Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, et al. (2007) Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab 5: 167-179.
7. Liu L, Zhang Y, Chen N, Shi X, Tsang B, et al. (2007) Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J Clin Invest 117: 1679-1689.
8. Schenk S, Horowitz JF (2007) Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest 117: 1690-1698.
9. Kelley DE, Simoneau JA (1994) Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest 94: 2349-2356.
10. Kelley DE, Goodpaster B, Wing RR, Simoneau JA (1999) Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 277: E1130-1141.
11. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, et al. (2005) Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54: 8-14.
12. Mootha VK, Lindgren CM, Eriksson KF, 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.
13. 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 U S A 100: 8466-8471.
14. Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, et al. (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56: 1592-1599.
15. Phielix E, Schrauwen-Hinderling VB, Mensink M, Lenaers E, Meex R, et al. (2008) Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes 57: 2943-2949.
16. Morino K, Petersen KF, Dufour S, Befroy D, Frattini J, et al. (2005) Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest 115: 3587-3593.
17. Ukropcova B, Sereda O, de Jonge L, Bogacka I, Nguyen T, et al. (2007) Family history of diabetes links impaired substrate switching and reduced mitochondrial content in skeletal muscle. Diabetes 56: 720-727.
18. Bruce CR, Hoy AJ, Turner N, Watt MJ, Allen TL, et al. (2008) Overexpression of carnitine palmitoyltransferase-1 in skeletal muscle is sufficient to enhance fatty acid oxidation and improve high fat diet-induced insulin resistance. Diabetes.
19. Guillaume-Gentil C, Assimacopoulos-Jeannet F, Jeanrenaud B (1993) Involvement of non-esterified fatty acid oxidation in glucocorticoid-induced peripheral insulin resistance in vivo in rats. Diabetologia 36: 899-906.
20. Finck BN, Bernal-Mizrachi C, Han DH, Coleman T, Sambandam N, et al. (2005) A potential link between muscle peroxisome proliferator-activated receptor-alpha signaling and obesity-related diabetes. Cell Metab 1: 133-144.
21. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, et al. (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.
22. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, et al. (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7: 45-56.
23. Hancock CR, Han DH, Chen M, Terada S, Yasuda T, et al. (2008) High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci U S A 105: 7815-7820.
24. Adams SH, Hoppel CL, Lok KH, Zhao L, Wong SW, et al. (2009) Plasma acylcarnitine profiles suggest incomplete long-chain fatty acid beta-oxidation and altered tricarboxylic acid cycle activity in type 2 diabetic African-American women. J Nutr 139: 1073-1081.
25. Brass EP, Hoppel CL (1980) Effect of carnitine on mitochondrial oxidation of palmitoylearnitine. Biochem J 188: 451-458.
26. Lysiak W, Lilly K, DiLisa F, Toth PP, Bieber LL (1988) Quantitation of the effect of L-carnitine on the levels of acid-soluble short-chain acyl-CoA and CoASH in rat heart and liver mitochondria. J Biol Chem 263: 1151-1156.
27. Makowski L, Noland RC, Koves TR, Xing W, Ilkayeva OR, et al. (2008) Metabolic profiling of PPAR{alpha}-/-mice reveals defects in carnitine and amino acid homeostasis that are partially reversed by oral carnitine supplementation. FASEB J.
28. Chappell JB, Perry SV (1954) Biochemical and osmotic properties of skeletal muscle mitochondria. Nature 173: 1094-1095.
29. Seifert EL, Bezaire V, Estey C, Harper ME (2008) Essential role for uncoupling protein-3 in mitochondrial adaptation to fasting but not in fatty acid oxidation or fatty acid anion export. J Biol Chem 283: 25124-25131.
30. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME (2005) Longterm caloric restriction increases UCP3 content but decreases proton leak and reactive oxygen species production in rat skeletal muscle mitochondria. Am J Physiol Endocrinol Metab 289: E429-438.
31. Fiehn O, Wohlgemuth G, Scholz M, Kind T, Lee do Y, et al. (2008) Quality control for plant metabolomics: reporting MSI-compliant studies. Plant J 53: 691-704.
32. Fiehn O, Wohlgemuth G, Scholz M (2005) Setup and annotation of metabolomic experiments by integrating biological and mass spectrometric metadata. Proc Lect Notes Bioinformatics 3615: 224-239.
33. Bland JM, Altman DG (1996) Transforming data. BMJ 312: 770.
34. Efron B, Tibshirani R, Storey JD, Tusher V (2001) Empirical Bayes analysis of a microarray experiment. J Am Statist Ass 96: 1151-1160.
35. Storey JD (2002) A direct approach to false discovery rates. Journal of the Royal Statistical Society Series B: Statistical Methodology 64: 479-498.
36. Bickel DR (2004) Error-rate and decision-theoretic methods of multiple testing: which genes have high objective probabilities of differential expression? Stat Appl Genet Mol Biol 3: Article8.
37. Saha AK, Vavvas D, Kurowski TG, Apazidis A, Witters LA, et al. (1997) Malonyl-CoA regulation in skeletal muscle: its link to cell citrate and the glucosefatty acid cycle. Am J Physiol 272: E641-648.
38. Saha AK, Laybutt DR, Dean D, Vavvas D, Sebokova E, et al. (1999) Cytosolic citrate and malonyl-CoA regulation in rat muscle in vivo. Am J Physiol 276: E1030-1037.
39. Khairallah M, Labarthe F, Bouchard B, Danialou G, Petrof BJ, et al. (2004) Profiling substrate fluxes in the isolated working mouse heart using 13C-labeled substrates: focusing on the origin and fate of pyruvate and citrate carbons. Am J Physiol Heart Circ Physiol 286: H1461-1470.
40. Poirier M, Vincent G, Reszko AE, Bouchard B, Kelleher JK, et al. (2002) Probing the link between citrate and malonyl-CoA in perfused rat hearts. Am J Physiol Heart Circ Physiol 283: H1379-1386.
41. Vincent G, Bouchard B, Khairallah M, Des Rosiers C (2004) Differential modulation of citrate synthesis and release by fatty acids in perfused working rat hearts. Am J Physiol Heart Circ Physiol 286: H257-266.
42. Maizels EZ, Ruderman NB, Goodman MN, Lau D (1977) Effect of acetoacetate on glucose metabolism in the soleus and extensor digitorum longus muscles of the rat. Biochem J 162: 557-568.
43. Bangsbo J, Gibala MJ, Howarth KR, Krustrup P (2006) Tricarboxylic acid cycle intermediates accumulate at the onset of intense exercise in man but are not essential for the increase in muscle oxygen uptake. Pflugers Arch 452: 737-743.
44. Brunengraber H, Roe CR (2006) Anaplerotic molecules: current and future. J Inherit Metab Dis 29: 327-331.
45. Messer JI, Jackman MR, Willis WT (2004) Pyruvate and citric acid cycle carbon requirements in isolated skeletal muscle mitochondria. Am J Physiol Cell Physiol 286: C565-572.
46. Gibala MJ, Young ME, Taegtmeyer H (2000) Anaplerosis of the citric acid cycle: role in energy metabolism of heart and skeletal muscle. Acta Physiol Scand 168: 657-665.
47. Mourtzakis M, Graham TE, Gonzalez-Alonso J, Saltin B (2008) Glutamate availability is important in intramuscular amino acid metabolism and TCA cycle intermediates but does not affect peak oxidative metabolism. J Appl Physiol 105: 547-554.
48. Roe CR, Sweetman L, Roe DS, David F, Brunengraber H (2002) Treatment of cardiomyopathy and rhabdomyolysis in long-chain fat oxidation disorders using an anaplerotic odd-chain triglyceride. J Clin Invest 110: 259-269.
49. Palmieri F (1994) Mitochondrial carrier proteins. FEBS Lett 346: 48-54.
50. Hegardt FG (1999) Mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase: a control enzyme in ketogenesis. Biochem J 338 (Pt3): 569-582.
51. Mascaro C, Buesa C, Ortiz JA, Haro D, Hegardt FG (1995) Molecular cloning and tissue expression of human mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase. Arch Biochem Biophys 317: 385-390.
52. Nosadini R, Avogaro A, Trevisan R, Duner E, Marescotti C, et al. (1985) Acetoacetate and 3-hydroxybutyrate kinetics in obese and insulin-dependent diabetic humans. Am J Physiol 248: R611-620.
53. Fink G, Desrochers S, Des Rosiers C, Garneau M, David F, et al. (1988) Pseudoketogenesis in the perfused rat heart. J Biol Chem 263: 18036-18042.
54. Pelletier A, Tardif A, Gingras MH, Chiasson JL, Coderre L (2007) Chronic exposure to ketone bodies impairs glucose uptake in adult cardiomyocytes in response to insulin but not vanadate: the role of PI3-K. Mol Cell Biochem 296: 97-108.
55. Tardif A, Julien N, Pelletier A, Thibault G, Srivastava AK, et al. (2001) Chronic exposure to beta-hydroxybutyrate impairs insulin action in primary cultures of adult cardiomyocytes. Am J Physiol Endocrinol Metab 281: E1205-1212.
56. Bulteau AL, Ikeda-Saito M, Szweda LI (2003) Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry 42: 14846-14855.
57. Tretter L, Adam-Vizi V (2000) Inhibition of Krebs cycle enzymes by hydrogen peroxide: A key role of [alpha]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J Neurosci 20: 8972-8979.
58. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277: 44784-44790.
59. Csordas G, Renken C, Varnai P, Walter L, Weaver D, et al. (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174: 915-921.
60. Shkryl VM, Shirokova N (2006) Transfer and tunneling of Ca2+ from sarcoplasmic reticulum to mitochondria in skeletal muscle. J Biol Chem 281: 1547-1554.
61. Wilson JE (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206: 2049-2057.
62. Anflous-Pharayra K, Cai ZJ, Craigen WJ (2007) VDAC1 serves as a mitochondrial binding site for hexokinase in oxidative muscles. Biochim Biophys Acta 1767: 136-142.
63. Dubouchaud H, Butterfield GE, Wolfel EE, Bergman BC, Brooks GA (2000) Endurance training, expression, and physiology of LDH, MCT1, and MCT4 in human skeletal muscle. Am J Physiol Endocrinol Metab 278: E571-579.
64. Mailloux RJ, Harper ME (2010) Glucose availability regulates the enzymatic source of NADPH in skeletal muscle mitochondria; a novel role for glucose-6-phosphate dehydrogenase. FASEB J. In press.