Comparison of in vivo postexercise phosphocreatine recovery and resting ATP synthesis flux for the assessment of skeletal muscle mitochondrial function

American Journal of Physiology - Cell Physiology

Volumn 299, Issue 5, 2010, Pages

  Van Den Broek, N M A ^a   Ciapaite, J ^a,b   Nicolay, K ^a   Prompers, J J ^a  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b Netherlands Consortium for Systems Biology   (Netherlands)

Author keywords

31P magnetic resonance spectroscopy; Complex I inhibition; Diphenyleneiodonium; High resolution respirometry; Saturation transfer

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE PHOSPHATE; DIPHENYLIODONIUM SALT; MALIC ACID; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME INHIBITION; EXERCISE RECOVERY; MALE; MUSCLE MITOCHONDRION; NONHUMAN; OXYGEN CONSUMPTION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ENZYME INHIBITORS; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; ONIUM COMPOUNDS; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHOSPHOCREATINE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR;

RATTUS; RATTUS NORVEGICUS;

EID: 78349262245     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00200.2010     Document Type: Article

References (68)

1. Brehm A, Krssak M, Schmid AI, Nowotny P, Waldhausl W , Roden M. Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 55: 136-140, 2006. (Pubitemid 43343308)
2. Brindle KM. 31P NMR magnetization-transfer measurements of flux between inorganic phosphate and adenosine 5′-triphosphate in yeast cells genetically modified to overproduce phosphoglycerate kinase. Biochemistry 27: 6187-6196, 1988.
3. Brindle KM, Blackledge MJ, Challiss RA , Radda GK. 31P NMR magnetization-transfer measurements of ATP turnover during steady-state isometric muscle contraction in the rat hind limb in vivo. Biochemistry 28: 4887-4893, 1989.
4. Brindle KM , Radda GK. 31P-NMR saturation transfer measurements of exchange between Pi and ATP in the reactions catalysed by glyceraldehyde-3- phosphate dehydrogenase and phosphoglycerate kinase in vitro. Biochim Biophys Acta 928: 45-55, 1987.
5. Brown TR, Ugurbil K , Shulman RG. 31P nuclear magnetic resonance measurements of ATPase kinetics in aerobic Escherichia coli cells. Proc Natl Acad Sci USA 74: 5551-5553, 1977.
6. Campbell-Burk SL, Jones KA , Shulman RG. 31P NMR saturation-transfer measurements in Saccharomyces cerevisiae: characterization of phosphate exchange reactions by iodoacetate and antimycin A inhibition. Biochemistry 26: 7483-7492, 1987.
7. Ciapaite J, Bakker SJ, Van Eikenhorst G, Wagner MJ, Teerlink T, Schalkwijk CG, Fodor M, Ouwens DM, Diamant M, Heine RJ, Westerhoff HV , Krab K. Functioning of oxidative phosphorylation in liver mitochondria of high-fat diet fed rats. Biochim Biophys Acta 1772: 307-316, 2007. (Pubitemid 46275431)
8. Clifford PS , Hellsten Y. Vasodilatory mechanisms in contracting skeletal muscle. J Appl Physiol 97: 393-403, 2004. (Pubitemid 38802543)
9. Cooper J, Petty R, Hayes D, Morgan-Hughes J , Clark J. Chronic administration of the oral hypoglycaemic agent diphenyleneiodonium to rats. An animal model of impaired oxidative phosphorylation (mitochondrial myopathy). Biochem Pharmacol 37: 687-694, 1988. (Pubitemid 18053750)
10. Cooper JM, Petty RK, Hayes DJ, Challiss RA, Brosnan MJ, Shoubridge EA, Radda GK, Morgan-Hughes JA , Clark JB. An animal model of mitochondrial myopathy: a biochemical and physiological investigation of rats treated in vivo with the NADH-CoQ reductase inhibitor, diphenyleneiodonium. J Neurol Sci 83: 335-347, 1988.
11. De Feyter HM, Lenaers E, Houten SM, Schrauwen P, Hesselink MK, Wanders RJ, Nicolay K , Prompers JJ. Increased intramyocellular lipid content but normal skeletal muscle mitochondrial oxidative capacity throughout the pathogenesis of type 2 diabetes. FASEB J 22: 3947-3955, 2008.
12. De Feyter HM, van den Broek NM, Praet SF, Nicolay K, van Loon LJ , Prompers JJ. Early or advanced stage type 2 diabetes is not accompanied by in vivo skeletal muscle mitochondrial dysfunction. Eur J Endocrinol 158: 643-653, 2008. (Pubitemid 351639601)
13. Gatley SJ , Sherratt HS. The effects of diphenyleneiodonium and of 2,4-dichlorodiphenyleneiodonium on mitochondrial reactions. Mechanism of the inhibition of oxygen uptake as a consequence of the catalysis of the chloride/hydroxyl-ion exchange. Biochem J 158: 317-326, 1976.
14. 125I] iodonium to mitochondria to the extent of inhibition of oxygen uptake. Biochem J 158: 307-315, 1976.
15. Hayes DJ, Byrne E, Shoubridge EA, Morgan-Hughes JA , Clark JB. Experimentally induced defects of mitochondrial metabolism in rat skeletal muscle. Biological effects of the NADH: coenzyme Q reductase inhibitor diphenyleneiodonium. Biochem J 229: 109-117, 1985. (Pubitemid 15068122)
16. He J, Watkins S , Kelley DE. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 50: 817-823, 2001. (Pubitemid 32242639)
17. Heilbronn LK, Gan SK, Turner N, Campbell LV , Chisholm DJ. Markers of mitochondrial biogenesis and metabolism are lower in overweight and obese insulin-resistant subjects. J Clin Endocrinol Metab 92: 1467-1473, 2007. (Pubitemid 46556427)
18. Hojlund K, Wrzesinski K, Larsen PM, Fey SJ, Roepstorff P, Handberg A, Dela F, Vinten J, McCormack JG, Reynet C , Beck-Nielsen H. Proteome analysis reveals phosphorylation of ATP synthase beta-subunit in human skeletal muscle and proteins with potential roles in type 2 diabetes. J Biol Chem 278: 10436-10442, 2003.
19. Holland PC, Clark MG, Bloxham DP , Lardy HA. Mechanism of action of the hypoglycemic agent diphenyleneiodonium. J Biol Chem 248: 6050-6056, 1973.
20. Holland PC , Sherratt HS. Biochemical effects of the hypoglycaemic compound diphenyleneiodonnium. Catalysis of anion-hydroxyl ion exchange across the inner membrane of rat liver mitochondria and effects on oxygen uptake. Biochem J 129: 39-54, 1972.
21. Holloszy JO. Skeletal muscle "mitochondrial deficiency" does not mediate insulin resistance. Am J Clin Nutr 89: 463S-466S, 2009.
22. Hood DA, Gorski J , Terjung RL. Oxygen cost of twitch and tetanic isometric contractions of rat skeletal muscle. Am J Physiol Endocrinol Metab 250: E449-E456, 1986.
23. Jeneson JA, Schmitz JP, van den Broek NM, van Riel NA, Hilbers PA, Nicolay K , Prompers JJ. Magnitude and control of mitochondrial sensitivity to ADP. Am J Physiol Endocrinol Metab 297: E774-E784, 2009.
24. Kelley DE, He J, Menshikova EV , Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
25. Kemp GJ. Interactions of mitochondrial ATP synthesis and the creatine kinase equilibrium in skeletal muscle. J Theor Biol 170: 239-246, 1994.
26. Kemp GJ. The interpretation of abnormal 31P magnetic resonance saturation transfer measurements of Pi/ATP exchange in insulin-resistant skeletal muscle. Am J Physiol Endocrinol Metab 294: E640-E642, 2008.
27. Kingsley-Hickman PB, Sako EY, Mohanakrishnan P, Robitaille PM, From AH, Foker JE , Ugurbil K. 31P NMR studies of ATP synthesis and hydrolysis kinetics in the intact myocardium. Biochemistry 26: 7501-7510, 1987.
28. Laurent D, Yerby B, Deacon R , Gao J. Diet-induced modulation of mitochondrial activity in rat muscle. Am J Physiol Endocrinol Metab 293: E1169-E1177, 2007.
29. Lawson JW , Veech RL. Effects of pH and free Mg2+ on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J Biol Chem 254: 6528-6537, 1979.
30. Majander A, Finel M , Wikstrom M. Diphenyleneiodonium inhibits reduction of iron-sulfur clusters in the mitochondrial NADH-ubiquinone oxidoreductase (Complex I). J Biol Chem 269: 21037-21042, 1994.
31. Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, Beck-Nielsen H , Hojlund K. Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56: 1592-1599, 2007.
32. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D , Groop LC. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273, 2003.
33. Morino K, Petersen KF, Dufour S, Befroy D, Frattini J, Shatzkes N, Neschen S, White MF, Bilz S, Sono S, Pypaert M , Shulman GI. 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, 2005.
34. Morino K, Petersen KF , Shulman GI. Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55, Suppl 2: S9-S15, 2006.
35. O'Donnell VB, Smith GC , Jones OT. Involvement of phenyl radicals in iodonium inhibition of flavoenzymes. Mol Pharmacol 46: 778-785, 1994.
36. Palladino GW, Wood JJ , Proctor HJ. Modified freeze clamp technique for tissue assay. J Surg Res 28: 188-190, 1980.
37. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, DeFronzo R, Finlayson J, Kahn CR , Mandarino LJ. 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, 2003.
38. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW , Shulman GI. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-1142, 2003.
39. Petersen KF, Dufour S, Befroy D, Garcia R , Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 664-671, 2004.
40. Petersen KF, Dufour S , Shulman GI. Decreased insulin-stimulated ATP synthesis and phosphate transport in muscle of insulin-resistant offspring of type 2 diabetic parents. PLoS Med 2: e233, 2005.
41. Polgreen KE, Kemp GJ, Leighton B , Radda GK. Modulation of Pi transport in skeletal muscle by insulin and IGF-1. Biochim Biophys Acta 1223: 279-284, 1994.
42. Quistorff B, Johansen L , Sahlin K. Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. Biochem J 291: 681-686, 1993.
43. Rabol R, Boushel R , Dela F. Mitochondrial oxidative function and type 2 diabetes. Appl Physiol Nutr Metab 31: 675-683, 2006.
44. Ragan CI , Bloxham DP. Specific labelling of a constituent polypeptide of bovine heart mitochondrial reduced nicotinamide-adenine dinucleotide-ubiquinone reductase by the inhibitor diphenyleneiodonium. Biochem J 163: 605-615, 1977.
45. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH , Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54: 8-14, 2005.
46. Sahlin K. Intracellular pH and energy metabolism in skeletal muscle of man. With special reference to exercise. Acta Physiol Scand Suppl 455: 1-56, 1978.
47. Saltin B, Radegran G, Koskolou MD , Roach RC. Skeletal muscle blood flow in humans and its regulation during exercise. Acta Physiol Scand 162: 421-436, 1998. (Pubitemid 28121421)
48. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK, Jeneson JA, Backes WH, van Echteld CJ, van Engelshoven JM, Mensink M , Schrauwen P. Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia 50: 113-120, 2007.
49. Schrauwen-Hinderling VB, Roden M, Kooi ME, Hesselink MK , Schrauwen P. Muscular mitochondrial dysfunction and type 2 diabetes mellitus. Curr Opin Clin Nutr Metab Care 10: 698-703, 2007. (Pubitemid 350293769)
50. Sheldon JG, Williams SP, Fulton AM , Brindle KM. 31P NMR magnetization transfer study of the control of ATP turnover in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 93: 6399-6404, 1996.
51. Short KR, Nair KS , Stump CS. Impaired mitochondrial activity and insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 2419-2421; author reply 2419-2421, 2004.
52. Simoneau JA , Kelley DE. Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J Appl Physiol 83: 166-171, 1997.
53. Sreekumar R , Nair KS. Skeletal muscle mitochondrial dysfunction & diabetes. Indian J Med Res 125: 399-410, 2007.
54. Stuehr DJ, Fasehun OA, Kwon NS, Gross SS, Gonzalez JA, Levi R , Nathan CF. Inhibition of macrophage and endothelial cell nitric oxide synthase by diphenyleneiodonium and its analogs. FASEB J 5: 98-103, 1991.
55. Szendroedi J , Roden M. Mitochondrial fitness and insulin sensitivity in humans. Diabetologia 51: 2155-2167, 2008.
56. Szendroedi J, Schmid AI, Chmelik M, Toth C, Brehm A, Krssak M, Nowotny P, Wolzt M, Waldhausl W , Roden M. Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med 4: e154, 2007.
57. Szuhai K, Ouweland J, Dirks R, Lemaitre M, Truffert J, Janssen G, Tanke H, Holme E, Maassen J , Raap A. Simultaneous A8344G heteroplasmy and mitochondrial DNA copy number quantification in myoclonus epilepsy and ragged-red fibers (MERRF) syndrome by a multiplex molecular beacon based real-time fluorescence PCR. Nucleic Acids Res 29: E13, 2001.
58. Taylor DJ, Bore PJ, Styles P, Gadian DG , Radda GK. Bioenergetics of intact human muscle. A 31P nuclear magnetic resonance study. Mol Biol Med 1: 77-94, 1983.
59. Taylor DJ, Coppack SW, Cadoux-Hudson TA, Kemp GJ, Radda GK, Frayn KN , Ng LL. Effect of insulin on intracellular pH and phosphate metabolism in human skeletal muscle in vivo. Clin Sci (Lond) 81: 123-128, 1991.
60. Trautschold I, Lamprecht W , Schweitzer G. Nucleotides, Coenzymes and related compounds. In: Methods of Enzymatic Analysis, edited by Bergmeyer H, Wiley-VCH, 1985.
61. Trenell MI, Hollingsworth KG, Lim EL , Taylor R. Increased daily walking improves lipid oxidation without changes in mitochondrial function in Type 2 diabetes. Diabetes Care 31: 1644-1649, 2008.
62. van den Broek NM, Ciapaite J, De Feyter HM, Houten SM, Wanders RJ, Jeneson JA, Nicolay K , Prompers JJ. Increased mitochondrial content rescues in vivo muscle oxidative capacity in long-term high-fat-diet-fed rats. FASEB J 24: 1354-1364, 2010.
63. van den Broek NM, De Feyter HM, de Graaf L, Nicolay K , Prompers JJ. Intersubject differences in the effect of acidosis on phosphocreatine recovery kinetics in muscle after exercise are due to differences in proton efflux rates. Am J Physiol Cell Physiol 293: C228-C237, 2007.
64. Vicini P , Kushmerick MJ. Cellular energetics analysis by a mathematical model of energy balance: estimation of parameters in human skeletal muscle. Am J Physiol Cell Physiol 279: C213-C224, 2000.
65. Wagenmakers AJ. Insulin resistance in the offspring of parents with type 2 diabetes. PLoS Med 2: e289, 2005.
66. Wu F, Jeneson JA , Beard DA. Oxidative ATP synthesis in skeletal muscle is controlled by substrate feedback. Am J Physiol Cell Physiol 292: C115-C124, 2007.
67. Yerby B, Deacon R, Beaulieu V, Liang J, Gao J , Laurent D. Insulin-stimulated mitochondrial adenosine triphosphate synthesis is blunted in skeletal muscles of high-fat-fed rats. Metabolism 57: 1584-1590, 2008.
68. Yu C, Chen Y, Cline GW, Zhang D, Zong H, Wang Y, Bergeron R, Kim JK, Cushman SW, Cooney GJ, Atcheson B, White MF, Kraegen EW , Shulman GI. 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, 2002.