Standard magnetic resonance-based measurements of the pi¡ATP rate do not index the rate of oxidative phosphorylation in cardiac and skeletal muscles

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 1, 2011, Pages

  From, Arthur H L ^a,b   Ugurbil, Kamil ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b Departments of Medicine (Cardiovascular Division)   (United States)

Author keywords

Magnetization transfer; Oxidative ATP synthesis; Striated muscle

Indexed keywords

ADENOSINE TRIPHOSPHATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; CELL FUNCTION; CELL ISOLATION; CHEMICAL REACTION; ENZYME ACTIVITY; GLYCOLYSIS; HEART MUSCLE; HUMAN; HYDROLYSIS KINETICS; INSULIN SENSITIVITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; SKELETAL MUSCLE; SYNTHESIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; ENERGY METABOLISM; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MITOCHONDRIA; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; MYOCARDIUM; OXIDATIVE PHOSPHORYLATION; PHOSPHORYLATION;

EID: 79959824208     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00345.2010     Document Type: Article

References (47)

1. Balaban RS, Koretsky AP. Interpretation of 31P NMR saturation transfer experiments: what you can't see might confuse you. Focus on "Standard magnetic resonance-based measurements of the Pi¡ATP rate do not index the rate of oxidative phosphorylation in cardiac and skeletal muscles." Am J Physiol Cell Physiol (April 13, 2011). doi:10.1152/ajpcell.00100.2011.
2. Befroy DE, Petersen KF, Dufour S, Mason GF, de Graaf RA, Rothman DL, Shulman GI. Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56: 1376-1381, 2007.
3. Befroy DE, Petersen KF, Dufour S, Mason GF, Rothman DL, Shulman GI. Increased substrate oxidation and mitochondrial uncoupling in skeletal muscle of endurance-trained individuals. Proc Natl Acad Sci USA 105: 16701-16706, 2008.
4. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsoe R, Dela F. Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50: 790-796, 2007.
5. 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.
6. 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.
7. Campbell-Burk SL, Jones KA, Shulman RG. 31P NMR saturationtransfer measurements in Saccharomyces cerevisiae: characterization of phosphate exchange reactions by iodoacetate and antimycin A inhibition. Biochemistry 26: 7483-7492, 1987.
8. Chance B, Leigh JS Jr, Kent J, McCully K, Nioka S, Clark BJ, Maris JM, Graham T. Multiple controls of oxidative metabolism in living tissues as studied by phosphorus magnetic resonance. Proc Natl Acad Sci USA 83: 9458-9462, 1986.
9. 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.
10. 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.
11. Decking UK, Skwirba S, Zimmermann MF, Preckel B, Thamer V, Deussen A, Schrader J. Spatial heterogeneity of energy turnover in the heart. Pflügers Arch 441: 663-673, 2001.
12. Du F, Zhu XH, Qiao H, Zhang X, Chen W. Efficient in vivo 31P magnetization transfer approach for noninvasively determining multiple kinetic parameters and metabolic fluxes of ATP metabolism in the human brain. Magn Reson Med 57: 103-114, 2007.
13. Erecinska M, Wilson DF, Nishiki K. Homeostatic regulation of cellular energy metabolism: experimental characterization in vivo and fit to a model. Am J Physiol Cell Physiol 234: C82-C89, 1978.
14. From AH, Zimmer SD, Michurski SP, Mohanakrishnan P, Ulstad VK, Thoma WJ, Ugurbil K. Regulation of the oxidative phosphorylation rate in the intact cell. Biochemistry 29: 3731-3743, 1990.
15. Holloszy JO. Skeletal muscle "mitochondrial deficiency" does not mediate insulin resistance. Am J Clin Nutr 89: 463S-466S, 2009.
16. 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.
17. Jucker BM, Dufour S, Ren J, Cao X, Previs SF, Underhill B, Cadman KS, Shulman GI. Assessment of mitochondrial energy coupling in vivo by 13C/31P NMR. Proc Natl Acad Sci USA 97: 6880-6884, 2000.
18. Jucker BM, Ren J, Dufour S, Cao X, Previs SF, Cadman KS, Shulman GI. 13C/31P NMR assessment of mitochondrial energy coupling in skeletal muscle of awake fed and fasted rats. Relationship with uncoupling protein 3 expression. J Biol Chem 275: 39279-39286, 2000.
19. Kalliokoski KK, Knuuti J, Nuutila P. Relationship between muscle blood flow and oxygen uptake during exercise in endurance-trained and untrained men. J Appl Physiol 98: 380-383, 2005.
20. Kemp GA. 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.
21. Kingsley-Hickman P, Sako EY, Andreone PA, St Cyr JA, Michurski S, Foker JE, From AH, Petein M, Ugurbil K. 31P NMR measurement of ATP synthesis rate in perfused intact rat hearts. FEBS Lett 198: 159-163, 1986.
22. 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.
23. Kingsley-Hickman PB, Sako EY, Ugurbil K, From AH, Foker JE. 31P NMR measurement of mitochondrial uncoupling in isolated rat hearts. J Biol Chem 265: 1545-1550, 1990.
24. Kobayashi K, Neely JR. Control of maximum rates of glycolysis in rat cardiac muscle. Circ Res 44: 166-175, 1979.
25. LaNoue KF, Jeffries FM, Radda GK. Kinetic control of mitochondrial ATP synthesis. Biochemistry 25: 7667-7675, 1986.
26. Lebon V, Dufour S, Petersen KF, Ren J, Jucker BM, Slezak LA, Cline GW, Rothman DL, Shulman GI. Effect of triiodothyronine on mitochondrial energy coupling in human skeletal muscle. J Clin Invest 108: 733-737, 2001.
27. Lei H, Ugurbil K, Chen W. Measurement of unidirectional Pi to ATP flux in human visual cortex at 7 T by using in vivo 31P magnetic resonance spectroscopy. Proc Natl Acad Sci USA 100: 14409-14414, 2003.
28. 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.
29. 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.
30. Nair KS, Bigelow ML, Asmann YW, Chow LS, Coenen-Schimke JM, Klaus KA, Guo ZK, Sreekumar R, Irving BA. Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance. Diabetes 57: 1166-1175, 2008.
31. Pellerin L, Magistretti PJ. Neuroenergetics: calling upon astrocytes to satisfy hungry neurons. Neuroscientist 10: 53-62, 2004.
32. 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.
33. Phillips D, Aponte AM, French SA, Chess DJ, Balaban RS. Succinyl-CoA synthetase is a phosphate target for the activation of mitochondrial metabolism. Biochemistry 48: 7140-7149, 2009.
34. Portman MA. Measurement of unidirectional P(i)->ATP flux in lamb myocardium in vivo. Biochim Biophys Acta 1185: 221-227, 1994.
35. Richardson RS, Grassi B, Gavin TP, Haseler LJ, Tagore K, Roca J, Wagner PD. Evidence of O2 supply-dependent V ̇ O2max in the exercisetrained human quadriceps. J Appl Physiol 86: 1048-1053, 1999.
36. Richardson RS, Saltin B. Human muscle blood flow and metabolism studied in the isolated quadriceps muscles. Med Sci Sports Exerc 30: 28-33, 1998.
37. Robitaille PM, Merkle H, Sako E, Lang G, Clack RM, Bianco R, From AH, Foker J, Ugurbil K. Measurement of ATP synthesis rates by 31P-NMR spectroscopy in the intact myocardium in vivo. Magn Reson Med 15: 8-24, 1990.
38. Sako EY, Kingsley-Hickman PB, From AH, Foker JE, Ugurbil K. ATP synthesis kinetics and mitochondrial function in the postischemic myocardium as studied by 31P NMR. J Biol Chem 263: 10600-10607, 1988.
39. Savage DB, Petersen KF, Shulman GI. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 87: 507-520, 2007.
40. Schmid AI, Chmelik M, Szendroedi J, Krssak M, Brehm A, Moser E, Roden M. Quantitative ATP synthesis in human liver measured by localized 31P spectroscopy using the magnetization transfer experiment. NMR Biomed 21: 437-443, 2008.
41. Shen W, Tian R, Saupe KW, Spindler M, Ingwall JS. Endogenous nitric oxide enhances coupling between O2 consumption and ATP synthesis in guinea pig hearts. Am J Physiol Heart Circ Physiol 281: H838-H846, 2001.
42. 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.
43. Thoma WJ, Ugurbil K. Saturation-transfer studies of ATP-Pi exchange in isolated perfused rat liver. Biochim Biophys Acta 893: 225-231, 1987.
44. Ugurbil K, Kingsley-Hickman PB, Sako EY, Zimmer S, Mohanakrishnan P, Robitaille PM, Thoma WJ, Johnson A, Foker JE, From AH. 31P NMR studies of the kinetics and regulation of oxidative phosphorylation in the intact myocardium. Ann NY Acad Sci 508: 265-286, 1987.
45. Xavier AR, Roselino JE, Resano NM, Garofalo MA, Migliorini RH, Kettelhut Ido C. Glyconeogenic pathway in isolated skeletal muscles of rats. Can J Physiol Pharmacol 80: 164-169, 2002.
46. Yan J, Young ME, Cui L, Lopaschuk GD, Liao R, Tian R. Increased glucose uptake and oxidation in mouse hearts prevent high fatty acid oxidation but cause cardiac dysfunction in diet-induced obesity. Circulation 119: 2818-2828, 2009.
47. Yerby B, Deacon R, Beaulieu V, Liang J, Gao J, Laurent D. Insulinstimulated mitochondrial adenosine triphosphate synthesis is blunted in skeletal muscles of high-fat-fed rats. Metabolism 57: 1584-1590, 2008.