Chapter 21 Assessment of In Vivo Mitochondrial Metabolism by Magnetic Resonance Spectroscopy

Methods in Enzymology

Volumn 457, Issue B, 2009, Pages 373-393

  Befroy, Douglas E ^a   Falk Petersen, Kitt ^a   Rothman, Douglas L ^a   Shulman, Gerald I ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ACETYL COENZYME A; CARBON; FATTY ACID; GLUTAMIC ACID; PHOSPHORUS;

CARBON NUCLEAR MAGNETIC RESONANCE; CITRIC ACID CYCLE; EXERCISE; FATTY ACID OXIDATION; GASTROCNEMIUS MUSCLE; HUMAN; IN VIVO STUDY; INSULIN RESISTANCE; MITOCHONDRIAL RESPIRATION; MUSCLE METABOLISM; MUSCLE MITOCHONDRION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; REST; REVIEW; SOLEUS MUSCLE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; METABOLISM; METHODOLOGY; OXIDATION REDUCTION REACTION;

ACETYL COENZYME A; ADENOSINE TRIPHOSPHATE; ANIMALS; CARBON ISOTOPES; FATTY ACIDS; GLUTAMIC ACID; HUMANS; INSULIN RESISTANCE; MAGNETIC RESONANCE SPECTROSCOPY; MITOCHONDRIA, MUSCLE; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PHOSPHORUS ISOTOPES;

EID: 65449187906     PISSN: 00766879     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0076-6879(09)05021-6     Document Type: Review

References (70)

1. Alger J.R., den Hollander J.A., and Shulman R.G. In vivo phosphorus-31 nuclear magnetic resonance saturation transfer studies of adenosinetriphosphatase kinetics in Saccharomyces cerevisiae. Biochemistry 21 (1982) 2957-2963
2. Befroy D.E., Petersen K.F., Dufour S., Mason G.F., de Graaf R.A., Rothman D.L., and Shulman G.I. Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56 (2007) 1376-1381
3. Befroy D.E., Petersen K.F., Dufour S., Mason G.F., Rothman D.L., and Shulman G.I. Increased substrate oxidation and mitochondrial uncoupling in skeletal muscle of endurance-trained individuals. Proc. Natl. Acad. Sci. USA 105 (2008) 16701-16706
4. Befroy D.E., Petersen K.F., Shulman G.I., and Rothman D.L. Localized 31P saturation transfer reveals differences in gastrocnemius and soleus rates of ATP synthesis in-vivo. Proc. Int. Soc. Mag. Reson. Med. (2008) 2565
5. Bloch F. Nuclear induction. Phys. Rev. 70 (1946) 460
6. Boden G., and Shulman G.I. Free fatty acids in obesity and type 2 diabetes: Defining their role in the development of insulin resistance and beta-cell dysfunction. Eur. J. Clin. Invest. 32 Suppl. 3 (2002) 14-23
7. 31P NMR magnetization-transfer measurements of ATP turnover during steady-state isometric muscle contraction in the rat hind limb in vivo. Biochemistry 28 (1989) 4887-4893
8. 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 (1987) 45-55
9. 31P nuclear magnetic resonance measurements of ATPase kinetics in aerobic Escherichia coli cells. Proc. Natl. Acad. Sci. USA 74 (1977) 5551-5553
10. Burum D.P., and Ernst R.R. Net polarization transfer via a J-ordered state for signal enhancement of low-sensitivity nuclei. J. Magn. Reson. (1969) 39 (1980) 163-168
11. 31P NMR saturation-transfer measurements in Saccharomyces cerevisiae: Characterization of phosphate exchange reactions by iodoacetate and antimycin A inhibition. Biochemistry 26 (1987) 7483-7492
12. 31P-MRS during incremental exercise in old and young humans. Eur. J. Appl. Physiol. Occup. Physiol. 78 (1998) 460-465
13. Choi C.S., Befroy D.E., Codella R., Kim S., Reznick R.M., Hwang Y., Liu Z., Lee H., Distefano A., Samuel V.T., Zhang D., Cline G.W., et al. Paradoxical effects of increased expression of PGC-1α on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc. Natl. Acad. Sci. USA 105 (2008) 19926-19931
14. Cline G.W., Vidal-Puig A.J., Dufour S., Cadman K.S., Lowell B.B., and Shulman G.I. In vivo effects of uncoupling protein-3 gene disruption on mitochondrial energy metabolism. J. Biol. Chem. 276 (2001) 20240-20244
15. Colberg S.R., Simoneau J.A., Thaete F.L., and Kelley D.E. Skeletal muscle utilization of free fatty acids in women with visceral obesity. J. Clin. Invest. 95 (1995) 1846-1853
16. De Feyter H.M., Lenaers E., Houten S.M., Schrauwen P., Hesselink M.K., Wanders R.J., Nicolay K., and Prompers J.J. Increased intramyocellular lipid content but normal skeletal muscle mitochondrial oxidative capacity throughout the pathogenesis of type 2 diabetes. FASEB J. 22 (2008) 3947-3955
17. de Graaf R.A. In Vivo NMR Spectroscopy: Principles and Techniques (2008), Wiley, Chichester
18. Dobbins R.L., and Malloy C.R. Measuring in-vivo metabolism using nuclear magnetic resonance. Curr. Opin. Clin. Nutr. Metab. Care 6 (2003) 501-509
19. Du F., Zhu X.H., Zhang Y., Friedman M., Zhang N., Ugurbil K., and Chen W. Tightly coupled brain activity and cerebral ATP metabolic rate. Proc. Natl. Acad. Sci. USA 105 (2008) 6409-6414
20. Essen B., Jansson E., Henriksson J., Taylor A.W., and Saltin B. Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiol. Scand. 95 (1975) 153-165
21. Forsen S., and Hoffman R.A. Study of moderately rapid chemical exchange reactions by means of nuclear magnetic double resonance. J. Chem. Phys. 39 (1963) 2892-2901
22. 31P-NMR. Biochim. Biophys. Acta 762 (1983) 325-336
23. Frontera W.R., Hughes V.A., Lutz K.J., and Evans W.J. A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J. Appl. Physiol. 71 (1991) 644-650
24. Haffner S.M., Stern M.P., Mitchell B.D., Hazuda H.P., and Patterson J.K. Incidence of type II diabetes in Mexican Americans predicted by fasting insulin and glucose levels, obesity, and body-fat distribution. Diabetes 39 (1990) 283-288
25. Hawkins R.A., and Mans A.M. Intermediary metabolism of carbohydrates and other fuels. In: Lajtha A. (Ed). Handbook of Neurochemistry 3 (1983), Plenum, New York 259-294
26. He J., Watkins S., and Kelley D.E. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 50 (2001) 817-823
27. Hoffman R.A., and Forsén S. High resolution nuclear magnetic double and multiple resonance. Prog. NMR Spectrosc. 1 (1966) 15-204
28. 31P nuclear magnetic resonance. Nature 252 (1974) 285-287
29. Houmard J.A., Weidner M.L., Gavigan K.E., Tyndall G.L., Hickey M.S., and Alshami A. Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging. J. Appl. Physiol. 85 (1998) 1337-1341
30. 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 (2000) 39279-39286
31. Kelley D.E., Goodpaster B., Wing R.R., and Simoneau J.A. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am. J. Physiol. Endocrinol. Metab. 277 (1999) E1130-E1141
32. Kelley D.E., He J., Menshikova E.V., and Ritov V.B. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51 (2002) 2944-2950
33. 31P magnetic resonance saturation transfer measurements of Pi/ATP exchange in insulin-resistant skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 294 (2008) E640-E642 author reply E643-E644
34. Kemp G.J., Meyerspeer M., and Moser E. Absolute quantification of phosphorus metabolite concentrations in human muscle in vivo by 31P MRS: A quantitative review. NMR Biomed. 20 (2007) 555-565
35. Kent-Braun J.A., and Ng A.V. Skeletal muscle oxidative capacity in young and older women and men. J. Appl. Physiol. 89 (2000) 1072-1078
36. Kingsley P.B., and Monahan W.G. Corrections for off-resonance effects and incomplete saturation in conventional (two-site) saturation-transfer kinetic measurements. Magn. Reson. Med. 43 (2000) 810-819
37. Kingsley P.B., and Monahan W.G. Effects of off-resonance irradiation, cross-relaxation, and chemical exchange on steady-state magnetization and effective spin-lattice relaxation times. J. Magn. Reson. 143 (2000) 360-375
38. 1H NMR spectroscopy study. Diabetologia 42 (1999) 113-116
39. Lanza I.R., Befroy D.E., and Kent-Braun J.A. Age-related changes in ATP-producing pathways in human skeletal muscle in vivo. J. Appl. Physiol. 99 (2005) 1736-1744
40. Lebon V., Dufour S., Petersen K.F., Ren J., Jucker B.M., Slezak L.A., Cline G.W., Rothman D.L., and Shulman G.I. Effect of triiodothyronine on mitochondrial energy coupling in human skeletal muscle. J. Clin. Invest. 108 (2001) 733-737
41. 31P magnetic resonance spectroscopy. Proc. Natl. Acad. Sci. USA 100 (2003) 14409-14414
42. Lillioja S., Young A.A., Culter C.L., Ivy J.L., Abbott W.G., Zawadzki J.K., Yki-Jarvinen H., Christin L., Secomb T.W., and Bogardus C. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J. Clin. Invest. 80 (1987) 415-424
43. MacFall J.R., Wehrli F.W., Breger R.K., and Johnson G.A. Methodology for the measurement and analysis of relaxation times in proton imaging. Magn. Reson. Imaging 5 (1987) 209-220
44. 31P NMR saturation transfer. Biochem. Biophys. Res. Commun. 103 (1981) 1052-1059
45. McConnell H.M. Reaction rates by nuclear magnetic resonance. J. Chem. Phys. 28 (1958) 430-431
46. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., Puigserver P., Carlsson E., Ridderstrale M., Laurila E., Houstis N., Daly M.J., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34 (2003) 267-273
47. Morino K., Petersen K.F., Dufour S., Befroy D., Frattini J., Shatzkes N., Neschen S., White M.F., Bilz S., Sono S., Pypaert M., and Shulman G.I. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J. Clin. Invest. 115 (2005) 3587-3593
48. Morino K., Petersen K.F., and Shulman G.I. Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55 Suppl. 2 (2006) S9-S15
49. Nair K.S., Bigelow M.L., Asmann Y.W., Chow L.S., Coenen-Schimke J.M., Klaus K.A., Guo Z.K., Sreekumar R., and Irving B.A. Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance. Diabetes 57 (2008) 1166-1175
50. Pan D.A., Lillioja S., Kriketos A.D., Milner M.R., Baur L.A., Bogardus C., Jenkins A.B., and Storlien L.H. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46 (1997) 983-988
51. Patti M.E., Butte A.J., Crunkhorn S., Cusi K., Berria R., Kashyap S., Miyazaki Y., Kohane I., Costello M., Saccone R., Landaker E.J., Goldfine A.B., et al. 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 (2003) 8466-8471
52. Perseghin G., Ghosh S., Gerow K., and Shulman G.I. Metabolic defects in lean nondiabetic offspring of NIDDM parents: A cross-sectional study. Diabetes 46 (1997) 1001-1009
53. 13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 48 (1999) 1600-1606
54. Petersen K.F., Befroy D., Dufour S., Dziura J., Ariyan C., Rothman D.L., DiPietro L., Cline G.W., and Shulman G.I. Mitochondrial dysfunction in the elderly: Possible role in insulin resistance. Science 300 (2003) 1140-1142
55. Petersen K.F., Dufour S., Befroy D., Garcia R., and Shulman G.I. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350 (2004) 664-671
56. Petersen K.F., Dufour S., Befroy D., Lehrke M., Hendler R.E., and Shulman G.I. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes 54 (2005) 603-608
57. Petersen K.F., Oral E.A., Dufour S., Befroy D., Ariyan C., Yu C., Cline G.W., DePaoli A.M., Taylor S.I., Gorden P., and Shulman G.I. Leptin reverses insulin resistance and hepatic steatosis in patients with severe lipodystrophy. J. Clin. Invest. 109 (2002) 1345-1350
58. Pette D., and Spamer C. Metabolic properties of muscle fibers. Fed. Proc. 45 (1986) 2910-2914
59. Prompers J.J., Jeneson J.A., Drost M.R., Oomens C.C., Strijkers G.J., and Nicolay K. Dynamic MRS and MRI of skeletal muscle function and biomechanics. NMR Biomed. 19 (2006) 927-953
60. Ritov V.B., Menshikova E.V., He J., Ferrell R.E., Goodpaster B.H., and Kelley D.E. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54 (2005) 8-14
61. Savage D.B., Petersen K.F., and Shulman G.I. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol. Rev. 87 (2007) 507-520
62. Seppala-Lindroos A., Vehkavaara S., Hakkinen A.M., Goto T., Westerbacka J., Sovijarvi A., Halavaara J., and Yki-Jarvinen H. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J. Clin. Endocrinol. Metab. 87 (2002) 3023-3028
63. 13C NMR. Proc. Natl. Acad. Sci. USA 96 (1999) 8235-8240
64. Shulman G.I. Cellular mechanisms of insulin resistance. J. Clin. Invest. 106 (2000) 171-176
65. Shulman R.G., Rothman D.L., and Price T.B. Nuclear magnetic resonance studies of muscle and applications to exercise and diabetes. Diabetes 45 Suppl. 1 (1996) S93-S98
66. Simoneau J.A., and Kelley D.E. Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J. Appl. Physiol. 83 (1997) 166-171
67. Simoneau J.A., Veerkamp J.H., Turcotte L.P., and Kelley D.E. Markers of capacity to utilize fatty acids in human skeletal muscle: Relation to insulin resistance and obesity and effects of weight loss. FASEB J. 13 (1999) 2051-2060
68. Szczepaniak L.S., Babcock E.E., Schick F., Dobbins R.L., Garg A., Burns D.K., McGarry J.D., and Stein D.T. Measurement of intracellular triglyceride stores by H spectroscopy: Validation in vivo. Am. J. Physiol. Endocrinol. Metab. 276 (1999) E977-E989
69. Warram J.H., Martin B.C., Krolewski A.S., Soeldner J.S., and Kahn C.R. Slow glucose removal rate and hyperinsulinemia precede the development of type II diabetes in the offspring of diabetic parents. Ann. Intern. Med. 113 (1990) 909-915
70. Wild S., Roglic G., Green A., Sicree R., and King H. Global prevalence of diabetes: Estimates for the year 2000 and projections for 2030. Diabetes Care 27 (2004) 1047-1053