Exercise training increases intramyocellular lipid and oxidative capacity in older adults

American Journal of Physiology - Endocrinology and Metabolism

Volumn 287, Issue 5 50-5, 2004, Pages

  Pruchnic, Ryan ^a   Katsiaras, Andreas ^a   He, Jing ^a   Kelley, David E ^a   Winters, Carena ^a   Goodpaster, Bret H ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Fiber type; Physical activity; Skeletal muscle; Triacylglycerol

Indexed keywords

FAT; INSULIN; LIPID; TRIACYLGLYCEROL;

AGED; ARTICLE; EXERCISE; FEMALE; HISTOCHEMISTRY; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; INSULIN RESISTANCE; MALE; MICROSCOPY; MUSCLE BIOPSY; NORMAL HUMAN; OXIDATION; PRIORITY JOURNAL; SKELETAL MUSCLE;

AGED; BODY COMPOSITION; EXERCISE; FEMALE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; LIPIDS; MALE; MUSCLE CELLS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PHYSICAL FITNESS; REFERENCE VALUES;

EID: 6044224890     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00459.2003     Document Type: Article

References (54)

1. American College of Sports Medicine. ACSM's Guidelines for Exercise Testing and Prescription. Philadelphia, PA: Lippincott, Williams, and Wilkens, 2000.
2. Askanas V and Engel WK. Distinct subtypes of type I fibers of human skeletal muscle. Neurology 25: 879-887, 1975.
3. Bruce CR, Anderson MJ, Carey AL, Newman DG, Bonen A, Kriketos AD, Cooney GJ, and Hawley JA. Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J Clin Endocrinol Metab 88: 5444-5451, 2003.
4. Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, and Holloszy JO. Histochemical and enzymatic comparison of gastrocnemius muscle of young and elderly men and women. J Gerontol Biol Sci 46B: 71-76, 1992.
5. Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, and Holloszy JO. Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J Appl Physiol 72: 1780-1786, 1992.
6. Coggan AR, Spina RJ, Rogers MA, King DS, Brown M, Nemeth PM, and Holloszy JO. Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J Appl Physiol 68: 1896-1901, 1990.
7. Cox JH, Cortright RN, Dohm GL, and Houmard JA. Effect of aging on response to exercise training in humans: skeletal muscle GLUT-4 and insulin sensitivity. J Appl Physiol 86: 2019-2025, 1999.
8. Defronzo RA. Glucose intolerance and aging: evidence for tissue insensitivity to insulin. Diabetes 28: 1095-1101, 1979.
9. Dubowitz V. Muscle Biopsy: A Practical Approach. London: Bailliere Tindall, 1985.
10. Elahi D, Muller DC, Egan JM, Andres R, Veldhuist J, and Meneilly GS. Glucose tolerance, glucose utilization and insulin secretion in ageing. Novartis Found Symp 242: 222-242, 2002.
11. Evans WJ, Phinney SD, and Young VR. Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc 14: 101-102, 1982.
12. Frayn KN. Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol 55: 628-634, 1983.
13. Gollnick PD and Saltin B. Significance of skeletal muscle oxidative enzyme enhancement with endurance training. Clin Physiol 2: 1-12, 1982.
14. Goodpaster B, Katsiaras A, and Kelley D. Enhanced fat oxidation through physical activity is associated with improvements in insulin sensitivity in obesity. Diabetes 51: 2191-2197, 2003.
15. Goodpaster B, Krishnaswami S, Resnick H, Kelley D, Haggerty C, Harris T, Schwartz A, Kritchevsky S, and Newman A. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care 26: 372-379, 2003.
16. Goodpaster BH, He J, Watkins S, and Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 86: 5755-5761, 2001.
17. Goodpaster BH, Thaete FL, Simoneau JA, and Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes 46: 1579-1585, 1997.
18. Goodpaster BH, Theriault R, Watkins SC, and Kelley DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 49: 467-472, 2000.
19. Guo Z, Mishra P, and Macura S. Sampling the intramyocellular triglycerides from skeletal muscle. J Lipid Res 42: 1041-1048, 2001.
20. Hambrecht R, Fiehn E, Yu J, Niebauer J, Weigl C, Hilbrich L, Adams V, Riede U, and Schuler G. Effects of endurance training on mitochondrial ultrastructure and fiber type distribution in skeletal muscle of patients with stable chronic heart failure. J Am Coll Cardiol 29: 1067-1073, 1997.
21. Harris MI, Flegal KM, Cowie CC, Eberhardt MS, Goldstein DE, Little RR, Wiedmeyer HM, and Byrd-Holt DD. Prevalence of diabetes, impaired fasting glucose, and impaired glucose tolerance in U.S. adults. The Third National Health and Nutrition Examination Survey, 1988-1994. Diabetes Care 21: 518-524, 1998.
22. He J, Watkins S, and 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.
23. Helge JW and Dela F. Effect of training on muscle triacylglycerol and structural lipids: a relation to insulin sensitivity? Diabetes 52: 1881-1887, 2003.
24. Howald H, Hoppeler H, Claassen H, Mathieu O, and Straub R. Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflügers Arch 403: 369-376, 1985.
25. Hughes VA, Fiatarone MA, Fielding RA, Ferrara CM, Elahi D, and Evans WJ. Long-term effects of a high-carbohydrate diet and exercise on insulin action in older subjects with impaired glucose tolerance. Am J Clin Nutr 62: 426-433, 1995.
26. Hulver MW, Berggren JR, Cortright RN, Dudek RW, Thompson RP, Pories WJ, MacDonald KG, Cline GW, Shulman GI, Dohm GL, and Houmard JA. Skeletal muscle lipid metabolism with obesity. Am J Physiol Endocrinol Metab 284: E741-E747, 2003.
27. Karlsson J and Saltin B. Diet, muscle glycogen, and endurance performance. J Appl Physiol 31: 203-206, 1971.
28. Kasahara K and Kikkawa U. Distinct effects of saturated fatty acids on protein kinase C subspecies. J Biochem (Tokyo) 117: 648-653, 1995.
29. Kelley DE, Goodpaster B, Wing RR, and Simoneau JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol Endocrinol Metab 277: E1130-E1141, 1999.
30. Kelley DE, Slasky BS, and Janosky J. Skeletal muscle density: effects of obesity and non-insulin-dependent diabetes mellitus. Am J Clin Nutr 54: 509-515, 1991.
31. Kiens B, Essén-Gustavsson B, Christensen NJ, and Saltin B. Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training. J Physiol 469: 459-478, 1993.
32. Kirwan JP, Kohrt WM, Wojta DM, Bourey RE, and Holloszy JO. Endurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-old men and women. J Gerontol 48: M84-M90, 1993.
33. Lexell J, Taylor CC, and Sjostrom M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84: 275-294, 1988.
34. Lillie R and Ashburn L. Super-saturated solutions of fat stains in dilute isopropanol for demonstration of acute fatty degenerations not shown by the Herxheimer technique. Arch Pathol 36: 432-440, 1943.
35. Majumdar S, Rossi MW, Fujiki T, Phillips WA, Disa S, Queen CF, Johnston RB Jr, Rosen OM, Corkey BE, and Korchak HM. Protein kinase C isotypes and signaling in neutrophils. Differential substrate specificities of a translocatable calcium- and phospholipid-dependent beta-protein kinase C and a phospholipid-dependent protein kinase which is inhibited by long chain fatty acyl coenzyme A. J Biol Chem 266: 9285-9294, 1991.
36. Martin TP, Vailas AC, Durivage JB, Edgerton VR, and Castleman KR. Quantitative histochemical determination of muscle enzymes: biochemical verification. J Histochem Cytochem 33: 1053-1059, 1985.
37. Mittendorfer B, Horowitz JF, and Klein S. Effect of gender on lipid kinetics during endurance exercise of moderate intensity in untrained subjects. Am J Physiol Endocrinol Metab 283: E58-E65, 2002.
38. Nesher M and Boneh A. Effect of fatty acids and their acyl-CoA esters on protein kinase C activity in fibroblasts: possible implications in fatty acid oxidation defects. Biochim Biophys Acta 1221: 66-72, 1994.
39. Orellana A, Hidalgo PC, Morales MN, Mezzano D, and Bronfman M. Palmitoyl-CoA and the acyl-CoA thioester of the carcinogenic peroxisome-proliferator ciprofibrate potentiate diacylglycerol-activated protein kinase C by decreasing the phosphatidylserine requirement of the enzyme. Eur J Biochem 190: 57-61, 1990.
40. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, and Storlien LH. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46: 983-988, 1997.
41. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, and Shulman GI. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-1142, 2003.
42. Petersen KF, Dufour S, Befroy D, Garcia R, and Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 664-671, 2004.
43. Phillips DI, Caddy S, Ilic V, Fielding BA, Frayn KN, Borthwick AC, and Taylor R. Intramuscular triglyceride and muscle insulin sensitivity: evidence for a relationship in nondiabetic subjects. Metabolism 45: 947-950, 1996.
44. Roepstorff C, Steffensen CH, Madsen M, Stallknecht B, Kanstrup IL, Richter EA, and Kiens B. Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects. Am J Physiol Endocrinol Metab 282: E435-E447, 2002.
45. Russell AP, Feilchenfeldt J, Schreiber S, Praz M, Crettenand A, Gobelet C, Meier CA, Bell DR, Kralli A, Giacobino JP, and Deriaz O. Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-gamma coactivator-1 and peroxisome proliferator-activated receptor-alpha in skeletal muscle. Diabetes 52: 2874-2881, 2003.
46. Russell JC, Shillabeer G, Bar-Tana J, Lau DC, Richardson M, Wenzel LM, Graham SE, and Dolphin PJ. Development of insulin resistance in the JCR:LA-cp rat: role of triacylglycerols and effects of MEDICA 16. Diabetes 47: 770-778, 1998.
47. Schmitz-Peiffer C. Signalling aspects of insulin resistance in skeletal muscle: mechanisms induced by lipid oversupply. Cell Signal 12: 583-594, 2000.
48. Schrauwen-Hinderling VB, Schrauwen P, Hesselink MK, van Engelshoven JM, Nicolay K, Saris WH, Kessels AG, and Kooi ME. The increase in intramyocellular lipid content is a very early response to training. J Clin Endocrinol Metab 88: 1610-1616, 2003.
49. Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA, CoenenSchimke JM, and Nair KS. Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52: 1888-1896, 2003.
50. Simoneau JA, Colberg SR, Thaete FL, and Kelley DE. Skeletal muscle glycolytic and oxidative enzyme capacities are determinants of insulin sensitivity and muscle composition in obese women. FASEB J 9: 273-278, 1995.
51. Simoneau JA, Veerkamp JH, Turcotte LP, and Kelley DE. 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: 2051-2060, 1999.
52. Skorjanc D, Heine G, and Pette D. Time-dependent increase of succinate dehydrogenase activity in low-frequency stimulated rabbit muscle: a comparison between microphotometric and biochemical methods. Histochem Cell Biol 107: 47-55, 1997.
53. Tyni-Lenne R, Jansson E, and Sylven C. Female-related skeletal muscle phenotype in patients with moderate chronic heart failure before and after dynamic exercise training. Cardiovasc Res 42: 99-103, 1999.
54. 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, and 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.