Intramyocellular lipid content and insulin sensitivity are increased following a short-term low-glycemic index diet and exercise intervention

American Journal of Physiology - Endocrinology and Metabolism

Volumn 301, Issue 3, 2011, Pages

  Haus, Jacob M ^a   Solomon, Thomas P J ^a   Lu, Lan ^b   Jesberger, John A ^b   Barkoukis, Hope ^d   Flask, Chris A ^b,c   Kirwan, John P ^a,b,d  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Case Western Reserve University   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Aging; Insulin resistance; Obesity; Substrate utilization

Indexed keywords

INSULIN; LIPID;

ADULT; AEROBIC EXERCISE; AGED; ARTICLE; BODY MASS; CELL LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; DIET THERAPY; FEMALE; GLYCEMIC INDEX; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; LOW GLYCEMIC INDEX DIET; MALE; MUSCLE LEVEL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SKELETAL MUSCLE; SOLEUS MUSCLE; TREATMENT OUTCOME;

AGED; AGING; BLOOD GLUCOSE; BODY COMPOSITION; DIET; EXERCISE; EXERCISE THERAPY; FEMALE; GLYCEMIC INDEX; HUMANS; INSULIN; INSULIN RESISTANCE; LIFE STYLE; LIPID PEROXIDATION; MALE; MIDDLE AGED; MUSCLE, SKELETAL; OBESITY; TREATMENT OUTCOME;

EID: 80052062344     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00221.2011     Document Type: Article

References (38)

1. Amati F, Dube JJ, Coen PM, Stefanovic-Racic M, Toledo FG, Goodpaster BH. Physical inactivity and obesity underlie the insulin resistance of aging. Diabetes Care 32: 1547-1549, 2009.
2. Boesch C, Machann J, Vermathen P, Schick F. Role of proton MR for the study of muscle lipid metabolism. NMR Biomed 19: 968-988, 2006.
3. Boesch C, Slotboom J, Hoppeler H, Kreis R. In vivo determination of intra-myocellular lipids in human muscle by means of localized 1H-MRspectroscopy. Magn Reson Med 37: 484-493, 1997.
4. Bottomley PA, Lee Y, Weiss RG. Total creatine in muscle: imaging and quantification with proton MR spectroscopy. Radiology 204: 403-410, 1997.
5. Brechtel K, Machann J, Jacob S, Strempfer A, Schick F, Haring HU, Claussen CD. [In-vivo 1H-MR spectroscopy: the determination of the intra- and extramyocellular lipid content depending on the insulin effect in the direct offspring of type-2 diabetics]. ROFO 171: 113-120, 1999.
6. Cui MH, Hwang JH, Tomuta V, Dong Z, Stein DT. Cross contamination of intramyocellular lipid signals through loss of bulk magnetic susceptibility effect differences in human muscle using (1)H-MRSI at 4 T. J Appl Physiol 103: 1290-1298, 2007.
7. Dube J, Goodpaster BH. Assessment of intramuscular triglycerides: contribution to metabolic abnormalities. Curr Opin Clin Nutr Metab Care 9: 553-559, 2006.
8. Dube JJ, Amati F, Stefanovic-Racic M, Toledo FG, Sauers SE, Goodpaster BH. Exercise-induced alterations in intramyocellular lipids and insulin resistance: the athlete's paradox revisited. Am J Physiol Endocrinol Metab 294: E882-E888, 2008.
9. Goodpaster BH, He J, Watkins S, 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.
10. Goodpaster BH, Kelley DE. Skeletal muscle triglyceride: marker or mediator of obesity-induced insulin resistance in type 2 diabetes mellitus? Curr Diab Rep 2: 216-222, 2002.
11. Houmard JA, Shaw CD, Hickey MS, Tanner CJ. Effect of short-term exercise training on insulin-stimulated PI 3-kinase activity in human skeletal muscle. Am J Physiol Endocrinol Metab 277: E1055-E1060, 1999.
12. Khuu A, Ren J, Dimitrov I, Woessner D, Murdoch J, Sherry AD, Malloy CR. Orientation of lipid strands in the extracellular compartment of muscle: effect on quantitation of intramyocellular lipids. Magn Reson Med 61: 16-21, 2009.
13. Kirwan JP, Solomon TP, Wojta DM, Staten MA, Holloszy JO. Effects of 7 days of exercise training on insulin sensitivity and responsiveness in type 2 diabetes mellitus. Am J Physiol Endocrinol Metab 297: E151-E156, 2009.
14. Kraniou GN, Cameron-Smith D, Hargreaves M. Effect of short-term training on GLUT-4 mRNA and protein expression in human skeletal muscle. Exp Physiol 89: 559-563, 2004.
15. Krssak M, Falk Petersen K, Dresner A, DiPietro L, Vogel SM, Rothman DL, Roden M, Shulman GI. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. [erratum appears in Diabetologia 1999 Mar; 42(3): 386]. Diabetologia 42: 113-116, 1999.
16. Lawrence JC, Newcomer BR, Buchthal SD, Sirikul B, Oster RA, Hunter GR, Gower BA. Relationship of intramyocellular lipid to insulin sensitivity may differ with ethnicity in healthy girls and women. Obesity (Silver Spring) 19: 43-48, 2011.
17. Ludwig DS. The glycemic index: physiological mechanisms relating to obesity, diabetes, and cardiovascular disease. JAMA 287: 2414-2423, 2002.
18. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and betacell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412-419, 1985.
19. Meex RC, Schrauwen-Hinderling VB, Moonen-Kornips E, Schaart G, Mensink M, Phielix E, van de Weijer T, Sels JP, Schrauwen P, Hesselink MK. Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity. Diabetes 59: 572-579, 2010.
20. Perseghin G, Scifo P, De Cobelli F, Pagliato E, Battezzati A, Arcelloni C, Vanzulli A, Testolin G, Pozza G, Del Maschio A, Luzi L. Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 48: 1600-1606, 1999.
21. Rico-Sanz J, Hajnal JV, Thomas EL, Mierisova S, Ala-Korpela M, Bell JD. Intracellular and extracellular skeletal muscle triglyceride metabolism during alternating intensity exercise in humans. J Physiol 510: 615-622, 1998.
22. Schenk S, Horowitz JF. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest 117: 1690-1698, 2007.
23. Schick F, Eismann B, Jung WI, Bongers H, Bunse M, Lutz O. Comparison of localized proton NMR signals of skeletal muscle and fat tissue in vivo: two lipid compartments in muscle tissue. Magn Reson Med 29: 158-167, 1993.
24. Schrauwen-Hinderling VB, Hesselink MK, Moonen-Kornips E, Schaart G, Kooi ME, Saris WH, Schrauwen P. Short-term training is accompanied by a down regulation of ACC2 mRNA in skeletal muscle. Int J Sports Med 27: 786-791, 2006.
25. Schrauwen-Hinderling VB, Schrauwen P, Hesselink MK, van Engelshoven JM, Nicolay K, Saris WH, Kessels AG, Kooi ME. The increase in intramyocellular lipid content is a very early response to training. J Clin Endocrinol Metab 88: 1610-1616, 2003.
26. Schrauwen-Hinderling VB, van Loon LJ, Koopman R, Nicolay K, Saris WH, Kooi ME. Intramyocellular lipid content is increased after exercise in nonexercising human skeletal muscle. J Appl Physiol 95: 2328-2332, 2003.
27. Shaw CS, Clark J, Wagenmakers AJ. The effect of exercise and nutrition on intramuscular fat metabolism and insulin sensitivity. Annu Rev Nutr 30: 13-34, 2010.
28. Sinha R, Dufour S, Petersen KF, LeBon V, Enoksson S, Ma YZ, Savoye M, Rothman DL, Shulman GI, Caprio S. Assessment of skeletal muscle triglyceride content by (1)H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes 51: 1022-1027, 2002.
29. Solomon TP, Haus JM, Kelly KR, Cook MD, Filion J, Rocco M, Kashyap SR, Watanabe RM, Barkoukis H, Kirwan JP. A low-glycemic index diet combined with exercise reduces insulin resistance, postprandial hyperinsulinemia, and glucose-dependent insulinotropic polypeptide responses in obese, prediabetic humans. Am J Clin Nutr 92: 1359-1368, 2010.
30. Solomon TP, Haus JM, Kelly KR, Cook MD, Riccardi M, Rocco M, Kashyap SR, Barkoukis H, Kirwan JP. Randomized trial on the effects of a 7-d low-glycemic diet and exercise intervention on insulin resistance in older obese humans. Am J Clin Nutr 90: 1222-1229, 2009.
31. Solomon TP, Sistrun SN, Krishnan RK, Del Aguila LF, Marchetti CM, O'Carroll SM, O'Leary VB, Kirwan JP. Exercise and diet enhance fat oxidation and reduce insulin resistance in older obese adults. J Appl Physiol 104: 1313-1319, 2008.
32. Stevenson EJ, Thelwall PE, Thomas K, Smith F, Brand-Miller J, Trenell MI. Dietary glycemic index influences lipid oxidation but not muscle or liver glycogen oxidation during exercise. Am J Physiol Endocrinol Metab 296: E1140-E1147, 2009.
33. Szczepaniak LS, Dobbins RL, Stein DT, McGarry JD. Bulk magnetic susceptibility effects on the assessment of intra- and extramyocellular lipids in vivo. Magn Reson Med 47: 607-610, 2002.
34. Tanner CJ, Koves TR, Cortright RL, Pories WJ, Kim YB, Kahn BB, Dohm GL, Houmard JA. Effect of short-term exercise training on insulin-stimulated PI 3-kinase activity in middle-aged men. Am J Physiol Endocrinol Metab 282: E147-E153, 2002.
35. Trenell MI, Stevenson E, Stockmann K, Brand-Miller J. Effect of high and low glycaemic index recovery diets on intramuscular lipid oxidation during aerobic exercise. Br J Nutr 99: 326-332, 2008.
36. van Loon LJ, Thomason-Hughes M, Constantin-Teodosiu D, Koopman R, Greenhaff PL, Hardie DG, Keizer HA, Saris WH, Wagenmakers AJ. Inhibition of adipose tissue lipolysis increases intramuscular lipid and glycogen use in vivo in humans. Am J Physiol Endocrinol Metab 289: E482-E493, 2005.
37. Virkamaki A, Korsheninnikova E, Seppala-Lindroos A, Vehkavaara S, Goto T, Halavaara J, Hakkinen AM, Yki-Jarvinen H. Intramyocellular lipid is associated with resistance to in vivo insulin actions on glucose uptake, antilipolysis, and early insulin signaling pathways in human skeletal muscle. Diabetes 50: 2337-2343, 2001.
38. Wadley GD, Konstantopoulos N, Macaulay L, Howlett KF, Garnham A, Hargreaves M, Cameron-Smith D. Increased insulin-stimulated Akt pSer473 and cytosolic SHP2 protein abundance in human skeletal muscle following acute exercise and short-term training. J Appl Physiol 102: 1624-1631, 2007.