Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes - PubMed (original) (raw)
Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes
B H Goodpaster et al. J Clin Endocrinol Metab. 2001 Dec.
Abstract
We examined the hypothesis that an excess accumulation of intramuscular lipid (IMCL) is associated with insulin resistance and that this may be mediated by the oxidative capacity of muscle. Nine sedentary lean (L) and 11 obese (O) subjects, 8 obese subjects with type 2 diabetes mellitus (D), and 9 lean, exercise-trained (T) subjects volunteered for this study. Insulin sensitivity (M) determined during a hyperinsulinemic (40 mU x m(-2)min(-1)) euglycemic clamp was greater (P < 0.01) in L and T, compared with O and D (9.45 +/- 0.59 and 10.26 +/- 0.78 vs. 5.51 +/- 0.61 and 1.15 +/- 0.83 mg x min(-1)kg fat free mass(-1), respectively). IMCL in percutaneous vastus lateralis biopsy specimens by quantitative image analysis of Oil Red O staining was approximately 2-fold higher in D than in L (3.04 +/- 0.39 vs. 1.40 +/- 0.28% area as lipid; P < 0.01). IMCL was also higher in T (2.36 +/- 0.37), compared with L (P < 0.01). The oxidative capacity of muscle determined with succinate dehydrogenase staining of muscle fibers was higher in T, compared with L, O, and D (50.0 +/- 4.4, 36.1 +/- 4.4, 29.7 +/- 3.8, and 33.4 +/- 4.7 optical density units, respectively; P < 0.01). IMCL was negatively associated with M (r = -0.57, P < 0.05) when endurance-trained subjects were excluded from the analysis, and this association was independent of body mass index. However, the relationship between IMCL and M was not significant when trained individuals were included. There was a positive association between the oxidative capacity and M among nondiabetics (r = 0.37, P < 0.05). In summary, skeletal muscle of trained endurance athletes is markedly insulin sensitive and has a high oxidative capacity, despite having an elevated lipid content. In conclusion, the capacity for lipid oxidation may be an important mediator of the association between excess muscle lipid accumulation and insulin resistance.
Similar articles
- Intramyocellular lipid content in type 2 diabetes patients compared with overweight sedentary men and highly trained endurance athletes.
van Loon LJ, Koopman R, Manders R, van der Weegen W, van Kranenburg GP, Keizer HA. van Loon LJ, et al. Am J Physiol Endocrinol Metab. 2004 Sep;287(3):E558-65. doi: 10.1152/ajpendo.00464.2003. Epub 2004 May 27. Am J Physiol Endocrinol Metab. 2004. PMID: 15165998 - Endurance training modulates intramyocellular lipid compartmentalization and morphology in skeletal muscle of lean and obese women.
Devries MC, Samjoo IA, Hamadeh MJ, McCready C, Raha S, Watt MJ, Steinberg GR, Tarnopolsky MA. Devries MC, et al. J Clin Endocrinol Metab. 2013 Dec;98(12):4852-62. doi: 10.1210/jc.2013-2044. Epub 2013 Sep 30. J Clin Endocrinol Metab. 2013. PMID: 24081737 - Exercise training increases intramyocellular lipid and oxidative capacity in older adults.
Pruchnic R, Katsiaras A, He J, Kelley DE, Winters C, Goodpaster BH. Pruchnic R, et al. Am J Physiol Endocrinol Metab. 2004 Nov;287(5):E857-62. doi: 10.1152/ajpendo.00459.2003. Epub 2004 Jun 29. Am J Physiol Endocrinol Metab. 2004. PMID: 15226098 Clinical Trial. - Increased intramuscular lipid storage in the insulin-resistant and endurance-trained state.
van Loon LJ, Goodpaster BH. van Loon LJ, et al. Pflugers Arch. 2006 Feb;451(5):606-16. doi: 10.1007/s00424-005-1509-0. Epub 2005 Sep 10. Pflugers Arch. 2006. PMID: 16155759 Review. - Intramyocellular lipid content in human skeletal muscle.
Schrauwen-Hinderling VB, Hesselink MK, Schrauwen P, Kooi ME. Schrauwen-Hinderling VB, et al. Obesity (Silver Spring). 2006 Mar;14(3):357-67. doi: 10.1038/oby.2006.47. Obesity (Silver Spring). 2006. PMID: 16648604 Review.
Cited by
- Insulin Resistance, Obesity, and Lipotoxicity.
Yazıcı D, Demir SÇ, Sezer H. Yazıcı D, et al. Adv Exp Med Biol. 2024;1460:391-430. doi: 10.1007/978-3-031-63657-8_14. Adv Exp Med Biol. 2024. PMID: 39287860 Review. - Age-adjusted Charlson comorbidity index and its association with body composition and overall survival in patients with colorectal cancer.
de Oliveira Bezerra MR, de Sousa IM, Miranda AL, Ferreira GMC, Chaves GV, Verde SMML, Maurício SF, da Costa Pereira JP, Gonzalez MC, Prado CM, Fayh APT. de Oliveira Bezerra MR, et al. Support Care Cancer. 2024 Jul 16;32(8):517. doi: 10.1007/s00520-024-08730-w. Support Care Cancer. 2024. PMID: 39014284 - Nicotinamide N-methyltransferase inhibition mimics and boosts exercise-mediated improvements in muscle function in aged mice.
Dimet-Wiley AL, Latham CM, Brightwell CR, Neelakantan H, Keeble AR, Thomas NT, Noehren H, Fry CS, Watowich SJ. Dimet-Wiley AL, et al. Sci Rep. 2024 Jul 5;14(1):15554. doi: 10.1038/s41598-024-66034-9. Sci Rep. 2024. PMID: 38969654 Free PMC article. - The DNA methyltransferase inhibitor decitabine blunts the response to a high-animal fat and protein diet in mice.
Flores-Sierra JJ, Muciño-Arellano MDR, Romo-Morales GDC, Sánchez-Palafox JE, Correa-Navarro VA, Colín-Castelán D, Pérez-Vázquez V, Rangel-Salazar R, Rivera-Bustamante R, de la Rocha C, Rodríguez-Ríos D, Trejo-Saavedra DL, Molina-Torres J, Ramírez-Chávez E, García-Rojas NS, Winkler R, Lund G, Zaina S. Flores-Sierra JJ, et al. J Lipid Res. 2024 Aug;65(8):100586. doi: 10.1016/j.jlr.2024.100586. Epub 2024 Jun 26. J Lipid Res. 2024. PMID: 38942113 Free PMC article. - Intramuscular diacylglycerol accumulates with acute hyperinsulinemia in insulin-resistant phenotypes.
McKenna CF, Stierwalt HD, Zemski Berry KA, Ehrlicher SE, Robinson MM, Zarini S, Kahn DE, Snell-Bergeon JK, Perreault L, Bergman BC, Newsom SA. McKenna CF, et al. Am J Physiol Endocrinol Metab. 2024 Aug 1;327(2):E183-E193. doi: 10.1152/ajpendo.00368.2023. Epub 2024 Jun 19. Am J Physiol Endocrinol Metab. 2024. PMID: 38895980
Publication types
MeSH terms
Substances
Grants and funding
- 1P30DK46204/DK/NIDDK NIH HHS/United States
- 5M01RR00056/RR/NCRR NIH HHS/United States
- K01 AG00851/AG/NIA NIH HHS/United States
- R01 DK-49200-04/DK/NIDDK NIH HHS/United States
LinkOut - more resources
Full Text Sources
Other Literature Sources
Research Materials