Both Higher Fitness Level and Higher Current Physical Activity Level May Be Required for Intramyocellular Lipid Accumulation in Non-athlete Men

Overview

Journal Sci Rep

Specialty Science

Date 2020 Mar 7

PMID 32139784

Authors

Nozomu Yamasaki

Yoshifumi Tamura

Kageumi Takeno

Saori Kakehi

Yuki Someya

Takashi Funayama

Yasuhiko Furukawa

Hideyoshi Kaga

Ruriko Suzuki

Daisuke Sugimoto

Satoshi Kadowaki

Motonori Sato

Takashi Nakagata

Miho Nishitani-Yokoyama

Kazunori Shimada

Hiroyuki Daida

Shigeki Aoki

Hiroaki Satoh

Ryuzo Kawamori

Hirotaka Watada

Affiliations

Soon will be listed here.

Abstract

Accumulation of intramyocellular lipid (IMCL) is observed in individuals with insulin resistance as well as insulin-sensitive endurance athletes with high peak oxygen consumption (VOpeak), which is called the athlete's paradox. It remains unclear whether non-athletes with higher fitness levels have IMCL accumulation and higher insulin sensitivity in general. In this study, we investigated the association between IMCL accumulation and muscle insulin sensitivity (M-IS) in subjects with high or low VOpeak. We studied 61 nonobese (BMI, 23 to 25 kg/m), non-athlete Japanese men. We divided the subjects into four groups based on the median value of VOpeak and IMCL in the soleus muscle. We evaluated M-IS using a two-step hyperinsulinemic-euglycemic clamp. Among subjects with higher VOpeak (n = 32), half of those (n = 16) had lower IMCL levels. Both High-VOpeak groups had higher M-IS than the Low-VOpeak groups. On the other hand, M-IS was comparable between the High-VOpeak/High-IMCL and High-VOpeak/Low-IMCL groups, whereas the High-VOpeak/High-IMCL group had IMCL levels that were twice as high as those in the High-VOpeak/Low-IMCL group. On the other hand, the High-VOpeak/High-IMCL group had significantly higher physical activity levels (approximately 1.8-fold) than the other three groups. In conclusion, in nonobese, non-athlete Japanese men, subjects with higher VOpeak and higher IMCL had higher physical activity levels. IMCL accumulation is not associated with insulin resistance in individuals with higher or lower fitness levels.

References

Thamer C, Machann J, Bachmann O, Haap M, Dahl D, Wietek B . Intramyocellular lipids: anthropometric determinants and relationships with maximal aerobic capacity and insulin sensitivity. J Clin Endocrinol Metab. 2003; 88(4):1785-91. DOI: 10.1210/jc.2002-021674. View

Okada-Iwabu M, Yamauchi T, Iwabu M, Honma T, Hamagami K, Matsuda K . A small-molecule AdipoR agonist for type 2 diabetes and short life in obesity. Nature. 2013; 503(7477):493-9. DOI: 10.1038/nature12656. View

Turban S, Hajduch E . Protein kinase C isoforms: mediators of reactive lipid metabolites in the development of insulin resistance. FEBS Lett. 2010; 585(2):269-74. DOI: 10.1016/j.febslet.2010.12.022. View

Pruchnic R, Katsiaras A, He J, Kelley D, Winters C, Goodpaster B . Exercise training increases intramyocellular lipid and oxidative capacity in older adults. Am J Physiol Endocrinol Metab. 2004; 287(5):E857-62. DOI: 10.1152/ajpendo.00459.2003. View

Pan D, Lillioja S, Kriketos A, Milner M, Baur L, Bogardus C . Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes. 1997; 46(6):983-8. DOI: 10.2337/diab.46.6.983. View

Tamura Y, Watada H, Igarashi Y, Nomiyama T, Onishi T, Takahashi K . Short-term effects of dietary fat on intramyocellular lipid in sprinters and endurance runners. Metabolism. 2008; 57(3):373-9. DOI: 10.1016/j.metabol.2007.10.013. View

Kotronen A, Seppala-Lindroos A, Bergholm R, Yki-Jarvinen H . Tissue specificity of insulin resistance in humans: fat in the liver rather than muscle is associated with features of the metabolic syndrome. Diabetologia. 2007; 51(1):130-8. DOI: 10.1007/s00125-007-0867-x. View

Kantartzis K, Peter A, Machicao F, Machann J, Wagner S, Konigsrainer I . Dissociation between fatty liver and insulin resistance in humans carrying a variant of the patatin-like phospholipase 3 gene. Diabetes. 2009; 58(11):2616-23. PMC: 2768178. DOI: 10.2337/db09-0279. View

Schenk S, Horowitz J . Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest. 2007; 117(6):1690-8. PMC: 1866251. DOI: 10.1172/JCI30566. View

10.

Sakurai Y, Tamura Y, Takeno K, Kumashiro N, Sato F, Kakehi S . Determinants of intramyocellular lipid accumulation after dietary fat loading in non-obese men. J Diabetes Investig. 2014; 2(4):310-7. PMC: 4014973. DOI: 10.1111/j.2040-1124.2010.00091.x. View

11.

Krssak M, Falk Petersen K, Dresner A, Dipietro L, Vogel S, Rothman D . Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia. 1999; 42(1):113-6. DOI: 10.1007/s001250051123. View

12.

Kelley D, McKolanis T, Hegazi R, Kuller L, Kalhan S . Fatty liver in type 2 diabetes mellitus: relation to regional adiposity, fatty acids, and insulin resistance. Am J Physiol Endocrinol Metab. 2003; 285(4):E906-16. DOI: 10.1152/ajpendo.00117.2003. View

13.

Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J . Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 1999; 257(1):79-83. DOI: 10.1006/bbrc.1999.0255. View

14.

Abdul-Ghani M, DeFronzo R . Fasting hyperglycemia impairs glucose- but not insulin-mediated suppression of glucagon secretion. J Clin Endocrinol Metab. 2007; 92(5):1778-84. DOI: 10.1210/jc.2006-1515. View

15.

Dube J, Goodpaster B . Assessment of intramuscular triglycerides: contribution to metabolic abnormalities. Curr Opin Clin Nutr Metab Care. 2006; 9(5):553-9. DOI: 10.1097/01.mco.0000241664.38385.12. View

16.

Ring-Dimitriou S, Paulweber B, von Duvillard S, Stadlmann M, LeMura L, Lang J . The effect of physical activity and physical fitness on plasma adiponectin in adults with predisposition to metabolic syndrome. Eur J Appl Physiol. 2006; 98(5):472-81. DOI: 10.1007/s00421-006-0291-9. View

17.

Kobayashi S, Honda S, Murakami K, Sasaki S, Okubo H, Hirota N . Both comprehensive and brief self-administered diet history questionnaires satisfactorily rank nutrient intakes in Japanese adults. J Epidemiol. 2012; 22(2):151-9. PMC: 3798594. DOI: 10.2188/jea.je20110075. View

18.

Petersen M, Shulman G . Mechanisms of Insulin Action and Insulin Resistance. Physiol Rev. 2018; 98(4):2133-2223. PMC: 6170977. DOI: 10.1152/physrev.00063.2017. View

19.

Dube J, Amati F, Stefanovic-Racic M, Toledo F, Sauers S, Goodpaster B . Exercise-induced alterations in intramyocellular lipids and insulin resistance: the athlete's paradox revisited. Am J Physiol Endocrinol Metab. 2008; 294(5):E882-8. PMC: 3804891. DOI: 10.1152/ajpendo.00769.2007. View

20.

Iwabu M, Yamauchi T, Okada-Iwabu M, Sato K, Nakagawa T, Funata M . Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1. Nature. 2010; 464(7293):1313-9. DOI: 10.1038/nature08991. View