Ectopic lipid storage in non-alcoholic fatty liver disease is not mediated by impaired mitochondrial oxidative capacity in skeletal muscle

Clinical Science

Volumn 127, Issue 12, 2014, Pages 655-663

  Cuthbertson, Daniel J ^a   Irwin, Andrew ^a   Sprung, Victoria S ^a,b   Jones, Helen ^b   Pugh, Christopher J A ^b   Daousi, Christina ^a   Adams, Valerie L ^a   Bimson, William E ^a   Shojaee Moradie, Fariba ^c   Richardson, Paul ^d   Umpleby, A Margot ^c   Wilding, John P ^a   Kemp, Graham J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF SURREY   (United Kingdom)

^d ROYAL LIVERPOOL UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

Lipid deposition; Mitochondrial function; Non alcoholic fatty liver disease; Skeletal muscle

Indexed keywords

CREATINE PHOSPHATE;

ADULT; ARTICLE; BODY COMPOSITION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; INTRAABDOMINAL FAT; LIPID STORAGE; MALE; METABOLIC SYNDROME X; MITOCHONDRION; NONALCOHOLIC FATTY LIVER; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATION; PREVALENCE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; QUADRICEPS FEMORIS MUSCLE; SKELETAL MUSCLE; SOLEUS MUSCLE; SUBCUTANEOUS FAT; TIBIALIS ANTERIOR MUSCLE;

ADULT; BODY COMPOSITION; CROSS-SECTIONAL STUDIES; FATTY LIVER; FEMALE; HUMANS; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; LIPID METABOLISM; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MIDDLE AGED; MITOCHONDRIA; MUSCLE, SKELETAL; SUBCUTANEOUS FAT;

EID: 84905905886     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20130404     Document Type: Article

References (39)

1. Marchesini, G., Brizi, M., Bianchi, G., Tomassetti, S., Bugianesi, E., Lenzi, M., McCullough, A. J., Natale, S., Forlani, G. and Melchionda, N. (2001) Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes 50, 1844-1850
2. Petersen, K. F., Dufour, S., Savage, D. B., Bilz, S., Solomon, G., Yonemitsu, S., Cline, G. W., Befroy, D., Zemany, L., Kahn, B. B., Papademetris, X., Rothman, D. L. and Shulman, G. I. (2007) The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc. Natl. Acad. Sci. U.S.A. 104, 12587-12594
3. Rabol, R., Petersen, K. F., Dufour, S., Flannery, C. and Shulman, G. I. (2011) Reversal of muscle insulin resistance with exercise reduces postprandial hepatic de novo lipogenesis in insulin resistant individuals. Proc. Natl. Acad. Sci. U.S.A. 108, 13705-13709
4. Kantartzis, K., Machann, J., Schick, F., Fritsche, A., Haring, H. U. and Stefan, N. (2010) The impact of liver fat vs visceral fat in determining categories of prediabetes. Diabetologia 53, 882-889
5. Samuel, V. T., Petersen, K. F. and Shulman, G. I. (2010) Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375, 2267-2277
6. Johannsen, D. L., Conley, K. E., Bajpeyi, S., Punyanitya, M., Gallagher, D., Zhang, Z., Covington, J., Smith, S. R. and Ravussin, E. (2012) Ectopic lipid accumulation and reduced glucose tolerance in elderly adults are accompanied by altered skeletal muscle mitochondrial activity. J. Clin. Endocrinol. Metab. 97, 242-250
7. Szendroedi, J., Kaul, K., Kloock, L., Strassburger, K., Schmid, A. I., Chmelik, M., Kacerovsky, M., Kacerovsky-Bielesz, G., Prikoszovich, T., Brehm, A. et al. (2014) Lower fasting muscle mitochondrial activity relates to hepatic steatosis in humans. Diabetes Care 37, 468-474
8. Prikoszovich, T., Winzer, C., Schmid, A. I., Szendroedi, J., Chmelik, M., Pacini, G., Krssak, M., Moser, E., Funahashi, T., Waldhausl, W., Kautzky-Willer, A. and Roden, M. (2011) Body and liver fat mass rather than muscle mitochondrial function determine glucose metabolism in women with a history of gestational diabetes mellitus. Diabetes Care 34, 430-436
9. Machado, M. V., Ferreira, D. M., Castro, R. E., Silvestre, A. R., Evangelista, T., Coutinho, J., Carepa, F., Costa, A., Rodrigues, C. M. and Cortez-Pinto, H. (2012) Liver and muscle in morbid obesity: the interplay of fatty liver and insulin resistance. PLoS ONE 7, e31738
10. Kemp, G. J. and Brindle, K. M. (2012) What do magnetic resonance-based measurements of Pi→ATP flux tell us about skeletal muscle metabolism?. Diabetes 61, 1927-1934
11. Browning, J. D., Szczepaniak, L. S., Dobbins, R., Nuremberg, P., Horton, J. D., Cohen, J. C., Grundy, S. M. and Hobbs, H. H. (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40, 1387-1395
12. Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III) (2001) Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 285, 2486-2497
13. Bruce, R. A., Kusumi, F. and Hosmer, D. (1973) Maximal oxygen intake and nomographic assessment of functional aerobic impairment in cardiovascular disease. Am. Heart J. 85, 546-562
14. Borg, G. (1998) Borg's Perceived Exertion and Pain Scales, Human Kinetics Publishers
15. Gardner, C. J., Irwin, A. J., Daousi, C., McFarlane, I. A., Joseph, F., Bell, J. D., Thomas, E. L., Adams, V. L., Kemp, G. J. and Cuthbertson, D. J. (2012) Hepatic steatosis, GH deficiency and the effects of GH replacement: a Liverpool magnetic resonance spectroscopy study. Eur. J. Endocrinol. 166, 993-1002
16. Gardner, C. J., Richardson, P., Wong, C., Polavarapu, N., Kemp, G. J. and Cuthbertson, D. J. (2011) Hypothyroidism in a patient with non-alcoholic fatty liver disease. BMJ 342, c7199
17. Jones, H., Sprung, V. S., Pugh, C. J., Daousi, C., Irwin, A., Aziz, N., Adams, V. L., Thomas, E. L., Bell, J. D., Kemp, G. J. and Cuthbertson, D. J. (2012) Polycystic ovary syndrome with hyperandrogenism is characterized by an increased risk of hepatic steatosis compared to nonhyperandrogenic PCOS phenotypes and healthy controls, independent of obesity and insulin resistance. J. Clin. Endocrinol. Metab. 97, 3709-3716
18. Cuthbertson, D. J., Irwin, A., Gardner, C. J., Daousi, C., Purewal, T., Furlong, N., Goenka, N., Thomas, E. L., Adams, V. L., Pushpakom, S. P. et al. (2012) Improved glycaemia correlates with liver fat reduction in obese, type 2 diabetes, patients given glucagon-like peptide-1 (GLP-1) receptor agonists. PLoS ONE 7, e50117
19. Kemp, G. J., Roberts, N., Bimson, W. E., Bakran, A., Harris, P. L., Gilling-Smith, G. L., Brennan, J., Rankin, A. and Frostick, S. P. (2001) Mitochondrial function and oxygen supply in normal and in chronically ischemic muscle: a combined 31P magnetic resonance spectroscopy and near infrared spectroscopy study in vivo. J. Vasc. Surg. 34, 1103-1110
20. Sleigh, A., Stears, A., Thackray, K., Watson, L., Gambineri, A., Nag, S., Campi, V. I., Schoenmakers, N., Brage, S., Carpenter, T. A. et al. (2012) Mitochondrial oxidative phosphorylation is impaired in patients with congenital lipodystrophy. J. Clin. Endocrinol. Metab. 97, E438-442
21. Bajpeyi, S., Pasarica, M., Moro, C., Conley, K., Jubrias, S., Sereda, O., Burk, D. H., Zhang, Z., Gupta, A., Kjems, L. and Smith, S. R. (2011) Skeletal muscle mitochondrial capacity and insulin resistance in type 2 diabetes. J. Clin. Endocrinol. Metab. 96, 1160-1168
22. Praet, S. F., De Feyter, H. M., Jonkers, R. A., Nicolay, K., van Pul, C., Kuipers, H., van Loon, L. J. and Prompers, J. J. (2006) 31P MR spectroscopy and in vitro markers of oxidative capacity in type 2 diabetes patients. Magma 19, 321-331
23. Petersen, K. F., Dufour, S., Befroy, D., Garcia, R. and Shulman, G. I. (2004) Impaired mitochondrial activity in the insulinresistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350, 664-671
24. 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. (2005) Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J. Clin. Invest. 115, 3587-3593
25. Hancock, C. R., Han, D. H., Chen, M., Terada, S., Yasuda, T., Wright, D. C. and Holloszy, J. O. (2008) High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc. Natl. Acad. Sci. U.S.A. 105, 7815-7820
26. Toledo, F. G., Menshikova, E. V., Azuma, K., Radikova, Z., Kelley, C. A., Ritov, V. B. and Kelley, D. E. (2008) Mitochondrial capacity in skeletal muscle is not stimulated by weight loss despite increases in insulin action and decreases in intramyocellular lipid content. Diabetes 57, 987-994
27. Sleigh, A., Raymond-Barker, P., Thackray, K., Porter, D., Hatunic, M., Vottero, A., Burren, C., Mitchell, C., McIntyre, M., Brage, S. et al. (2011) Mitochondrial dysfunction in patients with primary congenital insulin resistance. J. Clin. Invest. 121, 2457-2461
28. Sinha, R., Dufour, S., Petersen, K. F., LeBon, V., Enoksson, S., Ma, Y. Z., Savoye, M., Rothman, D. L., Shulman, G. I. and Caprio, S. (2002) Assessment of skeletal muscle triglyceride content by 1H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes 51, 1022-1027
29. Thomas, E. L., Hamilton, G., Patel, N., O'Dwyer, R., Dore, C. J., Goldin, R. D., Bell, J. D. and Taylor-Robinson, S. D. (2005) Hepatic triglyceride content and its relation to body adiposity: a magnetic resonance imaging and proton magnetic resonance spectroscopy study. Gut 54, 122-127
30. Brehm, A., Krssak, M., Schmid, A. I., Nowotny, P., Waldhausl, W. and Roden, M. (2006) Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 55, 136-140
31. Szendroedi, J., Schmid, A. I., Chmelik, M., Toth, C., Brehm, A., Krssak, M., Nowotny, P., Wolzt, M., Waldhausl, W. and Roden, M. (2007) Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med. 4, e154
32. Kacerovsky, M., Brehm, A., Chmelik, M., Schmid, A. I., Szendroedi, J., Kacerovsky-Bielesz, G., Nowotny, P., Lettner, A., Wolzt, M., Jones, J. G. and Roden, M. (2011) Impaired insulin stimulation of muscular ATP production in patients with type 1 diabetes. J. Intern. Med. 269, 189-199
33. Kacerovsky-Bielesz, G., Kacerovsky, M., Chmelik, M., Farukuoye, M., Ling, C., Pokan, R., Tschan, H., Szendroedi, J., Schmid, A. I., Gruber, S. et al. (2012) A single nucleotide polymorphism associates with the response of muscle ATP synthesis to long-term exercise training in relatives of type 2 diabetic humans. Diabetes Care 35, 350-357
34. Szendroedi, J., Zwettler, E., Schmid, A. I., Chmelik, M., Pacini, G., Kacerovsky, G., Smekal, G., Nowotny, P., Wagner, O., Schnack, C. et al. (2008) Reduced basal ATP synthetic flux of skeletal muscle in patients with previous acromegaly. PLoS ONE 3, e3958
35. Schmid, A. I., Schrauwen-Hinderling, V. B., Andreas, M., Wolzt, M., Moser, E. and Roden, M. (2012) Comparison of measuring energy metabolism by different 31P-magnetic resonance spectroscopy techniques in resting, ischemic, and exercising muscle. Magn. Reson. Med. 67, 898-905
36. Befroy, D. E., Rothman, D. L., Petersen, K. F. and Shulman, G. I. (2012) 31P-magnetization transfer magnetic resonance spectroscopy measurements of in vivo metabolism. Diabetes 61, 2669-2678
37. Korenblat, K. M., Fabbrini, E., Mohammed, B. S. and Klein, S. (2008) Liver, muscle, and adipose tissue insulin action is directly related to intrahepatic triglyceride content in obese subjects. Gastroenterology 134, 1369-1375
38. Lomonaco, R., Ortiz-Lopez, C., Orsak, B., Webb, A., Hardies, J., Darland, C., Finch, J., Gastaldelli, A., Harrison, S., Tio, F. and Cusi, K. (2012) Effect of adipose tissue insulin resistance on metabolic parameters and liver histology in obese patients with nonalcoholic fatty liver disease. Hepatology 55, 1389-1397
39. Alligier, M., Gabert, L., Meugnier, E., Lambert-Porcheron, S., Chanseaume, E., Pilleul, F., Debard, C., Sauvinet, V., Morio, B., Vidal-Puig, A. et al. (2013) Visceral fat accumulation during lipid overfeeding is related to subcutaneous adipose tissue characteristics in healthy men. J. Clin. Endocrinol. Metab. 98, 802-810