Effects of high-fat overfeeding on mitochondrial function, glucose and fat metabolism, and adipokine levels in low-birth-weight subjects

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 1, 2012, Pages

  Brøns, Charlotte ^a   Jacobsen, Stine ^a   Hiscock, Natalie ^b   White, Andrew ^b   Nilsson, Emma ^a   Dunger, David ^c   Astrup, Arne ^d   Quistorff, Bjørn ^e   Vaag, Allan ^a  

^a STENO DIABETES CENTER   (Denmark)

^b UNILEVER RESEARCH   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Coactivator 1 ; Incretin hormones; Insulin resistance; Oxidative phosphorylation genes; Peroxisome proliferator activated receptor

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADIPOCYTOKINE; CREATINE PHOSPHATE; GASTRIC INHIBITORY POLYPEPTIDE; INSULIN; PANCREAS POLYPEPTIDE;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; GLUCOSE METABOLISM; HUMAN; INSULIN METABOLISM; INSULIN RELEASE; INSULIN RESISTANCE; LIPID DIET; LOW BIRTH WEIGHT; MALE; MITOCHONDRION; PRIORITY JOURNAL; SATIETY;

ADENOSINE TRIPHOSPHATE; ADIPOKINES; ADULT; CROSS-OVER STUDIES; DENMARK; DIABETES MELLITUS, TYPE 2; DIETARY FATS; GASTRIC INHIBITORY POLYPEPTIDE; GLUCOSE; HUMANS; INFANT, LOW BIRTH WEIGHT; INFANT, NEWBORN; INSULIN RESISTANCE; LEPTIN; LIPID METABOLISM; MALE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; PANCREATIC POLYPEPTIDE; PHOSPHOCREATINE; PROTEIN PRECURSORS; REGISTRIES; YOUNG ADULT;

EID: 83455243036     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00095.2011     Document Type: Article

References (40)

1. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsøe R, Dela F. Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50: 790-796, 2007.
2. Brehm A, Krssak M, Schmid AI, Nowotny P, Waldhäusl W, Roden M. Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 55: 136-140, 2006.
3. Brøns C, Jacobsen S, Nilsson E, Rönn T, Jensen CB, Storgaard H, Poulsen P, Groop L, Ling C, Astrup A, Vaag A. Deoxyribonucleic acid methylation and gene expression of PPARGC1A in human muscle is influenced by high-fat overfeeding in a birth-weight-dependent manner. J Clin Endocrinol Metab 95: 3048-3056, 2010.
4. Brøns C, Jensen CB, Storgaard H, Alibegovic A, Jacobsen S, Nilsson E, Astrup A, Quistorff B, Vaag A. Mitochondrial function in skeletal muscle is normal and unrelated to insulin action in young men born with low birth weight. J Clin Endocrinol Metab 93: 3885-3892, 2008.
5. Brøns C, Jensen CB, Storgaard H, Hiscock NJ, White A, Appel JS, Jacobsen S, Nilsson E, Larsen CM, Astrup A, Quistorff B, Vaag A. Impact of short-term high-fat feeding on glucose and insulin metabolism in young healthy men. J Physiol 587: 2387-2397, 2009.
6. Chanseaume E, Malpuech-Brugère C, Patrac V, Bielicki G, Rousset P, Couturier K, Salles J, Renou JP, Boirie Y, Morio B. Diets high in sugar, fat, and energy induce muscle type-specific adaptations in mitochondrial functions in rats. J Nutr 136: 2194-2200, 2006.
7. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 23: 599-622, 2002.
8. FAO. Food And Nutrition Technical Report Series 1: Human Energy Requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. Rome, Italy, 17-24 October 2001-2007.
9. Hales CN, Barker DJP. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35: 595-601, 1992.
10. Hancock CR, Han DH, Chen M, Terada S, Yasuda T, Wright DC, Holloszy JO. High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci USA 105: 7815-7820, 2008.
11. Hanson MA, Gluckman PD. Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol 102: 90-93, 2008.
12. Harder T, Rodekamp E, Schellong K, Dudenhausen JW, Plagemann A. Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol 165: 849-857, 2007.
13. Hermann TS, Rask-Madsen C, Ihlemann N, Domínguez H, Jensen CB, Storgaard H, Vaag AA, Kober L, Torp-Pedersen C. Normal insulin-stimulated endothelial function and impaired insulin-stimulated muscle glucose uptake in young adults with low birth weight. J Clin Endocrinol Metab 88: 1252-1257, 2003.
14. Jensen CB, Storgaard H, Dela F, Holst JJ, Madsbad S, Vaag AA. Early differential defects of insulin secretion and action in 19-year-old caucasian men who had low birth weight. Diabetes 51: 1271-1280, 2002.
15. Jensen CB, Storgaard H, Madsbad S, Richter EA, Vaag AA. Altered skeletal muscle fiber composition and size precede whole-body insulin resistance in young men with low birth weight. J Clin Endocrinol Metab 92: 1530-1534, 2007.
16. Jeppesen TD, Quistorff B, Wibrand F, Vissing J. 31P-MRS of skeletal muscle is not a sensitive diagnostic test for mitochondrial myopathy. J Neurol 254: 29-37, 2007.
17. Jørgensen W, Gam C, Andersen JL, Schjerling P, Scheibye-Knudsen M, Mortensen OH, Grunnet N, Nielsen MO, Quistorff B. Changed mitochondrial function by pre- and/or postpartum diet alterations in sheep. Am J Physiol Endocrinol Metab 297: E1349-E1357, 2009.
18. Kahn SE. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes. Diabetologia 46: 3-19, 2003.
19. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
20. Kelley DE, Mandarino LJ. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 49: 677-683, 2000.
21. Kraegen EW, Cooney GJ, Turner N. Muscle insulin resistance: a case of fat overconsumption, not mitochondrial dysfunction. Proc Natl Acad Sci USA 105: 7627-7628, 2008.
22. Lowell BB, Shulman GI. Mitochondrial dysfunction and type 2 diabetes. Science 307: 384-387, 2005.
23. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC. PGC- 1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273, 2003.
24. Muoio DM, Koves TR. Lipid-induced metabolic dysfunction in skeletal muscle. Novartis Found Symp 286: 24-38, 2007.
25. Nair KS, Bigelow ML, Asmann YW, Chow LS, Coenen-Schimke JM, Klaus KA, Guo ZK, Sreekumar R, Irving BA. Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance. Diabetes 57: 1166-1175, 2008.
26. Ozanne SE, Jensen CB, Tingey KJ, Martin-Gronert MS, Grunnet L, Brons C, Storgaard H, Vaag AA. Decreased protein levels of key insulin signalling molecules in adipose tissue from young men with a low birthweight: potential link to increased risk of diabetes? Diabetologia 49: 2993-2999, 2006.
27. Ozanne SE, Jensen CB, Tingey KJ, Storgaard H, Madsbad S, Vaag AA. Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia 48: 547-552, 2005.
28. Parillo M, Riccardi G. Diet composition and the risk of type 2 diabetes: epidemiological and clinical evidence. Br J Nutr 92: 7-19, 2004.
29. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, DeFronzo R, Finlayson J, Kahn CR, Mandarino LJ. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100: 8466-8471, 2003.
30. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, Shulman GI. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-1142, 2003.
31. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 664-671, 2004.
32. Polgar J, Johnson MA, Weightman D, Appleton D. Data on fibre size in thirty-six human muscles. An autopsy study. J Neurol Sci 19: 307-318, 1973.
33. Poulsen P, Wojtaszewski JF, Richter EA, Beck-Nielsen H, Vaag A. Low birth weight and zygosity status is associated with defective muscle glycogen and glycogen synthase regulation in elderly twins. Diabetes db07-0155, 2007.
34. Rabøl R, Larsen S, Højberg PM, Almdal T, Boushel R, Haugaard SB, Andersen JL, Madsbad S, Dela F. Regional anatomic differences in skeletal muscle mitochondrial respiration in type 2 diabetes and obesity. J Clin Endocrinol Metab 95: 857-863, 2010.
35. Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1: 785-789, 1963.
36. Rasmussen EL, Malis C, Jensen CB, Jensen JE, Storgaard H, Poulsen P, Pilgaard K, Schou JH, Madsbad S, Astrup A, Vaag A. Altered fat tissue distribution in young adult men who had low birth weight. Diabetes Care 28: 151-153, 2005.
37. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, Smith SR. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54: 1926-1933, 2005.
38. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS, Cooney GJ. Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56: 2085-2092, 2007.
39. Vaag A, Alford F, Henriksen FL, Christopher M, Beck-Nielsen H. Multiple defects of both hepatic and peripheral intracellular glucose processing contribute to the hyperglycaemia of NIDDM. Diabetologia 38: 326-336, 1995.
40. Wang J, Obici S, Morgan K, Barzilai N, Feng Z, Rossetti L. Overfeeding rapidly induces leptin and insulin resistance. Diabetes 50: 2786-2791, 2001.