Reversal of muscle insulin resistance by weight reduction in young, lean, insulin-resistant offspring of parents with type 2 diabetes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 21, 2012, Pages 8236-8240

  Petersen, Kitt Falk ^a   Dufour, Sylvie ^a   Morino, Katsutaro ^a   Yoo, Peter S ^a   Cline, Gary W ^a   Shulman, Gerald I ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adipocytokines; Diacylglycerols; Insulin sensitivity index; Mitochondria; Visceral fat

Indexed keywords

ACYLCARNITINE; ADIPONECTIN; ALANINE; ASPARTIC ACID; C PEPTIDE; C REACTIVE PROTEIN; CHOLESTEROL; FAT DROPLET; FATTY ACID; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; GLYCINE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; INTERLEUKIN 6; INTRAMYOCELLULAR LIPID; ISOLEUCINE; LACTIC ACID; LEPTIN; LEUCINE; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PHENYLALANINE; RECOMBINANT HUMAN INSULIN; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; TYROSINE; UNCLASSIFIED DRUG; URIC ACID; VALINE;

ADULT; ARTICLE; BODY MASS; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; FATTY ACID BLOOD LEVEL; FEMALE; GLUCOSE CLAMP TECHNIQUE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HUMAN; HYPERINSULINEMIA; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LACTATE BLOOD LEVEL; LEAN BODY WEIGHT; LIPID STORAGE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOGENESIS; PRIORITY JOURNAL; PROGENY; PROTON NUCLEAR MAGNETIC RESONANCE; TRIACYLGLYCEROL BLOOD LEVEL; URIC ACID BLOOD LEVEL; WEIGHT REDUCTION;

ADIPOKINES; ADULT; BLOOD GLUCOSE; BODY WEIGHT; CHILD OF IMPAIRED PARENTS; DIABETES MELLITUS, TYPE 2; DIET, REDUCING; DIGLYCERIDES; FEMALE; GLUCOSE CLAMP TECHNIQUE; GLUCOSE INTOLERANCE; HUMANS; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; MALE; MITOCHONDRIA; MUSCLE, SKELETAL; PARENTS; WEIGHT LOSS; YOUNG ADULT;

EID: 84861443900     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1205675109     Document Type: Article

References (48)

1. Lillioja S, et al. (1988) Impaired glucose tolerance as a disorder of insulin action. Longitudinal and cross-sectional studies in Pima Indians. N Engl J Med 318:1217-1225.
2. Lillioja S, et al. (1993) Insulin resistance and insulin secretory dysfunction as precursors of non-insulin-dependent diabetes mellitus. Prospective studies of Pima Indians. N Engl J Med 329:1988-1992. (Pubitemid 24015042)
3. Warram JH, Martin BC, Krolewski AS, Soeldner JS, Kahn CR (1990) Slow glucose removal rate and hyperinsulinemia precede the development of type II diabetes in the offspring of diabetic parents. Ann Intern Med 113:909-915.
4. Zimmet P, Alberti KG, Shaw J (2001) Global and societal implications of the diabetes epidemic. Nature 414:782-787. (Pubitemid 34000780)
5. Rothman DL, Shulman RG, Shulman GI (1992) 31P nuclear magnetic resonance measurements of muscle glucose-6-phosphate. Evidence for reduced insulin-dependent muscle glucose transport or phosphorylation activity in non-insulin-dependent diabetes mellitus. J Clin Invest 89:1069-1075.
6. Perseghin G, et al. (1996) Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects. N Engl J Med 335:1357-1362. (Pubitemid 26360454)
7. Cline GW, et al. (1999) Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes. N Engl J Med 341:240-246. (Pubitemid 29334522)
8. Morino K, et al. (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. (Pubitemid 43121847)
9. Krssak M, et al. (1999) Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: A 1H NMR spectroscopy study. Diabetologia 42:113-116. (Pubitemid 29039748)
10. Jacob S, et al. (1999) Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes 48:1113-1119. (Pubitemid 29226360)
11. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664-671. (Pubitemid 38364625)
12. Itani SI, Ruderman NB, Schmieder F, Boden G (2002) Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 51:2005-2011. (Pubitemid 34729001)
13. Perseghin G, et al. (1999) 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. (Pubitemid 29356869)
14. Shulman GI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106:171-176.
15. Morino K, Petersen KF, Shulman GI (2006) Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55(Suppl 2):S9-S15. (Pubitemid 44927027)
16. Samuel VT, Petersen KF, Shulman GI (2010) Lipid-induced insulin resistance: Unravelling the mechanism. Lancet 375:2267-2277.
17. Olefsky JM (2009) IKKepsilon: A bridge between obesity and inflammation. Cell 138:834-836.
18. Olefsky JM, Glass CK (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72:219-246.
19. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860-867.
20. Lin HV, et al. (2007) Adiponectin resistance exacerbates insulin resistance in insulin receptor transgenic/knockout mice. Diabetes 56:1969-1976. (Pubitemid 47195822)
21. Newgard CB, et al. (2009) A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 9:311-326.
22. Wang TJ, et al. (2011) Metabolite profiles and the risk of developing diabetes. Nat Med 17:448-453.
23. Koves TR, et al. (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7:45-56.
24. Petersen KF, et al. (2006) Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men. Proc Natl Acad Sci USA 103:18273-18277. (Pubitemid 44871648)
25. Bell JA, et al. (2010) Lipid partitioning, incomplete fatty acid oxidation, and insulin signal transduction in primary human muscle cells: Effects of severe obesity, fatty acid incubation, and fatty acid translocase/CD36 overexpression. J Clin Endocrinol Metab 95:3400-3410.
26. Shoelson SE, Herrero L, Naaz A (2007) Obesity, inflammation, and insulin resistance. Gastroenterology 132:2169-2180. (Pubitemid 46693756)
27. Petersen KF, et al. (2002) Leptin reverses insulin resistance and hepatic steatosis in patients with severe lipodystrophy. J Clin Invest 109:1345-1350. (Pubitemid 34546899)
28. Petersen KF, et al. (2005) Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes 54:603-608. (Pubitemid 40322060)
29. Lim EL, et al. (2011) Reversal of type 2 diabetes: normalisation of beta cell function in association with decreased pancreas and liver triacylglycerol. Diabetologia 54:2506-2514.
30. Yu C, et al. (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem 277:50230-50236. (Pubitemid 36042170)
31. Summers SA (2006) Ceramides in insulin resistance and lipotoxicity. Prog Lipid Res 45:42-72.
32. Choi CS, et al. (2008) Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc Natl Acad Sci USA 105:19926-19931.
33. Samuel VT, et al. (2004) Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem 279:32345-32353. (Pubitemid 39014687)
34. Samuel VT, et al. (2007) Inhibition of protein kinase C epsilon prevents hepatic insulin resistance in nonalcoholic fatty liver disease. J Clin Invest 117:739-745. (Pubitemid 46348532)
35. Li Y, et al. (2004) Protein kinase C Theta inhibits insulin signaling by phosphorylating IRS1 at Ser(1101). J Biol Chem 279:45304-45307. (Pubitemid 39491511)
36. Høeg LD, et al. (2011) Lipid-induced insulin resistance affects women less than men and is not accompanied by inflammation or impaired proximal insulin signaling. Diabetes 60:64-73.
37. Befroy DE, et al. (2007) Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56:1376-1381. (Pubitemid 46715630)
38. Mootha VK, et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267-273. (Pubitemid 36792858)
39. Patti ME, et al. (2003) 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. (Pubitemid 36842568)
40. Morino K, et al. (2012) Regulation of mitochondrial biogenesis by lipoprotein lipase in muscle of insulin-resistant offspring of parents with type 2 diabetes. Diabetes 61:877-887.
41. Wang YX, et al. (2004) Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2:e294.
42. Matsuda M, DeFronzo RA (1999) Insulin sensitivity indices obtained from oral glucose tolerance testing: Comparison with the euglycemic insulin clamp. Diabetes Care 22:1462-1470. (Pubitemid 29418240)
43. Petersen KF, et al. (1998) 13C/31P NMR studies on the mechanism of insulin resistance in obesity. Diabetes 47:381-386. (Pubitemid 28104199)
44. Gruetter R (1993) Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn Reson Med 29:804-811.
45. Rabøl R, Petersen KF, Dufour S, Flannery C, Shulman GI (2011) Reversal of muscle insulin resistance with exercise reduces postprandial hepatic de novo lipogenesis in insulin resistant individuals. Proc Natl Acad Sci USA 108:13705-13709.
46. Petersen KF, et al. (2003) Mitochondrial dysfunction in the elderly: Possible role in insulin resistance. Science 300:1140-1142. (Pubitemid 36583097)
47. Vernez L, Wenk M, Krähenbühl S (2004) Determination of carnitine and acylcarnitines in plasma by high-performance liquid chromatography/electrospray ionization ion trap tandem mass spectrometry. Rapid Commun Mass Spectrom 18:1233-1238. (Pubitemid 38702390)
48. Leimer KR, Rice RH, Gehrke CW (1977) Complete mass spectra of N-trifluoroacetyl-n-butyl esters of amino acids. J Chromatogr A 141:121-144.