Tissue-specific differences in the development of insulin resistance in a mouse model for type 1 diabetes

Diabetes

Volumn 63, Issue 11, 2014, Pages 3856-3867

  Jelenik, Tomas ^a   Séquaris, Gilles ^a   Kaul, Kirti ^a   Ouwens, D Margriet ^a,b   Phielix, Esther ^a   Kotzka, Jörg ^a   Knebel, Birgit ^a   Weiß, Jürgen ^a   Reinbeck, Anna Lena ^a   Janke, Linda ^a   Nowotny, Peter ^a   Partke, Hans Joachim ^a   Zhang, Dongyan ^c   Shulman, Gerald I ^c   Szendroedi, Julia ^a,d   Roden, Michael ^a,d  

^a LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

^b GHENT UNIVERSITY HOSPITAL   (Belgium)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL; FETUIN A; LIPID PEROXIDE; PROTEIN KINASE C THETA; STRESS ACTIVATED PROTEIN KINASE; PROTEIN KINASE C;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; LIPOLYSIS; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PROTEIN BLOOD LEVEL; TISSUE SPECIFICITY; ANIMAL; BLOOD; DISEASE MODEL; IMPAIRED GLUCOSE TOLERANCE; LIVER; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PHYSIOLOGY;

ALPHA-2-HS-GLYCOPROTEIN; ANIMALS; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; INSULIN RESISTANCE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPID PEROXIDES; LIVER; MICE; PREDIABETIC STATE; PROTEIN KINASE C;

EID: 84908613782     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1794     Document Type: Article

References (50)

1. Kacerovsky M, Brehm A, Chmelik M, et al. Impaired insulin stimulation of muscular ATP production in patients with type 1 diabetes. J Intern Med 2011;269: 189-199
2. Perseghin G, Lattuada G, De Cobelli F, et al. Reduced intrahepatic fat content is associated with increased whole-body lipid oxidation in patients with type 1 diabetes. Diabetologia 2005;48:2615-2621
3. Gale EA. The rise of childhood type 1 diabetes in the 20th century. Diabetes 2002;51:3353-3361
4. Wilkin TJ. The accelerator hypothesis: a review of the evidence for insulin resistance as the basis for type I as well as type II diabetes. Int J Obes (Lond) 2009; 33:716-726
5. Rossetti L. Glucose toxicity: the implications of hyperglycemia in the pathophysiology of diabetes mellitus. Clin Invest Med 1995;18:255-260
6. Erion DM, Shulman GI. Diacylglycerol-mediated insulin resistance. Nat Med 2010;16:400-402
7. Roden M. Muscle triglycerides and mitochondrial function: possible mechanisms for the development of type 2 diabetes. Int J Obes (Lond) 2005;29 (Suppl. 2):S111-S115
8. Summers SA. Ceramides in insulin resistance and lipotoxicity. Prog Lipid Res 2006;45:42-72
9. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002;51:2944-2950
10. Stump CS, Short KR, Bigelow ML, Schimke JM, Nair KS. Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc Natl Acad Sci U S A 2003;100:7996-8001
11. Karakelides H, Asmann YW, Bigelow ML, et al. Effect of insulin deprivation on muscle mitochondrial ATP production and gene transcript levels in type 1 diabetic subjects. Diabetes 2007;56:2683-2689
12. Schmid AI, Szendroedi J, Chmelik M, Krssák M, Moser E, Roden M. Liver ATP synthesis is lower and relates to insulin sensitivity in patients with type 2 diabetes. Diabetes Care 2011;34:448-453
13. Szendroedi J, Chmelik M, Schmid AI, et al. Abnormal hepatic energy homeostasis in type 2 diabetes. Hepatology 2009;50:1079-1086
14. Pospisilik JA, Knauf C, Joza N, et al. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 2007;131:476-491
15. Makino S, Kunimoto K, Muraoka Y, Mizushima Y, Katagiri K, Tochino Y. Breeding of a non-obese, diabetic strain of mice. Jikken Dobutsu 1980;29:1-13
16. Ayala JE, Bracy DP, Malabanan C, et al. Hyperinsulinemic-euglycemic clamps in conscious, unrestrained mice [article online]. J Vis Exp 2011;(57):3188. Available from http://www.jove.com/video/3188/hyperinsulinemic-euglycemic-clampsin- conscious-unrestrained-mice?id=3188. Accessed 12 April 2014
17. Phielix E, Jelenik T, Nowotny P, Szendroedi J, Roden M. Reduction of nonesterified fatty acids improves insulin sensitivity and lowers oxidative stress, but fails to restore oxidative capacity in type 2 diabetes: a randomised clinical trial. Diabetologia 2014;57:572-581
18. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351-358
19. Kotzka J, Knebel B, Avci H, et al. Phosphorylation of sterol regulatory element-binding protein (SREBP)-1a links growth hormone action to lipid metabolism in hepatocytes. Atherosclerosis 2010;213:156-165
20. Fu M, Sun T, Bookout AL, et al. A nuclear receptor atlas: 3T3-L1 adipogenesis. Mol Endocrinol 2005;19:2437-2450
21. Mukherjee A, Sidis Y, Mahan A, et al. FSTL3 deletion reveals roles for TGFbeta family ligands in glucose and fat homeostasis in adults. Proc Natl Acad Sci U S A 2007;104:1348-1353
22. Jelenik T, Rossmeisl M, Kuda O, et al. AMP-activated protein kinase a2 subunit is required for the preservation of hepatic insulin sensitivity by n-3 polyunsaturated fatty acids. Diabetes 2010;59:2737-2746
23. Neschen S, Morino K, Hammond LE, et al. Prevention of hepatic steatosis and hepatic insulin resistance in mitochondrial acyl-CoA:glycerol-sn-3-phosphate acyltransferase 1 knockout mice. Cell Metab 2005;2:55-65
24. Inoue Y, Kaifu T, Sugahara-Tobinai A, Nakamura A, Miyazaki J, Takai T. Activating Fc gamma receptors participate in the development of autoimmune diabetes in NOD mice. J Immunol 2007;179:764-774
25. Steele R. Influences of glucose loading and of injected insulin on hepatic glucose output. Ann N Y Acad Sci 1959;82:420-430
26. Lee S, Muniyappa R, Yan X, et al. Comparison between surrogate indexes of insulin sensitivity and resistance and hyperinsulinemic euglycemic clamp estimates in mice. Am J Physiol Endocrinol Metab 2008;294:E261-E270
27. Uwaifo GI, Fallon EM, Chin J, Elberg J, Parikh SJ, Yanovski JA. Indices of insulin action, disposal, and secretion derived from fasting samples and clamps in normal glucose-tolerant black and white children. Diabetes Care 2002;25:2081-2087
28. Durant S, Alves V, Coulaud J, Homo-Delarche F. Nonobese diabetic (NOD) mouse dendritic cells stimulate insulin secretion by prediabetic islets. Autoimmunity 2002;35:449-455
29. Blondel O, Bailbe D, Portha B. In vivo insulin resistance in streptozotocindiabetic rats-evidence for reversal following oral vanadate treatment. Diabetologia 1989;32:185-190
30. Bevilacqua S, Barrett EJ, Smith D, et al. Hepatic and peripheral insulin resistance following streptozotocin-induced insulin deficiency in the dog. Metabolism 1985;34:817-825
31. Noguchi Y, Younes RN, Conlon KC, Vydelingum NA, Matsumoto A, Brennan MF. The effect of prolonged hyperglycemia on metabolic alterations in the subtotally pancreatectomized rat. Surg Today 1994;24:987-993
32. Bergman BC, Howard D, Schauer IE, et al. The importance of palmitoleic acid to adipocyte insulin resistance and whole-body insulin sensitivity in type 1 diabetes. J Clin Endocrinol Metab 2013;98:E40-E50
33. Anderson EJ, Lustig ME, Boyle KE, et al. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009;119:573-581
34. Cline GW, Magnusson I, Rothman DL, Petersen KF, Laurent D, Shulman GI. Mechanism of impaired insulin-stimulated muscle glucose metabolism in subjects with insulin-dependent diabetes mellitus. J Clin Invest 1997;99:2219-2224
35. Vuorinen-Markkola H, Koivisto VA, Yki-Jarvinen H. Mechanisms of hyperglycemia-induced insulin resistance in whole body and skeletal muscle of type I diabetic patients. Diabetes 1992;41:571-580
36. Yki-Järvinen H, Vuorinen-Markkola H, Koranyi L, et al. Defect in insulin action on expression of the muscle/adipose tissue glucose transporter gene in skeletal muscle of type 1 diabetic patients. J Clin Endocrinol Metab 1992;75:795-799
37. Perseghin G, Lattuada G, Danna M, et al. Insulin resistance, intramyocellular lipid content, and plasma adiponectin in patients with type 1 diabetes. Am J Physiol Endocrinol Metab 2003;285:E1174-E1181
38. Roden M, Price TB, Perseghin G, et al. Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 1996;97:2859-2865
39. Pal D, Dasgupta S, Kundu R, et al. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat Med 2012;18:1279-1285
40. Talior I, Yarkoni M, Bashan N, Eldar-Finkelman H. Increased glucose uptake promotes oxidative stress and PKC-delta activation in adipocytes of obese, insulin-resistant mice. Am J Physiol Endocrinol Metab 2003;285:E295-E302
41. Stefan N, Häring HU. Circulating fetuin-A and free fatty acids interact to predict insulin resistance in humans. Nat Med 2013;19:394-395
42. Galbo T, Perry RJ, Jurczak MJ, et al. Saturated and unsaturated fat induce hepatic insulin resistance independently of TLR-4 signaling and ceramide synthesis in vivo. Proc Natl Acad Sci U S A 2013;110:12780-12785
43. Lim JH, Lee HJ, Ho Jung M, Song J. Coupling mitochondrial dysfunction to endoplasmic reticulum stress response: a molecular mechanism leading to hepatic insulin resistance. Cell Signal 2009;21:169-177
44. Hruszkewycz AM. Evidence for mitochondrial DNA damage by lipid peroxidation. Biochem Biophys Res Commun 1988;153:191-197
45. Liu HY, Yehuda-Shnaidman E, Hong T, et al. Prolonged exposure to insulin suppresses mitochondrial production in primary hepatocytes. J Biol Chem 2009; 284:14087-14095
46. Liu HY, Cao SY, Hong T, Han J, Liu Z, Cao W. Insulin is a stronger inducer of insulin resistance than hyperglycemia in mice with type 1 diabetes mellitus (T1DM). J Biol Chem 2009;284:27090-27100
47. Takamura T, Misu H, Matsuzawa-Nagata N, et al. Obesity upregulates genes involved in oxidative phosphorylation in livers of diabetic patients. Obesity (Silver Spring) 2008;16:2601-2609
48. Li X, Monks B, Ge Q, Birnbaum MJ. Akt/PKB regulates hepatic metabolism by directly inhibiting PGC-1alpha transcription coactivator. Nature 2007;447:1012-1016
49. Civitarese AE, Carling S, Heilbronn LK, et al.; CALERIE Pennington Team. Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 2007;4:e76
50. Goustin AS, Derar N, Abou-Samra AB. Ahsg-fetuin blocks the metabolic arm of insulin action through its interaction with the 95-kD b-subunit of the insulin receptor. Cell Signal 2013;25:981-988