Metabolic remodelling in obesity and type 2 diabetes: Pathological or protective mechanisms in response to nutrient excess?

Clinical and Experimental Pharmacology and Physiology

Volumn 42, Issue 1, 2015, Pages 109-115

  Connor, Timothy ^a   Martin, Sheree D ^a   Howlett, Kirsten F ^a   McGee, Sean L ^a,b  

^a DEAKIN UNIVERSITY   (Australia)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

Cell survival; Gene expression; Heart; Insulin resistance; Liver; Mitochondria; Muscle

Indexed keywords

ARTICLE; CELL PROTECTION; CELL SURVIVAL; ENERGY BALANCE; GENETIC TRANSCRIPTION; HUMAN; INSULIN RESISTANCE; METABOLISM; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NUTRIENT; OBESITY; PATHOGENESIS; ANIMAL; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; OVERNUTRITION; PHYSIOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; HUMANS; INSULIN RESISTANCE; OBESITY; OVERNUTRITION;

EID: 84919658998     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12315     Document Type: Article

References (68)

1. Samuel VT, Shulman GI. Mechanisms for insulin resistance: Common threads and missing links. Cell 2012; 148: 852-71.
2. Saltiel AR. Insulin resistance in the defense against obesity. Cell Metab. 2012; 15: 798-804.
3. Hoehn KL, Salmon AB, Hohnen-Behrens C et al. Insulin resistance is a cellular antioxidant defense mechanism. Proc. Natl Acad. Sci. USA 2009; 106: 17787-92.
4. Biddinger SB, Hernandez-Ono A, Rask-Madsen C et al. Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab. 2008; 7: 125-34.
5. Wan M, Leavens KF, Hunter RW et al. A noncanonical, GSK3-independent pathway controls postprandial hepatic glycogen deposition. Cell Metab. 2013; 18: 99-105.
6. Taegtmeyer H, Beauloye C, Harmancey R, Hue L. Insulin resistance protects the heart from fuel overload in dysregulated metabolic states. Am. J. Physiol. Heart Circ. Physiol. 2013; 305: H1693-7.
7. Erol A. Insulin resistance is an evolutionarily conserved physiological mechanism at the cellular level for protection against increased oxidative stress. BioEssays 2007; 29: 811-18.
8. Tsatsoulis A, Mantzaris MD, Bellou S, Andrikoula M. Insulin resistance: An adaptive mechanism becomes maladaptive in the current environment: An evolutionary perspective. Metabolism 2013; 62: 622-33.
9. Unger RH. Lipid overload and overflow: Metabolic trauma and the metabolic syndrome. Trends in endocrinology and metabolism. Trends Endocrinol. Metab. 2003; 14: 398-403.
10. Agius L. High-carbohydrate diets induce hepatic insulin resistance to protect the liver from substrate overload. Biochem. Pharmacol. 2013; 85: 306-12.
11. Arad M, Benson DW, Perez-Atayde AR et al. Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J. Clin. Invest. 2002; 109: 357-62.
12. Demo E, Frush D, Gottfried M et al. Glycogen storage disease type III-hepatocellular carcinoma a long-term complication? J. Hepatol. 2007; 46: 492-8.
13. Lim JA, Li L, Raben N. Pompe disease: From pathophysiology to therapy and back again. Front. Aging Neurosci. 2014; 6: 177.
14. Kohlwein SD, Petschnigg J. Lipid-induced cell dysfunction and cell death: Lessons from yeast. Curr. Hypertens. Rep. 2007; 9: 455-61.
15. Feldstein AE, Canbay A, Angulo P et al. Hepatocyte apoptosis and fas expression are prominent features of human nonalcoholic steatohepatitis. Gastroenterology 2003; 125: 437-43.
16. Hegarty BD, Cooney GJ, Kraegen EW, Furler SM. Increased efficiency of fatty acid uptake contributes to lipid accumulation in skeletal muscle of high fat-fed insulin-resistant rats. Diabetes 2002; 51: 1477-84.
17. Listenberger LL, Han X, Lewis SE et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl Acad. Sci. USA 2003; 100: 3077-82.
18. Turcotte LP, Swenberger JR, Zavitz Tucker M, Yee AJ. Increased fatty acid uptake and altered fatty acid metabolism in insulin-resistant muscle of obese Zucker rats. Diabetes 2001; 50: 1389-96.
19. Watt MJ. Storing up trouble: Does accumulation of intramyocellular triglyceride protect skeletal muscle from insulin resistance? Clin. Exp. Pharmacol. Physiol. 2009; 36: 5-11.
20. Lu B, Bridges D, Yang Y et al. Metabolic crosstalk: Molecular links between glycogen and lipid metabolism in obesity. Diabetes 2014; 63: 2935-48.
21. Chou JY, Jun HS, Mansfield BC. Glycogen storage disease type I and G6Pase-beta deficiency: Etiology and therapy. Nat. Rev. Endocrinol. 2010; 6: 676-88.
22. Brandon AE, Hoy AJ, Wright LE et al. The evolution of insulin resistance in muscle of the glucose infused rat. Arch. Biochem. Biophys. 2011; 509: 133-41.
23. Hoy AJ, Brandon AE, Turner N et al. Lipid and insulin infusion-induced skeletal muscle insulin resistance is likely due to metabolic feedback and not changes in IRS-1, Akt, or AS160 phosphorylation. Am. J. Physiol. Endocrinol. Metab. 2009; 297: E67-75.
24. Roden M, Price TB, Perseghin G et al. Mechanism of free fatty acid-induced insulin resistance in humans. J. Clin. Invest. 1996; 97: 2859-65.
25. Fowelin J, Attvall S, von Schenck H, Bengtsson BA, Smith U, Lager I. Effect of prolonged hyperglycemia on growth hormone levels and insulin sensitivity in insulin-dependent diabetes mellitus. Metabolism 1993; 42: 387-94.
26. Dimitrakoudis D, Ramlal T, Rastogi S, Vranic M, Klip A. Glycaemia regulates the glucose transporter number in the plasma membrane of rat skeletal muscle. Biochem. J. 1992; 284: 341-8.
27. Giaccari A, Morviducci L, Pastore L et al. Relative contribution of glycogenolysis and gluconeogenesis to hepatic glucose production in control and diabetic rats. A re-examination in the presence of euglycaemia. Diabetologia 1998; 41: 307-14.
28. Harmancey R, Lam TN, Lubrano GM, Guthrie PH, Vela D, Taegtmeyer H. Insulin resistance improves metabolic and contractile efficiency in stressed rat heart. FASEB J. 2012; 26: 3118-26.
29. Christopher BA, Huang HM, Berthiaume JM et al. Myocardial insulin resistance induced by high fat feeding in heart failure is associated with preserved contractile function. Am. J. Physiol. Heart Circ. Physiol. 2010; 299: H1917-27.
30. Yun J, Finkel T. Mitohormesis. Cell Metab. 2014; 19: 757-66.
31. 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: 573-81.
32. Fisher-Wellman KH, Neufer PD. Linking mitochondrial bioenergetics to insulin resistance via redox biology. Trends in endocrinology and metabolism. Trends Endocrinol. Metab. 2012; 23: 142-53.
33. Gomez-Cabrera MC, Domenech E, Vina J. Moderate exercise is an antioxidant: Upregulation of antioxidant genes by training. Free Radic. Biol. Med. 2008; 44: 126-31.
34. Loh K, Deng H, Fukushima A et al. Reactive oxygen species enhance insulin sensitivity. Cell Metab. 2009; 10: 260-72.
35. Martin SD, Morrison S, Konstantopoulos N, McGee SL. Mitochondrial dysfunction has divergent, cell type-dependent effects on insulin action. Mol. Metab. 2014; 3: 408-18.
36. Brehm A, Krssak M, Schmid AI, Nowotny P, Waldhausl W, Roden M. Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 2006; 55: 136-40.
37. Hoeks J, van Herpen NA, Mensink M et al. Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as consequence rather than cause of human insulin resistance. Diabetes 2010; 59: 2117-25.
38. Koves TR, Ussher JR, Noland RC et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 2008; 7: 45-56.
39. Han DH, Hancock CR, Jung SR, Higashida K, Kim SH, Holloszy JO. Deficiency of the mitochondrial electron transport chain in muscle does not cause insulin resistance. PLoS One 2011; 6: e19739.
40. 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: 476-91.
41. Quintens R, Singh S, Lemaire K et al. Mice deficient in the respiratory chain gene Cox6a2 are protected against high-fat diet-induced obesity and insulin resistance. PLoS One 2013; 8: e56719.
42. Yee C, Yang W, Hekimi S. The intrinsic apoptosis pathway mediates the pro-longevity response to mitochondrial ROS in C. elegans. Cell 2014; 157: 897-909.
43. Cameron-Smith D, Burke LM, Angus DJ et al. A short-term, high-fat diet up-regulates lipid metabolism and gene expression in human skeletal muscle. Am. J. Clin. Nutr. 2003; 77: 313-18.
44. Sparks LM, Xie H, Koza RA et al. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 2005; 54: 1926-33.
45. Lemarie A, Grimm S. Mitochondrial respiratory chain complexes: Apoptosis sensors mutated in cancer? Oncogene 2011; 30: 3985-4003.
46. Turpin SM, Ryall JG, Southgate R et al. Examination of 'lipotoxicity' in skeletal muscle of high-fat fed and ob/ob mice. J. Physiol. 2009; 587: 1593-605.
47. Mootha VK, Lindgren CM, Eriksson KF et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 2003; 34: 267-73.
48. Patti ME, Butte AJ, Crunkhorn S et al. 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 2003; 100: 8466-71.
49. He J, Watkins S, Kelley DE. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 2001; 50: 817-23.
50. Kelley DE, Simoneau JA. Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J. Clin. Invest. 1994; 94: 2349-56.
51. Lim JH, Gerhart-Hines Z, Dominy JE et al. Oleic acid stimulates complete oxidation of fatty acids through protein kinase A-dependent activation of SIRT1-PGC1alpha complex. J. Biol. Chem. 2013; 288: 7117-26.
52. Yabaluri N, Bashyam MD. Hormonal regulation of gluconeogenic gene transcription in the liver. J. Biosci. 2010; 35: 473-84.
53. Chakravarty K, Hanson RW. Insulin regulation of phosphoenol-pyruvate carboxykinase-c gene transcription: The role of sterol regulatory element-binding protein 1c. Nutr. Rev. 2007; 65 (Suppl.): S47-56.
54. Stark R, Guebre-Egziabher F, Zhao X et al. A role for mitochondrial phosphoenolpyruvate carboxykinase (PEPCK-M) in the regulation of hepatic gluconeogenesis. J. Biol. Chem. 2014; 289: 7257-63.
55. Argaud D, Zhang Q, Pan W, Maitra S, Pilkis SJ, Lange AJ. Regulation of rat liver glucose-6-phosphatase gene expression in different nutritional and hormonal states. Gene structure and 5'-flanking sequence. Diabetes 1996; 45: 1563-71.
56. Consoli A. Role of liver in pathophysiology of NIDDM. Diabetes Care 1992; 15: 430-41.
57. She P, Shiota M, Shelton KD, Chalkley R, Postic C, Magnuson MA. Phosphoenolpyruvate carboxykinase is necessary for the integration of hepatic energy metabolism. Mol. Cell. Biol. 2000; 20: 6508-17.
58. Mutel E, Abdul-Wahed A, Ramamonjisoa N et al. Targeted deletion of liver glucose-6 phosphatase mimics glycogen storage disease type 1a including development of multiple adenomas. J. Hepatol. 2011; 54: 529-37.
59. Stumvoll M, Nurjhan N, Perriello G, Dailey G, Gerich JE. Metabolic effects of metformin in non-insulin-dependent diabetes mellitus. N. Engl. J. Med. 1995; 333: 550-4.
60. Mithieux G, Guignot L, Bordet JC, Wiernsperger N. Intrahepatic mechanisms underlying the effect of metformin in decreasing basal glucose production in rats fed a high-fat diet. Diabetes 2002; 51: 139-43.
61. Roumie CL, Greevy RA, Grijalva CG et al. Association between intensification of metformin treatment with insulin vs sulfonylureas and cardiovascular events and all-cause mortality among patients with diabetes. JAMA 2014; 311: 2288-96.
62. Nissen SE, Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N. Engl. J. Med. 2007; 356: 2457-71.
63. Kim A, Scharf K, Senthil M, Solomon N, Garberoglio C, Lum SS. The prevalence of overweight and obesity in a breast clinic population: Consideration for weight loss as a therapeutic intervention. Surg. Obes. Relat. Dis. 2014; 10: 348-53.
64. Tseng CH, Tseng FH. Diabetes and gastric cancer: The potential links. World J. Gastroenterol. 2014; 20: 1701-11.
65. Karagozian R, Derdak Z, Baffy G. Obesity-associated mechanisms of hepatocarcinogenesis. Metabolism 2014; 63: 607-17.
66. Ward PS, Thompson CB. Metabolic reprogramming: A cancer hallmark even warburg did not anticipate. Cancer Cell 2012; 21: 297-308.
67. Varga J, De Oliveira T, Greten FR. The architect who never sleeps: Tumor-induced plasticity. FEBS Lett. 2014; 588: 2422-7.
68. Talchai C, Xuan S, Lin HV, Sussel L, Accili D. Pancreatic beta cell dedifferentiation as a mechanism of diabetic beta cell failure. Cell 2012; 150: 1223-34.