Novel links between HIFs, type 2 diabetes, and metabolic syndrome

Trends in Endocrinology and Metabolism

Volumn 23, Issue 8, 2012, Pages 372-380

  Girgis, Christian M ^a   Cheng, Kim ^a   Scott, Christopher H ^a   Gunton, Jenny E ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DEFEROXAMINE; GLUCOSE TRANSPORTER 4; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; HYPOXIA INDUCIBLE FACTOR 3ALPHA; HYPOXIA INDUCIBLE FACTOR 3BETA; LEPTIN; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ADIPOSE TISSUE; CITRIC ACID CYCLE; FOOD INTAKE; GENE EXPRESSION; GLUCOSE HOMEOSTASIS; HEART INFARCTION SIZE; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HUMAN; HYPERGLYCEMIA; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; IRON OVERLOAD; LIVER CELL; METABOLIC SYNDROME X; MORBIDITY; MORTALITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; PANCREAS RESECTION; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; ULCER; VON HIPPEL LINDAU DISEASE;

ADIPOSE TISSUE; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DIABETES MELLITUS, TYPE 2; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; INFLAMMATION; INSULIN-SECRETING CELLS; LIVER; METABOLIC SYNDROME X;

EID: 84864323177     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2012.05.003     Document Type: Review

References (88)

1. Semenza G.L. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 2004, 19:176-182.
2. Rocha S. Gene regulation under low oxygen: holding your breath for transcription. Trends Biochem. Sci. 2007, 32:389-397.
3. Semenza G.L. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol. Med. 2001, 7:345-350.
4. Semenza G.L. HIF-1 and human disease: one highly involved factor. Genes Dev. 2000, 14:1983-1991.
5. Kopp R., et al. HIF signaling and overall gene expression changes during hypoxia and prolonged exercise differ considerably. Physiol. Genomics 2011, 43:506-516.
6. Zhang Y., et al. The HIF-1 hypoxia-inducible factor modulates lifespan in C. elegans. PLoS ONE 2009, 4:pe6348.
7. Maltepe E., et al. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 1997, 386:403-407.
8. Scortegagna M., et al. Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice. Nat. Genet. 2003, 35:331-340.
9. Scortegagno M., et al. The HIF family member EPAS1/HIF-2alpha is required for normal hematopoiesis in mice. Blood 2003, 102:1634-1640.
10. Zagorska A., Dulak J. HIF-1: the knowns and unknowns of hypoxia sensing. Acta Biochim. Pol. 2004, 51:563-585.
11. Hammel P.R., et al. Pancreatic involvement in von Hippel-Lindau disease. Gastroenterology 2000, 119:1087-1095.
12. Gunton J.E., et al. Loss of ARNT/HIF1beta mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell 2005, 122:337-349.
13. Cheng K., et al. Hypoxia-inducible factor-1alpha regulates beta cell function in mouse and human islets. J. Clin. Invest. 2010, 120:2171-2183.
14. Ochiai D., et al. Disruption of HIF-1alpha in hepatocytes impairs glucose metabolism in diet-induced obesity mice. Biochem. Biophys. Res. Commun. 2011, 415:445-449.
15. Yu J., et al. Conditioned medium from hypoxia-treated adipocytes renders muscle cells insulin resistant. Eur. J. Cell Biol. 2011, 90:1000-1015.
16. Halberg N., et al. Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue. Mol. Cell. Biol. 2009, 29:4467-4483.
17. Jiang C., et al. Disruption of hypoxia-inducible factor 1 in adipocytes improves insulin sensitivity and decreases adiposity in high-fat diet-fed mice. Diabetes 2011, 60:2484-2495.
18. + system. Genes Dev. 2012, 26:259-270.
19. Pillai R., et al. Aryl hydrocarbon receptor nuclear translocator/hypoxia-inducible factor-1{beta} plays a critical role in maintaining glucose-stimulated anaplerosis and insulin release from pancreatic {beta}-cells. J. Biol. Chem. 2011, 286:1014-1024.
20. Noordeen N.A., et al. Carbohydrate-responsive element-binding protein (ChREBP) is a negative regulator of ARNT/HIF-1beta gene expression in pancreatic islet beta-cells. Diabetes 2010, 59:153-160.
21. Cheng K., et al. Hypoxia-inducible factor-1alpha regulates beta cell function in mouse and human islets. J. Clin. Invest. 2010, 120:2171-2183.
22. Bensellam M., et al. Glucose-induced o(2) consumption activates hypoxia inducible factors 1 and 2 in rat insulin-secreting pancreatic Beta-cells. PLoS ONE 2012, 7:pe29807.
23. Cantley J., et al. Deletion of the von Hippel-Lindau gene in pancreatic beta cells impairs glucose homeostasis in mice. J. Clin. Invest. 2009, 119:125-135.
24. Choi D., et al. Vhl is required for normal pancreatic beta cell function and the maintenance of beta cell mass with age in mice. Lab. Invest. 2011, 91:527-538.
25. Puri S., et al. A role for von Hippel-Lindau protein in pancreatic beta-cell function. Diabetes 2009, 58:433-441.
26. Zehetner J., et al. pVHL is a regulator of glucose metabolism and insulin secretion in pancreatic {beta} cells. Genes Dev. 2008, 22:3135-3146.
27. Zhang N., et al. The asparaginyl hydroxylase factor inhibiting HIF-1alpha is an essential regulator of metabolism. Cell Metab. 2010, 11:364-378.
28. Cheng K., et al. Hypoxia-Inducible Factor-1α Regulates β-Cell Function in Mouse and Human Islets. J. Clin. Invest. 2010, 120:2171-2183.
29. Stokes, R.A. et al. Hypoxia-inducible factor 1α (HIF-1α) potentiates β-cell survival after islet transplantation of human and mouse islets. Cell Transplantation, 2012. (in press).
30. Zhang N., et al. The asparaginyl hydroxylase factor inhibiting HIF-1alpha is an essential regulator of metabolism. Cell Metab. 2010, 11:364-378.
31. Jungermann K., Kietzmann T. Oxygen: modulator of metabolic zonation and disease of the liver. Hepatology 2000, 31:255-260.
32. Nath B., Szabo G. Hypoxia and hypoxia inducible factors: Diverse roles in liver diseases. Hepatology 2012, 55:622-633.
33. Mishra P., et al. Apnoeic-hypopnoeic episodes during obstructive sleep apnoea are associated with histological nonalcoholic steatohepatitis. Liver Int. 2008, 28:1080-1086.
34. Jouet P., et al. Relationship between obstructive sleep apnea and liver abnormalities in morbidly obese patients: a prospective study. Obes. Surg. 2007, 17:478-485.
35. Rivera C.A. Risk factors and mechanisms of non-alcoholic steatohepatitis. Pathophysiology 2008, 15:109-114.
36. Musso G., et al. Non-alcoholic fatty liver disease from pathogenesis to management: an update. Obes. Rev. 2010, 11:430-445.
37. Brown M.S., Goldstein J.L. Selective versus total insulin resistance: a pathogenic paradox. Cell Metab. 2008, 7:95-96.
38. Basu R., et al. Obesity and type 2 diabetes impair insulin-induced suppression of glycogenolysis as well as gluconeogenesis. Diabetes 2005, 54:1942-1948.
39. Rizza R.A. Pathogenesis of fasting and postprandial hyperglycemia in type 2 diabetes: implications for therapy. Diabetes 2010, 59:2697-2707.
40. Basu R., et al. Both fasting glucose production and disappearance are abnormal in people with "mild" and "severe" type 2 diabetes. Am. J. Physiol. Endocrinol. Metab. 2004, 287:E55-E62.
41. Basu R., et al. Insulin dose-response curves for stimulation of splanchnic glucose uptake and suppression of endogenous glucose production differ in nondiabetic humans and are abnormal in people with type 2 diabetes. Diabetes 2004, 53:2042-2050.
42. Sparks J.D., Sparks C.E. Insulin regulation of triacylglycerol-rich lipoprotein synthesis and secretion. Biochim. Biophys. Acta 1994, 1215:9-32.
43. Taghibiglou C., et al. Hepatic very low density lipoprotein-ApoB overproduction is associated with attenuated hepatic insulin signaling and overexpression of protein-tyrosine phosphatase 1B in a fructose-fed hamster model of insulin resistance. J. Biol. Chem. 2002, 277:793-803.
44. Lewis G.F., et al. Effects of acute hyperinsulinemia on VLDL triglyceride and VLDL apoB production in normal weight and obese individuals. Diabetes 1993, 42:833-842.
45. Malmstrom R., et al. Defective regulation of triglyceride metabolism by insulin in the liver in NIDDM. Diabetologia 1997, 40:454-462.
46. Bourgeois C.S., et al. VLDL output by hepatocytes from obese Zucker rats is resistant to the inhibitory effect of insulin. Am. J. Physiol. 1995, 269(2 Pt 1):E208-E215.
47. Biddinger S.B., et al. Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab. 2008, 7:125-134.
48. Ginsberg H.N. Insulin resistance and cardiovascular disease. J. Clin. Invest. 2000, 106:453-458.
49. Ochiai D., et al. Disruption of HIF-1alpha in hepatocytes impairs glucose metabolism in diet-induced obesity mice. Biochem. Biophys. Res. Commun. 2011, 415:445-449.
50. Wang X.L., et al. Ablation of ARNT/HIF1beta in liver alters gluconeogenesis, lipogenic gene expression, and serum ketones. Cell Metab. 2009, 9:428-439.
51. Kucejova B., et al. Uncoupling hypoxia signaling from oxygen sensing in the liver results in hypoketotic hypoglycemic death. Oncogene 2011, 30:2147-2160.
52. Haase V.H., et al. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1583-1588.
53. Rankin E.B., et al. Hypoxia-inducible factor 2 regulates hepatic lipid metabolism. Mol. Cell. Biol. 2009, 29:4527-4538.
54. Dongiovanni P., et al. Iron depletion by deferoxamine up-regulates glucose uptake and insulin signaling in hepatoma cells and in rat liver. Am. J. Pathol. 2008, 172:738-747.
55. Mason S.D., et al. HIF-1alpha in endurance training: suppression of oxidative metabolism. Am. J. Physiol. 2007, 293:R2059-R2069.
56. Bhambhani Y.N. Muscle oxygenation trends during dynamic exercise measured by near infrared spectroscopy. Can. J. Appl. Physiol. 2004, 29:504-523.
57. Lunde I.G., et al. Hypoxia inducible factor 1 links fast-patterned muscle activity and fast muscle phenotype in rats. J. Physiol. 2011, 589(Pt 6):1443-1454.
58. Pisani D.F., Dechesne C.A. Skeletal muscle HIF-1alpha expression is dependent on muscle fiber type. J. Gen. Physiol. 2005, 126:173-178.
59. Hoppeler H., Vogt M. Muscle tissue adaptations to hypoxia. J. Exp. Biol. 2001, 204(Pt 18):3133-3139.
60. Mason S.D., et al. Loss of skeletal muscle HIF-1alpha results in altered exercise endurance. PLoS Biol. 2004, 2:pe288.
61. Ahmetov I.I., et al. Effect of HIF1A gene polymorphism on human muscle performance. Bull. Exp. Biol. Med. 2008, 146:351-353.
62. Lippi G., Guidi G.C. Gene manipulation and improvement of athletic performances: new strategies in blood doping. Br. J. Sports Med. 2004, 38:p641.
63. Lima G.A., et al. Contractile activity per se induces transcriptional activation of SLC2A4 gene in soleus muscle: involvement of MEF2D, HIF-1a, and TRalpha transcriptional factors. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E132-E138.
64. Zelzer E., et al. Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. EMBO J. 1998, 17:5085-5094.
65. He J., et al. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 2001, 50:817-823.
66. Trayhurn P., Beattie J.H. Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ. Proc. Nutr. Soc. 2001, 60:329-339.
67. Sell H., et al. The adipocyte-myocyte axis in insulin resistance. Trends Endocrinol. Metab. 2006, 17:416-422.
68. Colditz G.A., et al. Weight gain as a risk factor for clinical diabetes mellitus in women. Ann. Intern. Med. 1995, 122:481-486.
69. Chan J.M., et al. Obesity, fat distribution, and weight gain as risk factors for clinical diabetes in men. Diabetes Care 1994, 17:961-969.
70. Unger R.H., Scherer P.E. Gluttony, sloth and the metabolic syndrome: a roadmap to lipotoxicity. Trends Endocrinol. Metab. 2010, 21:345-352.
71. Samocha-Bonet D., et al. Insulin-sensitive obesity in humans - a 'favorable fat' phenotype?. Trends Endocrinol. Metab. 2012, 23:116-124.
72. Trayhurn P., Wood I.S. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br. J. Nutr. 2004, 92:347-355.
73. Wood I.S., et al. Cellular hypoxia and adipose tissue dysfunction in obesity. Proc. Nutr. Soc. 2009, 68:370-377.
74. Wang B., et al. Dysregulation of the expression and secretion of inflammation-related adipokines by hypoxia in human adipocytes. Pflugers Arch. 2007, 455:479-492.
75. Ye J., et al. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E1118-E1128.
76. Rausch M.E., et al. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int. J. Obes. 2008, 32:451-463.
77. Pasarica M., et al. Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes 2009, 58:718-725.
78. Hong S.J., et al. Impaired response of mature adipocytes of diabetic mice to hypoxia. Exp. Cell Res. 2011, 317:2299-2307.
79. Lee K.Y., et al. The differential role of Hif1beta/Arnt and the hypoxic response in adipose function, fibrosis, and inflammation. Cell Metab. 2011, 14:491-503.
80. Zhang J., et al. Hypoxia-inducible factor 1 activation from adipose protein 2-cre mediated knockout of von hippel-lindau gene leads to embryonic lethality. Clin. Exp. Pharmacol. Physiol. 2012, 39:145-150.
81. Weisberg S.P., et al. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112:1796-1808.
82. Zhang X., et al. Adipose tissue-specific inhibition of hypoxia-inducible factor 1{alpha} induces obesity and glucose intolerance by impeding energy expenditure in mice. J. Biol. Chem. 2010, 285:32869-32877.
83. Zhang H., et al. Hypoxia-inducible factor directs POMC gene to mediate hypothalamic glucose sensing and energy balance regulation. PLoS Biol. 2011, 9:pe1001112.
84. Catrina S.B., et al. Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function. Diabetes 2004, 53:3226-3232.
85. Marfella R., et al. Myocardial infarction in diabetic rats: role of hyperglycaemia on infarct size and early expression of hypoxia-inducible factor 1. Diabetologia 2002, 45:1172-1181.
86. Xue W., et al. Cardiac-specific overexpression of HIF-1{alpha} prevents deterioration of glycolytic pathway and cardiac remodeling in streptozotocin-induced diabetic mice. Am. J. Pathol. 2010, 177:97-105.
87. Mace K.A., et al. Sustained expression of Hif-1alpha in the diabetic environment promotes angiogenesis and cutaneous wound repair. Wound Repair Regen. 2007, 15:636-645.
88. Thangarajah H., et al. HIF-1alpha dysfunction in diabetes. Cell Cycle 2010, 9:75-79.