Dietary obesity-associated hif1α activation in adipocytes restricts fatty acid oxidation and energy expenditure via suppression of the Sirt2-NAD+ system

Genes and Development

Volumn 26, Issue 3, 2012, Pages 259-270

  Krishnan, Jaya ^a,b   Danzer, Carsten ^a,b   Simka, Tatiana ^a,b   Ukropec, Josef ^c   Walter, Katharina Manuela ^a,b   Kumpf, Susann ^a,b   Mirtschink, Peter ^a,b   Ukropcova, Barbara ^c   Gasperikova, Daniela ^c   Pedrazzini, Thierry ^d   Krek, Wilhelm ^a,b  

^a Institute of Cell Biology   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c INSTITUTE OF EXPERIMENTAL ENDOCRINOLOGY   (Slovakia)

^d University of Lausanne Medical Center   (Switzerland)

Author keywords

Adipocytes; Diabetes; Hif1 ; Metabolism; Obesity; Sirt2

Indexed keywords

FATTY ACID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SIRTUIN 2;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOMYOPATHY; CELL ACTIVATION; CONTROLLED STUDY; DEACETYLATION; DIETARY OBESITY; DISEASE ASSOCIATION; ENERGY EXPENDITURE; ENZYME REPRESSION; FATTY ACID OXIDATION; GLUCOSE INTOLERANCE; HUMAN; HUMAN TISSUE; INSULIN RESISTANCE; MITOCHONDRIAL GENE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ACETYLATION; ADIPOCYTES; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELLS, CULTURED; DIET; ENERGY METABOLISM; FATTY ACIDS; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; NAD; OBESITY; OXIDATION-REDUCTION; SEQUENCE ALIGNMENT; SIRTUIN 2; TRANS-ACTIVATORS;

MUS;

EID: 84856628731     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.180406.111     Document Type: Article

References (38)

1. Black JC, Mosley A, Kitada T, Washburn M, Carey M. 2008. The SIRT2 deacetylase regulates autoacetylation of p300. Mol Cell 32: 449-455.
2. Boudina S, Abel ED. 2010. Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord 11: 31-39.
3. Buettner R, Parhofer KG, Woenckhaus M, Wrede CE, Kunz-Schughart LA, Scholmerich J, Bollheimer LC. 2006. Defining high-fat-diet rat models: Metabolic and molecular effects of different fat types. J Mol Endocrinol 36: 485-501.
4. Cinti S. 2009. Transdifferentiation properties of adipocytes in the adipose organ. Am J Physiol 297: E977-E986. doi: 10.1152/ajpendo.00183.2009.
5. Donohoe CL, Doyle SL, Reynolds JV. 2011. Visceral adiposity, insulin resistance and cancer risk. Diabetol Metab Syndr 3: 12. doi: 10.1186/1758-5996-3-12.
6. Eltzschig HK, Abdulla P, Hoffman E, Hamilton KE, Daniels D, Schonfeld C, Loffler M, Reyes G, Duszenko M, Karhausen J, et al. 2005. HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J ExpMed 202: 1493-1505.
7. Finnin MS, Donigian JR, Pavletich NP. 2001. Structure of the histone deacetylase SIRT2. Nat Struct Biol 8: 621-625.
8. Gealekman O, Guseva N, Hartigan C, Apotheker S, Gorgoglione M, Gurav K, Tran KV, Straubhaar J, Nicoloro S, Czech MP, et al. 2011. Depot-specific differences and insufficient subcutaneous adipose tissue angiogenesis in human obesity. Circulation 123: 186-194.
9. Guerra C, Navarro P, Valverde AM, Arribas M, Bruning J, Kozak LP, Kahn CR, Benito M. 2001. Brown adipose tissuespecific insulin receptor knockout shows diabetic phenotype without insulin resistance. J Clin Invest 108: 1205-1213.
10. Halberg N, Khan T, Trujillo ME, Wernstedt-Asterholm I, Attie AD, Sherwani S, Wang ZV, Landskroner-Eiger S, Dineen S, Magalang UJ, et al. 2009. Hypoxia-inducible factor 1a induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol 29: 4467-4483.
11. Handschin C, Spiegelman BM. 2006. Peroxisome proliferatoractivated receptor g coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27: 728-735.
12. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. 2003. Differential roles of hypoxia-inducible factor 1a (HIF-1a) and HIF-2a in hypoxic gene regulation. Mol Cell Biol 23: 9361-9374.
13. Huang LE, Gu J, Schau M, Bunn HF. 1998. Regulation of hypoxia-inducible factor 1a is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci 95: 7987-7992.
14. Imagawa M, Tsuchiya T, Nishihara T. 1999. Identification of inducible genes at the early stage of adipocyte differentiation of 3T3-L1 cells. Biochem Biophys Res Commun 254: 299-305.
15. Imai T, Jiang M, Chambon P, Metzger D. 2001. Impaired adipogenesis and lipolysis in the mouse upon selective ablation of the retinoid X receptor a mediated by a tamoxifen-inducible chimeric Cre recombinase (Cre-ERT2) in adipocytes. Proc Natl Acad Sci 98: 224-228.
16. Jiang C, Qu A, Matsubara T, Chanturiya T, Jou W, Gavrilova O, Shah YM, Gonzalez FJ. 2011. Disruption of hypoxia-inducible factor 1 in adipocytes improves insulin sensitivity and decreases adiposity in high-fat diet-fed mice. Diabetes 60: 2484-2495.
17. ing E, Gesta S, Kahn CR. 2007. SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell Metab 6: 105-114.
18. Kaelin WG Jr, Ratcliffe PJ. 2008. Oxygen sensing by metazoans: The central role of the HIF hydroxylase pathway. Mol Cell 30: 393-402.
19. Kopecky J, Rossmeisl M, Flachs P, Brauner P, Sponarova J, Matejkova O, Prazak T, Ruzickova J, Bardova K, Kuda O. 2004. Energy metabolism of adipose tissue-physiological aspects and target in obesity treatment. Physiol Res 53: S225-S232.
20. Krishnan J, Suter M, Windak R, Krebs T, Felley A, Montessuit C, Tokarska-Schlattner M, Aasum E, Bogdanova A, Perriard E, et al. 2009. Activation of a HIF1a-PPARg axis underlies the integration of glycolytic and lipid anabolic pathways in pathologic cardiac hypertrophy. Cell Metab 9: 512-524.
21. Martens K, Bottelbergs A, Baes M. 2010. Ectopic recombination in the central and peripheral nervous system by aP2/FABP4- Cre mice: Implications for metabolism research. FEBS Lett 584: 1054-1058.
22. Montague CT, O'Rahilly S. 2000. The perils of portliness: Causes and consequences of visceral adiposity. Diabetes 49: 883-888.
23. North BJ, Verdin E. 2004. Sirtuins: Sir2-related NAD-dependent protein deacetylases. Genome Biol 5: 224. doi: 10.1186/gb- 2004-5-5-224.
24. North BJ, Marshall BL, Borra MT, Denu JM, Verdin E. 2003. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell 11: 437-444.
25. Nunn JF. 1972. Nomograms for calculation of oxygen consumption and respiratory exchange ratio. BMJ 4: 18-20.
26. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. 2005. Nutrient control of glucose homeostasis through a complex of PGC-1a and SIRT1. Nature 434: 113-118.
27. Tkacova R, Ukropec J, Skyba P, Ukropcova B, Pobeha P, Kurdiova T, Joppa P, Klimes I, Tkac I, Gasperikova D. 2010. Increased adipose tissue expression of proinflammatory CD40, MKK4 and JNK in patients with very severe chronic obstructive pulmonary disease. Respiration 81: 386-393.
28. Urs S, Harrington A, Liaw L, Small D. 2006. Selective expression of an aP2/fatty acid binding protein 4-Cre transgene in nonadipogenic tissues during embryonic development. Transgenic Res 15: 647-653.
29. Vague J. 1947. La differe ́nciation sexuelle, facteur determinant des formes de l'obe ́ site ́. Presse Med 55: 339-340.
30. van der Kuip M, de Meer K, Oosterveld MJ, Lafeber HN, Gemke RJ. 2004. Simple and accurate assessment of energy expenditure in ventilated paediatric intensive care patients. Clin Nutr 23: 657-663.
31. Wang F, Nguyen M, Qin FX, Tong Q. 2007. SIRT2 deacetylates FOXO3a in response to oxidative stress and caloric restriction. Aging Cell 6: 505-514.
32. Wang Y, Roche O, Yan MS, Finak G, Evans AJ, Metcalf JL, Hast BE, Hanna SC, Wondergem B, Furge KA, et al. 2009. Regulation of endocytosis via the oxygen-sensing pathway. Nat Med 15: 319-324.
33. Wellen KE, Thompson CB. 2010. Cellular metabolic stress: Considering how cells respond to nutrient excess. Mol Cell 40: 323-332.
34. Wood IS, de Heredia FP, Wang B, Trayhurn P. 2009. Cellular hypoxia and adipose tissue dysfunction in obesity. Proc Nutr Soc 68: 370-377.
35. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, et al. 1999. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
36. Ye J. 2009. Emerging role of adipose tissue hypoxia in obesity and insulin resistance. Int J Obes (Lond) 33: 54-66.
37. Ye J, Gao Z, Yin J, He Q. 2007. 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 293: E1118-E1128. doi: 10.1152/ajpendo.00435.2007.
38. Zhang X, Lam KS, Ye H, Chung SK, Zhou M, Wang Y, Xu A. 2010. Adipose tissue-specific inhibition of hypoxia-inducible factor 1a induces obesity and glucose intolerance by impeding energy expenditure in mice. J Biol Chem 285: 32869-32877.