Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation

Circulation

Volumn 124, Issue 1, 2011, Pages 67-76

  Goossens, Gijs H ^a   Bizzarri, Alessandro ^b   Venteclef, Nicolas ^c   Essers, Yvonne ^a   Cleutjens, Jack P ^a   Konings, Ellen ^a   Jocken, Johan W E ^a   Čajlaković, Merima ^b   Ribitsch, Volker ^b   Clément, Karine ^c   Blaak, Ellen E ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b JOANNEUM RESEARCH   (Austria)

^c CENTRE DE RECHERCHE DES CORDELIERS   (France)

Author keywords

blood flow; capillaries; hypoxia; inflammation; obesity

Indexed keywords

ANGIOTENSIN II; GLUCOSE; INSULIN; INTERLEUKIN 6; INTERLEUKIN 8; ISOPRENALINE; MESSENGER RNA; PLASMINOGEN ACTIVATOR INHIBITOR 1; TUMOR NECROSIS FACTOR ALPHA;

ABDOMINAL SUBCUTANEOUS FAT; ADIPOSE TISSUE BLOOD FLOW; ADULT; ARTICLE; BLOOD OXYGEN TENSION; CELL FUNCTION; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; FOOD INTAKE; GENE EXPRESSION; HEMODYNAMIC MONITORING; HUMAN; HYPEROXIA; IMPAIRED GLUCOSE TOLERANCE; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEAN BODY WEIGHT; MACROPHAGE; MALE; MICRODIALYSIS; MITOCHONDRION; OBESITY; OXYGEN CONSUMPTION; PRIORITY JOURNAL;

ADIPOSE TISSUE; ANGIOTENSIN II; HUMANS; HYPEROXIA; INFLAMMATION; INSULIN RESISTANCE; ISOPROTERENOL; MALE; MICROCIRCULATION; MIDDLE AGED; MITOCHONDRIA; OBESITY; OXYGEN; OXYGEN CONSUMPTION; REGIONAL BLOOD FLOW; THINNESS; VASOCONSTRICTOR AGENTS; VASODILATOR AGENTS;

EID: 79960359853     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.027813     Document Type: Article

References (45)

1. Goossens GH. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav. 2008;94:206-218. (Pubitemid 351615418)
2. Berg AH, Scherer PE. Adipose tissue, inflammation, and cardiovascular disease. Circ Res. 2005;96:939-949. (Pubitemid 40712793)
3. Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest. 2004;114:147-152. (Pubitemid 39071617)
4. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111-1119. (Pubitemid 40629025)
5. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest. 2003;112:1821-1830. (Pubitemid 38063705)
6. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004; 306:457-461. (Pubitemid 39372439)
7. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006;440:944-948.
8. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest. 2006;116:3015-3025. (Pubitemid 44684486)
9. Rausch ME, Weisberg S, Vardhana P, Tortoriello DV. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obes. 2008;32:451-463. (Pubitemid 351414814)
10. Ye J, Gao Z, Yin J, He Q. 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. 2007;293:E1118-E1128. (Pubitemid 47535846)
11. Hosogai N, Fukuhara A, Oshima K, Miyata Y, Tanaka S, Segawa K, Furukawa S, Tochino Y, Komuro R, Matsuda M, Shimomura I. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes. 2007;56:901-911. (Pubitemid 46525054)
12. Kabon B, Nagele A, Reddy D, Eagon C, Fleshman JW, Sessler DI, Kurz A. Obesity decreases perioperative tissue oxygenation. Anesthesiology. 2004;100:274-280. (Pubitemid 38133693)
13. Pasarica M, Sereda OR, Redman LM, Albarado DC, Hymel DT, Roan LE, Rood JC, Burk DH, Smith SR. Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes. 2009;58:718-725.
14. Brakenhielm E, Cao R, Gao B, Angelin B, Cannon B, Parini P, Cao Y. Angiogenesis inhibitor, TNP-470, prevents diet-induced and genetic obesity in mice. Circ Res. 2004;94:1579-1588. (Pubitemid 38856965)
15. Rupnick MA, Panigrahy D, Zhang CY, Dallabrida SM, Lowell BB, Langer R, Folkman MJ. Adipose tissue mass can be regulated through the vasculature. Proc Natl Acad Sci USA. 2002;99:10730-10735.
16. Trayhurn P, Wood IS. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr. 2004;92:347-355. (Pubitemid 40277057)
17. Ardilouze JL, Karpe F, Currie JM, Frayn KN, Fielding BA. Subcutaneous adipose tissue blood flow varies between superior and inferior levels of the anterior abdominal wall. Int J Obes. 2004;28:228-233. (Pubitemid 38223503)
18. Goossens GH, McQuaid SE, Dennis AL, van Baak MA, Blaak EE, Frayn KN, Saris WH, Karpe F. Angiotensin II: a major regulator of subcutaneous adipose tissue blood flow in humans. J Physiol. 2006;571:451-460.
19. Blaak EE, van Baak MA, Kemerink GJ, Pakbiers MT, Heidendal GA, Saris WH. Beta-adrenergic stimulation and abdominal subcutaneous fat blood flow in lean, obese, and reduced-obese subjects. Metabolism. 1995; 44:183-187.
20. Goossens GH, Jocken JW, Blaak EE, Schiffers PM, Saris WH, van Baak MA. Endocrine role of the renin-angiotensin system in human adipose tissue and muscle: effect of beta-adrenergic stimulation. Hypertension. 2007;49:542-547.
21. Jansson PA, Larsson A, Lonnroth PN. Relationship between blood pressure, metabolic variables and blood flow in obese subjects with or without non-insulin-dependent diabetes mellitus. Eur J Clin Invest. 1998; 28:813-818. (Pubitemid 28488114)
22. Karpe F, Fielding BA, Ilic V, Macdonald IA, Summers LK, Frayn KN. Impaired postprandial adipose tissue blood flow response is related to aspects of insulin sensitivity. Diabetes. 2002;51:2467-2473. (Pubitemid 34827395)
23. Goossens GH, Blaak EE, Saris WH, van Baak MA. Angiotensin II-induced effects on adipose and skeletal muscle tissue blood flow and lipolysis in normal-weight and obese subjects. J Clin Endocrinol Metab. 2004;89:2690-2696. (Pubitemid 38766351)
24. Bizzarri A, Koehler H, Cajlakovic M, Pasic A, Schaupp L, Klimant I, Ribitsch V. Continuous oxygen monitoring in subcutaneous adipose tissue using microdialysis. Anal Chim Acta. 2006;573-574:48-56. (Pubitemid 44066950)
25. Schiffelers SL, Akkermans JA, Saris WH, Blaak EE. Lipolytic and nutritive blood flow response to beta-adrenoceptor stimulation in situ in subcutaneous abdominal adipose tissue in obese men. Int J Obes. 2003;27:227-231. (Pubitemid 36255805)
26. Samra JS, Frayn KN, Giddings JA, Clark ML, Macdonald IA. Modification and validation of a commercially available portable detector for measurement of adipose tissue blood flow. Clin Physiol. 1995;15:241-248.
27. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol. 1979;237: E214-E223. (Pubitemid 9249478)
28. Dominguez de Villota ED, Ruiz Carmona MT, Rubio JJ, de Andres S. Equality of the in vivo and in vitro oxygen-binding capacity of haemoglobin in patients with severe respiratory disease. Br J Anaesth. 1981;53: 1325-1328. (Pubitemid 12248935)
29. O'Hagan KA, Cocchiglia S, Zhdanov AV, Tambuwala MM, Cummins EP, Monfared M, Agbor TA, Garvey JF, Papkovsky DB, Taylor CT, Allan BB. PGC-1alpha is coupled to HIF-1alpha-dependent gene expression by increasing mitochondrial oxygen consumption in skeletal muscle cells. Proc Natl Acad Sci USA. 2009;106:2188-2193.
30. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature. 2008;451: 1008-1012. (Pubitemid 351301733)
31. Lolmede K, Durand de Saint Front V, Galitzky J, Lafontan M, Bouloumie A. Effects of hypoxia on the expression of proangiogenic factors in differentiated 3T3-F442A adipocytes. Int J Obes. 2003;27:1187-1195. (Pubitemid 37281666)
32. Zhang K, Lu J, Mori T, Smith-Powell L, Synold TW, Chen S, Wen W. Baicalin increases VEGF expression and angiogenesis by activating the ERR{alpha}/PGC-1{alpha} pathway. Cardiovasc Res. 2011;89: 426-435.
33. Hausman GJ, Richardson RL. Adipose tissue angiogenesis. J Anim Sci. 2004;82:925-934. (Pubitemid 38572359)
34. Xue Y, Petrovic N, Cao R, Larsson O, Lim S, Chen S, Feldmann HM, Liang Z, Zhu Z, Nedergaard J, Cannon B, Cao Y. Hypoxia-independent angiogenesis in adipose tissues during cold acclimation. Cell Metab. 2009;9:99-109.
35. Ye J. Emerging role of adipose tissue hypoxia in obesity and insulin resistance. Int J Obes. 2009;33:54-66.
36. Levin BE, Finnegan MB, Marquet E, Sullivan AC. Defective brown adipose oxygen consumption in obese Zucker rats. Am J Physiol. 1984; 247:E94-E100. (Pubitemid 14096132)
37. Wilson-Fritch L, Nicoloro S, Chouinard M, Lazar MA, Chui PC, Leszyk J, Straubhaar J, Czech MP, Corvera S. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J Clin Invest. 2004;114:1281-1289. (Pubitemid 40385299)
38. Rong JX, Qiu Y, Hansen MK, Zhu L, Zhang V, Xie M, Okamoto Y, Mattie MD, Higashiyama H, Asano S, Strum JC, Ryan TE. Adipose mitochondrial biogenesis is suppressed in db/db and high-fat diet-fed mice and improved by rosiglitazone. Diabetes. 2007;56:1751-1760. (Pubitemid 47025441)
39. 2 consumption of human adipose tissue. Am J Physiol. 1989;256:E467-E474.
40. Perez-Matute P, Neville MJ, Tan GD, Frayn KN, Karpe F. Transcrip-tional control of human adipose tissue blood flow. Obesity. 2009;17: 681-688.
41. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C, Bracale R, Valerio A, Francolini M, Moncada S, Carruba MO. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science. 2003;299:896-899. (Pubitemid 36182449)
42. Nisoli E, Falcone S, Tonello C, Cozzi V, Palomba L, Fiorani M, Pisconti A, Brunelli S, Cardile A, Francolini M, Cantoni O, Carruba MO, Moncada S, Clementi E. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc Natl Acad Sci USA. 2004;101:16507-16512. (Pubitemid 39557743)
43. Valerio A, Cardile A, Cozzi V, Bracale R, Tedesco L, Pisconti A, Palomba L, Cantoni O, Clementi E, Moncada S, Carruba MO, Nisoli E. TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest. 2006;116:2791-2798. (Pubitemid 44511642)
44. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114:1752-1761. (Pubitemid 40385531)
45. Wang T, Si Y, Shirihai OS, Si H, Schultz V, Corkey RF, Hu L, Deeney JT, Guo W, Corkey BE. Respiration in adipocytes is inhibited by reactive oxygen species. Obesity. 2010;18:1493-1502.