Adipose tissue dysfunction and impaired metabolic health in human obesity: A matter of oxygen?

Frontiers in Endocrinology

Volumn 6, Issue APR, 2015, Pages

  Goossens, Gijs H ^a   Blaak, Ellen E ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Adipose tissue; Blood flow; Hyperoxia; Hypoxia; Inflammation; Metabolism; Obesity; Oxygen tension

Indexed keywords

DIPEPTIDYL PEPTIDASE IV; INTERLEUKIN 6; OXYGEN; REACTIVE OXYGEN METABOLITE; TRIACYLGLYCEROL;

ADIPOCYTE; ADIPOSE TISSUE; ADIPOSE TISSUE BLOOD FLOW; ANGIOGENESIS; ARTICLE; ENERGY METABOLISM; GENE EXPRESSION; HUMAN; HYPOXEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID STORAGE; METABOLIC RATE; METABOLISM; NONHUMAN; OBESITY; OXYGEN DIFFUSION; OXYGEN TENSION; OXYGEN TISSUE LEVEL; POSITIVE END EXPIRATORY PRESSURE; SLEEP DISORDERED BREATHING; TISSUE INJURY;

EID: 84930659522     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2015.00055     Document Type: Article

References (46)

1. Bluher M. Adipose tissue dysfunction contributes to obesity related metabolic diseases. Best Pract Res Clin Endocrinol Metab (2013) 27:163-77. doi: 10.1016/j.beem.2013.02.005.
2. Goossens GH. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav (2008) 94:206-18. doi:10.1016/j.physbeh.2007.10.010.
3. Berg AH, Scherer PE. Adipose tissue, inflammation, and cardiovascular disease. Circ Res (2005) 96:939-49. doi:10.1161/01.RES.0000163635.62927.34.
4. Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest (2004) 114:147-52. doi:10.1172/JCI22422.
5. Rosen ED, Spiegelman BM. What we talk about when we talk about fat. Cell (2014) 156:20-44. doi:10.1016/j.cell.2013.12.012.
6. Trayhurn P. Hypoxia and adipocyte physiology: implications for adipose tissue dysfunction in obesity. Annu Rev Nutr (2014) 34:207-36. doi:10.1146/annurev-nutr-071812-161156.
7. Ye J. Emerging role of adipose tissue hypoxia in obesity and insulin resistance. Int J Obes (Lond) (2009) 33:54-66. doi:10.1038/ijo.2008.229.
8. Trayhurn P, Wood IS. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr (2004) 92:347-55. doi:10.1079/BJN20041213.
9. Goossens GH, Bizzarri A, Venteclef N, Essers Y, Cleutjens JP, Konings E, et al. Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation. Circulation (2011) 124:67-76. doi:10.1161/CIRCULATIONAHA.111.027813.
10. Pasarica M, Sereda OR, Redman LM, Albarado DC, Hymel DT, Roan LE, et al. Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes (2009) 58:718-25. doi:10.2337/db08-1098.
11. 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) 49:542-7. doi:10.1161/01.HYP.0000256091.55393.92.
12. Goossens GH, McQuaid SE, Dennis AL, van Baak MA, Blaak EE, Frayn KN, et al. Angiotensin II: a major regulator of subcutaneous adipose tissue blood flow in humans. J Physiol (2006) 571:451-60. doi:10.1113/jphysiol.2005.101352.
13. 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) 51:2467-73. doi:10.2337/diabetes.51.8.2467.
14. Brahimi-Horn MC, Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett (2007) 581:3582-91. doi:10.1016/j.febslet.2007.06.018.
15. Goossens GH, Moors CC, van der Zijl NJ, Venteclef N, Alili R, Jocken JW, et al. Valsartan improves adipose tissue function in humans with impaired glucose metabolism: a randomized placebo-controlled double-blind trial. PLoS One (2012) 7:e39930. doi:10.1371/journal.pone.0039930.
16. Skurk T, Alberti-Huber C, Herder C, Hauner H. Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab (2007) 92:1023-33. doi:10.1210/jc.2006-1055.
17. 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) 32:451-63. doi:10.1038/sj.ijo.0803744.
18. 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 Endocrinol Metab (2007) 293:E1118-28. doi:10.1152/ajpendo.00435.2007.
19. Yin J, Gao Z, He Q, Zhou D, Guo Z, Ye J. Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue. Am J Physiol Endocrinol Metab (2009) 296:E333-42. doi:10.1152/ajpendo.90760.2008.
20. Goossens GH, Blaak EE. Adipose tissue oxygen tension: implications for chronic metabolic and inflammatory diseases. Curr Opin Clin Nutr Metab Care (2012) 15:539-46. doi:10.1097/MCO.0b013e328358fa87.
21. Hodson L, Humphreys SM, Karpe F, Frayn KN. Metabolic signatures of human adipose tissue hypoxia in obesity. Diabetes (2013) 62:1417-25. doi:10.2337/db12-1032.
22. Levin BE, Finnegan MB, Marquet E, Sullivan AC. Defective brown adipose oxygen consumption in obese Zucker rats. Am J Physiol (1984) 247: E94-100.
23. Wilson-Fritch L, Nicoloro S, Chouinard M, Lazar MA, Chui PC, Leszyk J, et al. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J Clin Invest (2004) 114:1281-9. doi:10.1172/JCI200421752.
24. Rong JX, Qiu Y, Hansen MK, Zhu L, Zhang V, Xie M, et al. Adipose mitochondrial biogenesis is suppressed in db/db and high-fat diet-fed mice and improved by rosiglitazone. Diabetes (2007) 56:1751-60. doi:10.2337/db06-1135.
25. Klimcakova E, Roussel B, Marquez-Quinones A, Kovacova Z, Kovacikova M, Combes M, et al. Worsening of obesity and metabolic status yields similar molecular adaptations in human subcutaneous and visceral adipose tissue: decreased metabolism and increased immune response. J Clin Endocrinol Metab (2011) 96:E73-82. doi:10.1210/jc.2010-1575.
26. Yin X, Lanza IR, Swain JM, Sarr MG, Nair KS, Jensen MD. Adipocyte mitochondrial function is reduced in human obesity independent of fat cell size. J Clin Endocrinol Metab (2014) 99:E209-16. doi:10.1210/jc.2013-3042.
27. Mazzatti D, Lim FL, O'Hara A, Wood IS, Trayhurn P. A microarray analysis of the hypoxia-induced modulation of gene expression in human adipocytes. Arch Physiol Biochem (2012) 118:112-20. doi:10.3109/13813455.2012.654611.
28. Wree A, Mayer A, Westphal S, Beilfuss A, Canbay A, Schick RR, et al. Adipokine expression in brown and white adipocytes in response to hypoxia. J Endocrinol Invest (2012) 35:522-7. doi:10.3275/7964.
29. Yu J, Shi L, Wang H, Bilan PJ, Yao Z, Samaan MC, et al. Conditioned medium from hypoxia-treated adipocytes renders muscle cells insulin resistant. Eur J Cell Biol (2011) 90:1000-15. doi:10.1016/j.ejcb.2011.06.004.
30. Hosogai N, Fukuhara A, Oshima K, Miyata Y, Tanaka S, Segawa K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes (2007) 56:901-11. doi:10.2337/db06-0911.
31. Chen B, Lam KS, Wang Y, Wu D, Lam MC, Shen J, et al. Hypoxia dysregulates the production of adiponectin and plasminogen activator inhibitor-1 independent of reactive oxygen species in adipocytes. Biochem Biophys Res Commun (2006) 341:549-56. doi:10.1016/j.bbrc.2006.01.004.
32. Wang B, Wood IS, Trayhurn P. Dysregulation of the expression and secretion of inflammation-related adipokines by hypoxia in human adipocytes. Pflugers Arch (2007) 455:479-92. doi:10.1007/s00424-007-0301-8.
33. O'Rourke RW, White AE, Metcalf MD, Olivas AS, Mitra P, Larison WG, et al. Hypoxia-induced inflammatory cytokine secretion in human adipose tissue stromovascular cells. Diabetologia (2011) 54:1480-90. doi:10.1007/s00125-011-2103-y.
34. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation (2004) 109:1292-8. doi:10.1161/01.CIR.0000121425.42966.F1.
35. Murdoch C, Muthana M, Lewis CE. Hypoxia regulates macrophage functions in inflammation. J Immunol (2005) 175:6257-63. doi:10.4049/jimmunol.175.10.6257.
36. Geiger K, Leiherer A, Muendlein A, Stark N, Geller-Rhomberg S, Saely CH, et al. Identification of hypoxia-induced genes in human SGBS adipocytes by microarray analysis. PLoS One (2011) 6:e26465. doi:10.1371/journal.pone.0026465.
37. Famulla S, Horrighs A, Cramer A, Sell H, Eckel J. Hypoxia reduces the response of human adipocytes towards TNFalpha resulting in reduced NF-kappaB signaling and MCP-1 secretion. Int J Obes (Lond) (2012) 36:986-92. doi:10.1038/ijo.2011.200.
38. Quintero P, Gonzalez-Muniesa P, Garcia-Diaz DF, Martinez JA. Effects of hyperoxia exposure on metabolic markers and gene expression in 3T3-L1 adipocytes. J Physiol Biochem (2012) 68:663-9. doi:10.1007/s13105-012-0169-8.
39. Famulla S, Schlich R, Sell H, Eckel J. Differentiation of human adipocytes at physiological oxygen levels results in increased adiponectin secretion and isoproterenol-stimulated lipolysis. Adipocyte (2012) 1:132-81. doi:10.4161/adip.19962.
40. Lamers D, Famulla S, Wronkowitz N, Hartwig S, Lehr S, Ouwens DM, et al. Dipeptidyl peptidase 4 is a novel adipokine potentially linking obesity to the metabolic syndrome. Diabetes (2011) 60:1917-25. doi:10.2337/db10-1707.
41. van den Borst B, Schols AM, de Theije C, Boots AW, Kohler SE, Goossens GH, et al. Characterization of the inflammatory and metabolic profile of adipose tissue in a mouse model of chronic hypoxia. J Appl Physiol (1985) (2013) 114:1619-28. doi:10.1152/japplphysiol.00460.2012.
42. Lecoultre V, Peterson CM, Covington JD, Ebenezer PJ, Frost EA, Schwarz JM, et al. Ten nights of moderate hypoxia improves insulin sensitivity in obese humans. Diabetes Care (2013) 36:e197-8. doi:10.2337/dc13-1350.
43. Goossens GH. Comment on Lecoultre et al. Ten nights of moderate hypoxia improves insulin sensitivity in obese humans. Diabetes care 2013;36:e197-e198. Diabetes Care (2014) 37:e155-6. doi:10.2337/dc14-0097.
44. Ip MS, Lam B, Ng MM, Lam WK, Tsang KW, Lam KS. Obstructive sleep apnea is independently associated with insulin resistance. Am J Respir Crit Care Med (2002) 165:670-6. doi:10.1164/ajrccm.165.5.2103001.
45. Punjabi NM, Shahar E, Redline S, Gottlieb DJ, Givelber R, Resnick HE. Sleep-disordered breathing, glucose intolerance, and insulin resistance: the Sleep Heart Health Study. Am J Epidemiol (2004) 160:521-30. doi:10.1093/aje/kwh261.
46. Sharma SK, Agrawal S, Damodaran D, Sreenivas V, Kadhiravan T, Lakshmy R, et al. CPAP for the metabolic syndrome in patients with obstructive sleep apnea. N Engl J Med (2011) 365:2277-86. doi:10.1056/NEJMoa1103944.