Table of Contents Author Guidelines Submit a Manuscript
International Journal of Endocrinology
Volume 2013, Article ID 402053, 8 pages
http://dx.doi.org/10.1155/2013/402053
Review Article

Mechanisms of Perivascular Adipose Tissue Dysfunction in Obesity

1Instituto Pluridisciplinar and Facultad de Farmacia, Universidad Complutense, Juan XXIII 1, 28040 Madrid, Spain
2Departamento de Ciencias Farmacéuticas y de la Salud, Facultad de Farmacia, Universidad CEU-San Pablo, 28660 Madrid, Spain

Received 26 July 2013; Accepted 29 August 2013

Academic Editor: Micaela Iantorno

Copyright © 2013 Maria S. Fernández-Alfonso et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Poirier, T. D. Giles, G. A. Bray et al., “Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on obesity and heart disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism,” Circulation, vol. 113, no. 6, pp. 898–918, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. J. E. Manson, W. C. Willett, M. J. Stampfer et al., “Body weight and mortality among women,” New England Journal of Medicine, vol. 333, no. 11, pp. 677–685, 1995. View at Publisher · View at Google Scholar · View at Scopus
  3. T. A. Kotchen, “Obesity-related hypertension: epidemiology, pathophysiology, and clinical management,” American Journal of Hypertension, vol. 23, no. 11, pp. 1170–1178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. E. E. Soltis and L. A. Cassis, “Influence of perivascular adipose tissue on rat aortic smooth muscle responsiveness,” Clinical and Experimental Hypertension A, vol. 13, no. 2, pp. 277–296, 1991. View at Google Scholar · View at Scopus
  5. M. Löhn, G. Dubrovska, B. Lauterbach, F. C. Luft, M. Gollasch, and A. M. Sharma, “Periadventitial fat releases a vascular relaxing factor,” FASEB Journal, vol. 16, no. 9, pp. 1057–1063, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Moncada, “Prostacyclin, EDRF and atherosclerosis,” Advances in Experimental Medicine and Biology, vol. 243, pp. 1–11, 1988. View at Google Scholar · View at Scopus
  7. M. Gollasch and G. Dubrovska, “Paracrine role for periadventitial adipose tissue in the regulation of arterial tone,” Trends in Pharmacological Sciences, vol. 25, no. 12, pp. 647–653, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. Y. J. Gao, “Dual modulation of vascular function by perivascular adipose tissue and its potential correlation with adiposity/lipoatrophy-related vascular dysfunction,” Current Pharmaceutical Design, vol. 13, no. 21, pp. 2185–2192, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. S. Fernández-Alfonso, M. Gil-Ortega, and B. Somoza, “Role of perivascular adipose tissue in vascular function,” in Advances in Vascular Medicine, pp. 175–186, Springer, New York, NY, USA, 2010. View at Google Scholar
  10. G. Dubrovska, S. Verlohren, F. C. Luft, and M. Gollasch, “Mechanisms of ADRF release from rat aortic adventitial adipose tissue,” American Journal of Physiology, vol. 286, no. 3, pp. H1107–H1113, 2004. View at Google Scholar · View at Scopus
  11. G. Fésüs, G. Dubrovska, K. Gorzelniak et al., “Adiponectin is a novel humoral vasodilator,” Cardiovascular Research, vol. 75, no. 4, pp. 719–727, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Gálvez, J. De Castro, D. Herold et al., “Perivascular adipose tissue and mesenteric vascular function in spontaneously hypertensive rats,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 6, pp. 1297–1302, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Verlohren, G. Dubrovska, S. Tsang et al., “Visceral periadventitial adipose tissue regulates arterial tone of mesenteric arteries,” Hypertension, vol. 44, no. 3, pp. 271–276, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Lu, L. Su, R. M. K. W. Lee, and Y. Gao, “Mechanisms for perivascular adipose tissue-mediated potentiation of vascular contraction to perivascular neuronal stimulation: the role of adipocyte-derived angiotensin II,” European Journal of Pharmacology, vol. 634, no. 1–3, pp. 107–112, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. J. Gao, K. Takemori, L. Y. Su et al., “Perivascular adipose tissue promotes vasoconstriction: the role of superoxide anion,” Cardiovascular Research, vol. 71, no. 2, pp. 363–373, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Gálvez-Prieto, B. Somoza, M. Gil-Ortega et al., “Anticontractile effect of perivascular adipose tissue and leptin are reduced in hypertension,” Front Pharmacol, vol. 3, no. 103, pp. 1–8, 2012. View at Google Scholar
  17. M. Gil-Ortega, P. Stucchi, R. Guzmán-Ruiz et al., “Adaptative nitric oxide overproduction in perivascular adipose tissue during early diet-induced obesity,” Endocrinology, vol. 151, no. 7, pp. 3299–3306, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Somoza, R. Guzmán, V. Cano et al., “Induction of cardiac uncoupling protein-2 expression and adenosine 5′-monophosphate-activated protein kinase phosphorylation during early states of diet-induced obesity in mice,” Endocrinology, vol. 148, no. 3, pp. 924–931, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Ma, S. Ma, H. He et al., “Perivascular fat-mediated vascular dysfunction and remodeling through the AMPK/mTOR pathway in high-fat diet-induced obese rats,” Hypertension Research, vol. 33, no. 5, pp. 446–453, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. A. S. Greenstein, K. Khavandi, S. B. Withers et al., “Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients,” Circulation, vol. 119, no. 12, pp. 1661–1670, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Iacobellis, M. C. Ribaudo, F. Assael et al., “Echocardiographic epicardial adipose tissue is related to anthropometric and clinical parameters of metabolic syndrome: a new indicator of cardiovascular risk,” Journal of Clinical Endocrinology and Metabolism, vol. 88, no. 11, pp. 5163–5168, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. J. Gao, A. C. Holloway, Z. Zeng et al., “Prenatal exposure to nicotine causes postnatal obesity and altered perivascular adipose tissue function,” Obesity Research, vol. 13, no. 4, pp. 687–692, 2005. View at Google Scholar · View at Scopus
  23. M. K. Owen, F. A. Witzmann, M. L. McKenney et al., “Perivascular adipose tissue potentiates contraction of coronary vascular smooth muscle: influence of obesity,” Circulation, vol. 128, no. 1, pp. 9–18, 2013. View at Google Scholar
  24. Y. J. Gao, Z. H. Zeng, K. Teoh et al., “Perivascular adipose tissue modulates vascular function in the human internal thoracic artery,” Journal of Thoracic and Cardiovascular Surgery, vol. 130, no. 4, pp. 1130–1136, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Malinowski, M. A. Deja, K. S. Gołba, T. Roleder, J. Biernat, and S. Woś, “Perivascular tissue of internal thoracic artery releases potent nitric oxide and prostacyclin-independent anticontractile factor,” European Journal of Cardio-thoracic Surgery, vol. 33, no. 2, pp. 225–231, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. C. Lee, H. H. Chang, C. L. Chiang et al., “Role of perivascular adipose tissue-derived methyl palmitate in vascular tone regulation and pathogenesis of hypertension,” Circulation, vol. 124, no. 10, pp. 1160–1171, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. A. H. Weston, I. Egner, Y. Dong, E. L. Porter, A. M. Heagerty, and G. Edwards, “Stimulated release of a hyperpolarizing factor (ADHF) from mesenteric artery perivascular adipose tissue: involvement of myocyte BKCa channels and adiponectin,” British Journal of Pharmacology, vol. 169, no. 7, pp. 1500–1509, 2013. View at Google Scholar
  28. M. Gil-Ortega, B. Somoza, I. Aranguez, M. Ruiz-Gayo, and M. S. Fernández-Alfonso, “Changes in resistance artery function during the development of diet-induced obesity,” Hypertension, vol. 54, no. 4, pp. 105–106, 2009. View at Google Scholar
  29. L. Fang, J. Zhao, Y. Chen et al., “Hydrogen sulfide derived from periadventitial adipose tissue is a vasodilator,” Journal of Hypertension, vol. 27, no. 11, pp. 2174–2185, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Schleifenbaum, C. Köhn, N. Voblova et al., “Systemic peripheral artery relaxation by KCNQ channel openers and hydrogen sulfide,” Journal of Hypertension, vol. 28, no. 9, pp. 1875–1882, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Gollasch, “Vasodilator signals from perivascular adipose tissue,” British Journal of Pharmacology, vol. 165, no. 3, pp. 633–642, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Yang, L. Wu, B. Jiang et al., “H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase,” Science, vol. 322, no. 5901, pp. 587–590, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Wójcicka, A. Jamroz-Wiśniewska, P. Atanasova, G. N. Chaldakov, B. Chylińska-Kula, and J. Bełtowski, “Differential effects of statins on endogenous H2S formation in perivascular adipose tissue,” Pharmacological Research, vol. 63, no. 1, pp. 68–76, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. J. D. Knudson, G. A. Payne, L. Borbouse, and J. D. Tune, “Leptin and mechanisms of endothelial dysfunction and cardiovascular disease,” Current Hypertension Reports, vol. 10, no. 6, pp. 434–439, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. C. F. Elias, C. Lee, J. Kelly et al., “Leptin activates hypothalamic CART neurons projecting to the spinal cord,” Neuron, vol. 21, no. 6, pp. 1375–1385, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Lembo, C. Vecchione, L. Fratta et al., “Leptin induces direct vasodilation through distinct endothelial mechanisms,” Diabetes, vol. 49, no. 2, pp. 293–297, 2000. View at Google Scholar · View at Scopus
  37. C. Vecchione, A. Maffei, S. Colella et al., “Leptin effect on endothelial nitric oxide is mediated through Akt-endothelial nitric oxide synthase phosphorylation pathway,” Diabetes, vol. 51, no. 1, pp. 168–173, 2002. View at Google Scholar · View at Scopus
  38. G. Frühbeck, “Pivotal role of nitric oxide in the control of blood pressure after leptin administration,” Diabetes, vol. 48, no. 4, pp. 903–908, 1999. View at Google Scholar · View at Scopus
  39. A. Rodríguez, A. Fortuño, J. Gómez-Ambrosi, G. Zalba, J. Díez, and G. Frühbeck, “The inhibitory effect of leptin on angiotensin II-induced vasoconstriction in vascular smooth muscle cells is mediated via a nitric oxide-dependent mechanism,” Endocrinology, vol. 148, no. 1, pp. 324–331, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Dashwood, D. Souza, and M. S. Fernández-Alfonso, “Perivascular tissue of internal thoracic artery releases potent nitric oxide and prostacyclin-independent anticontractile factor,” European Journal of Cardio-Thoracic Surgery, vol. 33, no. 6, pp. 1161–1162, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. M. R. Schroeter, N. Eschholz, S. Herzberg et al., “Leptin-dependent and leptin-independent paracrine effects of perivascular adipose tissue on neointima formation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, no. 5, pp. 980–987, 2013. View at Google Scholar
  42. G. A. Payne, L. Borbouse, S. Kumar et al., “Epicardial perivascular adipose-derived leptin exacerbates coronary endothelial dysfunction in metabolic syndrome via a protein kinase C-β pathway,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 9, pp. 1711–1717, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Hattori, M. Suzuki, S. Hattori, and K. Kasai, “Globular adiponectin upregulates nitric oxide production in vascular endothelial cells,” Diabetologia, vol. 46, no. 11, pp. 1543–1549, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Chen, M. Montagnani, T. Funahashi, I. Shimomura, and M. J. Quon, “Adiponectin stimulates production of nitric oxide in vascular endothelial cells,” Journal of Biological Chemistry, vol. 278, no. 45, pp. 45021–45026, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Ouchi, S. Kihara, T. Funahashi, Y. Matsuzawa, and K. Walsh, “Obesity, adiponectin and vascular inflammatory disease,” Current Opinion in Lipidology, vol. 14, no. 6, pp. 561–566, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. C. Kobashi, M. Urakaze, M. Kishida et al., “Adiponectin inhibits endothelial synthesis of interleukin-8,” Circulation Research, vol. 97, no. 12, pp. 1245–1252, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Ardanaz and P. J. Pagano, “Hydrogen peroxide as a paracrine vascular mediator: regulation and signaling leading to dysfunction,” Experimental Biology and Medicine, vol. 231, no. 3, pp. 237–251, 2006. View at Google Scholar · View at Scopus
  48. J. Gil-Longo and C. González-Vázquez, “Characterization of four different effects elicited by H2O2 in rat aorta,” Vascular Pharmacology, vol. 43, no. 2, pp. 128–138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Suvorava, N. Lauer, S. Kumpf, R. Jacob, W. Meyer, and G. Kojda, “Endogenous vascular hydrogen peroxide regulates arteriolar tension in vivo,” Circulation, vol. 112, no. 16, pp. 2487–2495, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. I. Al Ghouleh, G. Frazziano, A. I. Rodriguez et al., “Aquaporin 1, Nox1, and Ask1 mediate oxidant-induced smooth muscle cell hypertrophy,” Cardiovascular Research, vol. 1, no. 1, pp. 134–142, 2013. View at Google Scholar
  51. P. A. Rogers, G. M. Dick, J. D. Knudson et al., “H2O2-induced redox-sensitive coronary vasodilation is mediated by 4-aminopyridine-sensitive K+ channels,” American Journal of Physiology, vol. 291, no. 5, pp. H2473–H2482, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Ketonen, J. Shi, E. Martonen, and E. Mervaala, “Periadventitial adipose tissue promotes endothelial dysfunction via oxidative stress in diet-induced obese C57BL/6 mice,” Circulation Journal, vol. 74, no. 7, pp. 1479–1487, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Marchesi, T. Ebrahimian, O. Angulo, P. Paradis, and E. L. Schiffrin, “Endothelial nitric oxide synthase uncoupling and perivascular adipose oxidative stress and inflammation contribute to vascular dysfunction in a rodent model of metabolic syndrome,” Hypertension, vol. 54, no. 6, pp. 1384–1392, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Rebolledo, O. R. Rebolledo, C. A. Marra et al., “Early alterations in vascular contractility associated to changes in fatty acid composition and oxidative stress markers in perivascular adipose tissue,” Cardiovascular Diabetology, vol. 9, p. 65, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. L. C. Bailey-Downs, Z. Tucsek, P. Toth et al., “Aging exacerbates obesity-induced oxidative stress and inflammation in perivascular adipose tissue in mice: a paracrine mechanism contributing to vascular redox dysregulation and inflammation,” Journals of Gerontology A, vol. 68, no. 7, pp. 780–792, 2013. View at Google Scholar
  56. T. K. Chatterjee, L. L. Stoll, G. M. Denning et al., “Proinflammatory phenotype of perivascular adipocytes: influence of high-fat feeding,” Circulation Research, vol. 104, no. 4, pp. 541–549, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Wang, W. Luo, J. Wang et al., “Obesity-induced endothelial dysfunction is prevented by deficiency of p-selectin glycoprotein ligand-1,” Diabetes, vol. 61, no. 12, pp. 3219–3227, 2012. View at Publisher · View at Google Scholar
  58. T. P. Fitzgibbons, S. Kogan, M. Aouadi, G. M. Hendricks, J. Straubhaar, and M. P. Czech, “Similarity of mouse perivascular and brown adipose tissues and their resistance to diet-induced inflammation,” American Journal of Physiology, vol. 301, no. 4, pp. H1425–H1437, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. N. Hosogai, A. Fukuhara, K. Oshima et al., “Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation,” Diabetes, vol. 56, no. 4, pp. 901–911, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. M. E. Rausch, S. Weisberg, P. Vardhana, and D. V. Tortoriello, “Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration,” International Journal of Obesity, vol. 32, no. 3, pp. 451–463, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Maenhaut, C. Boydens, and J. Van de Voorde, “Hypoxia enhances the relaxing influence of perivascular adipose tissue in isolated mice aorta,” European Journal of Pharmacology, vol. 641, no. 2-3, pp. 207–212, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. L. C. Bailey-Downs, Z. Tucsek, P. Toth et al., “Aging exacerbates obesity-induced oxidative stress and inflammation in perivascular adipose tissue in mice: a paracrine mechanism contributing to vascular redox dysregulation and inflammation,” Journals of Gerontology A, vol. 68, no. 7, pp. 780–792, 2012. View at Google Scholar
  63. C. Barandier, J. Montani, and Z. Yang, “Mature adipocytes and perivascular adipose tissue stimulate vascular smooth muscle cell proliferation: effects of aging and obesity,” American Journal of Physiology, vol. 289, no. 5, pp. H1807–H1813, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. W. Kosmala, T. O'Moore-Sullivan, R. Plaksej, M. Przewlocka-Kosmala, and T. H. Marwick, “Improvement of left ventricular function by lifestyle intervention in obesity: contributions of weight loss and reduced insulin resistance,” Diabetologia, vol. 52, no. 11, pp. 2306–2316, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Cancello, C. Henegar, N. Viguerie et al., “Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss,” Diabetes, vol. 54, no. 8, pp. 2277–2286, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. R. Aghamohammadzadeh, A. S. Greenstein, R. Yadav et al., “Effects of bariatric surgery on human small artery function: evidence for reduction in perivascular adipocyte inflammation, and the restoration of normal anticontractile activity despite persistent obesity,” Journal of the American College of Cardiology, vol. 62, no. 2, pp. 128–135, 2013. View at Publisher · View at Google Scholar
  67. P. Stucchi, R. Guzmán-Ruiz, M. Gil-Ortega et al., “Leptin resistance develops spontaneously in mice during adult life in a tissue-specific manner. Consequences for hepatic steatosis,” Biochimie, vol. 93, no. 10, pp. 1779–1785, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. R. H. Unger, “The hyperleptinemia of obesity-regulator of caloric surpluses,” Cell, vol. 117, no. 2, pp. 145–146, 2004. View at Publisher · View at Google Scholar · View at Scopus