CGMP-dependent protein kinase (PKG) mediates the anticontractile capacity of perivascular adipose tissue

Cardiovascular Research

Volumn 101, Issue 1, 2014, Pages 130-137

  Withers, Sarah B ^a   Simpson, Laura ^a   Fattah, Sharif ^a   Werner, Matthias E ^b   Heagerty, Anthony M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b BAYER AG   (Germany)

Author keywords

Adipocyte; Adiponectin; PKG; PVAT; Small arteries

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; ADIPONECTIN; ATRIAL NATRIURETIC FACTOR; CYCLIC GMP DEPENDENT PROTEIN KINASE; NORADRENALIN;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY MUSCLE; ARTICLE; BLOOD VESSEL; CONTROLLED STUDY; ENDOTHELIUM; ENZYME INHIBITION; HEART MUSCLE CONTRACTILITY; HISTOLOGY; HYPOXIA; MALE; MESENTERIC ARTERY; MOUSE; MYOGRAPHY; NONHUMAN; OXYGENATION; PARACRINE SIGNALING; PERIVASCULAR ADIPOSE TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE;

ADIPOCYTE; ADIPONECTIN; PKG; PVAT; SMALL ARTERIES;

ADIPONECTIN; ADIPOSE TISSUE; ANIMALS; ANOXIA; ATRIAL NATRIURETIC FACTOR; CYCLIC GMP-DEPENDENT PROTEIN KINASES; MALE; MESENTERIC ARTERIES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOGRAPHY; SUPEROXIDE DISMUTASE; VASOCONSTRICTION;

EID: 84891361753     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt229     Document Type: Article

References (42)

1. Lohn M, Dubrovska G, Lauterbach B, Luft FC, Gollasch M, Sharma AM. Periadventitial fat releases a vascular relaxing factor. FASEB J 2002;16:1057-1063.
2. Dubrovska G, Verlohren S, Luft FC, Gollasch M. Mechanisms of ADRF release from rat aortic adventitial adipose tissue. Am J Physiol Heart Circ Physiol 2004;286:H1107-H1113.
3. Gao YJ, Lu C, Su LY, Sharma AM, Lee RM. Modulation of vascular function by perivascular adipose tissue: the role of endothelium and hydrogen peroxide. Br J Pharmacol 2007;151: 323-331.
4. Greenstein AS, Khavandi K, Withers SB, Sonoyama K, Clancy O, Jeziorska M et al. Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 2009;119:1661-1670.
5. Espinoza-Jimenez A, Peon AN, Terrazas LI. Alternatively activated macrophages in types 1 and 2 diabetes. Mediators Inflamm 2012;2012:815953.
6. 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 (Lond) 2008;32:451-463.
7. Aghamohammadzadeh R, Greenstein AS, Yadav R, Jeziorska M, Hama S, Soltani F 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. J Am Coll Cardiol 2013;62:128-135.
8. Egner I,Waseton A, Porter E, Edwards G. Hyperpolarising effect of perivascular adipose tissue in rat mesenteric artery myocyte: stimulation by b3 adrenoceptor activation. Proceedings of the British Pharmcalogical Society. http://wwwpa2onlineorg/abstracts/vol8issue1 2010.
9. Lynch FM, Withers SB, Yao Z,Werner ME, Edwards G,Weston AH et al. Perivascular adipose tissue-derived adiponectin activates BKca channels to induce anticontractile responses. Am J Physiol Heart Circ Physiol 2013;304:H786-H95.
10. Rapoport RM, Draznin MB, Murad F. Endothelium-dependent relaxation in rat aorta may be mediated through cyclic GMP-dependent protein phosphorylation. Nature 1983;306: 174-176.
11. Nikolic DM, Li Y, Liu S,Wang S. Overexpression of constitutively active PKG-I protects female, but not male mice from diet-induced obesity. Obesity (Silver Spring) 2011;19: 784-791.
12. Draijer R, Vaandrager AB, Nolte C, de Jonge HR,Walter U, van HinsberghVW. Expression of cGMP-dependent protein kinase I and phosphorylation of its substrate, vasodilator-stimulated phosphoprotein, in human endothelial cells of different origin. Circ Res 1995;77:897-905.
13. Alioua A, Huggins JP, Rousseau E. PKG-I alpha phosphorylates the alpha-subunit and upregulates reconstituted GKCa channels from tracheal smooth muscle. Am J Physiol 1995;268:L1057-L1063.
14. Archer SL, Huang JM, Hampl V, Nelson DP, Shultz PJ,Weir EK. Nitric oxide and cGMP cause vasorelaxation by activation of a charybdotoxin-sensitive K channel by cGMP-dependent protein kinase. Proc Natl Acad Sci USA 1994;91:7583-7587.
15. Michael SK, Surks HK,Wang Y, Zhu Y, Blanton R, JamnongjitMet al. High blood pressure arising from a defect in vascular function. Proc Natl Acad Sci USA 2008;105:6702-6707.
16. Withers SB, Agabiti-Rosei C, Livingstone DM, Little MC, Aslam R, Malik RA et al. Macrophage activation is responsible for loss of anticontractile function in inflamed perivascular fat. Arterioscler Thromb Vasc Biol 2011;31:908-913.
17. Zaloudikova M, Vizek M, Herget J. Hyperoxia blunts acute hypoxia-and PGF2alpha-induced pulmonary vasoconstriction in chronically hypoxic rats. Physiol Res 2009;58:917-920.
18. Nickl CK, Raidas SK, Zhao H, Sausbier M, Ruth P, Tegge W et al. (D)-Amino acid analogues of DT-2 as highly selective and superior inhibitors of cGMP-dependent protein kinase Ialpha. Biochim Biophys Acta 2010;1804:524-532.
19. Gil-Ortega M, Stucchi P, Guzman-Ruiz R, Cano V, Arribas S, GonzalezMCet al. Adaptative nitric oxide overproduction in perivascular adipose tissue during early diet-induced obesity. Endocrinology 2010;151:3299-3306.
20. Mehebik N, Jaubert AM, Sabourault D, Giudicelli Y, Ribiere C. Leptin-induced nitric oxide production in white adipocytes is mediated through PKA and MAP kinase activation. Am J Physiol Cell Physiol 2005;289:C379-C387.
21. Ribiere C, Jaubert AM, Sabourault D, Lacasa D, GiudicelliY. Insulin stimulates nitric oxide production in rat adipocytes. Biochem Biophys Res Commun 2002;291:394-399.
22. Pilon G, Penfornis P, Marette A. Nitric oxide production by adipocytes: a role in the pathogenesis of insulin resistance? Horm Metab Res 2000;32:480-484.
23. Tamaoki J, Tagaya E, Yamawaki I, Konno K. Hypoxia impairs nitrovasodilator-induced pulmonary vasodilation: role of Na-K-ATPase activity.AmJ Physiol 1996;271:L172-L177.
24. McQuillan LP, Leung GK, Marsden PA, Kostyk SK, Kourembanas S. Hypoxia inhibits expression of eNOS via transcriptional and posttranscriptional mechanisms. Am J Physiol 1994;267:H1921-H1927.
25. Neo BH, Kandhi S, Ahmad M, Wolin MS. Redox regulation of guanylate cyclase and protein kinase G in vascular responses to hypoxia. Respirat Physiol Neurobiol 2010;174: 259-264.
26. Chen H, Montagnani M, Funahashi T, Shimomura I, Quon MJ. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J Biol Chem 2003;278: 45021-45026.
27. Hattori Y, Suzuki M, Hattori S, Kasai K. Globular adiponectin upregulates nitric oxide production in vascular endothelial cells. Diabetologia 2003;46:1543-1549.
28. Joffin N, Niang F, Forest C, Jaubert AM. Is there NO help for leptin? Biochimie 2012;94: 2104-2110.
29. Yamawaki H, Tsubaki N, Mukohda M, Okada M, Hara Y. Omentin, a novel adipokine, induces vasodilation in rat isolated blood vessels. Biochem Biophys Res Commun 2010; 393:668-672.
30. Chen C, Jiang J, Lu JM, Chai H, Wang X, Lin PH et al. Resistin decreases expression of endothelial nitric oxide synthase through oxidative stress in human coronary artery endothelial cells. Am J Physiol Heart Circ Physiol 2010;299:H193-H201.
31. Francis SH, Busch JL, Corbin JD, Sibley D. cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 2010;62:525-563.
32. Koh EH, Kim M, Ranjan KC, Kim HS, Park HS, Oh KS et al. eNOS plays a major role in adiponectin synthesis in adipocytes. Am J Physiol Endocrinol Metab 2010;298:E846-E853.
33. Russo I, Del Mese P, Doronzo G, Mattiello L, Viretto M, Bosia A et al. Resistance to the nitric oxide/cyclic guanosine 5?-monophosphate/protein kinase G pathway in vascular smooth muscle cells from the obese Zucker rat, a classical animal model of insulin resistance: role of oxidative stress. Endocrinology 2008;149:1480-1489.
34. Barrett PQ, Isales CM. The role of cyclic nucleotides in atrial natriuretic peptidemediated inhibition of aldosterone secretion. Endocrinology 1988;122:799-808.
35. Tsukamoto O, Fujita M, Kato M, Yamazaki S, Asano Y, Ogai A et al. Natriuretic peptides enhance the production of adiponectin in human adipocytes and in patients with chronic heart failure. J Am Coll Cardiol 2009;53:2070-2077.
36. Nishikimi T, Iemura-Inaba C, Akimoto K, Ishikawa K, Koshikawa S, Matsuoka H. Stimulatory and Inhibitory regulation of lipolysis by the NPR-A/cGMP/PKG and NPR-C/G(i) pathways in rat cultured adipocytes. Regul Pept 2009;153:56-63.
37. Cao Y, Tao L, Yuan Y, Jiao X, Lau WB,Wang Y et al. Endothelial dysfunction in adiponectin deficiency and its mechanisms involved. J Mol Cell Cardiol 2009;46:413-419.
38. Kubota N, Terauchi Y, Yamauchi T, Kubota T, Moroi M, Matsui J et al. Disruption of adiponectin causes insulin resistance and neointimal formation. J Biol Chem 2002;277: 25863-25866.
39. Ohashi K, Kihara S, Ouchi N, Kumada M, Fujita K, Hiuge A et al. Adiponectin replenishment ameliorates obesity-related hypertension. Hypertension 2006;47:1108-1116.
40. Engeli S, Schling P, Gorzelniak K, Boschmann M, Janke J, Ailhaud G et al. The adiposetissue renin-angiotensin-aldosterone system: role in the metabolic syndrome? Int J Biochem Cell Biol 2003;35:807-825.
41. Kern PA, Di Gregorio GB, Lu T, Rassouli N, Ranganathan G. Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression. Diabetes 2003;52:1779-1785.
42. Pfeifer A, Klatt P, Massberg S,NyL, Sausbier M, HirneissCet al. Defectivesmooth muscle regulation in cGMP kinase I-deficient mice. EMBO J 1998;17:3045-3051.