Adipocyte-specific mineralocorticoid receptor overexpression in mice is associated with metabolic syndrome and vascular dysfunction: Role of redox-sensitive PKG-1 and Rho kinase

Diabetes

Volumn 65, Issue 8, 2016, Pages 2392-2403

  Cat, Aurelie Nguyen Dinh ^a   Antunes, Tayze T ^b   Callera, Glaucia E ^b   Sanchez, Ana ^c   Tsiropoulou, Sofia ^a   Dulak Lis, Maria G ^a   Anagnostopoulou, Aikaterini ^a   He, Ying ^b   Montezano, Augusto C ^a   Jaisser, Frederic ^d   Touyz, Rhian M ^a,b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALDOSTERONE; ANGIOTENSIN II; CORTICOSTERONE; CYCLIC GMP DEPENDENT PROTEIN KINASE 1; HYDROGEN PEROXIDE; INSULIN RECEPTOR SUBSTRATE 1; MINERALOCORTICOID RECEPTOR; RHO KINASE; CONDITIONED MEDIUM; ELASTIN;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONDITIONED MEDIUM; ENZYMATIC ASSAY; GENE OVEREXPRESSION; MESENTERIC ARTERY; METABOLIC SYNDROME X; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; GENETICS; HUMAN; INTRAABDOMINAL FAT; MALE; METABOLISM; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; VASCULAR SMOOTH MUSCLE;

ADIPOCYTES; ALDOSTERONE; ANGIOTENSIN II; ANIMALS; CELLS, CULTURED; CORTICOSTERONE; CULTURE MEDIA, CONDITIONED; ELASTIN; HUMANS; INTRA-ABDOMINAL FAT; MALE; METABOLIC SYNDROME X; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; OXIDATION-REDUCTION; PHOSPHORYLATION; RECEPTORS, MINERALOCORTICOID; RHO-ASSOCIATED KINASES;

EID: 84980317610     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-1627     Document Type: Article

References (57)

1. Sainte-Marie Y, Nguyen Dinh Cat A, Perrier R, et al. Conditional glucocorticoid receptor expression in the heart induces atrio-ventricular block. FASEB J 2007;21:3133-3141
2. Nguyen Dinh Cat A, Griol-Charhbili V, Loufrani L, et al. The endothelial mineralocorticoid receptor regulates vasoconstrictor tone and blood pressure. FASEB J 2010;24:2454-2463
3. McCurley A, Pires PW, Bender SB, et al. Direct regulation of blood pressure by smooth muscle cell mineralocorticoid receptors. Nat Med 2012;18:1429-1433
4. Lim HY, Müller N, Herold MJ, van den Brandt J, Reichardt HM. Glucocorticoids exert opposing effects on macrophage function dependent on their concentration. Immunology 2007;122:47-53
5. Usher MG, Duan SZ, Ivaschenko CY, et al. Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J Clin Invest 2010;120:3350-3364
6. Guo C, Ricchiuti V, Lian BQ, et al. Mineralocorticoid receptor blockade reverses obesity-related changes in expression of adiponectin, peroxisome proliferator-activated receptor-gamma, and proinflammatory adipokines. Circulation 2008;117:2253-2261
7. Leopold JA, Dam A, Maron BA, et al. Aldosterone impairs vascular reactivity by decreasing glucose-6-phosphate dehydrogenase activity. Nat Med 2007;13: 189-197
8. Messaoudi S, Azibani F, Delcayre C, Jaisser F. Aldosterone, mineralocorticoid receptor, and heart failure. Mol Cell Endocrinol 2012;350:266-272
9. Bender SB, McGraw AP, Jaffe IZ, Sowers JR. Mineralocorticoid receptormediated vascular insulin resistance: an early contributor to diabetes-related vascular disease? Diabetes 2013;62:313-319
10. Schäfer N, Lohmann C, Winnik S, et al. Endothelial mineralocorticoid receptor activation mediates endothelial dysfunction in diet-induced obesity. Eur Heart J 2013;34:3515-3524
11. Caprio M, Fève B, Claës A, Viengchareun S, Lombès M, Zennaro MC. Pivotal role of the mineralocorticoid receptor in corticosteroid-induced adipogenesis. FASEB J 2007;21:2185-2194
12. Nguyen Dinh Cat A, Briones AM, Callera GE, et al. Adipocyte-derived factors regulate vascular smooth muscle cells through mineralocorticoid and glucocorticoid receptors. Hypertension 2011;58:479-488
13. Briones AM, Nguyen Dinh Cat A, Callera GE, et al. Adipocytes produce aldosterone through calcineurin-dependent signaling pathways: implications in diabetes mellitus-associated obesity and vascular dysfunction. Hypertension 2012;59:1069-1078
14. Urbanet R, Nguyen Dinh Cat A, Feraco A, et al. Adipocyte mineralocorticoid receptor activation leads to metabolic syndrome and induction of prostaglandin D2 synthase. Hypertension 2015;66:149-157
15. Hirata A, Maeda N, Nakatsuji H, et al. Contribution of glucocorticoid-mineralocorticoid receptor pathway on the obesity-related adipocyte dysfunction. Biochem Biophys Res Commun 2012;419:182-187
16. Halberg N, Wernstedt-Asterholm I, Scherer PE. The adipocyte as an endocrine cell. Endocrinol Metab Clin North Am 2008;37:753-768, x-xi
17. Karastergiou K, Mohamed-Ali V. The autocrine and paracrine roles of adipokines. Mol Cell Endocrinol 2010;318:69-78
18. Hirata A, Maeda N, Hiuge A, et al. Blockade of mineralocorticoid receptor reverses adipocyte dysfunction and insulin resistance in obese mice. Cardiovasc Res 2009;84:164-172
19. Tirosh A, Garg R, Adler GK. Mineralocorticoid receptor antagonists and the metabolic syndrome. Curr Hypertens Rep 2010;12:252-257
20. Marzolla V, Armani A, Zennaro MC, et al. The role of the mineralocorticoid receptor in adipocyte biology and fat metabolism. Mol Cell Endocrinol 2012;350: 281-288
21. Yarmo MN, Landry A, Molgat AS, Gagnon A, Sorisky A. Macrophage-conditioned medium inhibits differentiation-induced Rb phosphorylation in 3T3-L1 preadipocytes. Exp Cell Res 2009;315:411-418
22. Omar A, Chatterjee TK, Tang Y, Hui DY, Weintraub NL. Proinflammatory phenotype of perivascular adipocytes. Arterioscler Thromb Vasc Biol 2014;34: 1631-1636
23. Taylor MS, Okwuchukwuasanya C, Nickl CK, Tegge W, Brayden JE, Dostmann WR. Inhibition of cGMP-dependent protein kinase by the cell-permeable peptide DT-2 reveals a novel mechanism of vasoregulation. Mol Pharmacol 2004;65: 1111-1119
24. Hirosumi J, Tuncman G, Chang L, et al. A central role for JNK in obesity and insulin resistance. Nature 2002;420:333-336
25. Sugita M, Sugita H, Kaneki M. Increased insulin receptor substrate 1 serine phosphorylation and stress-activated protein kinase/c-Jun N-terminal kinase activation associated with vascular insulin resistance in spontaneously hypertensive rats. Hypertension 2004;44:484-489
26. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 2002;277:1531-1537
27. Burgoyne JR, Madhani M, Cuello F, et al. Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science 2007;317:1393-1397
28. Noma K, Oyama N, Liao JK. Physiological role of ROCKs in the cardiovascular system. Am J Physiol Cell Physiol 2006;290:C661-C668
29. Cassis LA, Police SB, Yiannikouris F, Thatcher SE. Local adipose tissue renin-angiotensin system. Curr Hypertens Rep 2008;10:93-98
30. Bindom SM, Lazartigues E. The sweeter side of ACE2: physiological evidence for a role in diabetes. Mol Cell Endocrinol 2009;302:193-202
31. Santos SH, Fernandes LR, Pereira CS, et al. Increased circulating angiotensin-(1-7) protects white adipose tissue against development of a proinflammatory state stimulated by a high-fat diet. Regul Pept 2012;178:64-70
32. Caprio M, Antelmi A, Chetrite G, et al. Antiadipogenic effects of the mineralocorticoid receptor antagonist drospirenone: potential implications for the treatment of metabolic syndrome. Endocrinology 2011;152:113-125
33. Makki K, Froguel P, Wolowczuk I. Adipose tissue in obesity-related inflammation and insulin resistance: cells, cytokines, and chemokines. ISRN Inflamm 2013;2013:139239
34. Chen W, Liu DJ, Huo YM, Wu ZY, Sun YW. Reactive oxygen species are involved in regulating hypocontractility of mesenteric artery to norepinephrine in cirrhotic rats with portal hypertension. Int J Biol Sci 2014;10:386-395
35. Grace JA, Klein S, Herath CB, et al. Activation of the MAS receptor by angiotensin-(1-7) in the renin-angiotensin system mediates mesenteric vasodilatation in cirrhosis. Gastroenterology 2013;145:874-884.e5
36. Loirand G, Guilluy C, Pacaud P. Regulation of Rho proteins by phosphorylation in the cardiovascular system. Trends Cardiovasc Med 2006;16:199-204
37. Kimura K, Ito M, Amano M, et al. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 1996;273:245-248
38. Seko T, Ito M, Kureishi Y, et al. Activation of RhoA and inhibition of myosin phosphatase as important components in hypertension in vascular smooth muscle. Circ Res 2003;92:411-418
39. Guilluy C, Sauzeau V, Rolli-Derkinderen M, et al. Inhibition of RhoA/Rho kinase pathway is involved in the beneficial effect of sildenafil on pulmonary hypertension. Br J Pharmacol 2005;146:1010-1018
40. Laufs U, Endres M, Stagliano N, et al. Neuroprotection mediated by changes in the endothelial actin cytoskeleton. J Clin Invest 2000;106:15-24
41. Takemoto M, Sun J, Hiroki J, Shimokawa H, Liao JK. Rho-kinase mediates hypoxia-induced downregulation of endothelial nitric oxide synthase. Circulation 2002;106:57-62
42. Wolfrum S, Dendorfer A, Rikitake Y, et al. Inhibition of Rho-kinase leads to rapid activation of phosphatidylinositol 3-kinase/protein kinase Akt and cardiovascular protection. Arterioscler Thromb Vasc Biol 2004;24:1842-1847
43. Tokuyama H, Wakino S, Hara Y, et al. Role of mineralocorticoid receptor/Rho/Rho-kinase pathway in obesity-related renal injury. Int J Obes 2012;36:1062-1071
44. Noda K, Nakajima S, Godo S, et al. Rho-kinase inhibition ameliorates metabolic disorders through activation of AMPK pathway in mice. PLoS One 2014;9:e110446
45. Furukawa S, Fujita T, Shimabukuro M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752-1761
46. Chattopadhyay M, Khemka VK, Chatterjee G, Ganguly A, Mukhopadhyay S, Chakrabarti S. Enhanced ROS production and oxidative damage in subcutaneous white adipose tissue mitochondria in obese and type 2 diabetes subjects. Mol Cell Biochem 2015;399:95-103
47. Rodríguez-Martínez MA, García-Cohen EC, Baena AB, González R, Salaíces M, Marín J. Contractile responses elicited by hydrogen peroxide in aorta from normotensive and hypertensive rats. Endothelial modulation and mechanism involved. Br J Pharmacol 1998;125:1329-1335
48. Gao YJ, Lee RM. Hydrogen peroxide induces a greater contraction in mesenteric arteries of spontaneously hypertensive rats through thromboxane A(2) production. Br J Pharmacol 2001;134:1639-1646
49. Moreno JM, Rodriguez Gomez I, Wangensteen R, et al. Mechanisms of hydrogen peroxide-induced vasoconstriction in the isolated perfused rat kidney. J Physiol Pharmacol 2010;61:325-332
50. Yang Z, Zhang A, Altura BT, Altura BM. Hydrogen peroxide-induced endotheliumdependent relaxation of rat aorta involvement of Ca2+ and other cellular metabolites. Gen Pharmacol 1999;33:325-336
51. Matoba T, Shimokawa H, Nakashima M, et al. Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in mice. J Clin Invest 2000;106: 1521-1530
52. Fujimoto S, Asano T, Sakai M, et al. Mechanisms of hydrogen peroxideinduced relaxation in rabbit mesenteric small artery. Eur J Pharmacol 2001;459: 291-300
53. Waldman SA, Murad F. Biochemical mechanisms underlying vascular smooth muscle relaxation: the guanylate cyclase-cyclic GMP system. J Cardiovasc Pharmacol 1988;12(Suppl. 5):S115-S118
54. Fujimoto S, Mori M, Tsushima H. Mechanisms underlying the hydrogen peroxide-induced, endothelium-independent relaxation of the norepinephrine-contraction in guinea-pig aorta. Eur J Pharmacol 2003;459:65-73
55. Cai H. Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovasc Res 2005;68:26-36
56. 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
57. Prysyazhna O, Rudyk O, Eaton P. Single atom substitution in mouse protein kinase G eliminates oxidant sensing to cause hypertension. Nat Med 2012;18: 286-290