The role of the mineralocorticoid receptor in adipocyte biology and fat metabolism

Molecular and Cellular Endocrinology

Volumn 350, Issue 2, 2012, Pages 281-288

  Marzolla, Vincenzo ^b   Armani, Andrea ^a   Zennaro, Maria Christina ^c,d,e   Cinti, Francesca ^a   Mammi, Caterina ^a   Fabbri, Andrea ^f   Rosano, Giuseppe M C ^a   Caprio, Massimiliano ^a  

^a IRCCS SAN RAFFAELE PISANA   (Italy)

^b San Raffaele Sulmona   (Italy)

^c PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^f UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Adipocyte; Adipose tissue; Metabolic syndrome; Mineralocorticoid receptor

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; ALDOSTERONE; ANGIOTENSIN II; DROSPIRENONE; GLUCOCORTICOID; INSULIN; LEPTIN; MINERALOCORTICOID RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCOUPLING PROTEIN;

ADIPOCYTE; ALDOSTERONE RELEASE; ANGIOTENSIN BLOOD LEVEL; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CELL SIZE; CELL TRANSDIFFERENTIATION; GENE EXPRESSION; HUMAN; HYPERTENSION; INFLAMMATION; INSULIN RESISTANCE; LIPID METABOLISM; NONHUMAN; OBESITY; PRIORITY JOURNAL; RECEPTOR BLOCKING; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SUBCUTANEOUS FAT; WHITE ADIPOSE TISSUE;

ADIPOCYTES; ADIPOSE TISSUE; ADRENAL GLANDS; ALDOSTERONE ANTAGONISTS; ANIMALS; HUMANS; LIPID METABOLISM; MODELS, BIOLOGICAL; RECEPTORS, MINERALOCORTICOID;

EID: 84856330068     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.09.011     Document Type: Review

References (96)

1. Ahima R.S., Flier J.S. Adipose tissue as an endocrine organ. Trends Endocrinol. Metab. 2000, 11:327-332.
2. Archer D.F., Thorneycroft I.H., Foegh M., Hanes V., Glant M.D., Bitterman P., Kempson R.L. Long-term safety of drospirenone-estradiol for hormone therapy: a randomized, double-blind, multicenter trial. Menopause 2005, 12:716-727.
3. Armani A., Mammi C., Marzolla V., Calanchini M., Antelmi A., Rosano G.M., Fabbri A., Caprio M. Cellular models for understanding adipogenesis, adipose dysfunction, and obesity. J. Cell. Biochem. 2010, 110:564-572.
4. Armanini D., Strasser T., Weber P.C. Characterization of aldosterone binding sites in circulating human mononuclear leukocytes. Am. J. Physiol. 1985, 248:E388-E390.
5. Arriza J.L., Weinberger C., Cerelli G., Glaser T.M., Handelin B.L., Housman D.E., Evans R.M. Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science 1987, 237:268-275.
6. Barbatelli G., Murano I., Madsen L., Hao Q., Jimenez M., Kristiansen K., Giacobino J.P., De Matteis R., Cinti S. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E1244-E1253.
7. Berg A.H., Scherer P.E. Adipose tissue, inflammation, and cardiovascular disease. Circ. Res. 2005, 96:939-949.
8. Bjorntorp P. Metabolic implications of body fat distribution. Diabetes Care 1991, 14:1132-1143.
9. Bjorntorp P. Neuroendocrine factors in obesity. J. Endocrinol. 1997, 155:193-195.
10. Bjorntorp P., Sjostrom L. Adipose tissue cellularity. Int. J. Obes. 1979, 3:181-187.
11. Caprio M., Antelmi A., Chetrite G., Muscat A., Mammi C., Marzolla V., Fabbri A., Zennaro M.C., Feve B. Antiadipogenic effects of the mineralocorticoid receptor antagonist drospirenone: potential implications for the treatment of metabolic syndrome. Endocrinology 2011, 152:113-125.
12. Caprio M., Feve B., Claes A., Viengchareun S., Lombes M., Zennaro M.C. Pivotal role of the mineralocorticoid receptor in corticosteroid-induced adipogenesis. FASEB J. 2007, 21:2185-2194.
13. Caprio M., Newfell B.G., la Sala A., Baur W., Fabbri A., Rosano G., Mendelsohn M.E., Jaffe I.Z. Functional mineralocorticoid receptors in human vascular endothelial cells regulate intercellular adhesion molecule-1 expression and promote leukocyte adhesion. Circ. Res. 2008, 102:1359-1367.
14. Champigny O., Ricquier D. Evidence from in vitro differentiating cells that adrenoceptor agonists can increase uncoupling protein mRNA level in adipocytes of adult humans: an RT-PCR study. J. Lipid Res. 1996, 37:1907-1914.
15. Cinti S. Reversible physiological transdifferentiation in the adipose organ. Proc. Nutr. Soc. 2009, 68:340-349.
16. Cinti S. Transdifferentiation properties of adipocytes in the Adipose Organ. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E977-E986.
17. Cypess A.M., Lehman S., Williams G., Tal I., Rodman D., Goldfine A.B., Kuo F.C., Palmer E.L., Tseng Y.H., Doria A., Kolodny G.M., Kahn C.R. Identification and importance of brown adipose tissue in adult humans. New Engl. J. Med. 2009, 360:1509-1517.
18. Despres J.P., Lemieux I. Abdominal obesity and metabolic syndrome. Nature 2006, 444:881-887.
19. Duclos M., Gatta B., Corcuff J.B., Rashedi M., Pehourcq F., Roger P. Fat distribution in obese women is associated with subtle alterations of the hypothalamic-pituitary-adrenal axis activity and sensitivity to glucocorticoids. Clin. Endocrinol. (Oxf.) 2001, 55:447-454.
20. Edwards C.R., Stewart P.M., Burt D., Brett L., McIntyre M.A., Sutanto W.S., de Kloet E.R., Monder C. Localisation of 11 beta-hydroxysteroid dehydrogenase--tissue specific protector of the mineralocorticoid receptor. Lancet 1988, 2:986-989.
21. Ehrhart-Bornstein M., Lamounier-Zepter V., Schraven A., Langenbach J., Willenberg H.S., Barthel A., Hauner H., McCann S.M., Scherbaum W.A., Bornstein S.R. Human adipocytes secrete mineralocorticoid-releasing factors. Proc. Natl. Acad. Sci. USA 2003, 100:14211-14216.
22. Ehrhart-Bornstein M., Arakelyan K., Krug A.W., Scherbaum W.A., Bornstein S.R. Fat cells may be the obesity-hypertension link: human adipogenic factors stimulate aldosterone secretion from adrenocortical cells. Endocr. Res. 2004, 30:865-870.
23. Engeli S., Bohnke J., Gorzelniak K., Janke J., Schling P., Bader M., Luft F.C., Sharma A.M. Weight loss and the renin-angiotensin-aldosterone system. Hypertension 2005, 45:356-362.
24. Engeli S., Schling P., Gorzelniak K., Boschmann M., Janke J., Ailhaud G., Teboul M., Massiera F., Sharma A.M. The adipose-tissue renin-angiotensin-aldosterone system: role in the metabolic syndrome?. Int. J. Biochem. Cell Biol. 2003, 35:807-825.
25. Farquharson C.A., Struthers A.D. Aldosterone induces acute endothelial dysfunction in vivo in humans: evidence for an aldosterone-induced vasculopathy. Clin. Sci. (Lond.) 2002, 103:425-431.
26. Foidart J.M., Faustmann T. Advances in hormone replacement therapy: weight benefits of drospirenone, a 17alpha-spirolactone-derived progestogen. Gynecol. Endocrinol. 2007, 23:692-699.
27. Frontini A., Cinti S. Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab. 2010, 11:253-256.
28. Fu M., Sun T., Bookout A.L., Downes M., Yu R.T., Evans R.M., Mangelsdorf D.J. A Nuclear Receptor Atlas: 3T3-L1 adipogenesis. Mol. Endocrinol. 2005, 19:2437-2450.
29. Funder J.W. Mineralocorticoid receptor activation and oxidative stress. Hypertension 2007, 50:840-841.
30. Funder J.W. Mineralocorticoid receptors: distribution and activation. Heart Fail. Rev. 2005, 10:15-22.
31. Funder J.W., Feldman D., Edelman I.S. Specific aldosterone binding in rat kidney and parotid. J. Steroid Biochem. 1972, 3:209-218.
32. Funder J.W., Pearce P.T., Smith R., Smith A.I. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science 1988, 242:583-585.
33. Garrison R.J., Kannel W.B., Stokes J., Castelli W.P. Incidence and precursors of hypertension in young adults: the Framingham Offspring Study. Prev. Med. 1987, 16:235-251.
34. Goodfriend T.L., Ball D.L., Egan B.M., Campbell W.B., Nithipatikom K. Epoxy-keto derivative of linoleic acid stimulates aldosterone secretion. Hypertension 2004, 43:358-363.
35. Guo C., Ricchiuti V., Lian B.Q., Yao T.M., Coutinho P., Romero J.R., Li J., Williams G.H., Adler G.K. Mineralocorticoid receptor blockade reverses obesity-related changes in expression of adiponectin, peroxisome proliferator-activated receptor-gamma, and proinflammatory adipokines. Circulation 2008, 117:2253-2261.
36. Han F., Ozawa H., Matsuda K., Nishi M., Kawata M. Colocalization of mineralocorticoid receptor and glucocorticoid receptor in the hippocampus and hypothalamus. Neurosci. Res. 2005, 51:371-381.
37. Harte A., McTernan P., Chetty R., Coppack S., Katz J., Smith S., Kumar S. Insulin-mediated upregulation of the renin angiotensin system in human subcutaneous adipocytes is reduced by rosiglitazone. Circulation 2005, 111:1954-1961.
38. Hauner H., Entenmann G., Wabitsch M., Gaillard D., Ailhaud G., Negrel R., Pfeiffer E.F. Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J. Clin. Invest. 1989, 84:1663-1670.
39. Hirata A., Maeda N., Hiuge A., Hibuse T., Fujita K., Okada T., Kihara S., Funahashi T., Shimomura I. Blockade of mineralocorticoid receptor reverses adipocyte dysfunction and insulin resistance in obese mice. Cardiovasc. Res. 2009, 84:164-172.
40. Hoppmann J., Perwitz N., Meier B., Fasshauer M., Hadaschik D., Lehnert H., Klein J. The balance between gluco- and mineralo-corticoid action critically determines inflammatory adipocyte responses. J. Endocrinol. 2010, 204:153-164.
41. Ingelsson E., Pencina M.J., Tofler G.H., Benjamin E.J., Lanier K.J., Jacques P.F., Fox C.S., Meigs J.B., Levy D., Larson M.G., Selhub J., D'Agostino R.B., Wang T.J., Vasan R.S. Multimarker approach to evaluate the incidence of the metabolic syndrome and longitudinal changes in metabolic risk factors: the Framingham Offspring Study. Circulation 2007, 116:984-992.
42. Kenouch S., Lombes M., Delahaye F., Eugene E., Bonvalet J.P., Farman N. Human skin as target for aldosterone: coexpression of mineralocorticoid receptors and 11 beta-hydroxysteroid dehydrogenase. J. Clin. Endocrinol. Metab. 1994, 79:1334-1341.
43. Kershaw E.E., Morton N.M., Dhillon H., Ramage L., Seckl J.R., Flier J.S. Adipocyte-specific glucocorticoid inactivation protects against diet-induced obesity. Diabetes 2005, 54:1023-1031.
44. Kidambi S., Kotchen J.M., Grim C.E., Raff H., Mao J., Singh R.J., Kotchen T.A. Association of adrenal steroids with hypertension and the metabolic syndrome in blacks. Hypertension 2007, 49:704-711.
45. Kraus D., Jager J., Meier B., Fasshauer M., Klein J. Aldosterone inhibits uncoupling protein-1, induces insulin resistance, and stimulates proinflammatory adipokines in adipocytes. Horm. Metab. Res. 2005, 37:455-459.
46. Krozowski Z.S., Rundle S.E., Wallace C., Castell M.J., Shen J.H., Dowling J., Funder J.W., Smith A.I. Immunolocalization of renal mineralocorticoid receptors with an antiserum against a peptide deduced from the complementary deoxyribonucleic acid sequence. Endocrinology 1989, 125:192-198.
47. Krozowski Z., Funder J.W. Mineralocorticoid receptors in the rat lung. Endocrinology 1981, 109:1811-1813.
48. Licata G., Scaglione R., Ganguzza A., Corrao S., Donatelli M., Parrinello G., Dichiara M.A., Merlino G., Cecala M.G. Central obesity and hypertension. Relationship between fasting serum insulin, plasma renin activity, and diastolic blood pressure in young obese subjects. Am. J. Hypertens. 1994, 7:314-320.
49. Lombes M., Farman N., Oblin M.E., Baulieu E.E., Bonvalet J.P., Erlanger B.F., Gasc J.M. Immunohistochemical localization of renal mineralocorticoid receptor by using an anti-idiotypic antibody that is an internal image of aldosterone. Proc. Natl. Acad. Sci. USA 1990, 87:1086-1088.
50. Lombes M., Oblin M.E., Gasc J.M., Baulieu E.E., Farman N., Bonvalet J.P. Immunohistochemical and biochemical evidence for a cardiovascular mineralocorticoid receptor. Circ. Res. 1992, 71:503-510.
51. Marken Lichtenbelt W.D., Vanhommerig J.W., Smulders N.M., Drossaerts J.M., Kemerink G.J., Bouvy N.D., Schrauwen P., Teule G.J. Cold-activated brown adipose tissue in healthy men. New Engl. J. Med. 2009, 360:1500-1508.
52. Marver D., Stewart J., Funder J.W., Feldman D., Edelman I.S. Renal aldosterone receptors: studies with (3H)aldosterone and the anti-mineralocorticoid (3H)spirolactone (SC-26304). Proc. Natl. Acad. Sci. USA 1974, 71:1431-1435.
53. Masuzaki H., Paterson J., Shinyama H., Morton N.M., Mullins J.J., Seckl J.R., Flier J.S. A transgenic model of visceral obesity and the metabolic syndrome. Science 2001, 294:2166-2170.
54. Matsui H., Ando K., Kawarazaki H., Nagae A., Fujita M., Shimosawa T., Nagase M., Fujita T. Salt excess causes left ventricular diastolic dysfunction in rats with metabolic disorder. Hypertension 2008, 52:287-294.
55. Mirshahi M., Mirshahi A., Sedighian R., Hecquet C., Faure J.P., Agarwal M.K. Immunochemical demonstration of the mineralocorticoid receptor in ocular tissues. Neuroendocrinology 1997, 65:70-78.
56. Mitts T.F., Bunda S., Wang Y., Hinek A. Aldosterone and mineralocorticoid receptor antagonists modulate elastin and collagen deposition in human skin. J. Invest. Dermatol. 2010, 130:2396-2406.
57. Moguilewsky M., Raynaud J.P. Evidence for a specific mineralocorticoid receptor in rat pituitary and brain. J. Steroid Biochem. 1980, 12:309-314.
58. Murano I., Barbatelli G., Parisani V., Latini C., Muzzonigro G., Castellucci M., Cinti S. Dead adipocytes, detected as crown-like structures, are prevalent in visceral fat depots of genetically obese mice. J. Lipid Res. 2008, 49:1562-1568.
59. Nagase M., Matsui H., Shibata S., Gotoda T., Fujita T. Salt-induced nephropathy in obese spontaneously hypertensive rats via paradoxical activation of the mineralocorticoid receptor: role of oxidative stress. Hypertension 2007, 50:877-883.
60. Nagase M., Yoshida S., Shibata S., Nagase T., Gotoda T., Ando K., Fujita T. Enhanced aldosterone signaling in the early nephropathy of rats with metabolic syndrome: possible contribution of fat-derived factors. J. Am. Soc. Nephrol. 2006, 17:3438-3446.
61. Neels J.G., Olefsky J.M. Inflamed fat: what starts the fire? J. Clin. Invest. 2006, 116:33-35.
62. Nicholls D.G., Locke R.M. Thermogenic mechanisms in brown fat. Physiol. Rev. 1984, 64:1-64.
63. Oelkers W., Foidart J.M., Dombrovicz N., Welter A., Heithecker R. Effects of a new oral contraceptive containing an antimineralocorticoid progestogen, drospirenone, on the renin-aldosterone system, body weight, blood pressure, glucose tolerance, and lipid metabolism. J. Clin. Endocrinol. Metab. 1995, 80:1816-1821.
64. Palacios S., Foidart J.M., Genazzani A.R. Advances in hormone replacement therapy with drospirenone, a unique progestogen with aldosterone receptor antagonism. Maturitas 2006, 55:297-307.
65. Penfornis P., Viengchareun S., Le Menuet D., Cluzeaud F., Zennaro M.C., Lombes M. The mineralocorticoid receptor mediates aldosterone-induced differentiation of T37i cells into brown adipocytes. Am. J. Physiol. Endocrinol. Metab. 2000, 279:E386-E394.
66. Prat-Larquemin L., Oppert J.M., Clement K., Hainault I., Basdevant A., Guy-Grand B., Quignard-Boulange A. Adipose angiotensinogen secretion, blood pressure, and AGT M235T polymorphism in obese patients. Obes. Res. 2004, 12:556-561.
67. Pressley L., Funder J.W. Glucocorticoid and mineralocorticoid receptors in gut mucosa. Endocrinology 1975, 97:588-596.
68. Preston R.A., Norris P.M., Alonso A.B., Ni P., Hanes V., Karara A.H. Randomized, placebo-controlled trial of the effects of drospirenone-estradiol on blood pressure and potassium balance in hypertensive postmenopausal women receiving hydrochlorothiazide. Menopause 2007, 14:408-414.
69. Rebuffe-Scrive M., Lundholm K., Bjorntorp P. Glucocorticoid hormone binding to human adipose tissue. Eur. J. Clin. Invest. 1985, 15:267-271.
70. Rickard A.J., Morgan J., Tesch G., Funder J.W., Fuller P.J., Young M.J. Deletion of mineralocorticoid receptors from macrophages protects against deoxycorticosterone/salt-induced cardiac fibrosis and increased blood pressure. Hypertension 2009, 54:537-543.
71. Ronconi V., Turchi F., Bujalska I.J., Giacchetti G., Boscaro M. Adipose cell-adrenal interactions: current knowledge and future perspectives. Trends Endocrinol. Metab. 2008, 19:100-103.
72. Rondinone C.M., Rodbard D., Baker M.E. Aldosterone stimulated differentiation of mouse 3T3-L1 cells into adipocytes. Endocrinology 1993, 132:2421-2426.
73. Sainte-Marie Y., Toulon A., Paus R., Maubec E., Cherfa A., Grossin M., Descamps V., Clemessy M., Gasc J.M., Peuchmaur M., Glick A., Farman N., Jaisser F. Targeted skin overexpression of the mineralocorticoid receptor in mice causes epidermal atrophy, premature skin barrier formation, eye abnormalities, and alopecia. Am. J. Pathol. 2007, 171:846-860.
74. Saito M., Okamatsu-Ogura Y., Matsushita M., Watanabe K., Yoneshiro T., Nio-Kobayashi J., Iwanaga T., Miyagawa M., Kameya T., Nakada K., Kawai Y., Tsujisaki M. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 2009, 58:1526-1531.
75. Sethi J.K., Vidal-Puig A.J. Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J. Lipid Res. 2007, 48:1253-1262.
76. Skurk T., Alberti-Huber C., Herder C., Hauner H. Relationship between adipocyte size and adipokine expression and secretion. J. Clin. Endocrinol. Metab. 2007, 92:1023-1033.
77. Tanko L.B., Christiansen C. Effects of 17beta-oestradiol plus different doses of drospirenone on adipose tissue, adiponectin and atherogenic metabolites in postmenopausal women. J. Intern. Med. 2005, 258:544-553.
78. Thakur V., Richards R., Reisin E. Obesity, hypertension, and the heart. Am. J. Med. Sci. 2001, 321:242-248.
79. Turgeon J.L., Carr M.C., Maki P.M., Mendelsohn M.E., Wise P.M. Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: Insights from basic science and clinical studies. Endocr. Rev. 2006, 27:575-605.
80. Urbanet R., Pilon C., Calcagno A., Peschechera A., Hubert E.L., Giacchetti G., Gomez-Sanchez C., Mulatero P., Toffanin M., Sonino N., Zennaro M.C., Giorgino F., Vettor R., Fallo F. Analysis of insulin sensitivity in adipose tissue of patients with primary aldosteronism. J. Clin. Endocrinol. Metab. 2010, 95:4037-4042.
81. Viengchareun S., Penfornis P., Zennaro M.C., Lombes M. Mineralocorticoid and glucocorticoid receptors inhibit UCP expression and function in brown adipocytes. Am. J. Physiol. Endocrinol. Metab. 2001, 280:E640-E649.
82. Virtanen K.A., Lidell M.E., Orava J., Heglind M., Westergren R., Niemi T., Taittonen M., Laine J., Savisto N.J., Enerback S., Nuutila P. Functional brown adipose tissue in healthy adults. New Engl. J. Med. 2009, 360:1518-1525.
83. Wada T., Ohshima S., Fujisawa E., Koya D., Tsuneki H., Sasaoka T. Aldosterone inhibits insulin-induced glucose uptake by degradation of insulin receptor substrate (IRS) 1 and IRS2 via a reactive oxygen species-mediated pathway in 3T3-L1 adipocytes. Endocrinology 2009, 150:1662-1669.
84. Wajchenberg B.L. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr. Rev. 2000, 21:697-738.
85. Walker B.R., Andrew R. Tissue production of cortisol by 11beta-hydroxysteroid dehydrogenase type 1 and metabolic disease. Ann. N.Y. Acad. Sci. 2006, 1083:165-184.
86. Wang H., Shimosawa T., Matsui H., Kaneko T., Ogura S., Uetake Y., Takenaka K., Yatomi Y., Fujita T. Paradoxical mineralocorticoid receptor activation and left ventricular diastolic dysfunction under high oxidative stress conditions. J. Hypertens. 2008, 26:1453-1462.
87. Weaver J.U., Kopelman P.G., McLoughlin L., Forsling M.L., Grossman A. Hyperactivity of the hypothalamo-pituitary-adrenal axis in obesity: a study of ACTH, AVP, beta-lipotrophin and cortisol responses to insulin-induced hypoglycaemia. Clin. Endocrinol. (Oxf.) 1993, 39:345-350.
88. Wellen K.E., Hotamisligil G.S. Inflammation, stress, and diabetes. J. Clin. Invest. 2005, 115:1111-1119.
89. White W.B., Hanes V., Chauhan V., Pitt B. Effects of a new hormone therapy, drospirenone and 17-beta-estradiol, in postmenopausal women with hypertension. Hypertension 2006, 48:246-253.
90. White W.B., Pitt B., Preston R.A., Hanes V. Antihypertensive effects of drospirenone with 17beta-estradiol, a novel hormone treatment in postmenopausal women with stage 1 hypertension. Circulation 2005, 112:1979-1984.
91. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., Sole J., Nichols A., Ross J.S., Tartaglia L.A., 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.
92. Yang G., Merrill D.C., Thompson M.W., Robillard J.E., Sigmund C.D. Functional expression of the human angiotensinogen gene in transgenic mice. J. Biol. Chem. 1994, 269:32497-32502.
93. Young M.J. Mechanisms of mineralocorticoid receptor-mediated cardiac fibrosis and vascular inflammation. Curr. Opin. Nephrol. Hypertens. 2008, 17:174-180.
94. Zhao M., Valamanesh F., Celerier I., Savoldelli M., Jonet L., Jeanny J.C., Jaisser F., Farman N., Behar-Cohen F. The neuroretina is a novel mineralocorticoid target: aldosterone up-regulates ion and water channels in Muller glial cells. FASEB J. 2010, 24:3405-3415.
95. Zingaretti M.C., Crosta F., Vitali A., Guerrieri M., Frontini A., Cannon B., Nedergaard J., Cinti S. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 2009, 23:3113-3120.
96. Zennaro M.C., Le Menuet D., Viengchareun S., Walker F., Ricquier D., Lombes M. Hibernoma development in transgenic mice identifies brown adipose tissue as a novel target of aldosterone action. J. Clin. Invest. 1998, 101:1254-1260.