Aldosterone-induced vascular remodeling and endothelial dysfunction require functional angiotensin type 1a receptors

Hypertension

Volumn 67, Issue 5, 2016, Pages 897-905

  Briet, Marie ^a,b,c   Barhoumi, Tlili ^a   Mian, Muhammad Oneeb Rehman ^a   Coelho, Suellen C ^a   Ouerd, Sofiane ^a   Rautureau, Yohann ^a,e   Coffman, Thomas M ^d   Paradis, Pierre ^a   Schiffrin, Ernesto L ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c ANGERS UNIVERSITY HOSPITAL   (France)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MONTREAL HEART INSTITUTE   (Canada)

Author keywords

inflammation; mineralocorticoids; oxidative stress; potassium channels, calcium activated; sodium; vascular remodeling

Indexed keywords

ALDOSTERONE; ANGIOTENSIN 1A RECEPTOR; CALCIUM ACTIVATED POTASSIUM CHANNEL; COLLAGEN; EPLERENONE; FIBRONECTIN; LOSARTAN; MINERALOCORTICOID RECEPTOR; NORADRENALIN; SODIUM CHLORIDE; ANGIOTENSIN 1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL INJURY; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; MESENTERIC ARTERY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SODIUM EXCRETION; SODIUM RETENTION; SYSTOLIC BLOOD PRESSURE; VASCULAR REMODELING; VASCULITIS; VASODILATATION; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECTS; HYPERTENSION; KNOCKOUT MOUSE; MALE; METABOLISM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; REFERENCE VALUE; VASCULAR ENDOTHELIUM; VASCULAR RESISTANCE;

ALDOSTERONE; ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HYPERTENSION; LOSARTAN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NOREPINEPHRINE; OXIDATIVE STRESS; RANDOM ALLOCATION; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTORS, MINERALOCORTICOID; REFERENCE VALUES; VASCULAR REMODELING; VASCULAR RESISTANCE;

EID: 84962385415     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.07074     Document Type: Article

References (57)

1. Briet M, Schiffrin EL, Aldosterone: effects on the kidney and cardiovascular system. Nat Rev Nephrol 2010 6 261 273. doi: 10.1038/nrneph.2010.30
2. Briet M, Schiffrin EL, Vascular actions of aldosterone. J Vasc Res 2013 50 89 99. doi: 10.1159/000345243
3. Virdis A, Neves MF, Amiri F, Viel E, Touyz RM, Schiffrin EL, Spironolactone improves angiotensin-induced vascular changes and oxidative stress. Hypertension 2002 40 504 510
4. Pitt B, Remme W, Zannad F, Neaton J, Martinez F, Roniker B, Bittman R, Hurley S, Kleiman J, Gatlin M, Eplerenone Post-Acute Myocardial Infarction Heart Failure Efficacy and Survival Study Investigators Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med 2003 348 1309 1321. doi: 10.1056/NEJMoa030207
5. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, Palensky J, Wittes J, The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N Engl J Med 1999 341 709 717. doi: 10.1056/NEJM199909023411001
6. Lemarié CA, Schiffrin EL, The angiotensin II type 2 receptor in cardiovascular disease. J Renin Angiotensin Aldosterone Syst 2010 11 19 31. doi: 10.1177/1470320309347785
7. Ito M, Oliverio MI, Mannon PJ, Best CF, Maeda N, Smithies O, Coffman TM, Regulation of blood pressure by the type 1A angiotensin II receptor gene. Proc Natl Acad Sci U S A 1995 92 3521 3525
8. Oliverio MI, Best CF, Kim HS, Arendshorst WJ, Smithies O, Coffman TM, Angiotensin II responses in AT1A receptor-deficient mice: a role for AT1B receptors in blood pressure regulation. Am J Physiol 1997 272 4 pt 2 F515 F520
9. Oliverio MI, Kim HS, Ito M, Le T, Audoly L, Best CF, Hiller S, Kluckman K, Maeda N, Smithies O, Coffman TM, Reduced growth, abnormal kidney structure, and type 2 (AT2) angiotensin receptor-mediated blood pressure regulation in mice lacking both AT1A and AT1B receptors for angiotensin II. Proc Natl Acad Sci U S A 1998 95 15496 15501
10. Schiffrin EL, Franks DJ, Gutkowska J, Effect of aldosterone on vascular angiotensin II receptors in the rat. Can J Physiol Pharmacol 1985 63 1522 1527
11. Mazak I, Fiebeler A, Muller DN, Park JK, Shagdarsuren E, Lindschau C, Dechend R, Viedt C, Pilz B, Haller H, Luft FC, Aldosterone potentiates angiotensin II-induced signaling in vascular smooth muscle cells. Circulation 2004 109 2792 2800. doi: 10.1161/01.CIR.0000131860.80444.AB
12. Jaffe IZ, Mendelsohn ME, Angiotensin II and aldosterone regulate gene transcription via functional mineralocortocoid receptors in human coronary artery smooth muscle cells. Circ Res 2005 96 643 650. doi: 10.1161/01.RES.0000159937.05502.d1
13. McCurley A, Pires PW, Bender SB, Aronovitz M, Zhao MJ, Metzger D, Chambon P, Hill MA, Dorrance AM, Mendelsohn ME, Jaffe IZ, Direct regulation of blood pressure by smooth muscle cell mineralocorticoid receptors. Nat Med 2012 18 1429 1433. doi: 10.1038/nm.2891
14. Min LJ, Mogi M, Li JM, Iwanami J, Iwai M, Horiuchi M, Aldosterone and angiotensin II synergistically induce mitogenic response in vascular smooth muscle cells. Circ Res 2005 97 434 442. doi: 10.1161/01.RES.0000180753.63183.95
15. Montezano AC, Callera GE, Yogi A, He Y, Tostes RC, He G, Schiffrin EL, Touyz RM, Aldosterone and angiotensin II synergistically stimulate migration in vascular smooth muscle cells through c-Src-regulated redox-sensitive RhoA pathways. Arterioscler Thromb Vasc Biol 2008 28 1511 1518. doi: 10.1161/ATVBAHA.108.168021
16. Min LJ, Mogi M, Iwanami J, Li JM, Sakata A, Fujita T, Tsukuda K, Iwai M, Horiuchi M, Cross-Talk between aldosterone and angiotensin II in vascular smooth muscle cell senescence. Cardiovasc Res 2007 76 506 516. doi: 10.1016/j.cardiores.2007.07.008
17. Lemarié CA, Simeone SM, Nikonova A, Ebrahimian T, Deschênes ME, Coffman TM, Paradis P, Schiffrin EL, Aldosterone-induced activation of signaling pathways requires activity of angiotensin type 1a receptors. Circ Res 2009 105 852 859. doi: 10.1161/CIRCRESAHA.109.196576
18. Gembardt F, Heringer-Walther S, van Esch JH, Sterner-Kock A, van Veghel R, Le TH, Garrelds IM, Coffman TM, Danser AH, Schultheiss HP, Walther T, Cardiovascular phenotype of mice lacking all three subtypes of angiotensin II receptors. FASEB J 2008 22 3068 3077. doi: 10.1096/fj.08-108316
19. Oliverio MI, Madsen K, Best CF, Ito M, Maeda N, Smithies O, Coffman TM, Renal growth and development in mice lacking AT1A receptors for angiotensin II. Am J Physiol 1998 274 1 pt 2 F43 F50
20. Barhoumi T, Kasal DA, Li MW, Shbat L, Laurant P, Neves MF, Paradis P, Schiffrin EL, T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension 2011 57 469 476. doi: 10.1161/HYPERTENSIONAHA.110.162941
21. Diep QN, El Mabrouk M, Cohn JS, Endemann D, Amiri F, Virdis A, Neves MF, Schiffrin EL, Structure, endothelial function, cell growth, and inflammation in blood vessels of angiotensin II-infused rats: role of peroxisome proliferator-Activated receptor-gamma. Circulation 2002 105 2296 2302
22. Leibovitz E, Ebrahimian T, Paradis P, Schiffrin EL, Aldosterone induces arterial stiffness in absence of oxidative stress and endothelial dysfunction. J Hypertens 2009 27 2192 2200. doi: 10.1097/HJH.0b013e328330a963
23. Li MW, Mian MO, Barhoumi T, Rehman A, Mann K, Paradis P, Schiffrin EL, Endothelin-1 overexpression exacerbates atherosclerosis and induces aortic aneurysms in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol 2013 33 2306 2315. doi: 10.1161/ATVBAHA.113.302028
24. Hu C, Dandapat A, Sun L, Marwali MR, Inoue N, Sugawara F, Inoue K, Kawase Y, Jishage K, Suzuki H, Hermonat PL, Sawamura T, Mehta JL, Modulation of angiotensin II-mediated hypertension and cardiac remodeling by lectin-like oxidized low-density lipoprotein receptor-1 deletion. Hypertension 2008 52 556 562. doi: 10.1161/HYPERTENSIONAHA.108.115287
25. Kamat NV, Thabet SR, Xiao L, Saleh MA, Kirabo A, Madhur MS, Delpire E, Harrison DG, McDonough AA, Renal transporter activation during angiotensin-II hypertension is blunted in interferon-γ-/-And interleukin-17A-/-mice. Hypertension 2015 65 569 576. doi: 10.1161/HYPERTENSIONAHA.114.04975
26. Rossier BC, Staub O, Hummler E, Genetic dissection of sodium and potassium transport along the aldosterone-sensitive distal nephron: importance in the control of blood pressure and hypertension. FEBS Lett 2013 587 1929 1941. doi: 10.1016/j.febslet.2013.05.013
27. Soundararajan R, Pearce D, Hughey RP, Kleyman TR, Role of epithelial sodium channels and their regulators in hypertension. J Biol Chem 2010 285 30363 30369. doi: 10.1074/jbc.R110.155341
28. Soundararajan R, Pearce D, Ziera T, The role of the ENaC-regulatory complex in aldosterone-mediated sodium transport. Mol Cell Endocrinol 2012 350 242 247. doi: 10.1016/j.mce.2011.11.003
29. DuPont JJ, Hill MA, Bender SB, Jaisser F, Jaffe IZ, Aldosterone and vascular mineralocorticoid receptors: regulators of ion channels beyond the kidney. Hypertension 2014 63 632 637. doi: 10.1161/HYPERTENSIONAHA.113.01273
30. Park JB, Schiffrin EL, ET(A) receptor antagonist prevents blood pressure elevation and vascular remodeling in aldosterone-infused rats. Hypertension 2001 37 1444 1449
31. Levy BI, Michel JB, Salzmann JL, Devissaguet M, Safar ME, Remodeling of heart and arteries by chronic converting enzyme inhibition in spontaneously hypertensive rats. Am J Hypertens 1991 4 3 pt 2 240S 245S
32. Park JB, Schiffrin EL, Small artery remodeling is the most prevalent (earliest?) form of target organ damage in mild essential hypertension. J Hypertens 2001 19 921 930
33. Beggah AT, Escoubet B, Puttini S, Cailmail S, Delage V, Ouvrard-Pascaud A, Bocchi B, Peuchmaur M, Delcayre C, Farman N, Jaisser F, Reversible cardiac fibrosis and heart failure induced by conditional expression of an antisense mRNA of the mineralocorticoid receptor in cardiomyocytes. Proc Natl Acad Sci U S A 2002 99 7160 7165. doi: 10.1073/pnas.102673599
34. Sun Y, Ramires FJ, Weber KT, Fibrosis of atria and great vessels in response to angiotensin II or aldosterone infusion. Cardiovasc Res 1997 35 138 147
35. Nakano S, Kobayashi N, Yoshida K, Ohno T, Matsuoka H, Cardioprotective mechanisms of spironolactone associated with the angiotensin-converting enzyme/epidermal growth factor receptor/extracellular signal-regulated kinases, NAD(P)H oxidase/lectin-like oxidized low-density lipoprotein receptor-1, and Rho-kinase pathways in aldosterone/salt-induced hypertensive rats. Hypertens Res 2005 28 925 936. doi: 10.1291/hypres.28.925
36. Favre J, Gao J, Zhang AD, Remy-Jouet I, Ouvrard-Pascaud A, Dautreaux B, Escoubet B, Thuillez C, Jaisser F, Richard V, Coronary endothelial dysfunction after cardiomyocyte-specific mineralocorticoid receptor overexpression. Am J Physiol Heart Circ Physiol 2011 300 H2035 H2043. doi: 10.1152/ajpheart.00552.2010
37. Garnier A, Bendall JK, Fuchs S, Escoubet B, Rochais F, Hoerter J, Nehme J, Ambroisine ML, De Angelis N, Morineau G, d'Estienne P, Fischmeister R, Heymes C, Pinet F, Delcayre C, Cardiac specific increase in aldosterone production induces coronary dysfunction in aldosterone synthase-Transgenic mice. Circulation 2004 110 1819 1825. doi: 10.1161/01.CIR.0000142858.44680.27
38. Griol-Charhbili V, Fassot C, Messaoudi S, Perret C, Agrapart V, Jaisser F, Epidermal growth factor receptor mediates the vascular dysfunction but not the remodeling induced by aldosterone/salt. Hypertension 2011 57 238 244. doi: 10.1161/HYPERTENSIONAHA.110.153619
39. Leopold JA, Dam A, Maron BA, Scribner AW, Liao R, Handy DE, Stanton RC, Pitt B, Loscalzo J, Aldosterone impairs vascular reactivity by decreasing glucose-6-phosphate dehydrogenase activity. Nat Med 2007 13 189 197. doi: 10.1038/nm1545
40. Kagiyama S, Matsumura K, Fukuhara M, Sakagami K, Fujii K, Iida M, Aldosterone-And-salt-induced cardiac fibrosis is independent from angiotensin II type 1a receptor signaling in mice. Hypertens Res 2007 30 979 989. doi: 10.1291/hypres.30.979
41. Guyton AC, Renal function curve-A key to understanding the pathogenesis of hypertension. Hypertension 1987 10 1 6
42. Li XC, Shao Y, Zhuo JL, AT1a receptor knockout in mice impairs urine concentration by reducing basal vasopressin levels and its receptor signaling proteins in the inner medulla. Kidney Int 2009 76 169 177. doi: 10.1038/ki.2009.134
43. Oliverio MI, Delnomdedieu M, Best CF, Li P, Morris M, Callahan MF, Johnson GA, Smithies O, Coffman TM, Abnormal water metabolism in mice lacking the type 1A receptor for ANG II. Am J Physiol Renal Physiol 2000 278 F75 F82
44. Cervenka L, Mitchell KD, Oliverio MI, Coffman TM, Navar LG, Renal function in the AT1A receptor knockout mouse during normal and volume-expanded conditions. Kidney Int 1999 56 1855 1862. doi: 10.1046/j.1523-1755.1999.00757.x
45. Lai L, Feng X, Liu D, Chen J, Zhang Y, Niu B, Gu Y, Cai H, Dietary salt modulates the sodium chloride cotransporter expression likely through an aldosterone-mediated WNK4-ERK1/2 signaling pathway. Pflugers Arch 2012 463 477 485. doi: 10.1007/s00424-011-1062-y
46. Muller OG, Parnova RG, Centeno G, Rossier BC, Firsov D, Horisberger JD, Mineralocorticoid effects in the kidney: correlation between alphaENaC, GILZ, and Sgk-1 mRNA expression and urinary excretion of Na+ and K+. J Am Soc Nephrol 2003 14 1107 1115
47. Shibata S, Rinehart J, Zhang J, Moeckel G, Castañeda-Bueno M, Stiegler AL, Boggon TJ, Gamba G, Lifton RP, Mineralocorticoid receptor phosphorylation regulates ligand binding and renal response to volume depletion and hyperkalemia. Cell Metab 2013 18 660 671. doi: 10.1016/j.cmet.2013.10.005
48. Funder JW, Reconsidering the roles of the mineralocorticoid receptor. Hypertension 2009 53 286 290. doi: 10.1161/HYPERTENSIONAHA.108.119966
49. Ambroisine ML, Favre J, Oliviero P, Rodriguez C, Gao J, Thuillez C, Samuel JL, Richard V, Delcayre C, Aldosterone-induced coronary dysfunction in transgenic mice involves the calcium-Activated potassium (BKCa) channels of vascular smooth muscle cells. Circulation 2007 116 2435 2443. doi: 10.1161/CIRCULATIONAHA.107.722009
50. Ledoux J, Werner ME, Brayden JE, Nelson MT, Calcium-Activated potassium channels and the regulation of vascular tone. Physiology (Bethesda) 2006 21 69 78. doi: 10.1152/physiol.00040.2005
51. Rajagopalan S, Kurz S, Münzel T, Tarpey M, Freeman BA, Griendling KK, Harrison DG, Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest 1996 97 1916 1923. doi: 10.1172/JCI118623
52. Laursen JB, Rajagopalan S, Galis Z, Tarpey M, Freeman BA, Harrison DG, Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation 1997 95 588 593
53. Wang D, Chen Y, Chabrashvili T, Aslam S, Borrego Conde LJ, Umans JG, Wilcox CS, Role of oxidative stress in endothelial dysfunction and enhanced responses to angiotensin II of afferent arterioles from rabbits infused with angiotensin II. J Am Soc Nephrol 2003 14 2783 2789
54. Wang D, Jose P, Wilcox CS, beta(1) Receptors protect the renal afferent arteriole of angiotensin-infused rabbits from norepinephrine-induced oxidative stress. J Am Soc Nephrol 2006 17 3347 3354. doi: 10.1681/ASN.2006030212
55. Calhoun DA, White WB, Effectiveness of the selective aldosterone blocker, eplerenone, in patients with resistant hypertension. J Am Soc Hypertens 2008 2 462 468. doi: 10.1016/j.jash.2008.05.005
56. Václavík J, Sedlák R, Plachy M, Navrátil K, Plásek J, Jarkovsky J, Václavík T, Husár R, Kociánová E, Táborsky M, Addition of spironolactone in patients with resistant arterial hypertension (ASPIRANT): a randomized, double-blind, placebo-controlled trial. Hypertension 2011 57 1069 1075. doi: 10.1161/HYPERTENSIONAHA.111.169961
57. Williams B, MacDonald TM, Morant S, Webb DJ, Sever P, McInnes G, Ford I, Cruickshank JK, Caulfield MJ, Salsbury J, Mackenzie I, Padmanabhan S, Brown MJ, British Hypertension Society's PATHWAY Studies Group Spironolactone versus placebo, bisoprolol, and doxazosin to determine the optimal treatment for drug-resistant hypertension (PATHWAY-2): a randomised, double-blind, crossover trial. Lancet 2015 386 2059 2068. doi: 10.1016/S0140-6736(15)00257-3