Persistent phenotypic shift in cardiac fibroblasts: Impact of transient renin angiotensin system inhibition

Journal of Molecular and Cellular Cardiology

Volumn 93, Issue , 2016, Pages 125-132

  Hale, Taben M ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

ACE inhibitor; Apoptosis; AT1 receptor antagonist; Calcium channel blocker; Fibrosis; Hypertension

Indexed keywords

AGING; APOPTOSIS; ARTERIAL PRESSURE; CARDITIS; HEART FIBROBLAST; HEART INJURY; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE FIBROSIS; HEART PROTECTION; HUMAN; HYPERTENSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CELL TRANSDIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; FIBROSIS; HEART VENTRICLE REMODELING; HYPERTROPHY, LEFT VENTRICULAR; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RAT;

ANGIOTENSIN RECEPTOR ANTAGONIST; ANTIHYPERTENSIVE AGENT; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR;

ANGIOTENSIN RECEPTOR ANTAGONISTS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; ANTIHYPERTENSIVE AGENTS; APOPTOSIS; CELL TRANSDIFFERENTIATION; FIBROBLASTS; FIBROSIS; HUMANS; HYPERTROPHY, LEFT VENTRICULAR; MYOCARDIUM; MYOCYTES, CARDIAC; PHENOTYPE; RATS; RENIN-ANGIOTENSIN SYSTEM; VENTRICULAR REMODELING;

EID: 84953256704     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.11.027     Document Type: Review

References (99)

1. Schocken D.D., Benjamin E.J., Fonarow G.C., Krumholz H.M., Levy D., Mensah G.A., et al. Prevention of heart failure: a scientific statement from the American Heart Association councils on epidemiology and prevention, clinical cardiology, cardiovascular nursing, and high blood pressure research; quality of care and outcomes research interdisciplinary working group; and functional genomics and translational biology interdisciplinary working group. Circulation 2008, 117:2544-2565.
2. Berk B.C., Fujiwara K., Lehoux S. ECM remodeling in hypertensive heart disease. J. Clin. Invest. 2007, 117:568-575.
3. Roger V.L., Go A.S., Lloyd-Jones D.M., Benjamin E.J., Berry J.D., Borden W.B., et al. Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 2012, 125:e2-e220.
4. Schuetze K.B., McKinsey T.A., Long C.S. Targeting cardiac fibroblasts to treat fibrosis of the heart: focus on HDACs. J. Mol. Cell. Cardiol. 2014, 70:100-107.
5. Horn M., Trafford A.W. Aging and the cardiac collagen matrix: novel mediators of fibrotic remodelling. J. Mol. Cell. Cardiol. 2016, 93:175-185.
6. Porter K.E., Turner N.A. Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol. Ther. 2009, 123:255-278.
7. Diez J., Lopez B., Gonzalez A., Querejeta R. Clinical aspects of hypertensive myocardial fibrosis. Curr. Opin. Cardiol. 2001, 16:328-335.
8. Weber K.T., Brilla C.G. Pathological hypertrophy and cardiac interstitium. Fibrosis and renin-angiotensin-aldosterone system. Circulation 1991, 83:1849-1865.
9. Kong P., Christia P., Frangogiannis N. The pathogenesis of cardiac fibrosis. Cell. Mol. Life Sci. 2014, 71:549-574.
10. Brilla C.G., Funck R.C., Rupp H. Lisinopril-mediated regression of myocardial fibrosis in patients with hypertensive heart disease. Circulation 2000, 102:1388-1393.
11. Diez J. Towards a new paradigm about hypertensive heart disease. Med. Clin. N. Am. 2009, 93:637-645.
12. McLenachan J.M., Dargie H.J. Ventricular arrhythmias in hypertensive left ventricular hypertrophy. Relationship to coronary artery disease, left ventricular dysfunction, and myocardial fibrosis. Am. J. Hypertens. 1990, 3:735-740.
13. Khan R., Sheppard R. Fibrosis in heart disease: understanding the role of transforming growth factor-beta in cardiomyopathy, valvular disease and arrhythmia. Immunology 2006, 118:10-24.
14. Schwartzkopff B., Brehm M., Mundhenke M., Strauer B.E. Repair of coronary arterioles after treatment with perindopril in hypertensive heart disease. Hypertension 2000, 36:220-225.
15. Camelliti P., Borg T.K., Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc. Res. 2005, 65:40-51.
16. Jugdutt B.I. Remodeling of the myocardium and potential targets in the collagen degradation and synthesis pathways. Curr. Drug Targets Cardiovasc. Haematol. Disord. 2003, 3:1-30.
17. Lindsey M., Iyer R., Jung M., DeLeon-Pennell K., Ma Y. Matrix metalloproteinases as input and output signals for post-myocardial infarction remodeling. J. Mol. Cell. Cardiol. 2016, 91:134-140.
18. Souders C.A., Bowers S.L., Baudino T.A. Cardiac fibroblast: the renaissance cell. Circ. Res. 2009, 105:1164-1176.
19. Cunnington R.H., Nazari M., Dixon I.M. c-Ski, Smurf2, and Arkadia as regulators of TGF-beta signaling: new targets for managing myofibroblast function and cardiac fibrosis. Can. J. Physiol. Pharmacol. 2009, 87:764-772.
20. Hermans K., Daskalapoulos E., Blankensteijn W. The Janus face of myofibroblasts in the remodeling heart. J. Mol. Cell. Cardiol. 2016, 91:35-41.
21. Krenning G., Zeisberg E.M., Kalluri R. The origin of fibroblasts and mechanism of cardiac fibrosis. J. Cell. Physiol. 2010, 225:631-637.
22. Thum T., Gross C., Fiedler J., Fischer T., Kissler S., Bussen M., et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008, 456:980-984. (Epub 2008 Nov 30). 10.1038/nature07511.
23. Marko L., Kvakan H., Park J.K., Qadri F., Spallek B., Binger K.J., et al. Interferon-gamma signaling inhibition ameliorates angiotensin II-induced cardiac damage. Hypertension 2012, 60:1430-1436.
24. Liu J., Yang F., Yang X.-P., Jankowski M., Pagano P.J. NAD(P)H oxidase mediates angiotensin II-induced vascular macrophage infiltration and medial hypertrophy. Arterioscler. Thromb. Vasc. Biol. 2003, 23:776-782.
25. Cieslik K.A., Trial J., Crawford J.R., Taffet G.E., Entman M.L. Adverse fibrosis in the aging heart depends on signaling between myeloid and mesenchymal cells; role of inflammatory fibroblasts. J. Mol. Cell. Cardiol. 2014, 70:56-63.
26. Frangogiannis N.G., Dewald O., Xia Y., Ren G., Haudek S., Leucker T., et al. Critical role of monocyte chemoattractant protein-1/CC chemokine ligand 2 in the pathogenesis of ischemic cardiomyopathy. Circulation 2007, 115:584-592.
27. Kawaguchi M., Takahashi M., Hata T., Kashima Y., Usui F., Morimoto H., et al. Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation 2011, 123:594-604.
28. Rossini A., Zacheo A., Mocini D., Totta P., Facchiano A., Castoldi R., et al. HMGB1-stimulated human primary cardiac fibroblasts exert a paracrine action on human and murine cardiac stem cells. J. Mol. Cell. Cardiol. 2008, 44:683-693.
29. Chen G.Y., Nunez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10:826-837.
30. DiPietro L.A. Wound healing: the role of the macrophage and other immune cells. Shock 1995, 4:233-240.
31. Weidenbach R., Schulz R., Gres P., Behrends M., Post H., Heusch G. Enhanced reduction of myocardial infarct size by combined ACE inhibition and AT(1)-receptor antagonism. Br. J. Pharmacol. 2000, 131:138-144.
32. Ito N., Ohishi M., Yamamoto K., Tatara Y., Shiota A., Hayashi N., et al. Renin-angiotensin inhibition reverses advanced cardiac remodeling in aging spontaneously hypertensive rats. Am. J. Hypertens. 2007, 20:792-799.
33. Katoh M., Egashira K., Mitsui T., Chishima S., Takeshita A., Narita H. Angiotensin-converting enzyme inhibitor prevents plasminogen activator inhibitor-1 expression in a rat model with cardiovascular remodeling induced by chronic inhibition of nitric oxide synthesis. J. Mol. Cell. Cardiol. 2000, 32:73-83.
34. Liang B., Leenen F.H. Prevention of salt induced hypertension and fibrosis by angiotensin converting enzyme inhibitors in Dahl S rats. Br. J. Pharmacol. 2007, 152:903-914.
35. Peng H., Carretero O.A., Vuljaj N., Liao T.D., Motivala A., Peterson E.L., et al. Angiotensin-converting enzyme inhibitors: a new mechanism of action. Circulation 2005, 112:2436-2445.
36. Stein M., Boulaksil M., Jansen J.A., Herold E., Noorman M., Joles J.A., et al. Reduction of fibrosis-related arrhythmias by chronic renin-angiotensin-aldosterone system inhibitors in an aged mouse model. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H310-H321.
37. Brilla C.G. Regression of myocardial fibrosis in hypertensive heart disease: diverse effects of various antihypertensive drugs. Cardiovasc. Res. 2000, 46:324-331.
38. Susic D., Varagic J., Frohlich E.D. Pharmacologic agents on cardiovascular mass, coronary dynamics and collagen in aged spontaneously hypertensive rats. J. Hypertens. 1999, 17:1209-1215.
39. Leuschner F., Panizzi P., Chico-Calero I., Lee W.W., Ueno T., Cortez-Retamozo V., et al. Angiotensin-converting enzyme inhibition prevents the release of monocytes from their splenic reservoir in mice with myocardial infarction. Circ. Res. 2010, 107:1364-1373.
40. Baumann M., Hermans J.R., Janssen B.J., Peutz-Kootstra C., Witzke O., Heemann U., et al. Transient prehypertensive treatment in spontaneously hypertensive rats: a comparison of spironolactone and losartan regarding long-term blood pressure and target organ damage. J. Hypertens. 2007, 25:2504-2511.
41. 1 receptor-inhibition in prehypertensive spontaneously hypertensive rats results in maintained cardiac protection until advanced age. J. Hypertens. 2007, 25:207-215.
42. Peng F., Lin J., Lin L., Tang H. Transient prehypertensive treatment in spontaneously hypertensive rats: a comparison of losartan and amlodipine regarding long-term blood pressure, cardiac and renal protection. Int. J. Mol. Med. 2012, 30:1376-1386.
43. Fornes P., Richer C., Vacher E., Bruneval P., Giudicelli J.F. Losartan's protective effects in stroke-prone spontaneously hypertensive rats persist durably after treatment withdrawal. J. Cardiovasc. Pharmacol. 1993, 22:305-313.
44. Aceros H., Farah G., Cobos-Puc L., Stabile A.M., Noiseux N., Mukaddam-Daher S. Moxonidine improves cardiac structure and performance in SHR through inhibition of cytokines, p38 MAPK and Akt. Br. J. Pharmacol. 2011, 164:946-957.
45. Guerrero E.I., Ardanaz N., Sevilla M.A., Arevalo M.A., Montero M.J. Cardiovascular effects of nebivolol in spontaneously hypertensive rats persist after treatment withdrawal. J. Hypertens. 2006, 24:151-158.
46. Sevilla M.A., Voces F., Carron R., Guerrero E.I., Ardanaz N., San Roman L., et al. Amlodipine decreases fibrosis and cardiac hypertrophy in spontaneously hypertensive rats: persistent effects after withdrawal. Life Sci. 2004, 75:881-891.
47. Lu J.-C., Cui W., Zhang H.-L., Liu F., Han M., Liu D.-M., et al. Additive beneficial effects of amlodipine and atorvastatin in reversing advanced cardiac hypertrophy in elderly spontaneously hypertensive rats. Clin. Exp. Pharmacol. Physiol. 2009, 36:1110-1119.
48. Nakamura T., Fukuda M., Kataoka K., Nako H., Tokutomi Y., Dong Y.F., et al. Eplerenone potentiates protective effects of amlodipine against cardiovascular injury in salt-sensitive hypertensive rats. Hypertens. Res. 2011, 34:817-824. (Epub Apr 7). 10.1038/hr.2011.35.
49. Sandmann S., Claas R., Cleutjens J.P., Daemen M.J., Unger T. Calcium channel blockade limits cardiac remodeling and improves cardiac function in myocardial infarction-induced heart failure in rats. J. Cardiovasc. Pharmacol. 2001, 37:64-77.
50. Jia Y., Xu J., Yu Y., Guo J., Liu P., Chen S., et al. Nifedipine inhibits angiotensin II-induced cardiac fibrosis via downregulating Nox4-derived ROS generation and suppressing ERK1/2, JNK signaling pathways. Pharmazie 2013, 68:435-441.
51. Ciulla M.M., Paliotti R., Esposito A., Diez J., Lopez B., Dahlof B., et al. Different effects of antihypertensive therapies based on losartan or atenolol on ultrasound and biochemical markers of myocardial fibrosis: results of a randomized trial. Circulation 2004, 110:552-557.
52. Díez J., Querejeta R., López B., González A., Larman M., Martínez Ubago J.L. Losartan-dependent regression of myocardial fibrosis is associated with reduction of left ventricular chamber stiffness in hypertensive patients. Circulation 2002, 105:2512-2517.
53. Shimada Y.J., Passeri J.J., Baggish A.L., O'Callaghan C., Lowry P.A., Yannekis G., et al. Effects of losartan on left ventricular hypertrophy and fibrosis in patients with nonobstructive hypertrophic cardiomyopathy. JACC Heart Fail. 2013, 1:480-487.
54. Ciulla M.M., Paliotti R., Esposito A., Cuspidi C., Muiesan M.L., Rosei E.A., et al. Effects of antihypertensive treatment on ultrasound measures of myocardial fibrosis in hypertensive patients with left ventricular hypertrophy: results of a randomized trial comparing the angiotensin receptor antagonist, candesartan and the angiotensin-converting enzyme inhibitor, enalapril. J. Hypertens. 2009, 27:626-632.
55. Muller-Brunotte R., Kahan T., Lopez B., Edner M., Gonzalez A., Diez J., et al. Myocardial fibrosis and diastolic dysfunction in patients with hypertension: results from the Swedish irbesartan left ventricular hypertrophy investigation versus atenolol (SILVHIA). J. Hypertens. 2007, 25:1958-1966.
56. Fogari R., Mugellini A., Destro M., Corradi L., Lazzari P., Zoppi A., et al. Losartan and amlodipine on myocardial structure and function: a prospective, randomized, clinical trial. Diabet. Med. 2012, 29:24-31.
57. Kosmala W., Przewlocka-Kosmala M., Szczepanik-Osadnik H., Mysiak A., O'Moore-Sullivan T., Marwick T.H. A randomized study of the beneficial effects of aldosterone antagonism on LV function, structure, and fibrosis markers in metabolic syndrome. JACC Cardiovasc. Imaging 2011, 4:1239-1249.
58. Kurrelmeyer K.M., Ashton Y., Xu J., Nagueh S.F., Torre-Amione G., Deswal A. Effects of spironolactone treatment in elderly women with heart failure and preserved left ventricular ejection fraction. J. Card. Fail. 2014, 20:560-568.
59. Ishimitsu T., Kobayashi T., Honda T., Takahashi M., Minami J., Ohta S., et al. Protective effects of an angiotensin II receptor blocker and a long-acting calcium channel blocker against cardiovascular organ injuries in hypertensive patients. Hypertens. Res. 2005, 28:351-359.
60. Yamada T., Horiuchi M., Dzau V.J. Angiotensin II type 2 receptor mediates programmed cell death. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:156-160.
61. Guo C., Wang Y., Liang H., Zhang J. ADAMTS-1 contributes to the antifibrotic effect of captopril by accelerating the degradation of type I collagen in chronic viral myocarditis. Eur. J. Pharmacol. 2010, 629:104-110.
62. Meng G., Wu F., Yang L., Zhu H., Gu J., He M., et al. Synergistic attenuation of myocardial fibrosis in spontaneously hypertensive rats by joint treatment with benazepril and candesartan. J. Cardiovasc. Pharmacol. 2009, 54:16-24.
63. Katwa L.C., Campbell S.E., Tyagi S.C., Lee S.J., Cicila G.T., Weber K.T. Cultured myofibroblasts generate angiotensin peptidesde novo. J. Mol. Cell. Cardiol. 1997, 29:1375-1386.
64. Weber K.T., Sun Y., Campbell S.E. Structural remodelling of the heart by fibrous tissue: role of circulating hormones and locally produced peptides. Eur. Heart J. 1995, 16:12-18.
65. Peng H., Carretero O.A., Peterson E.L., Rhaleb N.E. Ac-SDKP inhibits transforming growth factor-beta1-induced differentiation of human cardiac fibroblasts into myofibroblasts. Am. J. Physiol. Heart Circ. Physiol. 2010, 298:H1357-H1364.
66. Pokharel S., Rasoul S., Roks A.J., van Leeuwen R.E., van Luyn M.J., Deelman L.E., et al. N-acetyl-Ser-Asp-Lys-Pro inhibits phosphorylation of Smad2 in cardiac fibroblasts. Hypertension 2002, 40:155-161.
67. Akashiba A., Ono H., Ono Y., Ishimitsu T., Matsuoka H. Valsartan improves L-NAME-exacerbated cardiac fibrosis with TGF-beta inhibition and apoptosis induction in spontaneously hypertensive rats. J. Cardiol. 2008, 52:239-246.
68. Ono Y., Ono H., Matsuoka H., Fujimori T., Frohlich E.D. Apoptosis, coronary arterial remodeling, and myocardial infarction after nitric oxide inhibition in SHR. Hypertension 1999, 34:609-616.
69. Hale T.M., Robertson S.J., Burns K.D., deBlois D. Short-term ACE inhibition confers long-term protection against target organ damage. Hypertens. Res. 2012, 35:604-610.
70. Biwer L.A., D'Souza K.M., Abidali A., Tu D., Siniard A.L., DeBoth M., et al. Time course of cardiac inflammation during nitric oxide synthase inhibition in SHR: impact of prior transient ACE inhibition. Hypertens. Res. 2015.
71. Biwer L.A., Broderick T.L., Xu H., Carroll C., Hale T.M. Protection against L-NAME-induced reduction in cardiac output persists even after cessation of angiotensin-converting enzyme inhibitor treatment. Acta Physiol. (Oxf.) 2013, 207:156-165.
72. Usui M., Egashira K., Tomita H., Koyanagi M., Katoh M., Shimokawa H., et al. Important role of local angiotensin II activity mediated via type 1 receptor in the pathogenesis of cardiovascular inflammatory changes induced by chronic blockade of nitric oxide synthesis in rats. Circulation 2000, 101:305-310.
73. Sano H., Okamoto H., Kitabatake A., Iizuka K., Murakami T., Kawaguchi H. Increased mRNA expression of cardiac renin-angiotensin system and collagen synthesis in spontaneously hypertensive rats. Mol. Cell. Biochem. 1998, 178:51-58.
74. Smith R.S., Smith T.J., Blieden T.M., Phipps R.P. Fibroblasts as sentinel cells. Synthesis of chemokines and regulation of inflammation. Am. J. Pathol. 1997, 151:317-322.
75. Turner N. Inflammatory and fibrotic responses of cardiac fibroblasts to myocardial damage associated patterns (DAMPs). J. Mol. Cell. Cardiol. 2016, 10.1016/j.yjmcc.2015.11.002.
76. D'Souza K.M., Biwer L.A., Madhavpeddi L., Ramaiah P., Shahid W., Hale T.M. Persistent change in cardiac fibroblast physiology after transient ACE inhibition. Am. J. Physiol. Heart Circ. Physiol. 2015, 309:H1346-H1353.
77. Williams S.M., Golden-Mason L., Ferguson B.S., Schuetze K.B., Cavasin M.A., Demos-Davies K., et al. Class I HDACs regulate angiotensin II-dependent cardiac fibrosis via fibroblasts and circulating fibrocytes. J. Mol. Cell. Cardiol. 2014, 67:112-125.
78. Reddy M.A., Sumanth P., Lanting L., Yuan H., Wang M., Mar D., et al. Losartan reverses permissive epigenetic changes in renal glomeruli of diabetic db/db mice. Kidney Int. 2014, 85:362-373.
79. Hayashi K., Sasamura H., Nakamura M., Sakamaki Y., Azegami T., Oguchi H., et al. Renin-angiotensin blockade resets podocyte epigenome through Kruppel-like factor 4 and attenuates proteinuria. Kidney Int. 2015, 88:745-753.
80. Xu W.P., Yao T.Q., Jiang Y.B., Zhang M.Z., Wang Y.P., Yu Y., et al. Effect of the angiotensin II receptor blocker valsartan on cardiac hypertrophy and myocardial histone deacetylase expression in rats with aortic constriction. Exp. Ther. Med. 2015, 9:2225-2228.
81. Jiang X., Ning Q., Wang J. Angiotensin II induced differentially expressed microRNAs in adult rat cardiac fibroblasts. J. Physiol. Sci. 2013, 63:31-38.
82. Zhang Y., Huang X.R., Wei L.H., Chung A.C., Yu C.M., Lan H.Y. miR-29b as a therapeutic agent for angiotensin II-induced cardiac fibrosis by targeting TGF-beta/Smad3 signaling. Mol. Ther. 2014, 22:974-985. (Epub Feb 26). 10.1038/mt.2014.25.
83. Ning Q., Jiang X. Angiotensin II upregulated the expression of microRNA-224 but not microRNA-21 in adult rat cardiac fibroblasts. Biomed. Rep. 2013, 1:776-780. (Epub 2013 Jul 22).
84. Der Sarkissian S., Marchand E.L., Duguay D., Hamet P., deBlois D. Reversal of interstitial fibroblast hyperplasia via apoptosis in hypertensive rat heart with valsartan or enalapril. Cardiovasc. Res. 2003, 57:775-783.
85. Der Sarkissian S., Tea B.S., Touyz R.M., deBlois D., Hale T.M. Role of angiotensin II type 2 receptor during regression of cardiac hypertrophy in spontaneously hypertensive rats. J. Am. Soc. Hypertens. 2013, 7:118-127.
86. Duguay D., Pesant S., Deschepper C.F., deBlois D. Fibroblast apoptosis precedes cardiomyocyte mass reduction during left ventricular remodeling in hypertensive rats treated with amlodipine. J. Hypertens. 2007, 25:1291-1299.
87. Tea B.S., Dam T.V., Moreau P., Hamet P., deBlois D. Apoptosis during regression of cardiac hypertrophy in spontaneously hypertensive rats. Temporal regulation and spatial heterogeneity. Hypertension 1999, 34:229-235.
88. deBlois D., Tea B.S., Beaudry D., Hamet P. Regulation of therapeutic apoptosis: a potential target in controlling hypertensive organ damage. Can. J. Physiol. Pharmacol. 2005, 83:29-41.
89. Paull J.R., Widdop R.E. Persistent cardiovascular effects of chronic renin-angiotensin system inhibition following withdrawal in adult spontaneously hypertensive rats. J. Hypertens. 2001, 19:1393-1402.
90. Stewart J.A., Massey E.P., Fix C., Zhu J., Goldsmith E.C., Carver W. Temporal alterations in cardiac fibroblast function following induction of pressure overload. Cell Tissue Res. 2010, 340:117-126.
91. Burgess M.L., Terracio L., Hirozane T., Borg T.K. Differential integrin expression by cardiac fibroblasts from hypertensive and exercise-trained rat hearts. Cardiovasc. Pathol. 2002, 11:78-87.
92. MacKenna D., Summerour S.R., Villarreal F.J. Role of mechanical factors in modulating cardiac fibroblast function and extracellular matrix synthesis. Cardiovasc. Res. 2000, 46:257-263.
93. Qi G., Jia L., Li Y., Bian Y., Cheng J., Li H., et al. Angiotensin II infusion-induced inflammation, monocytic fibroblast precursor infiltration, and cardiac fibrosis are pressure dependent. Cardiovasc. Toxicol. 2011, 11:157-167.
94. Ikeda Y., Nakamura T., Takano H., Kimura H., Obata J.E., Takeda S., et al. Angiotensin II-induced cardiomyocyte hypertrophy and cardiac fibrosis in stroke-prone spontaneously hypertensive rats. J. Lab. Clin. Med. 2000, 135:353-359.
95. Fernandes-Santos C., de Souza Mendonca L., Mandarim-de-Lacerda C.A. Favorable cardiac and aortic remodeling in olmesartan-treated spontaneously hypertensive rats. Heart Vessel. 2009, 24:219-227.
96. Mill J.G., Milanez Mda C., de Resende M.M., Gomes Mda G., Leite C.M. Spironolactone prevents cardiac collagen proliferation after myocardial infarction in rats. Clin. Exp. Pharmacol. Physiol. 2003, 30:739-744.
97. Tomita H., Egashira K., Ohara Y., Takemoto M., Koyanagi M., Katoh M., et al. Early induction of transforming growth factor-beta via angiotensin II type 1 receptors contributes to cardiac fibrosis induced by long-term blockade of nitric oxide synthesis in rats. Hypertension 1998, 32:273-279.
98. Kim S., Ohta K., Hamaguchi A., Yukimura T., Miura K., Iwao H. Angiotensin II induces cardiac phenotypic modulation and remodeling in vivo in rats. Hypertension 1995, 25:1252-1259.
99. Neves M.F., Amiri F., Virdis A., Diep Q.N., Schiffrin E.L. Role of aldosterone in angiotensin II-induced cardiac and aortic inflammation, fibrosis, and hypertrophy. Can. J. Physiol. Pharmacol. 2005, 83:999-1006.