Abstract
Cardiac fibrosis represented as perivascular/interstial fibrosis occurs in patients with hypertension. Oxidative stress has been demonstrated to contribute to such structural remodeling. The underlying mechanisms, however, remain to be elucidated. Herein, we tested the hypothesis that oxidative stress mediates cardiac fibrogenesis by stimulating transforming growth factor (TGF)-beta1 expression, which in turn triggers a series of fibrogenic responses. Sprague-Dawley rats were treated with angiotensin (Ang)II (9 microg/h s) for 4 weeks with/without co-treatment of combined antioxidants, apocynin, and tempol (120 mg/kg/day each, oral). Untreated rats served as controls. Appearance of cardiac oxidative stress and its potential effect on the expression of TGF-beta1, population of myofibroblasts, collagen synthesis/degradation, and fibrosis in hearts were examined. Chronic AngII infusion elevated systemic blood pressure (210 +/- 5 mmHg). Extensive perivascular and interstitial fibrosis was found in both ventricles, which were co-localized with oxidative stress represented as upregulated NADPH oxidase (gp91(phox) subunit) expression. Co-treatment with antioxidants led to: (1) markedly decreased cardiac gp91(phox); (2) significantly attenuated gene expression of TGF-beta1, type-I collagen, and tissue inhibitors of matrix metalloproteinase (TIMP)-I/II in the heart; (3) largely reduced population of myofibroblasts at sites of fibrosis; (4) significantly reduced cardiac collagen volume; (5) and partially suppressed blood pressure (190 +/- 4 mmHg). Thus, cardiac oxidative stress promotes the development of cardiac fibrosis by upregulating TGF-beta1 expression, which subsequently enhances cardiac collagen synthesis and suppresses collagen degradation in hypertensive rats.
MeSH Terms
Angiotensin II/pharmacology
Animals
Antioxidants/pharmacology
Blood Pressure/drug effects
Collagen Type I/genetics,metabolism
Fibroblasts/drug effects,metabolism
Fibrosis
Gene Expression Regulation/drug effects
Hypertension/complications,genetics,physiopathology
Immunohistochemistry
Membrane Glycoproteins/genetics,metabolism
Models, Biological
Myocardium/enzymology,pathology
NADPH Oxidase 2
NADPH Oxidases/genetics,metabolism
Oxidative Stress/drug effects
RNA, Messenger/genetics,metabolism
Rats
Systole/drug effects
Tissue Inhibitor of Metalloproteinase-1/genetics,metabolism
Tissue Inhibitor of Metalloproteinase-2/genetics,metabolism
Transforming Growth Factor beta1/genetics,metabolism
Chemicals
Antioxidants
Collagen Type I
Membrane Glycoproteins
RNA, Messenger
Tissue Inhibitor of Metalloproteinase-1
Transforming Growth Factor beta1
Angiotensin II
Tissue Inhibitor of Metalloproteinase-2
Cybb protein, rat
NADPH Oxidase 2
NADPH Oxidases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Zhao Wenyuan
Division of Cardiovascular Diseases, Department of Medicine, University of Tennessee Health Science Center, 956 Court Avenue Rm B310, Memphis, TN, 38163, USA.
Zhao Tieqiang
Chen Yuanjian
Ahokas Robert A
Sun Yao
References (30)
30 references, click to expand
-
N-acetylcysteine treatment normalizes serum tumor necrosis factor-alpha level and hinders the progression of cardiac injury in hypertensive rats.
Circulation. 2004 Oct 5;110(14):2003-9
PMID: 15451797
-
NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis.
J Clin Invest. 2003 Nov;112(9):1383-94
PMID: 14597764
-
NADPH oxidases in cardiovascular health and disease.
Antioxid Redox Signal. 2006 May-Jun;8(5-6):691-728
PMID: 16771662
-
Pressure-independent effects of angiotensin II on hypertensive myocardial fibrosis.
Hypertension. 2004 Feb;43(2):499-503
PMID: 14699000
-
Local cardiac renin-angiotensin system: hypertension and cardiac failure.
J Mol Cell Cardiol. 2002 Nov;34(11):1435-42
PMID: 12431442
-
Fibrosis in hypertensive heart disease: role of the renin-angiotensin-aldosterone system.
Med Clin North Am. 2004 Jan;88(1):83-97
PMID: 14871052
-
Transforming growth factor beta-1 in acute myocardial infarction in rats.
Growth Factors. 1988;1(1):91-9
PMID: 3078566
-
Role of myofibroblasts during normal tissue repair and excessive scarring: interest of their assessment in nephropathies.
Histol Histopathol. 2000 Jan;15(1):269-80
PMID: 10668216
-
Cardiac myofibroblasts express alpha smooth muscle actin during right ventricular pressure overload in the rabbit.
Am J Pathol. 1991 Jul;139(1):207-16
PMID: 1853934
-
Time-dependent expression pattern of nitric oxide and superoxide after myocardial infarction in rats.
Pharmacol Res. 2007 Jan;55(1):72-9
PMID: 17158059
-
Role of oxidative stress in remodeling of the myocardial microcirculation in hypertension.
Arterioscler Thromb Vasc Biol. 2006 Aug;26(8):1746-52
PMID: 16709946
-
Role of xanthine oxidoreductase in the reversal of diastolic heart failure by candesartan in the salt-sensitive hypertensive rat.
Hypertension. 2007 Oct;50(4):657-62
PMID: 17709654
-
Differential effects of angiotensin II on cardiac cell proliferation and intramyocardial perivascular fibrosis in vivo.
Circulation. 1998 Dec 15;98(24):2765-73
PMID: 9851965
-
NF-kappa B as a central mediator in the induction of TGF-beta in monocytes from patients with idiopathic myelofibrosis: an inflammatory response beyond the realm of homeostasis.
J Immunol. 2000 Aug 15;165(4):2271-7
PMID: 10925316
-
Pressure overload-induced transient oxidative stress mediates perivascular inflammation and cardiac fibrosis through angiotensin II.
Hypertens Res. 2006 Sep;29(9):711-8
PMID: 17249527
-
Angiotensin-converting enzyme and myocardial fibrosis in the rat receiving angiotensin II or aldosterone.
J Lab Clin Med. 1993 Oct;122(4):395-403
PMID: 8228553
-
Scar myofibroblasts of the infarcted rat heart express natriuretic peptides.
J Cell Physiol. 2006 Apr;207(1):165-73
PMID: 16270351
-
Tissue angiotensin II and myocardial infarction.
EXS. 1996;76:479-88
PMID: 8805813
-
Redox-dependent signalling by angiotensin II and vascular remodelling in hypertension.
Clin Exp Pharmacol Physiol. 2003 Nov;30(11):860-6
PMID: 14678251
-
NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure.
Cardiovasc Res. 2006 Jul 15;71(2):208-15
PMID: 16631149
-
Transforming growth factor beta stimulates the production of the tissue inhibitor of metalloproteinases (TIMP) by human synovial and skin fibroblasts.
Biochim Biophys Acta. 1991 Sep 3;1094(2):207-10
PMID: 1654118
-
NF-kappa B involved in transcription enhancement of TGF-beta 1 induced by Ox-LDL in rat mesangial cells.
Chin Med J (Engl). 2004 Feb;117(2):225-30
PMID: 14975207
-
NADPH oxidases in the kidney.
Antioxid Redox Signal. 2006 Sep-Oct;8(9-10):1597-607
PMID: 16987014
-
Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts.
J Cell Biol. 1993 Jul;122(1):103-11
PMID: 8314838
-
Inhibition of angiotensin-converting enzyme and attenuation of myocardial fibrosis by lisinopril in rats receiving angiotensin II.
J Lab Clin Med. 1995 Jul;126(1):95-101
PMID: 7602241
-
Transforming growth factor Beta1 induction of tissue inhibitor of metalloproteinases 3 in articular chondrocytes is mediated by reactive oxygen species.
Free Radic Biol Med. 2004 Jul 15;37(2):196-207
PMID: 15203191
-
Sustained expression of TGF-beta 1 underlies development of progressive kidney fibrosis.
Kidney Int. 1994 Mar;45(3):916-27
PMID: 8196298
-
Oxidative stress in hypertension and chronic kidney disease: role of angiotensin II.
Semin Nephrol. 2004 Mar;24(2):101-14
PMID: 15017522
-
Aldosterone-induced inflammation in the rat heart : role of oxidative stress.
Am J Pathol. 2002 Nov;161(5):1773-81
PMID: 12414524
-
ANG II-induced cardiac molecular and cellular events: role of aldosterone.
Am J Physiol Heart Circ Physiol. 2006 Jul;291(1):H336-43
PMID: 16489102