Angiotensin II Downregulates Catalase Expression and Activity in Vascular Adventitial Fibroblasts Through an AT1R/ERK1/2-dependent Pathway

Overview

Journal Mol Cell Biochem

Publisher Springer

Specialty Biochemistry

Date 2011 Jun 11

PMID 21660462

Citations 13

Authors

Weiwei Yang

Jia Zhang

Haiya Wang

Pingjin Gao

Manpreet Singh

Kai Shen

Ningyuan Fang

Affiliations

Soon will be listed here.

Abstract

Angiotensin II (Ang II) plays a profound regulatory effect on NADPH oxidase and the functional features of vascular adventitial fibroblasts, but its role in antioxidant enzyme defense remains unclear. This study investigated the effect of Ang II on expressions and activities of superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPx) in adventitial fibroblasts and the possible mechanism involved. Ang II decreased the expression and activity of CAT in a dose- and time-dependent manner, but not that of SOD and GPx. The effects were abolished by the angiotensin II type 1 receptor (AT1R) blocker losartan and AT1R small-interfering RNA (siRNA). Incubation with polyethylene glycol-CAT prevented the Ang II-induced effects on reactive oxygen species (ROS) generation and myofibroblast differentiation. Moreover, Ang II rapidly induced phosphorylation of ERK1/2, which was reversed by losartan and AT1R siRNA. Pharmacological blockade of ERK1/2 improved Ang II-induced decrease in CAT protein expression. These in vitro results indicate that Ang II induces ERK1/2 activation, contributing to the downregulation of CAT as well as promoting oxidative stress and adventitial fibroblast phenotypic differentiation in an AT1R-mediated manner.

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References

Godin N, Liu F, Lau G, Brezniceanu M, Chenier I, Filep J . Catalase overexpression prevents hypertension and tubular apoptosis in angiotensinogen transgenic mice. Kidney Int. 2010; 77(12):1086-97. DOI: 10.1038/ki.2010.63. View

Choi S, Kim T, Kim K, Kim B, Ahn S, Cho H . Decreased catalase expression and increased susceptibility to oxidative stress in primary cultured corneal fibroblasts from patients with granular corneal dystrophy type II. Am J Pathol. 2009; 175(1):248-61. PMC: 2708811. DOI: 10.2353/ajpath.2009.081001. View

Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman B, Griendling K . 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(8):1916-23. PMC: 507261. DOI: 10.1172/JCI118623. View

Lijnen P, Papparella I, Petrov V, Semplicini A, Fagard R . Angiotensin II-stimulated collagen production in cardiac fibroblasts is mediated by reactive oxygen species. J Hypertens. 2006; 24(4):757-66. DOI: 10.1097/01.hjh.0000217860.04994.54. View

Zhu D, Herembert T, Marche P . Increased proliferation of adventitial fibroblasts from spontaneously hypertensive rat aorta. J Hypertens. 1991; 9(12):1161-8. View

Viedt C, Soto U, Krieger-Brauer H, Fei J, Elsing C, Kubler W . Differential activation of mitogen-activated protein kinases in smooth muscle cells by angiotensin II: involvement of p22phox and reactive oxygen species. Arterioscler Thromb Vasc Biol. 2000; 20(4):940-8. DOI: 10.1161/01.atv.20.4.940. View

Takeda K, Ichiki T, Tokunou T, Iino N, Takeshita A . 15-Deoxy-delta 12,14-prostaglandin J2 and thiazolidinediones activate the MEK/ERK pathway through phosphatidylinositol 3-kinase in vascular smooth muscle cells. J Biol Chem. 2001; 276(52):48950-5. DOI: 10.1074/jbc.M108722200. View

Chan Y, Leung P . Involvement of redox-sensitive extracellular-regulated kinases in angiotensin II-induced interleukin-6 expression in pancreatic acinar cells. J Pharmacol Exp Ther. 2009; 329(2):450-8. DOI: 10.1124/jpet.108.148353. View

Touyz R . The role of angiotensin II in regulating vascular structural and functional changes in hypertension. Curr Hypertens Rep. 2003; 5(2):155-64. DOI: 10.1007/s11906-003-0073-2. View

10.

Leung P, Chan Y . Role of oxidative stress in pancreatic inflammation. Antioxid Redox Signal. 2008; 11(1):135-65. DOI: 10.1089/ars.2008.2109. View

11.

Beltran A, Briones A, Garcia-Redondo A, Rodriguez C, Miguel M, Alvarez Y . p38 MAPK contributes to angiotensin II-induced COX-2 expression in aortic fibroblasts from normotensive and hypertensive rats. J Hypertens. 2009; 27(1):142-54. DOI: 10.1097/hjh.0b013e328317a730. View

12.

Touyz R . Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: what is the clinical significance?. Hypertension. 2004; 44(3):248-52. DOI: 10.1161/01.HYP.0000138070.47616.9d. View

13.

Griendling K, Sorescu D, Lassegue B, Ushio-Fukai M . Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol. 2000; 20(10):2175-83. DOI: 10.1161/01.atv.20.10.2175. View

14.

Zhu H, Itoh K, Yamamoto M, Zweier J, Li Y . Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: protection against reactive oxygen and nitrogen species-induced cell injury. FEBS Lett. 2005; 579(14):3029-36. DOI: 10.1016/j.febslet.2005.04.058. View

15.

Baas A, Berk B . Differential activation of mitogen-activated protein kinases by H2O2 and O2- in vascular smooth muscle cells. Circ Res. 1995; 77(1):29-36. DOI: 10.1161/01.res.77.1.29. View

16.

Sousa T, Pinho D, Morato M, Marques-Lopes J, Fernandes E, Afonso J . Role of superoxide and hydrogen peroxide in hypertension induced by an antagonist of adenosine receptors. Eur J Pharmacol. 2008; 588(2-3):267-76. DOI: 10.1016/j.ejphar.2008.04.044. View

17.

Lassegue B, Griendling K . Reactive oxygen species in hypertension; An update. Am J Hypertens. 2004; 17(9):852-60. DOI: 10.1016/j.amjhyper.2004.02.004. View

18.

Dieterich S, Bieligk U, Beulich K, Hasenfuss G, Prestle J . Gene expression of antioxidative enzymes in the human heart: increased expression of catalase in the end-stage failing heart. Circulation. 2000; 101(1):33-9. DOI: 10.1161/01.cir.101.1.33. View

19.

Pearson G, Robinson F, Beers Gibson T, Xu B, Karandikar M, Berman K . Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev. 2001; 22(2):153-83. DOI: 10.1210/edrv.22.2.0428. View

20.

Okutan H, Ozcelik N, Yilmaz H, Uz E . Effects of caffeic acid phenethyl ester on lipid peroxidation and antioxidant enzymes in diabetic rat heart. Clin Biochem. 2005; 38(2):191-6. DOI: 10.1016/j.clinbiochem.2004.10.003. View