Angiotensin II-stimulated collagen production in cardiac fibroblasts is mediated by reactive oxygen species

Journal of Hypertension

Volumn 24, Issue 4, 2006, Pages 757-766

  Lijnen, Paul ^a,c   Papparella, Italia ^b   Petrov, Victor ^a   Semplicini, Andrea ^b   Fagard, Robert ^a  

^a KU LEUVEN DEPARTMENT OF REHABILITATION SCIENCES   (Belgium)

^b UNIVERSITY OF PADUA MEDICAL SCHOOL   (Italy)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Angiotensin II; Collagen; Fibroblasts; NAD(P)H oxidase; Oxygen radicals

Indexed keywords

ALLOPURINOL; ANGIOTENSIN II; APOCYNIN; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; CYTOCHROME C; CYTOCHROME P450 REDUCTASE; DICHLORODIHYDROFLUORESCEIN DIACETATE; INDOMETACIN; KETOCONAZOLE; LIPOXYGENASE INHIBITOR; MESSENGER RNA; N(G) NITROARGININE; NITRIC OXIDE SYNTHASE INHIBITOR; NORDIHYDROGUAIARETIC ACID; PROLINE; PROSTAGLANDIN SYNTHASE INHIBITOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROTENONE; SUPEROXIDE; SUPEROXIDE DISMUTASE; XANTHINE OXIDASE INHIBITOR;

ANIMAL CELL; ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 33645517324     PISSN: 02636352     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.hjh.0000217860.04994.54     Document Type: Article

References (69)

1. 2α in pericardial fluid of patients with heart failure: a potential role for in vivo oxidant stress in ventricular dilatation and progression to heart failure. Circulation 1998; 97:1536-1539.
2. Dhalla AK, Hill MF, Singal PK. Role of oxidative stress in transition of hypertrophy to heart failure. J Am Coll Cardiol 1996; 28:506-514.
3. Hill MF, Singal PK. Antioxidant and oxidative stress changes during heart failure subsequent to myocardial infarction in rats. Am J Pathol 1996; 1489:291-300.
4. Touyz RM. Reactive oxygen species, vascular oxidative stress and redox signaling in hypertension. Hypertension 2004; 44:248-252.
5. Redon J, Oliva MR, Tormos C, Giner V, Chaves J, Iradi A, Saéz GT. Antioxidant activities and oxidative stress byproducts in human hypertension. Hypertension 2003; 41:1096-1101.
6. Lassègue B, Griendling KK. Reactive oxygen species in hypertension. Am J Hypertens 2004; 17:739-741.
7. Di Wang HD, Xu S, Johns DG, Du Y, Quinn MT, Cayatte AJ, Cohen RA. Role of NADPH oxidase in the vascular hypertrophy and oxidative stress response to angiotensin II in mice. Circ Res 2001; 88:947-953.
8. phox in aortas from angiotensin II-infused mice. Am J Physiol Heart Circ Physiol 2000; 279:H2234-H2240.
9. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular muscle cells. Circ Res 1994; 74:1141-1148.
10. Xie Z, Pimental DR, Lohan S, Vasertriger A, Pligavkos C, Colucci WS, Singh K. Regulation of angiotensin II-stimulated osteopontin expression in cardiac microvascular endothelial cells: role of p24/p44 mitogen-activated protein kinase and reactive oxygen species. J Cell Physiol 2001; 188:132-138.
11. Nakamura K, Fushimi K, Kouchi H, Mihara K, Miyazaki M, Ohe T, Namba M. Inhibiting effects of antioxidants on neonatal rat cardiac myocyte hypertrophy induced by tumor necrosis factor-α and angiotensin II. Circulation 1998; 98:794-799.
12. Siwik DA, Tzortzis JD, Pimental DR, Chang DLF, Pagano PJ, Singh K, et al. Inhibition of copper-zinc superoxide dismutase induces cell growth, hypertrophic phenotype and apoptosis in neonatal rat cardiac myocytes in vitro. Circ Res 1999; 85:147-153.
13. Bataller R, Schwabe RF, Choi YH, Yang L, PaikYH. Linquist J, et al. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J Clin Invest 2003; 112:1383-1394.
14. phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ Res 2002; 90:1205-1213.
15. Rajagopalan S, Kurz S, Manzel T, Tarpey M, Freeman BA, Griendling KK. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. J Clin Invest 1966; 97:1916-1923.
16. phox mRNA expression and NAD(P)H oxidase superoxide generation in rabbit adventitial fibroblasts. Hypertension 1998; 32: 331-337.
17. Touyz RM, Schiffrin EL. Angiotensin II-stimulated superoxide production is mediated via phospholipidase D in human vascular smooth muscle cells. Hypertension 1999; 34:976-982.
18. Virdis A, Naves MF, Amiri F, Viel E, Touyz RM, Schiffrin EL. Spironolactone improves angiotensin-induced vascular changes and oxidative stress. Hypertension 2002; 40:504-510.
19. phox-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation 2002; 105:293-296.
20. 2 expression. Lab Invest 1997; 77:533-539.
21. Pardo A, Barrios R, Maldonado V, Melendez J, Perez J, Ruiz V, et al. Gelatinases A and B are up-regulated in rat lungs by subacute hyperoxic pathogenetic implications. Am J Pathol 1998; 153:833-844.
22. Kawaguchi Y, Tanaka K, Okada T, Konishi H, Takahashi M, Ito M, Asai J. The effects of ultraviolet A and reactive oxygen species on the mRNA expression of 72-kDa type IV collagenase and its tissue inhibitor in cultured human dermal fibroblasts. Arch Derm Res 1996; 88:39-44.
23. Sun Y, Ratajska A, Zhou G, Weber KT. Angiotensin converting enzyme and myocardial fibrosis in the rat receiving angiotensin II or aldosterone. J Lab Clin Med 1993; 122:395-403.
24. Kato H, Suzuki H, Tajima S, Ogata Y, Tominaya T, Sato A, Saruta T. Angiotensin II stimulates collagen synthesis in cultured vascular smooth muscle cells. J Hypertens 1991; 9:17-22.
25. Wolf G, Haberstroh U, Neilson EG. Angiotensin II stimulates the proliferation and biosynthesis of type I collagen in cultural murine mesangial cells. Am J Pathol 1992; 140:95-107.
26. Border WA, Noble NA. Interactions of transforming growth factor-β and angiotensin II in renal fibrosis. Hypertension 1998; 31:181-188.
27. Kayami S, Border WA, Miller DE, Noble NA. .Angiotensin II stimulates extracellular matrix protein synthesis through interaction of transforming growth factor-β expression in rat glomerular mesangial cells. J Clin Invest 1994; 93:2431-2437.
28. Sano H, Okada H, Kawaguchi H, Yasuda H. Increased angiotensin II-stimulated collagen synthesis in cultured cardiac fibroblasts from spontaneously hypertensive rats. Circulation 1991; 84:II48.
29. Villareal FJ, Kim NN, Ungab GD, Printz MP, Dilmann WH. Identification of functional angiotensin II receptors on rat cardiac fibroblasts. Circulation 1993; 88:2849-2861.
30. Crabos M, Roth M, Hahn AWA, Erne P. Characterization of angiotensin II receptors in cultured rat fibroblasts: coupling to signaling systems and gene expression. J Clin Invest 1994; 93:2372-2378.
31. Brilla CG, Zhou G, Weber KT. Collagen metabolism in cultured rat cardiac fibroblasts: Response to angiotensin II and aldosterone. J Mol Cell Cardiol 1994; 26:809-820.
32. Lijnen P, Petrov V, Fagard R. Angiotensin II.-induced stimulation of collagen secretion and production in cardiac fibroblasts is mediated via angiotensin II subtype 1 receptors. J Renin Angiotensin Aldosterone Syst 2001; 2:117-122.
33. 1 induces angiotensin converting enzyme synthesis in rat cardiac fibroblasts during their differentiation to myofibroblasts. J Renin Angiotensin Aldosterone Syst 2000; 1:342-352.
34. Huang M, Sharma S, Zhu LX, Keane MP, Luo J, Zhang L, et al. IL-7 inhibits fibroblast TGF-β production and signaling in pulmonary fibrosis. J Clin Invest 2002; 109:931-937.
35. Lijnen P, Petrov V, Fagard R. Collagen production in cardiac fibroblasts during inhibition of angiotensin converting enzyme and aminopeptidases. J Hypertens 2004; 22:209-216.
36. Katwa LC. Cardiac myofibroblasts isolated from the site of myocardial infarction express endothelin de novo. Am J Physiol Heart Circ Physiol 2003; 285:H1132-H1139.
37. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 1979; 18:5294-5299.
38. Chomzynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156-157.
39. 1. J Biol Chem 1995; 270:30334-30338.
40. Siwik DA, Pagano PJ, Colucci WS. Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am J Physiol Cell Physiol 2001; 280:C53-C60.
41. Lang D, Mosfer SI, Shakesby A, Donaldson F, Lewis MJ. Coronary microvascular endothelial cell redox state in left ventricular hypertrophy. The role of angiotensin II. Circ Res 2000; 86:463-469.
42. Chen K, Chen J, Li D, Zhang X, Mehta JL. Angiotensin II regulation of collagen type I expression in cardiac fibroblasts. Modulation by PPAR-γ ligand pioglitazone. Hypertension 2004; 44:655-661.
43. Stolk J, Hiltermann TJN, Dijkman JH, Verhoeven AJ. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substitiuted catechol. Am J Respir Cell Mol Biol 1994; 11:95-102.
44. Doussière J, Vignas PV. Diphylene iodonium as an inhibitor of the NADPH oxidase complex of bovine neutrophils. Eur J Biochem 1992; 208:61-71.
45. Peng J, Gurantz D, Tran V, et al. Tumor necrosis factor-alpha-induced AT receptor upregulation enhances angiotensin II-mediated cardiac fibroblasts responses that favor fibrosis. Circ Res 2002; 91:1119-1126.
46. Seeger H, Lippert C, Wallwiener D, Mueck AO. Valsartan and candesartan can inhibit deteriorating effects of angiotensin Ii on coronary endothelial function. J Renin Angiotensin Aldosterone Syst 2001; 2:141-143.
47. Rouet-Benzineb P, Gontero B, Dreyfus P, Lafuma C. Angiotensin II induces nuclear factor-kappa B activation in cultured neonatal rat cardiomyocytes through protein kinase C signaling pathway. J Mol Cell Cardiol 2000; 32:1767-1778.
48. Solini A, Santini E, Ferrannini E. Enhanced angiotensin II-mediated effects in fibroblasts of patients with familial hypercholesterolemia. J Hypertens 2005; 23:367-374.
49. Virdis A, Neves MF, Amiri F, Touyz RM, Schiffrin EL. Role of NAD(P)H oxidase on vascular alterations in angiotensin II-infused mice. J Hypertens 2004; 22:535-542.
50. Park YM, Park MY, Suh YL, Park JB. NAD(P)H oxidase inhibitor prevents blood pressure elevation and cardiovascular hypertrophy in aldosterone-infused rats. Biochem Biophys Res Commun 2004; 313:812-817.
51. - and systolic blood pressure in mice. Circ Res 2001; 89:408-414.
52. Sun Y, Zhang J, Lu L, Chen SS, Quinn MT, Weber KT. Aldosterone-induced inflammation in the rat heart. Role of oxidative stress. Am J Pathol 2002; 161:1773-1781.
53. Iglarz M, Touyz RM, Viel EC, Amiri F, Schiffrin EL. Involvement of oxidative stress in the profibrotic action of aldosterone. Am J Hypertens 2004; 17:597-603.
54. Sousa T, Pinto D, Morato M, Fernandes E, Carvalho F, Albino-Teixeira A. Effect of the NADPH oxidase inhibitor apocynin on systolic blood pressure and on vascular anti-oxidant defenses in hypertensive rats with activation of the renin-angiotensin-system. J Hypertens 2005; 23:S361.
55. Pagano PJ, Ito Y, Tornheim K, Gallop PM, Tauber AI, Cohen RA. An NADPH oxidase superoxide-generating system in the rabbit aorta. Am J Physiol Heart Circ Physiol 1995; 268:H2274-H2280.
56. Ellmark SHM, Dusting GJ, Fui MNT, Guzzo-Pernell N, Drummond GR. The contribution of NOX4 to NADPH oxidase activity in mouse vascular smooth musle cells. Cardiovasc Res 2005; 65:495-504.
57. Meier B, Radeke HH, Selle S, Younes M, Sies H, Resch K, Habermehl G. Human fibroblasts release reactive oxygen species in response to interleukin-1 or tumour necrosis factor-α. Biochem J 1989; 263:539-545.
58. Nakagami H, Takemoto M, Liao JK. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced cardiac hypertrophy. J Mol Cell Cardiol 2003; 35:851-859.
59. Ding Y, Chen ZJ, Liu S, Che D, Vetter M, Chang CH. Inhibition of NOX4 activity by plumbagin. J Pharm Pharmacol 2005; 57:111-116.
60. Brightmann AO, Wang J, Miu R, Sun IL, Barr R, Crane FL, Morré DJ. A growth factor- and hormone-stimulated NADH oxidase from rat liver plasma membrane. Biochim Biophys Acta 1992; 1105:109-117.
61. Sano M, Fukuda K, Sato T, Kawaguchi H, Suematsu M, Matsuda S, et al. ERK and p38 MAPK, but not NF-κB, are critically involved in reactive oxygen species-mediated induction of IL-6 by angiotensin II in cardiac fibroblasts. Circ Res 2001; 89:661-669.
62. Cheng TH, Cheng PY, Shih NL, Chen IB, Wang DL, Chen JJ. Involvement of reactive oxygen species in angiotensin II-induced endothelin-1 gene expression in rat cardiac fibroblasts. J Am Coll Cardiol 2003; 42:1845-1854.
63. Ushio-Fukai M, Alexander RW, Akers M, Griendling KK. p38Mitogen-activated protein kinase is a critical component of the redox-sensitive signaling pathways activated by angiotensin II. J Biol Chem 1998; 273:15022-15029.
64. Touyz RM, He G, Elmabrouk M, Schiffrin EL. p38MAPKinase regulates vascular smooth muscle cell collagen synthesis by angiotensin II in SHR but not in WKY. Hypertension 2001; 37:574-580.
65. Li N, Karin M. Is NF-κB the sensor of oxidative stress? FASEB J 1999; 13:1137-1143.
66. Touyz RM. Reactive oxygen species as mediators of calcium signaling by angiotensin II. Implications in vascular physiology and pathophysiology. Antiox Redox Signal 2005; 7:1302-1314.
67. Shivakunar K, Kumaran C. L-Type calcium channel blockers and EGTA enhance superoxide production in cardiac fibroblasts. J Mol Cell Cardiol 2001; 33:373-377.
68. Kumaran C, Shivakunar K. Superoxide-mediated activation of cardiac fibroblasts by serum factors in hypomagnesemia. Free Radic Biol Med 2001; 31:882-886.
69. 1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 2005; 97:900-907.