The angiotensin-converting enzyme 2/angiotensin (1-7)/mas axis protects against lung fibroblast migration and lung fibrosis by inhibiting the NOX4-derived ROS-mediated RhoA/Rho kinase pathway

Antioxidants and Redox Signaling

Volumn 22, Issue 3, 2015, Pages 241-258

  Meng, Ying ^a   Li, Ting ^a   Zhou, Gao Su ^b   Chen, Yan ^a   Yu, Chang Hui ^a   Pang, Miao Xia ^a   Li, Wei ^a   Li, Yang ^a   Zhang, Wen Yong ^a   Li, Xu ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b Breast Cancer Department of 307   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ALPHA SMOOTH MUSCLE ACTIN; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN II; ANGIOTENSIN[1-7]; COLLAGEN TYPE 1; DIPHENYLIODONIUM SALT; MEMBRANE PROTEIN; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ROCK PROTEIN; UNCLASSIFIED DRUG; ANGIOTENSIN I; ANGIOTENSIN I (1-7); COLLAGEN TYPE I, ALPHA 1 CHAIN; DIPEPTIDYL CARBOXYPEPTIDASE; G PROTEIN COUPLED RECEPTOR; NOX4 PROTEIN, RAT; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTO-ONCOGENE PROTEINS C-MAS-1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLEOMYCIN-INDUCED PULMONARY FIBROSIS; CELL MIGRATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; IN VITRO STUDY; LUNG FIBROBLAST; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL CULTURE; CELL MOTION; ENZYMOLOGY; FIBROBLAST; LUNG FIBROSIS; METABOLISM; PATHOLOGY; PHYSIOLOGY; WISTAR RAT;

LENTIVIRUS;

ANGIOTENSIN I; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN TYPE I; FIBROBLASTS; MALE; NADPH OXIDASE; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; PROTO-ONCOGENE PROTEINS; PULMONARY FIBROSIS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RECEPTORS, G-PROTEIN-COUPLED; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN;

EID: 84921047426     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5818     Document Type: Article

References (59)

1. Amara N, Goven D, Prost F, Muloway R, Crestani B, and Boczkowski J. NOX4/NADPH oxidase expression is increased in pulmonary fibroblasts from patients with idiopathic pulmonary fibrosis and mediates TGFbeta1-induced fibroblast differentiation into myofibroblast. Thorax 65: 733-738, 2010.
2. Ambasta RK, Kumar P, Griendling KK, et al. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J Biol Chem 279: 45935-45941, 2004.
3. Artaud-Macari E, Goven D, Brayer S, Hamimi A, Besnard V, Marchal-Somme J, Ali ZE, Crestani B, Kerdine-Romer S, Boutten A, and Bonay M. Nuclear factor erythroid 2-related factor 2 nuclear translocation induces myofibroblastic dedifferentiation in idiopathic pulmonary fibrosis. Antioxid Redox Signal 18: 66-79, 2013.
4. Ashcroft T, Simpson JM, and Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol 41: 467-470, 1988.
5. Bataller R, Schwabe RF, Choi Y H, Yang L, Paik YH, Lindquist J, Qian T, Schoonhoven R, Hagedorn CH, Lemasters JJ, and Brenner DA. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J Clin Invest 112: 1383-1394, 2003.
6. Bedard K and Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313, 2007.
7. Bocchino M, Agnese S, Fagone E, Svegliati S, Grieco D, Vancheri C, Gabrielli A, Sanduzzi A, and Avvedimento EV. Reactive oxygen species are required for maintenance and differentiation of primary lung fibroblasts in idiopathic pulmonary fibrosis. PLoS One 5: e14003, 2010.
8. Brown DI and Griendling KK. Nox proteins in signal transduction. Free Radic Biol Med 47: 1239-1253, 2009.
9. Cai GQ, Zheng A, Tang Q,White ES, Chou CF, Gladson CL, Olman MA, and Ding Q. Downregulation of FAK-related non-kinase mediates the migratory phenotype of human fibrotic lung fibroblast. Exp Cell Res 316: 1600-1609, 2010.
10. Carnesecchi S, Deffert C, Donati Y, Basset O, Hinz B, Preynat-Seauve O, Guichard C, Arbiser JL, Banfi B, Pache JC, Barazzone-Argiroffo C, and Krause KH. A key role for NOX4 in epithelial cell death during development of lung fibrosis. Antioxid Redox Signal 15: 607-619, 2011.
11. Chen J, Xiao X, Chen S, Zhang C, Chen J, Yi D, Shenoy V, Raizada MK, Zhao B, and Chen Y. Angiotensin-converting enzyme 2 priming enhances the function of endothelial progenitor cells and their therapeutic efficacy. Hypertension 61: 681-689, 2013.
12. Cook KL, Metheny-Barlow LJ, Tallant EA, and Gallagher PE. Angiotensin-(1-7) reduces fibrosis in orthotopic breast tumors. Cancer Res 70: 8319-8328, 2010.
13. Giani JF, Gironacci MM, Munoz MC, Turyn D, and Dominici FP. Angiotensin-(1-7) has a dual role on growthpromoting signalling pathways in rat heart in vivo by stimulating STAT3 and STAT5a/b phosphorylation and inhibiting angiotensin II-stimulated ERK1/2 and Rho kinase activity. Exp Physiol 93: 570-578, 2008.
14. Goldstein RH and Fine A. Fibrotic reactions in the lung: the activation of the lung fibroblast. Exp Lung Res 11: 245-261, 1986.
15. Hagiwara SI, Ishii Y, and Kitamura S. Aerosolized administration of N-acetylcysteine attenuates lung fibrosis induced by bleomycin in mice. Am J Respir Crit Care Med 162: 225-231, 2000.
16. Hecker L, Cheng J, and Thannickal VJ. Targeting NOX enzymes in pulmonary fibrosis. Cell Mol Life Sci 69: 2365-2371, 2012.
17. Hecker L, Vittal R, Jones T, Jagirdar R, Luckhardt TR, Horowitz JC, Pennathur S, Martinez FJ, and Thannickal VJ. NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat Med 15: 1077-1081, 2009.
18. Hsu HH, Hoffmann S, Endlich N, Velic A, Schwab A, Weide T, Schlatter E, and Pavenstadt H. Mechanisms of angiotensin II signaling on cytoskeleton of podocytes. J Mol Med (Berl) 86: 1379-1394, 2008.
19. Jiang T, Gao L, Shi J, Lu J, Wang Y, and Zhang Y. Angiotensin-(1-7) modulates renin-angiotensin system associated with reducing oxidative stress and attenuating neuronal apoptosis in the brain of hypertensive rats. Pharmacol Res 67: 84-93, 2013.
20. Kliment CR and Oury TD. Oxidative stress, extracellular matrix targets, and idiopathic pulmonary fibrosis. Free Radic Biol Med 49: 707-717, 2010.
21. Kondrikov D, Caldwell RB, Dong Z, and Su Y. Reactive oxygen species-dependent RhoA activation mediates collagen synthesis in hyperoxic lung fibrosis. Free Radic Biol Med 50: 1689-1698, 2011.
22. Konigshoff M, Wilhelm A, Jahn A, Sedding D, Amarie OV, Eul B, Seeger W, Fink L, Gunther A, Eickelberg O, and Rose F. The angiotensin II receptor 2 is expressed and mediates angiotensin II signaling in lung fibrosis. Am J Respir Cell Mol Biol 37: 640-650, 2007.
23. Kostenis E, Milligan G, Christopoulos A, Sanchez-Ferrer CF, Heringer-Walther S, Sexton PM, Gembardt F, Kellett E, Martini L, Vanderheyden P, Schultheiss HP, and Walther T. G-protein-coupled receptor Mas is a physiological antagonist of the angiotensin II type 1 receptor. Circulation 111: 1806-1813, 2005.
24. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189, 2004.
25. Lang YD, Hung CL, Wu TY, Wang LF, and Chen CM. The renin-angiotensin system mediates hyperoxia-induced collagen production in human lung fibroblast. Free Radic Biol Med 49: 88-95, 2010.
26. Lyle AN, Deshpande NN, Taniyama Y, Seidel-Rogol B, Pounkova L, Du P, Papaharalambus C, Lassegue B, and Griendling KK. Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ Res 105: 249-259, 2009.
27. Manoury B, Nenan S, Leclerc O, Guenon I, Boichot E, Planquois JM, Bertrand CP, and Lagente V. The absence of reactive oxygen species production protects mice against bleomycin-induced pulmonary fibrosis. Respir Res 6: 11, 2005.
28. Marshall RP, Gohlke P, Chambers RC, Howell DC, Bottoms SE, Unger T, McAnulty RJ, and Laurent GJ. Angiotensin II and the fibroproliferative response to acute lung injury. Am J Physiol Lung Cell Mol Physiol 286: L156-L164, 2004.
29. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, and Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18: 69-82, 2006.
30. Meng Y, Yu CH, Li W, Li T, Luo W, Huang S, Wu PS, Cai SX, and Li X. Angiotensin-converting enzyme 2/angiotensin-(1-7)/Mas axis protects against lung fibrosis by inhibiting the MAPK/NF-jB pathway. Am J Respir Cell Mol Biol 50: 723-736, 2014.
31. Montezano AC, Callera GE, Yogi A, He Y, Tostes RC, He G, Schiffrin EL, and 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 28: 1511-1518, 2008.
32. Moon JY, Tanimoto M, Gohda T, Hagiwara S, Yamazaki T, Ohara I, Murakoshi M, Aoki T, Ishikawa Y, Lee SH, Jeong KH, Lee TW, Ihm CG, Lim SJ, and Tomino Y. Attenuating effect of angiotensin-(1-7) on angiotensin IImediated NAD(P)H oxidase activation in type 2 diabetic nephropathy of KK-AyTa mice. Am J Physiol Renal Physiol 6: F1271-F1282, 2011.
33. Ni J, Dong Z, Han W, Kondrikov D, and Su Y. The role of RhoA and cytoskeleton in myofibroblast transformation in hyperoxic lung fibrosis. Free Radic Biol Med 61C: 26-39, 2013.
34. Ni L, Feng Y, Wan H, Ma Q, Fan L, Qian Y, Li Q, Xiang Y, and Gao B. Angiotensin-(1-7) inhibits the migration and invasion of A549 human lung adenocarcinoma cells through inactivation of the PI3K/Akt and MAPK signaling pathways. Oncol Rep 27: 783-790, 2012.
35. Nlandu KS, Dizin E, Sossauer G, Szanto I, Martin PY, Feraille E, Krause KH, and de Seigneux S. NADPHoxidase 4 protects against kidney fibrosis during chronic renal injury. J Am Soc Nephrol 23: 1967-1976, 2012.
36. Otsuka M, Takahashi H, Shiratori M, Chiba H, and Abe S. Reduction of bleomycin induced lung fibrosis by candesartan cilexetil, an angiotensin II type 1 receptor antagonist. Thorax 59: 31-38, 2004.
37. Park S, Ahn JY, Lim MJ, Kim MH, Yun YS, Jeong G, and Song JY. Sustained expression of NADPH oxidase 4 by p38 MAPK-Akt signaling potentiates radiation-induced differentiation of lung fibroblast. J Mol Med (Berl) 88: 807-816, 2010.
38. Rey-Parra GJ, Vadivel A, Coltan L, Hall A, Eaton F, Schuster M, Loibner H, Penninger JM, Kassiri Z, Oudit GY, and Thebaud B. Angiotensin converting enzyme 2 abrogates bleomycin-induced lung injury. J Mol Med (Berl) 90: 637-647, 2012.
39. Serrander L, Cartier L, Bedard K, Banfi B, Lardy B, Plastre O, Sienkiewicz A, Forro L, Schlegel W, and Krause KH. NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J 406: 105-114, 2007.
40. Serrano-Mollar A, Closa D, Prats N, Blesa S, Martinez-Losa M, Cortijo J, Estrela JM, Morcillo EJ, and Bulbena O. In vivo antioxidant treatment protects against bleomycininduced lung damage in rats. Br J Pharmacol 138: 1037-1048, 2003.
41. Shenoy V, Ferreira AJ, Qi Y, Fraga-Silva RA, Déz-Freire C, Dooies A, Jun JY, Sriramula S, Mariappan N, Pourang D, Venugopal CS, Francis J, Reudelhuber T, Santos RA, Patel JM, Raizada MK, and Katovich MJ. The angiotensinconverting enzyme 2/angiogenesis-(1-7)/Mas axis confers cardiopulmonary protectionagainst lung fibrosis and pulmonary hypertension. Am J Respir Crit Care Med 182: 1065-1072, 2010.
42. Shinohara M, Shang WH, Kubodera M, Harada S, Mitsushita J, Kato M, Miyazaki H, Sumimoto H, and Kamata T. Nox1 redox signaling mediates oncogenic Ras-induced disruption of stress fibers and focal adhesions by downregulating Rho. J Biol Chem 282: 17640-17648, 2007.
43. Suganuma H, Sato A, Tamura R, and Chida K. Enhaced migration of fibroblasts derived from lungs with fibrotic lesions. Thorax 50: 984-989, 1995.
44. Takahashi F, Takahashi K, Okazaki T, Maeda K, Ienaga H, Maeda M, Kon S, Uede T, and Fukuchi Y. Role of osteopontin in the pathogenesis of bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 24: 264-271, 2001.
45. Thomas J, Gross MD, Gary W, and Hunningchake MD. Idiopathic pulmonary fibrosis. N Engl J Med 345: 517-525, 2001.
46. Tufvesson E and Westergren-Thorsson G. Biglycan and decorin induce morphological and cytoskeletal changes involving signalling by the small GTPases RhoA and Rac1 resulting in lung fibroblast migration. J Cell Sci 116: 4857-4864, 2003.
47. Ushio-Fukai M, Hilenski L, Santanam N, Becker PL, Ma Y, Griendling KK, and Alexander RW. Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells: role of cholesterol-rich microdomains and focal adhesions in angiotensin II signaling. J Biol Chem 276: 48269-48275, 2001.
48. White ES, Thannickal VJ, Carskadon SL, Dickie EG, Livant DL, Markwart S, Toews GB, and Arenberg DA. Integrin a4b1 regulates migration across basement membranes by lung fibroblasts: a role for phosphatase and tensin homologue deleted on chromosome 10. Am J Respir Crit Care Med 168: 436-442, 2003.
49. Wingler K, Wunsch S, Kreutz R, Rothermund L, Paul M, and Schmidt HH. Upregulation of the vascular NAD(P)Hoxidase isoforms Nox1 and Nox4 by the renin-angiotensin system in vitro and in vivo. Free Radic Biol Med 31: 1456-1464, 2001.
50. Wu RF, Ma Z, Myers DP, and Terada LS. HIV-1 Tat activates dual Nox pathways leading to independent activation of ERK and JNK MAP kinases. J Biol Chem 282: 37412-37419, 2007.
51. Xia H, Suda S, Bindom S, Feng Y, Gurley SB, Seth D, Navar LG, and Lazartigues E. ACE2-mediated reduction of oxidative stress in the central nervous system is associated with improvement of autonomic function. PLoS One 6: e22682, 2011.
52. Yamagishi S, Nakamura K, Ueda S, Kato S, and Imaizumi T. Pigment epithelium-derived factor (PEDF) blocks angiotensin II signaling in endothelial cells via suppression of NADPH oxidase: a novel anti-oxidative mechanism of PEDF. Cell Tissue Res 320: 437-445, 2005.
53. Yang J, Tan Y, Zhao F, Ma Z, Wang Y, Zheng S, Epstein PN, Yu J, Yin X, Zheng Y, Li X, Miao L, and Cai L. Angiotensin II plays a critical role in diabetic pulmonary fibrosis most likely via activation of NADPH oxidase-mediated nitrosative damage. Am J Physiol Endocrinol Metab 301: E132-E144, 2011.
54. Zhang C, Zhao YX, Zhang YH, Zhu L, Deng BP, Zhou ZL, Li SY, Lu XT, Song LL, Lei XM, Tang WB, Wang N, Pan CM, Song HD, Liu CX, Dong B, Zhang Y, and Cao Y. Angiotensin-converting enzyme 2 attenuates atherosclerotic lesions by targeting vascular cells. Proc Natl Acad Sci USA 107: 15886-15891, 2010.
55. Zhang F, Hu Y, Xu Q, and Ye S. Different effects of angiotensin II and angiotensin-(1-7) on vascular smooth muscle cell proliferation and migration. PLoS One 5: e12323, 2010.
56. Zhang R, Wu Y, Zhao M, Liu C, Zhou L, Shen S, Liao S, Yang K, Li Q, and Wan H. Role of HIF-1alpha in the regulation ACE and ACE2 expression in hypoxic human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 297: L631-L640, 2009.
57. Zhao W, Chen SS, Chen Y, Ahokas RA, and Sun Y. Kidney fibrosis in hypertensive rats: role of oxidative stress. Am J Nephrol 28: 548-554, 2008.
58. Zhao W, Zhao T, Chen Y, Ahokas RA, and Sun Y. Oxidative stress mediates cardiac fibrosis by enhancing transforming growth factor-beta1 in hypertensive rats. Mol Cell Biochem 317: 43-50, 2008.
59. Zhong J, Basu R, Guo D, Chow FL, Byrns S, Schuster M, Loibner H, Wang XH, Penninger JM, Kassiri Z, and Oudit GY. Angiotensin-converting enzyme 2 suppresses pathological hypertrophy, myocardial fibrosis, and cardiac dysfunction. Circulation 122: 717-728, 2010.