Adenoviral gene transfer of endothelin-1 in the lung induces pulmonary fibrosis through the activation of focal adhesion kinase

American Journal of Respiratory Cell and Molecular Biology

Volumn 47, Issue 6, 2012, Pages 834-842

  Lagares, David ^a,c   Busnadiego, Oscar ^a   García Fernández, Rosa Ana ^b   Lamas, Santiago ^a   Rodríguez Pascual, Fernando ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Endothelin; Focal adhesion kinase; Lung fibrosis; Myofibroblast differentiation

Indexed keywords

ADENOVIRUS VECTOR; COLLAGEN; ENDOTHELIN 1; FOCAL ADHESION KINASE; PF 562271;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CONTROLLED STUDY; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; GENE TRANSFER; LUNG FIBROBLAST; LUNG FIBROSIS; LUNG INFILTRATE; LYMPHOCYTE COUNT; MOUSE; MYOFIBROBLAST; NONHUMAN;

ADENOVIRIDAE; ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; ENDOTHELIN-1; ENZYME ACTIVATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENETIC VECTORS; HUMANS; INDOLES; LUNG; MICE; MICE, INBRED C57BL; MYOFIBROBLASTS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PULMONARY FIBROSIS; RECOMBINANT PROTEINS; SCLERODERMA, SYSTEMIC; SULFONAMIDES; T-LYMPHOCYTES;

MURINAE; MUS;

EID: 84870520373     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2011-0446OC     Document Type: Article

References (49)

1. Katzenstein AL, Myers JL. Idiopathic pulmonary fibrosis: clinical relevance of pathologic classification. Am J Respir Crit Care Med 1998;157:1301-1315.
2. Martinez FJ, Safrin S, Weycker D, Starko KM, Bradford WZ, King TE Jr, Flaherty KR, Schwartz DA, Noble PW, Raghu G, et al. The clinical course of patients with idiopathic pulmonary fibrosis. Ann Intern Med 2005;142:963-967.
3. Varga J, Abraham D. Systemic sclerosis: a prototypic multisystem fibrotic disorder. J Clin Invest 2007;117:557-567.
4. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007;117:524-529.
5. Leask A, Abraham DJ. TGF-beta signaling and the fibrotic response. FASEB J 2004;18:816-827.
6. Mori T, Kawara S, Shinozaki M, Hayashi N, Kakinuma T, Igarashi A, Takigawa M, Nakanishi T, Takehara K. Role and interaction of connective tissue growth factor with transforming growth factor-beta in persistent fibrosis: a mouse fibrosis model. J Cell Physiol 1999;181:153-159.
7. Park SH, Saleh D, Giaid A, Michel RP. Increased endothelin-1 in bleomycin-induced pulmonary fibrosis and the effect of an endothelin receptor antagonist. Am J Respir Crit Care Med 1997;156:600-608.
8. Abraham DJ, Vancheeswaran R, Dashwood MR, Rajkumar VS, Pantelides P, Xu SW, du Bois RM, Black CM. Increased levels of endothelin-1 and differential endothelin Type A and B receptor expression in scleroderma-associated fibrotic lung disease. Am J Pathol 1997;151:831-841.
9. Vancheeswaran R, Azam A, Black C, Dashwood MR. Localization of endothelin-1 and its binding sites in scleroderma skin. J Rheumatol 1994;21:1268-1276.
10. Uguccioni M, Pulsatelli L, Grigolo B, Facchini A, Fasano L, Cinti C, Fabbri M, Gasbarrini G, Meliconi R. Endothelin-1 in idiopathic pulmonary fibrosis. J Clin Pathol 1995;48:330-334.
11. Odoux C, Crestani B, Lebrun GL, Rolland C, Aubin P, Seta N, Kahn M-F, Fiet J, Aubier M. Endothelin-1 secretion by alveolar macrophages in systemic sclerosis. Am J Respir Crit Care Med 1997;156:1429-1435.
12. Shi-Wen X, Chen Y, Denton CP, Eastwood M, Renzoni EA, Bou-Gharios G, Pearson JD, Dashwood M, du Bois RM, Black CM, et al. Endothelin-1 promotes myofibroblast induction through the eta receptor via a RAC/phosphoinositide 3-kinase/AKT-dependent pathway and is essential for the enhanced contractile phenotype of fibrotic fibroblasts. Mol Biol Cell 2004;15:2707-2719.
13. King TE Jr, Brown KK, Raghu G, du Bois RM, Lynch DA, Martinez F, Valeyre D, Leconte I, Morganti A, Roux S, et al. BUILD-3: a randomized, controlled trial of bosentan in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2011;184:92-99.
14. Noble PW, Richeldi L, Kaminski N. End of an era: lessons from negative clinical trials in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2011;184:4-5.
15. Warshamana GS, Pociask DA, Fisher KJ, Liu JY, Sime PJ, Brody AR. Titration of non-replicating adenovirus as a vector for transducing active TGF-beta1 gene expression causing inflammation and fibrogenesis in the lungs of C57BL/6 mice. Int J Exp Pathol 2002;83:183-201.
16. Sime PJ, Xing Z, Graham FL, Csaky KG, Gauldie J. Adenovector-mediated gene transfer of active transforming growth factor-beta1 induces prolonged severe fibrosis in rat lung. J Clin Invest 1997;100:768-776.
17. Lagares D, Busnadiego O, Garcia-Fernandez RA, Kapoor M, Liu S, Carter DE, Abraham DJ, Shi-Wen X, Carreira P, Fontaine BA, et al. Inhibition of focal adhesion kinase prevents experimental lung fibrosis and myofibroblast formation. Arthritis Rheum 2012;64:1653-1664.
18. Hubner RH, Gitter W, El Mokhtari NE, Mathiak M, Both M, Bolte H, Freitag-Wolf S, Bewig B. Standardized quantification of pulmonary fibrosis in histological samples. BioTechniques 2008;44:507-511, 514-507.
19. Lagares D, Garcia-Fernandez RA, Jimenez CL, Magan-Marchal N, Busnadiego O, Lamas S, Rodriguez-Pascual F. Endothelin 1 contributes to the effect of transforming growth factor beta1 on wound repair and skin fibrosis. Arthritis Rheum 2010;62:878-889.
20. Liu S, Xu SW, Blumbach K, Eastwood M, Denton CP, Eckes B, Krieg T, Abraham DJ, Leask A. Expression of integrin beta1 by fibroblasts is required for tissue repair in vivo. J Cell Sci 2010;123:3674-3682.
21. Liu S, Xu SW, Kennedy L, Pala D, Chen Y, Eastwood M, Carter DE, Black CM, Abraham DJ, Leask A. FAK is required for TGFbetainduced JNK phosphorylation in fibroblasts: implications for acquisition of a matrix-remodeling phenotype. Mol Biol Cell 2007;18:2169-2178.
22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(2delta delta C(t)) method. Methods 2001;25:402-408.
23. Shi-Wen X, Renzoni EA, Kennedy L, Howat S, Chen Y, Pearson JD, Bou-Gharios G, Dashwood MR, du Bois RM, Black CM, et al. Endogenous endothelin-1 signaling contributes to Type I collagen and CCN2 overexpression in fibrotic fibroblasts. Matrix Biol 2007;26:625-632.
24. Shi-Wen X, Rodriguez-Pascual F, Lamas S, Holmes A, Howat S, Pearson JD, Dashwood MR, du Bois RM, Denton CP, Black CM, et al. Constitutive ALK5-independent c-Jun N-terminal kinase activation contributes to endothelin-1 overexpression in pulmonary fibrosis: evidence of an autocrine endothelin loop operating through the endothelin A and B receptors. Mol Cell Biol 2006;26:5518-5527.
25. Mutsaers SE, Marshall RP, Goldsack NR, Laurent GJ, McAnulty RJ. Effect of endothelin receptor antagonists (BQ-485, RO 47-0203) on collagen deposition during the development of bleomycin-induced pulmonary fibrosis in rats. Pulm Pharmacol Ther 1998;11:221-225.
26. Schroll S, Arzt M, Sebah D, Nuchterlein M, Blumberg F, Pfeifer M. Improvement of bleomycin-induced pulmonary hypertension and pulmonary fibrosis by the endothelin receptor antagonist bosentan. Respir Physiol Neurobiol 2010;170:32-36.
27. Daher Z, Noel J, Claing A. Endothelin-1 promotes migration of endothelial cells through the activation of ARF6 and the regulation of FAK activity. Cell Signal 2008;20:2256-2265.
28. Tan TW, Lai CH, Huang CY, Yang WH, Chen HT, Hsu HC, Fong YC, Tang CH. CTGF enhances migration and MMP-13 up-regulation via alphaVbeta3 integrin, FAK, ERK, and NF-kappaB-dependent pathway in human chondrosarcoma cells. J Cell Biochem 2009;107:345-356.
29. Teixeira A, Chaverot N, Schroder C, Strosberg AD, Couraud PO, Cazaubon S. Requirement of caveolae microdomains in extracellular signal-regulated kinase and focal adhesion kinase activation induced by endothelin-1 in primary astrocytes. J Neurochem 1999;72:120-128.
30. Thannickal VJ, Lee DY, White ES, Cui Z, Larios JM, Chacon R, Horowitz JC, Day RM, Thomas PE. Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem 2003;278:12384-12389.
31. Bagi CM, Christensen J, Cohen DP, Roberts WG, Wilkie D, Swanson T, Tuthill T, Andresen CJ. Sunitinib and PF-562,271 (FAK/Pyk2 inhibitor) effectively block growth and recovery of human hepatocellular carcinoma in a rat xenograft model. Cancer Biol Ther 2009;8:856-865.
32. Bagi CM, Roberts GW, Andresen CJ. Dual focal adhesion kinase/Pyk2 inhibitor has positive effects on bone tumors: implications for bone metastases. Cancer 2008;112:2313-2321.
33. Roberts WG, Ung E, Whalen P, Cooper B, Hulford C, Autry C, Richter D, Emerson E, Lin J, Kath J, et al. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res 2008;68:1935-1944.
34. Serrels A, McLeod K, Canel M, Kinnaird A, Graham K, Frame MC, Brunton VG. The role of focal adhesion kinase catalytic activity on the proliferation and migration of squamous cell carcinoma cells. Int J Cancer 2012;131:287-297.
35. Slack-Davis JK, Hershey ED, Theodorescu D, Frierson HF, Parsons JT. Differential requirement for focal adhesion kinase signaling in cancer progression in the transgenic adenocarcinoma of mouse prostate model. Mol Cancer Ther 2009;8:2470-2477.
36. Stokes JB, Adair SJ, Slack-Davis JK, Walters DM, Tilghman RW, Hershey ED, Lowrey B, Thomas KS, Bouton AH, Hwang RF, et al. Inhibition of focal adhesion kinase by PF-562,271 inhibits the growth and metastasis of pancreatic cancer concomitant with altering the tumor microenvironment. Mol Cancer Ther 2011;10:2135-2145.
37. Sun H, Pisle S, Gardner ER, Figg WD. Bioluminescent imaging study: FAK inhibitor, PF-562,271, preclinical study in PC3M-LUC-C6 local implant and metastasis xenograft models. Cancer Biol Ther 2010;10:38-43.
38. Wendt MK, Smith JA, Schiemann WP. Transforming growth factor-beta-induced epithelial-mesenchymal transition facilitates epidermal growth factor-dependent breast cancer progression. Oncogene 2010;29:6485-6498.
39. Razzaque MS, Taguchi T. Pulmonary fibrosis: cellular and molecular events. Pathol Int 2003;53:133-145.
40. Bonniaud P, Margetts PJ, Kolb M, Haberberger T, Kelly M, Robertson J, Gauldie J. Adenoviral gene transfer of connective tissue growth factor in the lung induces transient fibrosis. Am J Respir Crit Care Med 2003;168:770-778.
41. Holmes A, Abraham DJ, Sa S, Shi-Wen X, Black CM, Leask A. CTGF and SMADs, maintenance of scleroderma phenotype is independent of SMAD signaling. J Biol Chem 2001;276:10594-10601.
42. Rodriguez-Pascual F, Redondo-Horcajo M, Lamas S. Functional cooperation between SMAD proteins and activator protein-1 regulates transforming growth factor-beta-mediated induction of endothelin-1 expression. Circ Res 2003;92:1288-1295.
43. Moeller A, Ask K, Warburton D, Gauldie J, Kolb M. The bleomycin animal model: a useful tool to investigate treatment options for idiopathic pulmonary fibrosis? Int J Biochem Cell Biol 2008;40:362-382.
44. Kolb M, Margetts PJ, Anthony DC, Pitossi F, Gauldie J. Transient expression of IL-1beta induces acute lung injury and chronic repair leading to pulmonary fibrosis. J Clin Invest 2001;107:1529-1536.
45. Sime PJ, Marr RA, Gauldie D, Xing Z, Hewlett BR, Graham FL, Gauldie J. Transfer of tumor necrosis factor-alpha to rat lung induces severe pulmonary inflammation and patchy interstitial fibrogenesis with induction of transforming growth factor-beta1 and myofibroblasts. Am J Pathol 1998;153:825-832.
46. Mutsaers SE, Foster ML, Chambers RC, Laurent GJ, McAnulty RJ. Increased endothelin-1 and its localization during the development of bleomycin-induced pulmonary fibrosis in rats. Am J Respir Cell Mol Biol 1998;18:611-619.
47. Horowitz JC, Ajayi IO, Kulasekaran P, Rogers DS, White JB, Townsend SK, White ES, Nho RS, Higgins PD, Huang SK, et al. Survivin expression induced by endothelin-1 promotes myofibroblast resistance to apoptosis. Int J Biochem Cell Biol 2012;44:158-169.
48. Kennedy L, Shi-Wen X, Carter DE, Abraham DJ, Leask A. Fibroblast adhesion results in the induction of a matrix remodeling gene expression program. Matrix Biol 2008;27:274-281.
49. Guo F, Carter DE, Leask A. Mechanical tension increases CCN2/CTGF expression and proliferation in gingival fibroblasts via a TGFbeta-dependent mechanism. PLoS ONE 2011;6:e19756.