Endothelin-1 induces alveolar epithelial-mesenchymal transition through endothelin type A receptor-mediated production of TGF-β1

American Journal of Respiratory Cell and Molecular Biology

Volumn 37, Issue 1, 2007, Pages 38-47

  Jain, Raksha ^b   Shaul, Philip W ^b   Borok, Zea ^b   Willis, Brigham C ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b NONE

Author keywords

Alveolar epithelial cells; Lung injury; Polar secretion; Pulmonary fibrosis

Indexed keywords

ENDOTHELIN 1; ENDOTHELIN A RECEPTOR; ENDOTHELIN B RECEPTOR; NEUTRALIZING ANTIBODY; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FIBROSING ALVEOLITIS; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROSIS; MESENCHYME; NONHUMAN; PATHOGENESIS; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RAT;

ANIMALS; APOPTOSIS; ENDOTHELIN-1; EPITHELIUM; GENE EXPRESSION REGULATION; LUNG; MALE; MESODERM; MODELS, BIOLOGICAL; PHENOTYPE; PULMONARY FIBROSIS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ENDOTHELIN A; TRANSFORMING GROWTH FACTOR BETA1;

EID: 34347228684     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2006-0353OC     Document Type: Article

References (60)

1. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 1988;332:411-415.
2. Fagan KA, McMurtry IF, Rodman DM. Role of endothelin-1 in lung disease. Respir Res 2001;2:90-101.
3. Kadono T, Kikuchi K, Sato S, Soma Y, Tamaki K, Takehara K. Elevated plasma endothelin levels in systemic sclerosis. Arch Dermatol Res 1995;287:439-442.
4. Cambrey AD, Harrison NK, Dawes KE, Southcott AM, Black CM, du Bois RM, Laurent GJ, McAnulty RJ. Increased levels of endothelin-1 in bronchoalveolar lavage fluid from patients with systemic sclerosis contribute to fibroblast mitogenic activity in vitro. Am J Respir Cell Mol Biol 1994;11:439-445.
5. 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.
6. Saleh D, Furukawa K, Tsao MS, Maghazachi A, Corrin B, Yanagisawa M, Barnes PJ, Giaid A. Elevated expression of endothelin-1 and endothelin- converting enzyme-1 in idiopathic pulmonary fibrosis: possible involvement of proinflammatory cytokines. Am J Respir Cell Mol Biol 1997;16:187-193.
7. 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.
8. Hocher B, Schwarz A, Fagan KA, Thone-Reineke C, El-Hag K, Kusserow H, Elitok S, Bauer C, Neumayer HH, Rodman DM, et al. Pulmonary fibrosis and chronic lung inflammation in ET-1 transgenic mice. Am J Respir Cell Mol Biol 2000;23:19-26.
9. 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.
10. Phan SH. The myofibroblast in pulmonary fibrosis. Chest 2002;122:286S-289S.
11. Abdelaziz MM, Samman YS, Wali SO, Hamad MM. Treatment of idiopathic pulmonary fibrosis: is there anything new? Respirology 2005;10:284-289.
12. Willis BC, duBois RM, Borok Z. Epithelial origin of myofibroblasts during fibrosis in the lung. Proc Am Thorac Soc 2006;3:377-382.
13. Hashimoto N, Jin H, Liu T, Chensue SW, Phan SH. Bone marrow-derived progenitor cells in pulmonary fibrosis. J Clin Invest 2004;113:243-252.
14. Moore BB, Murray L, Das A, Wilke CA, Herrygers AB, Toews GB. The role of CCL12 in the recruitment of fibrocytes and lung fibrosis. Am J Respir Cell Mol Biol 2006;35:175-181.
15. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, du Bois RM, Borok Z. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am J Pathol 2005;166:1321-1332.
16. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003;112:1776-1784.
17. 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.
18. Jain R, Shaul PW, Borok Z, Willis BC. Role of endothelin-1 in epithelial-mesenchymal transition in alveolar epithelium. Proc Am Thorac Soc 2006;3:A560.
19. Borok Z, Danto S, Zabski S, Crandall ED. Defined medium for primary culture de novo of rat alveolar epithelial cells. In Vitro Cell Dev Biol Anim 1994;30A:99-104.
20. Kao WW, Prockop DJ. Proline analogue removes fibroblasts from cultured mixed cell populations. Nature 1977;266:63-64.
21. Tsang ML, Zhou L, Zheng BL, Wenker J, Fransen G, Humphrey J, Smith JM, O'Connor-McCourt M, Lucas R, Weatherbee JA. Characterization of recombinant soluble human transforming growth factor-beta receptor type II (rhTGF-beta sRII). Cytokine 1995;7:389-397.
22. Shichiri M, Kato H, Marumo F, Hirata Y. Endothelin-1 as an autocrine/paracrine apoptosis survival factor for endothelial cells. Hypertension 1997;30:1198-1203.
23. Hayasaki-Kajiwara Y, Naya N, Shimamura T, Iwasaki T, Nakajima M. Endothelin generating pathway through endothelinl-31 in human cultured bronchial smooth muscle cells. Br J Pharmacol 1999;127:1415-1421.
24. Gandhi CR, Kuddus RH, Uemura T, Rao AS. Endothelin stimulates transforming growth factor-beta1 and collagen synthesis in stellate cells from control but not cirrhotic rat liver. Eur J Pharmacol 2000;406:311-318.
25. 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.
26. Anguelova E, Beuvon F, Leonard N, Chaverot N, Varlet P, Couraud PO, Daumas-Duport C, Cazaubon S. Functional endothelin ET B receptors are selectively expressed in human oligodendrogliomas. Brain Res Mol Brain Res 2005;137:77-88.
27. Babiker A, Andersson O, Lund E, Xiu RJ, Deeb S, Reshef A, Leitersdorf E, Diczfalusy U, Bjorkhem I. Elimination of cholesterol in macrophages and endothelial cells by the sterol 27-hydroxylase mechanism. Comparison with high density lipoprotein-mediated reverse cholesterol transport. J Biol Chem 1997;272:26253-26261.
28. Mineo C, Gormley AK, Yuhanna IS, Osborne-Lawrence S, Gibson LL, Hahner L, Shohet RV, Black S, Salmon JE, Samols D, et al. Fcgamma-RIIB mediates C-reactive protein inhibition of endothelial NO synthase. Circ Res 2005;97:1124-1131.
29. Horstmeyer A, Licht C, Scherr G, Eckes B, Krieg T. Signalling and regulation of collagen I synthesis by ET-1 and TGF-beta1. FEBS J 2005;272:6297-6309.
30. Willis BC, Kim KJ, Li X, Liebler J, Crandall ED, Borok Z. Modulation of ion conductance and active transport by TGF-beta 1 in alveolar epithelial cell monolayers. Am J Physiol Lung Cell Mol Physiol 2003;285:L1192-L1200.
31. Liu L, Sanz S, Heggestad AD, Antharam V, Notterpek L, Fletcher BS. Endothelial targeting of the Sleeping Beauty transposon within lung. Mol Ther 2004;10:97-105.
32. Markewitz BA, Kohan DE, Michael JR. Endothelin-1 synthesis, receptors, and signal transduction in alveolar epithelium: evidence for an autocrine role. Am J Physiol 1995;268:L192-L200.
33. Wagner OF, Christ G, Wojta J, Vierhapper H, Parzer S, Nowotny PJ, Schneider B, Waldhausl W, Binder BR. Polar secretion of endothelin-1 by cultured endothelial cells. J Biol Chem 1992;267:16066-16068.
34. Demuth K, Atger V, Borderie D, Benoit MO, Sauvaget D, Lotersztajn S, Moatti N. Homocysteine decreases endothelin-1 production by cultured human endothelial cells. Eur J Biochem 1999;263:367-376.
35. Bilsel AS, Moini H, Tetik E, Aksungar F, Kaynak B, Ozer A. 17Beta-estradiol modulates endothelin-1 expression and release in human endothelial cells. Cardiovasc Res 2000;46:579-584.
36. Jacques D, Sader S, Perreault C, Abdel-Samad D, Jules F, Provost C. NPY, ET-1, and Ang II nuclear receptors in human endocardial endothelial cells. Can J Physiol Pharmacol 2006;84:299-307.
37. Ahmed SI, Thompson J, Coulson JM, Woll PJ. Studies on the expression of endothelin, its receptor subtypes, and converting enzymes in lung cancer and in human bronchial epithelium. Am J Respir Cell Mol Biol 2000;22:422-431.
38. Aubert JD, Carnal B, Ricou J, Fioroni P, Juillerat-Jeanneret L, Pinet F. Characterization of the enzyme involved in the processing of big endothelin-1 in human lung epithelial cells. Pulm Pharmacol Ther 1998;11:209-213.
39. Deprez-Roy I, Coge F, Bertry L, Galizzi JP, Feletou M, Vanhoutte PM, Canet E. Endothelin-1 pathway in human alveolar epithelial cell line A549 and human umbilical vein endothelial cells. Acta Pharmacol Sin 2000;21:499-506.
40. Wendel M, Petzold A, Koslowski R, Kasper M, Augstein A, Knels L, Bleyl JU, Koch T. Localization of endothelin receptors in bleomycin-induced pulmonary fibrosis in the rat. Histochem Cell Biol 2004;122:507-517.
41. 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.
42. Kernochan LE, Tran BN, Tangkijvanich P, Melton AC, Tam SP, Yee HF Jr. Endothelin-1 stimulates human colonic myofibroblast contraction and migration. Gut 2002;50:65-70.
43. Savagner P. Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 2001;23:912-923.
44. Rosano L, Spinella F, Di Castro V, Nicotra MR, Dedhar S, de Herreros AG, Natali PG, Bagnato A. Endothelin-1 promotes epithelial-to-mesenchymal transition in human ovarian cancer cells. Cancer Res 2005;65:11649-11657.
45. Rodriguez-Pascual F, Reimunde FM, Redondo-Horcajo M, Lamas S. Transforming growth factor-beta induces endothelin-1 expression through activation of the Smad signaling pathway. J Cardiovasc Pharmacol 2004;44:S39-S42.
46. Markewitz BA, Farrukh IS, Chen Y, Li Y, Michael JR. Regulation of endothelin-1 synthesis in human pulmonary arterial smooth muscle cells: effects of transforming growth factor-beta and hypoxia. Cardiovasc Res 2001;49:200-206.
47. Johnson JA, Waller J. Transforming growth factor beta-1 attenuates endothelin-1-induced functions in neonatal cardiac myocytes. Life Sci 2002;71:99-113.
48. Dube J, Chakir J, Dube C, Grimard Y, Laviolette M, Boulet LP. Synergistic action of endothelin (ET)-1 on the activation of bronchial fibroblast isolated from normal and asthmatic subjects. Int J Exp Pathol 2000;81:429-437.
49. Khalil N, O'Connor RN, Unruh HW, Warren PW, Flanders KC, Kemp A, Bereznay OH, Greenberg AH. Increased production and immunohistochemical localization of transforming growth factor-beta in idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol 1991;5:155-162.
50. Xu YD, Hua J, Mui A, O'Connor R, Grotendorst G, Khalil N. Release of biologically active TGF-beta1 by alveolar epithelial cells results in pulmonary fibrosis. Am J Physiol 2003;285:L527-L539.
51. Cutroneo KR, Phan SH. TGF-beta1-induced Smad 3 binding to the Smad 7 gene: knockout of Smad 7 gene transcription by sense phosphorothioate oligos, autoregulation, and effect on TGF-beta1 secretion: bleomycin acts through TGF-betal. J Cell Biochem 2003;89:474-483.
52. Adamson IY, Young L, Bowden DH. Relationship of alveolar epithelial injury and repair to the induction of pulmonary fibrosis. Am J Pathol 1988;130:377-383.
53. Kwong K, Literat A, Zhu NL, Huang H, Li C, Jones C, Minoo P. Expression of transforming growth factor beta in human epithelial alveolar cells: a pro-inflammatory mediator independent pathway. Life Sci 2004;74:2941-2957.
54. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D, Chapman HA. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA 2006;103:13180-13185.
55. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 2002;110:341-350.
56. Saika S, Kono-Saika S, Ohnishi Y, Sato M, Muragaki Y, Ooshima A, Flanders KC, Yoo J, Anzano M, Liu CY, et al. Smad3 signaling is required for epithelial-mesenchymal transition of lens epithelium after injury. Am J Pathol 2004;164:651-663.
57. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003;112:1776-1784.
58. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, Wang J, McCulloch CAG, Rosivall L, Mucsi I, Kapus A. Central role for Rho in TGF-β1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol 2003;284:F911-F924.
59. Chang S, Hypolite JA, Changolkar A, Wein AJ, Chacko S, DiSanto ME. Increased contractility of diabetic rabbit corpora smooth muscle in response to endothelin is mediated via Rho-kinase beta. Int J Impot Res 2003;15:53-62.
60. Chu L, Norota I, Endoh M. Differential inhibition by the Rho kinase inhibitor Y-27632 of the increases in contractility and Ca2+ transients induced by endothelin-1 in rabbit ventricular myocytes. Naunyn Schmiedebergs Arch Pharmacol 2005;371:185-194.