TGF-β1 induces tissue factor expression in human lung fibroblasts in a PI3K/JNK/Akt-dependent and AP-1-dependent manner

American Journal of Respiratory Cell and Molecular Biology

Volumn 47, Issue 5, 2012, Pages 614-627

  Wygrecka, Malgorzata ^a   Zakrzewicz, Dariusz ^b   Taborski, Brigitte ^b   Didiasova, Miroslava ^b   Kwapiszewska, Grazyna ^c   Preissner, Klaus T ^a   Markart, Philipp ^a  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

Author keywords

Idiopathic pulmonary fibrosis; Tissue factor; Transforming growth factor 1

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; JANUS KINASE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN C FOS; PROTEIN KINASE B; SOMATOMEDIN C; THREONINE; THROMBOPLASTIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR JUND; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CELL PROLIFERATION; CELL SURFACE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRANSCRIPTION; HALF LIFE TIME; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; INHIBITION KINETICS; LUNG FIBROBLAST; LUNG PARENCHYMA; MYOFIBROBLAST; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; WESTERN BLOTTING;

CELLS, CULTURED; FIBROBLASTS; GENE EXPRESSION REGULATION; HALF-LIFE; IDIOPATHIC PULMONARY FIBROSIS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUNG; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA STABILITY; SIGNAL TRANSDUCTION; THROMBOPLASTIN; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84867818057     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0097OC     Document Type: Article

References (49)

1. American Thoracic Society. Idiopathic pulmonary fibrosis: diagnosis and treatment: international consensus statement: American Thoracic Society (ATS), and the European Respiratory Society (ERS). Am J Respir Crit Care Med 2000;161:646-664.
2. Pardo A, Selman M. Idiopathic pulmonary fibrosis: new insights in its pathogenesis. Int J Biochem Cell Biol 2002;34:1534-1538.
3. Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 2011;183:788-824.
4. Imokawa S, Sato A, Hayakawa H, KotaniM, Urano T, Takada A. Tissue factor expression and fibrin deposition in the lungs of patients with idiopathic pulmonary fibrosis and systemic sclerosis. Am J Respir Crit Care Med 1997;156:631-636.
5. Fujii M, Hayakawa H, Urano T, Sato A, Chida K, Nakamura H, Takada A. Relevance of tissue factor and tissue factor pathway inhibitor for hypercoagulable state in the lungs of patients with idiopathic pulmonary fibrosis. Thromb Res 2000;99:111-117.
6. Mackman N. The role of tissue factor and factor VIIa in hemostasis. Anesth Analg 2009;108:1447-1452.
7. Wygrecka M, Kwapiszewska G, Jablonska E, von Gerlach S, Henneke I, Zakrzewicz D, Guenther A, Preissner KT, Markart P. Role of protease-activated receptor-2 in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2011;183:1703-1714.
8. Kirchhofer D, Tschopp TB, Hadvary P, Baumgartner HR. Endothelial cells stimulated with tumor necrosis factor-alpha express varying amounts of tissue factor resulting in inhomogenous fibrin deposition in a native blood flow system: effects of thrombin inhibitors. J Clin Invest 1994;93:2073-2083.
9. Schwager I, Jungi TW. Effect of human recombinant cytokines on the induction of macrophage procoagulant activity. Blood 1994;83:152-160.
10. Schecter AD, Giesen PL, Taby O, Rosenfield CL, Rossikhina M, Fyfe BS, Kohtz DS, Fallon JT, Nemerson Y, Taubman MB. Tissue factor expression in human arterial smooth muscle cells: TF is present in three cellular pools after growth factor stimulation. J Clin Invest 1997;100:2276-2285.
11. Gebhard C, Akhmedov A, Mocharla P, Angstenberger J, Sahbai S, Camici GG, Luscher TF, Tanner FC. PDGF-CC induces tissue factor expression: role of PDGF receptor alpha/beta. Basic Res Cardiol 2010;105:349-356.
12. Kaneko T, Fujii S, Matsumoto A, Goto D, Makita N, Hamada J, Moriuchi T, Kitabatake A. Induction of tissue factor expression in endothelial cells by basic fibroblast growth factor and its modulation by fenofibric acid. Thromb J 2003;1:6.
13. Felts SJ, Stang MT, Getz MJ. A c-Fos and E1A-interacting component of the tissue factor basal promoter complex mediates synergistic activation of transcription by transforming growth factor-beta1. Oncogene 1997;14:1679-1685.
14. Bastarache JA, Wang L, Geiser T, Wang Z, Albertine KH, Matthay MA, Ware LB. The alveolar epithelium can initiate the extrinsic coagulation cascade through expression of tissue factor. Thorax 2007;62:608-616.
15. Car BD, Slauson DO, Suyemoto MM, Dore M, Neilsen NR. Expression and kinetics of induced procoagulant activity in bovine pulmonary alveolar macrophages. Exp Lung Res 1991;17:939-957.
16. Bloem LJ, Chen L, Konigsberg WH, Bach R. Serum stimulation of quiescent human fibroblasts induces the synthesis of tissue factor mRNA followed by the appearance of tissue factor antigen and procoagulant activity. J Cell Physiol 1989;139:418-423.
17. Jablonska E, Markart P, Zakrzewicz D, Preissner KT, Wygrecka M. Transforming growth factor-beta1 induces expression of human coagulation factor XII via Smad3 and JNK signaling pathways in human lung fibroblasts. J Biol Chem 2010;285:11638-11651.
18. Wygrecka M, Wilhelm J, Jablonska E, Zakrzewicz D, Preissner KT, Seeger W, Guenther A, Markart P. Shedding of low-density lipoprotein receptor-related protein-1 in acute respiratory distress syndrome. Am J Respir Crit Care Med 2011;184:438-448.
19. Ueki K, Fruman DA, Yballe CM, Fasshauer M, Klein J, Asano T, Cantley LC, Kahn CR. Positive and negative roles of p85 alpha and p85 beta regulatory subunits of phosphoinositide 3-kinase in insulin signaling. J Biol Chem 2003;278:48453-48466.
20. Utsugi M, Dobashi K, Ono A, Ishizuka T, Matsuzaki S, Hisada T, Shimizu Y, Kawata T, Aoki H, Kamide Y, et al. PI3K p110beta positively regulates lipopolysaccharide-induced IL-12 production in human macrophages and dendritic cells and JNK1 plays a novel role. J Immunol 2009;182:5225-5231.
21. Cui MZ, Parry GC, Edgington TS, Mackman N. Regulation of tissue factor gene expression in epithelial cells: induction by serum and phorbol 12-myristate 13-acetate. Arterioscler Thromb 1994;14:807-814.
22. Eferl R, Wagner EF. AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 2003;3:859-868.
23. Liberati NT, Datto MB, Frederick JP, Shen X, Wong C, Rougier-Chapman EM, Wang XF. Smads bind directly to the Jun family of AP-1 transcription factors. Proc Natl Acad Sci USA 1999;96:4844-4849.
24. Moons AH, Levi M, Peters RJ. Tissue factor and coronary artery disease. Cardiovasc Res 2002;53:313-325.
25. Schouten M, Wiersinga WJ, Levi M, van der Poll T. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol 2008;83:536-545.
26. Wygrecka M, Jablonska E, Guenther A, Preissner KT, Markart P. Current view on alveolar coagulation and fibrinolysis in acute inflammatory and chronic interstitial lung diseases. Thromb Haemost 2008;99:494-501.
27. Ruf W, Yokota N, Schaffner F. Tissue factor in cancer progression and angiogenesis. Thromb Res 2010;2:S36-S38.
28. Ahern SM, Miyata T, Sadler JE. Regulation of human tissue factor expression by mRNA turnover. J Biol Chem 1993;268:2154-2159.
29. Egorina EM, Sovershaev MA, Osterud B. Regulation of tissue factor procoagulant activity by post-translational modifications. Thromb Res 2008;122:831-837.
30. Steffel J, Akhmedov A, Greutert H, Luscher TF, Tanner FC. Histamine induces tissue factor expression: implications for acute coronary syndromes. Circulation 2005;112:341-349.
31. Noble PW. Idiopathic pulmonary fibrosis: new insights into classification and pathogenesis usher in a new era therapeutic approaches. Am J Respir Cell Mol Biol 2003;29:S27-S31.
32. Zhu T, Goh EL, LeRoith D, Lobie PE. Growth hormone stimulates the formation of a multiprotein signaling complex involving p130 (Cas) and CrkII: resultant activation of c-Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK). J Biol Chem 1998;273:33864-33875.
33. Fritz G, Kaina B.Activation of c-Jun N-terminal kinase 1 by UV irradiation is inhibited by Wortmannin without affecting c-Jun expression. Mol Cell Biol 1999;19:1768-1774.
34. Skov S, Klausen P, Claesson MH. Ligation of major histocompatability complex (MHC) Class I molecules on human T cells induces cell death through PI-3 kinase-induced c-Jun NH2-terminal kinase activity: a novel apoptotic pathway distinct from Fas-induced apoptosis. J Cell Biol 1997;139:1523-1531.
35. Liao Y, Hung MC. Physiological regulation of Akt activity and stability. Am J Transl Res 2010;2:19-42.
36. Wei L, Liu Y, Kaneto H, Fanburg BL. JNK regulates serotonin-mediated proliferation and migration of pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2010;298:L863-L869.
37. Shao Z, Bhattacharya K, Hsich E, Park L, Walters B, Germann U, Wang YM, Kyriakis J, Mohanlal R, Kuida K, et al. c-Jun N-terminal kinases mediate reactivation of Akt and cardiomyocyte survival after hypoxic injury in vitro and in vivo. Circ Res 2006;98:111-118.
38. Bogoyevitch MA, Kobe B. Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol Mol Biol Rev 2006;70: 1061-1095.
39. Wang XM, Zhang Y, Kim HP, Zhou Z, Feghali-Bostwick CA, Liu F, Ifedigbo E, Xu X, Oury TD, Kaminski N, et al. Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J Exp Med 2006;203:2895-2906.
40. Alcorn JF, van der Velden J, Brown AL,McElhinney B, Irvin CG, Janssen-Heininger YM. c-Jun N-terminal kinase 1 is required for the development of pulmonary fibrosis. Am J Respir Cell Mol Biol 2009;40:422-432.
41. Khalil N, Xu YD, O'Connor R, Duronio V. Proliferation of pulmonary interstitial fibroblasts is mediated by transforming growth factor beta1 induced release of extracellular fibroblast growth factor 2 and phosphorylation of p38MAPK and JNK. J Biol Chem 2005;280:43000-43009.
42. Hashimoto S, Gon Y, Takeshita I, Matsumoto K, Maruoka S, Horie T. Transforming growth factor-beta1 induces phenotypic modulation of human lung fibroblasts to myofibroblast through a c-Jun NH2 terminal kinase-dependent pathway. Am J Respir Crit Care Med 2001; 163:152-157.
43. Russo RC, Garcia CC, Barcelos LS, Rachid MA, Guabiraba R, Roffe E, Souza AL, Sousa LP, Mirolo M, Doni A, et al. Phosphoinositide 3 kinase gamma plays a critical role in bleomycin-induced pulmonary inflammation and fibrosis in mice. J Leukoc Biol 2011;89:269-282.
44. Wei X, Han J, Chen ZZ, Qi BW, Wang GC, Ma YH, Zheng H, Luo YF, Wei YQ, Chen LJ. A phosphoinositide 3-kinase-gamma inhibitor, AS605240 prevents bleomycin-induced pulmonary fibrosis in rats. Biochem Biophys Res Commun 2010;397:311-317.
45. Le Cras TD, Korfhagen TR, Davidson C, Schmidt S, Fenchel M, Ikegami M, Whitsett JA, Hardie WD. Inhibition of PI3K by PX-866 prevents transforming growth factor-alpha-induced pulmonary fibrosis. Am J Pathol 2010;176:679-686.
46. Conte E, Fruciano M, Fagone E, Gili E, Caraci F, Iemmolo M, Crimi N, Vancheri C. Inhibition of PI3K prevents the proliferation and differentiation of human lung fibroblasts into myofibroblasts: the role of class I P110 isoforms. PLoS ONE 2011;6:e24663.
47. Kulkarni AA, Thatcher TH, Olsen KC, Maggirwar SB, Phipps RP, Sime PJ. PPAR-gamma ligands repress TGFbeta-induced myofibroblast differentiation by targeting the PI3K/Akt pathway: implications for therapy of fibrosis. PLoS ONE 2011;6:e15909.
48. Avouac J, Palumbo K, Tomcik M, Zerr P, Dees C, Horn A, Maurer B, Akhmetshina A, Beyer C, Sadowski A, et al. Inhibition of AP-1 signaling abrogates TGF-ss mediated activation of fibroblasts and prevents experimental fibrosis. Arthritis Rheum 2011;64:1642-1652.
49. Palumbo K, Zerr P, Tomcik M, Vollath S, Dees C, Akhmetshina A, Avouac J, Yaniv M, Distler O, Schett G, et al. The transcription factor JunD mediates transforming growth factor {beta}-induced fibroblast activation and fibrosis in systemic sclerosis. Ann Rheum Dis 2011;70:1320-1326.