Fra-1/AP-1 transcription factor negatively regulates pulmonary fibrosis in vivo

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Rajasekaran, Subbiah ^a,b   Vaz, Michelle ^b   Reddy, Sekhar P ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b The Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; COLLAGEN TYPE 1; COLLAGENASE 3; INTERSTITIAL COLLAGENASE; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FRA 1; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DOWN REGULATION; FIBROSING ALVEOLITIS; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PNEUMONIA; UPREGULATION;

ANIMALS; BLEOMYCIN; CYTOKINES; EPITHELIAL CELLS; GENE DELETION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INFLAMMATION MEDIATORS; LUNG; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; PNEUMONIA; PROTO-ONCOGENE PROTEINS C-FOS; PULMONARY FIBROSIS; TISSUE INHIBITOR OF METALLOPROTEINASES; TRANSCRIPTION FACTOR AP-1; TRANSFORMING GROWTH FACTOR BETA1;

MUS;

EID: 84864231083     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041611     Document Type: Article

References (62)

1. Ramos C, Montano M, Garcia-Alvarez J, Ruiz V, Uhal BD, et al. (2001) Fibroblasts from idiopathic pulmonary fibrosis and normal lungs differ in growth rate, apoptosis, and tissue inhibitor of metalloproteinases expression. Am J Respir Cell Mol Biol 24: 591-598.
2. Zhang K, Flanders KC, Phan SH, (1995) Cellular localization of transforming growth factor-beta expression in bleomycin-induced pulmonary fibrosis. Am J Pathol 147: 352-361.
3. Broekelmann TJ, Limper AH, Colby TV, McDonald JA, (1991) Transforming growth factor beta 1 is present at sites of extracellular matrix gene expression in human pulmonary fibrosis. Proc Natl Acad Sci U S A 88: 6642-6646.
4. Cutroneo KR, (2003) How is Type I procollagen synthesis regulated at the gene level during tissue fibrosis. J Cell Biochem 90: 1-5.
5. McKeown S, Richter AG, O'Kane C, McAuley DF, Thickett DR, (2009) MMP expression and abnormal lung permeability are important determinants of outcome in IPF. Eur Respir J 33: 77-84.
6. Selman M, Ruiz V, Cabrera S, Segura L, Ramirez R, et al. (2000) TIMP-1,-2,-3, and-4 in idiopathic pulmonary fibrosis. A prevailing nondegradative lung microenvironment? Am J Physiol Lung Cell Mol Physiol 279: L562-574.
7. Swiderski RE, Dencoff JE, Floerchinger CS, Shapiro SD, Hunninghake GW, (1998) Differential expression of extracellular matrix remodeling genes in a murine model of bleomycin-induced pulmonary fibrosis. Am J Pathol 152: 821-828.
8. Eferl R, Wagner EF, (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3: 859-868.
9. Angel P, Hattori K, Smeal T, Karin M, (1988) The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell 55: 875-885.
10. Chung KY, Agarwal A, Uitto J, Mauviel A, (1996) An AP-1 binding sequence is essential for regulation of the human alpha2(I) collagen (COL1A2) promoter activity by transforming growth factor-beta. J Biol Chem 271: 3272-3278.
11. Ortiz LA, Champion HC, Lasky JA, Gambelli F, Gozal E, et al. (2002) Enalapril protects mice from pulmonary hypertension by inhibiting TNF-mediated activation of NF-kappaB and AP-1. Am J Physiol Lung Cell Mol Physiol 282: L1209-1221.
12. Adiseshaiah P, Vaz M, Machireddy N, Kalvakolanu DV, Reddy SP, (2008) A Fra-1-dependent, matrix metalloproteinase driven EGFR activation promotes human lung epithelial cell motility and invasion. J Cell Physiol 216: 405-412.
13. Vincenti MP, (2001) The matrix metalloproteinase (MMP) and tissue inhibitor of metalloproteinase (TIMP) genes. Transcriptional and posttranscriptional regulation, signal transduction and cell-type-specific expression. Methods Mol Biol 151: 121-148.
14. Westermarck J, Kahari VM, (1999) Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J 13: 781-792.
15. Tower GB, Coon CI, Belguise K, Chalbos D, Brinckerhoff CE, (2003) Fra-1 targets the AP-1 site/2G single nucleotide polymorphism (ETS site) in the MMP-1 promoter. Eur J Biochem 270: 4216-4225.
16. Ho HH, Antoniv TT, Ji JD, Ivashkiv LB, (2008) Lipopolysaccharide-induced expression of matrix metalloproteinases in human monocytes is suppressed by IFN-gamma via superinduction of ATF-3 and suppression of AP-1. J Immunol 181: 5089-5097.
17. Eferl R, Hoebertz A, Schilling AF, Rath M, Karreth F, et al. (2004) The Fos-related antigen Fra-1 is an activator of bone matrix formation. EMBO J 23: 2789-2799.
18. Tallquist MD, Soriano P, (2000) Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic vs. extra-embryonic gene function. Genesis 26: 113-115.
19. Eitzman DT, McCoy RD, Zheng X, Fay WP, Shen T, et al. (1996) Bleomycin-induced pulmonary fibrosis in transgenic mice that either lack or overexpress the murine plasminogen activator inhibitor-1 gene. J Clin Invest 97: 232-237.
20. Sisson TH, Mendez M, Choi K, Subbotina N, Courey A, et al. (2010) Targeted injury of type II alveolar epithelial cells induces pulmonary fibrosis. Am J Respir Crit Care Med 181: 254-263.
21. Piao CQ, Liu L, Zhao YL, Balajee AS, Suzuki M, et al. (2005) Immortalization of human small airway epithelial cells by ectopic expression of telomerase. Carcinogenesis 26: 725-731.
22. Janick-Buckner D, Ranges GE, Hacker MP, (1989) Alteration of bronchoalveolar lavage cell populations following bleomycin treatment in mice. Toxicol Appl Pharmacol 100: 465-473.
23. Schrier DJ, Kunkel RG, Phan SH, (1983) The role of strain variation in murine bleomycin-induced pulmonary fibrosis. Am Rev Respir Dis 127: 63-66.
24. Izbicki G, Segel MJ, Christensen TG, Conner MW, Breuer R, (2002) Time course of bleomycin-induced lung fibrosis. Int J Exp Pathol 83: 111-119.
25. Phan SH, Armstrong G, Sulavik MC, Schrier D, Johnson KJ, et al. (1983) A comparative study of pulmonary fibrosis induced by bleomycin and an O2 metabolite producing enzyme system. Chest 83: 44S-45S.
26. Gharaee-Kermani M, Hatano K, Nozaki Y, Phan SH, (2005) Gender-based differences in bleomycin-induced pulmonary fibrosis. Am J Pathol 166: 1593-1606.
27. Lawson WE, Polosukhin VV, Stathopoulos GT, Zoia O, Han W, et al. (2005) Increased and prolonged pulmonary fibrosis in surfactant protein C-deficient mice following intratracheal bleomycin. Am J Pathol 167: 1267-1277.
28. Daniels CE, Wilkes MC, Edens M, Kottom TJ, Murphy SJ, et al. (2004) Imatinib mesylate inhibits the profibrogenic activity of TGF-beta and prevents bleomycin-mediated lung fibrosis. J Clin Invest 114: 1308-1316.
29. Smith RE, Strieter RM, Phan SH, Lukacs N, Kunkel SL, (1998) TNF and IL-6 mediate MIP-1alpha expression in bleomycin-induced lung injury. J Leukoc Biol 64: 528-536.
30. Keane MP, Belperio JA, Moore TA, Moore BB, Arenberg DA, et al. (1999) Neutralization of the CXC chemokine, macrophage inflammatory protein-2, attenuates bleomycin-induced pulmonary fibrosis. J Immunol 162: 5511-5518.
31. Liu JY, Brass DM, Hoyle GW, Brody AR, (1998) TNF-alpha receptor knockout mice are protected from the fibroproliferative effects of inhaled asbestos fibers. Am J Pathol 153: 1839-1847.
32. Smith RE, Strieter RM, Phan SH, Lukacs NW, Huffnagle GB, et al. (1994) Production and function of murine macrophage inflammatory protein-1 alpha in bleomycin-induced lung injury. J Immunol 153: 4704-4712.
33. Mitsuhashi H, Asano S, Nonaka T, Hamamura I, Masuda K, et al. (1996) Administration of truncated secretory leukoprotease inhibitor ameliorates bleomycin-induced pulmonary fibrosis in hamsters. Am J Respir Crit Care Med 153: 369-374.
34. Jones HA, Schofield JB, Krausz T, Boobis AR, Haslett C, (1998) Pulmonary fibrosis correlates with duration of tissue neutrophil activation. Am J Respir Crit Care Med 158: 620-628.
35. Cailes JB, O'Connor C, Pantelidis P, Southcott AM, Fitzgerald MX, et al. (1996) Neutrophil activation in fibrosing alveolitis: a comparison of lone cryptogenic fibrosing alveolitis and systemic sclerosis. Eur Respir J 9: 992-999.
36. Cobelens PM, Tiebosch IA, Dijkhuizen RM, van der Meide PH, Zwartbol R, et al. (2010) Interferon-beta attenuates lung inflammation following experimental subarachnoid hemorrhage. Crit Care 14: R157.
37. Pardo A, Ruiz V, Arreola JL, Ramirez R, Cisneros-Lira J, et al. (2003) Bleomycin-induced pulmonary fibrosis is attenuated in gamma-glutamyl transpeptidase-deficient mice. Am J Respir Crit Care Med 167: 925-932.
38. Tan RJ, Fattman CL, Niehouse LM, Tobolewski JM, Hanford LE, et al. (2006) Matrix metalloproteinases promote inflammation and fibrosis in asbestos-induced lung injury in mice. Am J Respir Cell Mol Biol 35: 289-297.
39. Nagase H, Woessner JF Jr, (1999) Matrix metalloproteinases. J Biol Chem 274: 21491-21494.
40. Yan S, Chen GM, Yu CH, Zhu GF, Li YM, et al. (2005) Expression pattern of matrix metalloproteinases-13 in a rat model of alcoholic liver fibrosis. Hepatobiliary Pancreat Dis Int 4: 569-572.
41. Asano Y, Ihn H, Kubo M, Jinnin M, Mimura Y, et al. (2006) Clinical significance of serum matrix metalloproteinase-13 levels in patients with localized scleroderma. Clin Exp Rheumatol 24: 394-399.
42. Pardo A, Selman M, (2002) Idiopathic pulmonary fibrosis: new insights in its pathogenesis. Int J Biochem Cell Biol 34: 1534-1538.
43. Yoshiji H, Kuriyama S, Miyamoto Y, Thorgeirsson UP, Gomez DE, et al. (2000) Tissue inhibitor of metalloproteinases-1 promotes liver fibrosis development in a transgenic mouse model. Hepatology 32: 1248-1254.
44. Kim H, Pennie WD, Sun Y, Colburn NH, (1997) Differential functional significance of AP-1 binding sites in the promoter of the gene encoding mouse tissue inhibitor of metalloproteinases-3. Biochem J 324 (Pt 2): 547-553.
45. Bonniaud P, Margetts PJ, Kolb M, Schroeder JA, Kapoun AM, et al. (2005) Progressive transforming growth factor beta1-induced lung fibrosis is blocked by an orally active ALK5 kinase inhibitor. Am J Respir Crit Care Med 171: 889-898.
46. Kalluri R, Neilson EG, (2003) Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784.
47. Willis BC, Borok Z, (2007) TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 293: L525-534.
48. Wu Z, Yang L, Cai L, Zhang M, Cheng X, et al. (2007) Detection of epithelial to mesenchymal transition in airways of a bleomycin induced pulmonary fibrosis model derived from an alpha-smooth muscle actin-Cre transgenic mouse. Respir Res 8: 1.
49. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, et al. (2005) Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am J Pathol 166: 1321-1332.
50. Andreolas C, Kalogeropoulou M, Voulgari A, Pintzas A, (2008) Fra-1 regulates vimentin during Ha-RAS-induced epithelial mesenchymal transition in human colon carcinoma cells. Int J Cancer 122: 1745-1756.
51. Stinson S, Lackner MR, Adai AT, Yu N, Kim HJ, et al. (2011) TRPS1 targeting by miR-221/222 promotes the epithelial-to-mesenchymal transition in breast cancer. Sci Signal 4: ra41.
52. Mejlvang J, Kriajevska M, Berditchevski F, Bronstein I, Lukanidin EM, et al. (2007) Characterization of E-cadherin-dependent and-independent events in a new model of c-Fos-mediated epithelial-mesenchymal transition. Exp Cell Res 313: 380-393.
53. Schorpp M, Jager R, Schellander K, Schenkel J, Wagner EF, et al. (1996) The human ubiquitin C promoter directs high ubiquitous expression of transgenes in mice. Nucleic Acids Res 24: 1787-1788.
54. Jochum W, David JP, Elliott C, Wutz A, Plenk H Jr, et al. (2000) Increased bone formation and osteosclerosis in mice overexpressing the transcription factor Fra-1. Nat Med 6: 980-984.
55. Meixner A, Karreth F, Kenner L, Wagner EF, (2004) JunD regulates lymphocyte proliferation and T helper cell cytokine expression. EMBO J 23: 1325-1335.
56. Smart DE, Green K, Oakley F, Weitzman JB, Yaniv M, et al. (2006) JunD is a profibrogenic transcription factor regulated by Jun N-terminal kinase-independent phosphorylation. Hepatology 44: 1432-1440.
57. Grigoriadis AE, Schellander K, Wang ZQ, Wagner EF, (1993) Osteoblasts are target cells for transformation in c-fos transgenic mice. J Cell Biol 122: 685-701.
58. Eferl R, Hasselblatt P, Rath M, Popper H, Zenz R, et al. (2008) Development of pulmonary fibrosis through a pathway involving the transcription factor Fra-2/AP-1. Proc Natl Acad Sci U S A 105: 10525-10530.
59. Kireva T, Erhardt A, Tiegs G, Tilg H, Denk H, et al. (2011) Transcription factor Fra-1 induces cholangitis and liver fibrosis. Hepatology 53: 1259-1269.
60. Yamaguchi T, Takada Y, Maruyama K, Shimoda K, Arai Y, et al. (2009) Fra-1/AP-1 impairs inflammatory responses and chondrogenesis in fracture healing. J Bone Miner Res 24: 2056-2065.
61. Takada Y, Gresh L, Bozec A, Ikeda E, Kamiya K, et al. (2011) Interstitial lung disease induced by gefitinib and toll-like receptor ligands is mediated by Fra-1. Oncogene 30: 3821-3832.
62. Vaz M, Reddy NM, Rajasekaran S, Reddy SP, (2011) Genetic disruption of Fra-1 decreases susceptibility to endotoxin-induced acute lung injury and mortality in mice. Am J Respir Cell Mol Biol 46: 55-62.