The Epstein-Barr virus latent membrane protein 1 and transforming growth factor-β1 synergistically induce epithelial-mesenchymal transition in lung epithelial cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 44, Issue 6, 2011, Pages 852-862

  Sides, Mark D ^a   Klingsberg, Ross C ^a   Shan, Bin ^a   Gordon, Kristin A ^a   Nguyen, Hong T ^a   Lin, Zhen ^a,b   Takahashi, Takashi ^c   Flemington, Erik K ^a,b   Lasky, Joseph A ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Louisiana Cancer Research Consortium   (United States)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Epithelial mesenchymal transition; Epstein Barr virus; Idiopathic pulmonary fibrosis; Latent membrane protein 1; Transforming growth factor 1

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LATENT MEMBRANE PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL MOTILITY; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; HUMAN; HUMAN TISSUE; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROSIS; MESENCHYME CELL; PROTEIN EXPRESSION; VIRUS LATENCY;

CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROSIS; HERPESVIRUS 4, HUMAN; HUMANS; LUNG; MESODERM; MODELS, BIOLOGICAL; NF-KAPPA B; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 80051558446     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0232OC     Document Type: Article

References (44)

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. Mora AL, Torres-Gonzalez E, Rojas M, Xu J, Ritzenthaler J, Speck SH, Roman J, Brigham K, Stecenko A. Control of virus reactivation arrests pulmonary herpesvirus-induced fibrosis in IFN-gamma receptor-deficient mice. Am J Respir Crit Care Med 2007;175:1139-1150. (Pubitemid 46855455)
3. Selman M, King TE, Pardo A. Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med 2001;134:136-151. (Pubitemid 32096342)
4. Vergnon JM, Vincent M, de The G, Mornex JF, Weynants P, Brune J. Cryptogenic fibrosing alveolitis and Epstein-Barr virus: an association? Lancet 1984;2:768-771.
5. Egan JJ, Stewart JP, Hasleton PS, Arrand JR, Carroll KB, Woodcock AA. Epstein-Barr virus replication within pulmonary epithelial cells in cryptogenic fibrosing alveolitis. Thorax 1995;50:1234-1239.
6. Stewart JP, Egan JJ, Ross AJ, Kelly BG, Lok SS, Hasleton PS, Woodcock AA. The detection of Epstein-Barr virus DNA in lung tissue from patients with idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 1999;159:1336-1341. (Pubitemid 29202576)
7. Tang YW, Johnson JE, Browning PJ, Cruz-Gervis RA, Davis A, Graham BS, Brigham KL, Oates JA, Jr., Loyd JE, Stecenko AA. Herpesvirus DNA is consistently detected in lungs of patients with idiopathic pulmonary fibrosis. J Clin Microbiol 2003;41:2633-2640. (Pubitemid 36712478)
8. Tsukamoto K, Hayakawa H, Sato A, Chida K, Nakamura H, Miura K. Involvement of Epstein-Barr virus latent membrane protein 1 in disease progression in patients with idiopathic pulmonary fibrosis. Thorax 2000;55:958-961.
9. Yonemaru M, Kasuga I, Kusumoto H, Kunisawa A, Kiyokawa H, Kuwabara S, Ichinose Y, Toyama K. Elevation of antibodies to cytomegalovirus and other herpes viruses in pulmonary fibrosis. Eur Respir J 1997;10:2040-2045. (Pubitemid 27406438)
10. Eliopoulos AG, Young LS. LMP1 structure and signal transduction. Semin Cancer Biol 2001;11:435-444. (Pubitemid 33105022)
11. Dawson CW, Laverick L, Morris MA, Tramoutanis G, Young LS. Epstein-Barr virus-encoded LMP1 regulates epithelial cell motility and invasion via the ERK-MAPK pathway. J Virol 2008;82:3654-3664. (Pubitemid 351429941)
12. Dawson CW, Rickinson AB, Young LS. Epstein-Barr virus latent membrane protein inhibits human epithelial cell differentiation. Nature 1990;344:777-780.
13. Dawson CW, Tramountanis G, Eliopoulos AG, Young LS. Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodeling. J Biol Chem 2003;278:3694-3704. (Pubitemid 36801094)
14. Horikawa T, Yang J, Kondo S, Yoshizaki T, Joab I, Furukawa M, Pagano JS. Twist and epithelial-mesenchymal transition are induced by the EBV oncoprotein latent membrane protein 1 and are associated with metastatic nasopharyngeal carcinoma. Cancer Res 2007;67:1970-1978. (Pubitemid 46424213)
15. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol 2006;7:131-142. (Pubitemid 43278296)
16. 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. (Pubitemid 44338936)
17. Willis BC, duBois RM, Borok Z. Epithelial origin of myofibroblasts during fibrosis in the lung. Proc Am Thorac Soc 2006;3:377-382. (Pubitemid 43845416)
18. Letterio JJ, Roberts AB. Regulation of immune responses by TGF-beta. Annu Rev Immunol 1998;16:137-161.
19. Lin HK, Bergmann S, Pandolfi PP. Cytoplasmic PML function in TGF-beta signalling. Nature 2004;431:205-211. (Pubitemid 39243475)
20. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003;113:685-700. (Pubitemid 36724933)
21. Willis BC, Borok Z. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007;293:L525-L534. (Pubitemid 47358808)
22. Kasai H, Allen JT, Mason RM, Kamimura T, Zhang Z. TGF-beta1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res 2005;6:56.
23. Malizia AP, Keating DT, Smith SM, Walls D, Doran PP, Egan JJ. Alveolar epithelial cell injury with Epstein-Barr virus upregulates TGFbeta1 expression. Am J Physiol Lung Cell Mol Physiol 2008;295:L451-L460.
24. Masuda A, Kondo M, Saito T, Yatabe Y, Kobayashi T, Okamoto M, Suyama M, Takahashi T. Establishment of human peripheral lung epithelial cell lines (HPL1) retaining differentiated characteristics and responsiveness to epidermal growth factor, hepatocyte growth factor, and transforming growth factor beta1. Cancer Res 1997;57:4898-4904. (Pubitemid 27469000)
25. Shan B, Yao TP, Nguyen HT, Zhuo Y, Levy DR, Klingsberg RC, Tao H, Palmer ML, Holder KN, Lasky JA. Requirement of HDAC6 for transforming growth factor-beta1-induced epithelial-mesenchymal transition. J Biol Chem 2008;283:21065-21073.
26. Cameron JE, Yin Q, Fewell C, Lacey M, McBride J, Wang X, Lin Z, Schaefer BC, Flemington EK. Epstein-Barr virus latent membrane protein 1 induces cellular MicroRNA miR-146a, a modulator of lymphocyte signaling pathways. J Virol 2008;82:1946-1958. (Pubitemid 351206940)
27. Brockman JA, Scherer DC, McKinsey TA, Hall SM, Qi X, Lee WY, Ballard DW. Coupling of a signal response domain in I kappa B alpha to multiple pathways for NF-kappa B activation. Mol Cell Biol 1995;15:2809-2818.
28. Gottschalk S, Edwards OL, Sili U, Huls MH, Goltsova T, Davis AR, Heslop HE, Rooney CM. Generating CTLs against the subdominant Epstein-Barr virus LMP1 antigen for the adoptive immunotherapy of EBV-associated malignancies. Blood 2003;101:1905-1912. (Pubitemid 36237592)
29. Yue X, Li X, Nguyen HT, Chin DR, Sullivan DE, Lasky JA. Transforming growth factor-beta1 induces heparan sulfate 6-O-endosulfatase 1 expression in vitro and in vivo. J Biol Chem 2008;283:20397-20407.
30. Yang L, Amann JM, Kikuchi T, Porta R, Guix M, Gonzalez A, Park KH, Billheimer D, Arteaga CL, Tai HH, et al. Inhibition of epidermal growth factor receptor signaling elevates 15-hydroxyprostaglandin dehydrogenase in non-small-cell lung cancer. Cancer Res 2007;67:5587-5593. (Pubitemid 46984987)
31. Molesworth SJ, Lake CM, Borza CM, Turk SM, Hutt-Fletcher LM. Epstein-Barr virus gH is essential for penetration of B cells but also plays a role in attachment of virus to epithelial cells. J Virol 2000;74:6324-6332. (Pubitemid 30429797)
32. Shan B, Zhuo Y, Chin D, Morris CA, Morris GF, Lasky JA. Cyclin-dependent kinase 9 is required for tumor necrosis factor-alpha-stimulated matrix metalloproteinase-9 expression in human lung adenocarcinoma cells. J Biol Chem 2005;280:1103-1111.
33. Vannella KM, Luckhardt TR, Wilke CA, van Dyk LF, Toews GB, Moore BB. Latent herpesvirus infection augments experimental pulmonary fibrosis. Am J Respir Crit Care Med 2010;181:465-477.
34. Ranganathan P, Agrawal A, Bhushan R, Chavalmane AK, Kalathur RK, Takahashi T, Kondaiah P. Expression profiling of genes regulated by TGF-beta: differential regulation in normal and tumour cells. BMC Genomics 2007;8:98.
35. Xie L, Law BK, Chytil AM, Brown KA, Aakre ME, Moses HL. Activation of the Erk pathway is required for TGF-beta1-induced EMT in vitro. Neoplasia 2004;6:603-610. (Pubitemid 39411098)
36. Tsai CN, Tsai CL, Tse KP, Chang HY, Chang YS. The Epstein-Barr virus oncogene product, latent membrane protein 1, induces the downregulation of E-cadherin gene expression via activation of DNA methyltransferases. Proc Natl Acad Sci USA 2002;99:10084-10089.
37. Tester AM, Ruangpanit N, Anderson RL, Thompson EW. MMP-9 secretion and MMP-2 activation distinguish invasive and metastatic sublines of a mouse mammary carcinoma system showing epithelial-mesenchymal transition traits. Clin Exp Metastasis 2000;18:553-560. (Pubitemid 32964317)
38. Suga M, Iyonaga K, Okamoto T, Gushima Y, Miyakawa H, Akaike T, Ando M. Characteristic elevation of matrix metalloproteinase activity in idiopathic interstitial pneumonias. Am J Respir Crit Care Med 2000;162:1949-1956.
39. McKeown S, Richter AG, O'Kane C, McAuley DF, Thickett DR. MMP expression and abnormal lung permeability are important determinants of outcome in IPF. Eur Respir J 2009;33:77-84.
40. Liu LT, Peng JP, Chang HC, Hung WC. RECK is a target of Epstein-Barr virus latent membrane protein 1. Oncogene 2003;22:8263-8270.
41. Yan C, Boyd DD. Regulation of matrix metalloproteinase gene expression. J Cell Physiol 2007;211:19-26. (Pubitemid 46363892)
42. Virgin HWt, Latreille P, Wamsley P, Hallsworth K, Weck KE, Dal Canto AJ, Speck SH. Complete sequence and genomic analysis of murine gammaherpesvirus 68. J Virol 1997;71:5894-5904.
43. Kulwichit W, Edwards RH, Davenport EM, Baskar JF, Godfrey V, Raab-Traub N. Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc Natl Acad Sci USA 1998;95:11963-11968. (Pubitemid 28460522)
44. Panagopoulos D, Victoratos P, Alexiou M, Kollias G, Mosialos G. Comparative analysis of signal transduction by CD40 and the Epstein-Barr virus oncoprotein LMP1 in vivo. J Virol 2004;78:13253-13261. (Pubitemid 39507830)