Epstein-Barr virus facilitates the malignant potential of immortalized epithelial cells: From latent genome to viral production and maintenance

Laboratory Investigation

Volumn 90, Issue 2, 2010, Pages 196-209

  Lu, Jian Hong ^a   Tang, Yun Lian ^a,b   Yu, Hai Bo ^a   Zhou, Jian Hua ^a   Fu, Chun Yan ^a   Zeng, Xi ^a   Yu, Zheng Yuan ^a   Yin, Hong Ling ^a   Wu, Ming Hua ^a   Zhang, Jun Yi ^a,c   Li, Xiao Ling ^a   Li, Gui Yuan ^a  

^a Central South University   (China)

^b UNIVERSITY OF SOUTH CHINA   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Epstein Barr virus; Latent infection; Lytic cycle; Malignancy; Viral maintenance

Indexed keywords

LATENT MEMBRANE PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CARCINOGENICITY; CELL CYCLE; CELL DENSITY; CELL GROWTH; CELL STRAIN; CELL STRAIN 293; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VIRUS GENOME; VIRUS PARTICLE; VIRUS REPLICATION;

ANIMALS; CARCINOMA; CELL LINE, TRANSFORMED; HERPESVIRUS 4, HUMAN; HUMANS; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE 9; NEOPLASM TRANSPLANTATION; NF-KAPPA B; UP-REGULATION; VIRUS LATENCY;

EID: 75949084496     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2009.130     Document Type: Article

References (53)

1. Bornkamm GW, Hammerschmidt W. Molecular virology of Epstein-Barr virus. Philos Trans R Soc Lond B Biol Sci 2001;356:437-459.
2. zur Hausen H, Schulte-Holthausen H, Klein G, et al. EBV DNA in biopsies of Burkitt tumours and anaplastic carcinomas of the nasopharynx. Nature 1970;228:1056-1058.
3. Raab-Traub N, Flynn K, Pearson G, et al. The differentiated form of nasopharyngeal carcinoma contains Epstein-Barr virus DNA. Int J Cancer 1987;39:25-29.
4. Robertson ES. Epstein-Barr Virus. Caister Academic Press: Wymondham, England, 2005.
5. Metzenberg S. Levels of Epstein-Barr virus DNA in lymphoblastoid cell lines are correlated with frequencies of spontaneous lytic growth but not with levels of expression of EBNA-1, EBNA-2, or latent membrane protein. J Virol 1990;64:437-444.
6. Young LS, Rickinson AB. Epstein-Barr virus: 40 years on. Nat Rev Cancer 2004;4:757-768.
7. Young LS, Murray PG. Epstein-Barr virus and oncogenesis: from latent genes to tumours. Oncogene 2003;22:5108-5121.
8. Li HP, Chang YS. Epstein-Barr virus latent membrane protein 1: structure and functions. J Biomed Sci 2003;10:490-504.
9. Macsween KF, Crawford DH. Epstein-Barr virus-recent advances. Lancet Infect Dis 2003;3:131-140.
10. Rickinson A. Concluding overview: looking back, looking forward. Philos Trans R Soc Lond B Biol Sci 2001;356:595-604.
11. Li QX, Young LS, Niedobitek G, et al. Epstein-Barr virus infection and replication in a human epithelial cell system. Nature 1992; 356:347-350.
12. Lo KW, To KF, Huang DP. Focus on nasopharyngeal carcinoma. Cancer Cell 2004;5:423-428.
13. Lo AKF, Lo KW, Tsao SW, et al. Epstein-Barr virus infection alters cellular signal cascades in human nasopharyngeal epithelial cells. Neoplasia 2006;8:173-180.
14. Danve C, Decaussin G, Busson P, et al. Growth transformation of primary epithelial cells with a NPC-derived Epstein-Barr Virus strain. Virology 2001;288:223-235.
15. Li BM, Ji ZW, Liu ZS, et al. Epstein-Barr virus in synergy with tumor-promoter-induced malignant transformation of immortalized human epithelial cells. J Cancer Res Clin Oncol 1997;123:441-446.
16. Sam CK, Brooks LA, Niedobitek G, et al. Analysis of Epstein-Barr virus infection in nasopharyngeal biopsies from a group at high risk of nasopharyngeal carcinoma. Int J Cancer 1993;53:957-962.
17. Zeng ZY, Zhou YH, Zhang WL, et al. Gene expression profiling of nasopharyngeal carcinoma reveals the abnormally regulated Wnt signaling pathway. Hum Pathol 2007;38:120-133.
18. Raab-Traub N. Epstein-Barr virus in the pathogenesis of NPC. Semin Cancer Biol 2002;12:431-441.
19. Guasparri I, Bubman D, Cesarman E. EBV LMP2A affects LMP1-mediated NF-\{kappa\}B signal. Blood 2008;111:3813-3820.
20. Sheng W, Decaussin G, Ligout A, et al. Malignant transformation of Epstein-Barr virus-negative akata cells by introduction of the BARF1 gene carried by Epstein-Barr virus. J Virol 2003;77:3859-3865.
21. Delecluse HJ, Hammerschmidt W. The genetic approach to the Epstein-Barr virus: from basic virology to gene therapy. J Clin Pathol Mol Pathol 2000;53:270-279.
22. Delecluse HJ, Hilsendegen T, Pich D, et al. Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc Natl Acad Sci USA 1998;95:8245-8250.
23. Fingeroth JD, Weis JJ, Tedder TF, et al. Epstein-Barr virus receptor of human B lymphocytes in the C3d receptor CR2. Proc Natl Acad Sci USA 1984;81:4510-4514.
24. Tang YL, Lu JH, Wu MH, et al. Lytic replication and inductive production of recombinant Epstein-Barr virus visualized. Prog Biochem Biophys 2007;34:418-424.
25. Tsao SW, Wang X, Liu Y, et al. Establishment of two immortalized nasopharyngeal epithelial cell lines using SV40 large T and HPV16E6/E7 viral oncogenes. Biochim Biophys Acta 2002;1590: 150-158.
26. Cooper JK, Sykes G, King S, et al. Species identification in cell culture: a two-pronged molecular approach. In Vitro Cell Dev Biol-Animal 2007;43:344-351.
27. He Z, Xin B, Yang X, et al. Nuclear factor-kB activation is involved in LMP1-mediated transformation and tumorigenesis of rat-1 fibroblasts. Cancer Res 2000;60:1845-1848.
28. Kieser A, Kilger E, Gires O, et al. Epstein-Barr virus latent membrane protein 1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade. EMBO J 1997;16:6478-6485.
29. Sylla BS, Hung SC, Davidson DM, et al. Epstein-Barr virus-transforming protein latent infection membrane protein 1 activates transcription factor NF-kappaB through a pathway that includes the NF-kappaB-inducing kinase and the IkappaB kinases IKKalpha and IKKbeta. Proc Natl Acad Sci USA 1998;95:10106-10111.
30. Angel P, Karin M. The role of Jun, Fos, and the AP-1 complex in cell proliferation and transformation. Biochem Biophys Acta 1991;1072:129-157.
31. Pulverer BJ, Kyriakis JM, Avruch J, et al. Phosphorylation of c-Jun mediated by MAP kinases. Nature 1991;353:670-674.
32. Wagner M, Ruzsics Z, Koszinowski UH. Herpesvirus genetics has come of age. Trends Microbiol 2002;10:318-324.
33. Shen C, Gu M, Song C, et al. The tumorigenicity diversification in human embryonic kidney 293 cell line cultured in vitro. Biologicals 2008;36:263-268.
34. Moore M, Horikoshi N, Shenk T. Oncogenic potential of the adenovirus E4orf6 protein. Proc Natl Acad Sci USA 1996;93:11295-11301.
35. Guan LS, Li GC, Liu LQ, et al. Rb-associated protein 46 (RbAp46) suppresses the tumorigenicity of adenovirus-transformed human embryonic kidney 293 cells. Int J Cancer 2001;93:333-338.
36. Dirmeier U, Neuhierl B, Kilger E, et al. Latent membrane protein 1 is critical for efficient growth transformation of human B cells by Epstein-Barr virus. Cancer Res 2003;63:2982-2989.
37. Feederle R, Neuhierl B, Bannert H, et al. Epstein-Barr virus B95.8 produced in 293 cells shows marked tropism for differentiated primary epithelial cells and reveals interindividual variation in susceptibility to viral infection. Int J Cancer 2007;121:588-594.
38. Kaltschmidt B, Kaltschmidt C, Hehner SP, et al. Repression of NF-kappaB impairs HeLa cell proliferation by functional interference with cell cycle checkpoint regulators. Oncogene 1999;18:3213-3225.
39. Wang D, Liebowitz D, Kieff E. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell 1985;43:831-840.
40. Larcher C, Bernhard D, Schaadt E, et al. Functional analysis of the mutated Epstein-Barr virus oncoprotein LMP1(69del): implications for a new role of naturally occurring LMP1 variants. Haematologica 2003;88:1324-1335.
41. Desgranges C, Bornkamm GW, Zeng Y, et al. Detection of Epstein-Barr viral DNA internal repeats in the nasopharyngeal mucosa of Chinese with IgA/EBV-specific antibodies. Int J Cancer 1982;29:87-91.
42. Gu AD, Xie YB, Mo HY, et al. Antibodies against Epstein-Barr virus gp78 antigen: a novel marker for serological diagnosis of nasopharyngeal carcinoma detected by xMAP technology. J Gen Virol 2008;89: 1152-1158.
43. Trumper PA, Epstein MA, Giovanella BC, et al. Isolation of infectious EB virus from the epithelial tumor cells of nasopharyngeal carcinoma. Int J Cancer 1977;20:655-662.
44. Meisler AI, Schuster V, Pukrop T, et al. Epstein-Barr virus and nasopharyngeal cancer. N Engl J Med 1996;334:122-123.
45. Luka J, Kallin B, Klein G. Induction of the Epstein-Barr virus (EBV) lytic cycle in latently infected cells by n-butyrate. Virology 1979;94:228-231.
46. Takada K, Ono Y. Synchronous and sequential activation of latently infected Epstein-Barr virus genomes. J Virol 1989;63:445-449.
47. Tovey MG, Lenoir G, Begon-Lours J. Activation of latent Epstein-Barr virus by antibody to human IgM. Nature 1978;276:270-272.
48. Shannon-Lowe CD, Neuhierl B, Baldwin G, et al. Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells. Proc Natl Acad Sci USA 2006;103:7065-7070.
49. Chang Y, Tung CH, Huang YT, et al. Requirement for cell-to-cell contact in Epstein-Barr virus infection of nasopharyngeal carcinoma cells and keratinocytes. J Virol 1999;73:8857-8866.
50. Pathmanathan R, Prasad U, Sadler R, et al. Clonal proliferations of cells infected with Epstein-Barr Virus in preinvasive lesions related to nasopharyngeal carcinoma. N Engl J Med 1995;333:693-698.
51. Teramoto N, Maeda A, Kobayashi K, et al. Epstein-Barr virus infection to Epstein-Barr virus-negative nasopharyngeal carcinoma cell line TW03 enhances its tumorigenicity. Lab Invest 2000;80:303-312.
52. Raab-Traub N, Flynn K. The structure of the termini of the Epstein-Barr virus as a marker of clonal cellular proliferation. Cell 1986;47:883-889.
53. Glaser R, Zhang HY, Yao KT, et al. Two epithelial tumor cell lines (HNE-1 and HONE-1) latently infected with Epstein-Barr virus that were derived from nasopharyngeal carcinomas. Proc Natl Acad Sci USA 1989;86:9524-9528.