Expression of epstein-barr virus-encoded LMP1 and hTERT extends the life span and immortalizes primary cultures of nasopharyngeal epithelial cells

Journal of Medical Virology

Volumn 82, Issue 10, 2010, Pages 1711-1723

  Yip, Yim Ling ^a   Tsang, Chi Man ^a   Deng, Wen ^a   Cheung, Pak Yan ^a   Jin, Yuesheng ^b   Cheung, Annie Lai Man ^a   Lung, Maria Li ^c   Tsao, Sai Wah ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

EGFR; Immortalization; LMP1; Nasopharyngeal carcinoma; Telomerase

Indexed keywords

BMI1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P16; PROTEIN P21; PROTEIN P53; PROTEIN P63; TELOMERASE REVERSE TRANSCRIPTASE;

ADULT; ARTICLE; CARCINOGENICITY; CELL IMMORTALIZATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOGENETICS; DNA DAMAGE; DOWN REGULATION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; NASOPHARYNX; NASOPHARYNX CARCINOMA; ONCOGENE; ONCOGENE C MYC; ONCOGENE LMP1; PROTEIN EXPRESSION; UPREGULATION;

ADULT; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MALE; NASOPHARYNX; TELOMERASE; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4; MUS MUSCULUS;

EID: 77956601081     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.21875     Document Type: Article

References (59)

1. Akerman GS, Tolleson WH, Brown KL, Zyzak LL, Mourateva E, Engin TS, Basaraba A, Coker AL, Creek KE, Pirisi L. 2001. Human papillomavirus type 16 E6 and E7 cooperate to increase epidermal growth factor receptor (EGFR) mRNA levels, overcoming mechanisms by which excessive EGFR signaling shortens the life span of normal human keratinocytes. Cancer Res 61:3837-3843.
2. Alani RM, Hasskarl J, Grace M, Hernandez MC, Israel MA, Munger K. 1999. Immortalization of primary human keratinocytes by the helix- loop-helix protein, Id-1. Proc Natl Acad Sci USA 96:9637-9641.
3. Basile JR, Eichten A, Zacny V, Munger K. 2003. NF-kappaB-mediated induction of p21(Cip1/Waf1) by tumor necrosis factor alpha induces growth arrest and cytoprotection in normal human keratinocytes. Mol Cancer Res 1:262-270.
4. Brozovic S, Sahoo R, Barve S, Shiba H, Uriarte S, Blumberg RS, Kinane DF. 2006. Porphyromonas gingivalis enhances FasL expression via up-regulation of NFkappaB-mediated gene transcription and induces apoptotic cell death in human gingival epithelial cells. Microbiology 152:797-806.
5. Bryce LA, Morrison N, Hoare SF, Muir S, Keith WN. 2000.Mapping of the gene for the human telomerase reverse transcriptase, hTERT, to chromosome 5p15.33 by fluorescence in situ hybridization. Neoplasia 2:197-201.
6. Chan AS, To KF, Lo KW, Mak KF, Pak W, Chiu B, Tse GM, Ding M, Li X, Lee JC, Huang DP. 2000. High frequency of chromosome 3p deletion in histologically normal nasopharyngeal epithelia from southern Chinese. Cancer Res 60:5365-5370.
7. Chan AS, To KF, Lo KW, Ding M, Li X, Johnson P, Huang DP. 2002. Frequent chromosome 9p losses in histologically normal nasopharyngeal epithelia from southern Chinese. Int J Cancer 102:300-303.
8. Chan SY, Choy KW, Tsao SW, Tao Q, Tang T, Chung GT, Lo KW. 2008. Authentication of nasopharyngeal carcinoma tumor lines. Int J Cancer 122:2169-2171.
9. Chen JS, Tzeng CC, Tsao CJ, Su WC, Chen TY, Jung YC, Su IJ. 1997. Clonal karyotype abnormalities in EBV-associated hemophagocytic syndrome. Haematologica 82:572-576.
10. Cheung PY, Deng W, Man C, Tse WW, Srivastava G, Law S, Tsao SW, Cheung AL. 2010. Genetic alterations in a telomerase-immortalized human esophageal epithelial cell line: Implications for carcinogenesis. Cancer Lett 293:41-51.
11. Chung CM, Man C, Jin Y, Jin C, Guan XY, Wang Q, Wan TS, Cheung AL, Tsao SW. 2005. Amplification and overexpression of aurora kinase A (AURKA) in immortalized human ovarian epithelial (HOSE) cells. Mol Carcinog 43:165-174.
12. Colgin LM, Reddel RR. 1999. Telomere maintenance mechanisms and cellular immortalization. Curr Opin Genet Dev 9:97-103.
13. Dawson CW, Tramountanis G, Eliopoulos AG, Young LS. 2003. 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 278:3694-3704.
14. Deng W, Tsao SW, Lucas JN, Leung CS, Cheung AL. 2003. A new method for improving metaphase chromosome spreading. Cytometry A 51:46-51.
15. Deng W, Tsao SW, Guan XY, Lucas JN, Si HX, Leung CS, Mak P, Wang LD, Cheung AL. 2004. Distinct profiles of critically short telomeres are a key determinant of different chromosome aberrations in immortalized human cells: Whole-genome evidence from multiple cell lines. Oncogene 23:9090-9101.
16. Dutton A, Woodman CB, Chukwuma MB, Last JI, Wei W, Vockerodt M, Baumforth KR, Flavell JR, Rowe M, Taylor AM, Young LS, Murray PG. 2007. Bmi-1 is induced by the Epstein-Barr virus oncogene LMP1 and regulates the expression of viral target genes in Hodgkin lymphoma cells. Blood 109:2597-2603.
17. Eliopoulos AG, Young LS. 2001. LMP1 structure and signal transduction. Semin Cancer Biol 11:435-444.
18. Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, Waters CM, Penn LZ, Hancock DC. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128.
19. Feederle R, Neuhierl B, Bannert H, Geletneky K, Shannon-Lowe C, Delecluse HJ. 2007. 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 121:588-594.
20. Gires O, Zimber-Strobl U, Gonnella R, Ueffing M, Marschall G, Zeidler R, Pich D, Hammerschmidt W. 1997. Latentmembrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J 16:6131-6140.
21. Glinsky GV, Berezovska O, Glinskii AB. 2005. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest 115:1503-1521.
22. Goessel G, Quante M, Hahn WC, Harada H, Heeg S, Suliman Y, Doebele M, von Werder A, Fulda C, Nakagawa H, Rustgi AK, Blum HE, Opitz OG. 2005. Creating oral squamous cancer cells: A cellular model of oral-esophageal carcinogenesis. Proc Natl Acad Sci USA 102:15599-15604.
23. Gottifredi V, McKinney K, Poyurovsky MV, Prives C. 2004. Decreased p21 levels are required for efficient restart of DNA synthesis after S phase block. J Biol Chem 279:5802-5810.
24. Gullo C, Low WK, Teoh G. 2008. Association of Epstein-Barr virus with nasopharyngeal carcinoma and current status of development of cancer-derived cell lines. Ann Acad Med Singapore 37:769-777.
25. Haga K, Ohno S, Yugawa T, Narisawa-Saito M, Fujita M, Sakamoto M, Galloway DA, Kiyono T. 2007. Efficient immortalization of primary human cells by p16INK4a-specific short hairpin RNA or Bmi-1, combined with introduction of hTERT. Cancer Sci 98:147-154.
26. Hahn WC. 2002. Immortalization and transformation of human cells. Mol Cells 13:351-361.
27. Hammerschmidt W, Sugden B, Baichwal VR. 1989. The transforming domain alone of the latent membrane protein of Epstein-Barr virus is toxic to cells when expressed at high levels. J Virol 63:2469-2475.
28. Humme S, Reisbach G, Feederle R, Delecluse HJ, Bousset K, Hammerschmidt W, Schepers A. 2003. The EBV nuclear antigen 1 (EBNA1) enhances B cell immortalization several thousandfold. Proc Natl Acad Sci USA 100:10989-10994.
29. Izumi KM, Kieff ED. 1997. The Epstein-Barr virus oncogene product latent membrane protein 1 engages the tumor necrosis factor receptor-associated death domain protein to mediate B lymphocyte growth transformation and activate NF-kappaB. Proc Natl Acad Sci USA 94:12592-12597.
30. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. 1999a. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397:164-168.
31. Jacobs JJ, Scheijen B, Voncken JW, Kieboom K, Berns A, van Lohuizen M. 1999b. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev 13:2678-2690.
32. Kieff E. 1996. Epstein-Barr virus and its replication. In: Fields BN, Knipe DM, Howley PM, editors. Fields virology, 3rd edition. Philadelphia, PA: Raven Press. pp. 2343-2396.
33. Kulwichit W, Edwards RH, Davenport EM, Baskar JF, Godfrey V, Raab-Traub N. 1998. Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc Natl Acad Sci USA 95:11963-11968.
34. Kwong J, Lo KW, To KF, Teo PM, Johnson PJ, Huang DP. 2002. Promoter hypermethylation of multiple genes in nasopharyngeal carcinoma. Clin Cancer Res 8:131-137. (Pubitemid 34101468)
35. Li HM, Zhuang ZH, Wang Q, Pang JC, Wang XH, Wong HL, Feng HC, Jin DY, Ling MT, Wong YC, Eliopoulos AG, Young LS, Huang DP, Tsao SW. 2004. Epstein-Barr virus latent membrane protein 1 (LMP1) upregulates Id1 expression in nasopharyngeal epithelial cells. Oncogene 23:4488-4494.
36. Li HM, Man C, Jin Y, Deng W, Yip YL, Feng HC, Cheung YC, Lo KW, Meltzer PS, Wu ZG, Kwong YL, Yuen AP, Tsao SW. 2006. Molecular and cytogenetic changes involved in the immortalization of nasopharyngeal epithelial cells by telomerase. Int J Cancer 119:1567-1576.
37. Lo AK, Huang DP, Lo KW, Chui YL, Li HM, Pang JC, Tsao SW. 2004. Phenotypic alterations induced by the Hong Kong-prevalent Epstein-Barr virus-encoded LMP1 variant (2117-LMP1) in nasopharyngeal epithelial cells. Int J Cancer 109:919-925.
38. Lu J, Chua HH, Chen SY, Chen JY, Tsai CH. 2003. Regulation of matrix metalloproteinase-1 by Epstein-Barr virus proteins. Cancer Res 63:256-262.
39. Man C, Rosa J, Lee LT, Lee VH, Chow BK, Lo KW, Doxsey S, Wu ZG, Kwong YL, Jin DY, Cheung AL, Tsao SW. 2007. Latent membrane protein 1 suppresses RASSF1A expression, disrupts microtubule structures and induces chromosomal aberrations in human epithelial cells. Oncogene 26:3069-3080.
40. McMurray HR, McCance DJ. 2004. Degradation of p53, not telomerase activation, by E6 is required for bypass of crisis and immortalization by human papillomavirus type 16 E6/E7. J Virol 78:5698-5706.
41. Miller WE, Earp HS, Raab-Traub N. 1995. The Epstein-Barr virus latent membrane protein 1 induces expression of the epidermal growth factor receptor. J Virol 69:4390-4398.
42. Murono S, Inoue H, Tanabe T, Joab I, Yoshizaki T, Furukawa M, Pagano JS. 2001. Induction of cyclooxygenase-2 by Epstein-Barr virus latentmembrane protein 1 is involved in vascular endothelial growth factor production in nasopharyngeal carcinoma cells. Proc Natl Acad Sci USA 98:6905-6910.
43. O'Nions J, Allday MJ. 2003. Epstein-Barr virus can inhibit genotoxin-induced G1 arrest downstream of p53 by preventing the inactivation of CDK2. Oncogene 22:7181-7191.
44. O'Nions J, Turner A, Craig R, Allday MJ. 2006. Epstein-Barr virus selectively deregulates DNA damage responses in normal B cells but has no detectable effect on regulation of the tumor suppressor p53. J Virol 80:12408-12413.
45. Pathmanathan R, Prasad U, Sadler R, Flynn K, Raab-Traub N. 1995. Clonal proliferations of cells infected with Epstein-Barr virus in preinvasive lesions related to nasopharyngeal carcinoma. N Engl J Med 333:693-698.
46. Polsky D, Young AZ, Busam KJ, Alani RM. 2001. The transcriptional repressor of p16/Ink4a, Id1, is up-regulated in early melanomas. Cancer Res 61:6008-6011.
47. Raab-Traub N. 2002. Epstein-Barr virus in the pathogenesis of NPC. Semin Cancer Biol 12:431-441.
48. Reznikoff CA, Belair C, Savelieva E, Zhai Y, Pfeifer K, Yeager T, Thompson KJ, DeVries S, Bindley C, Newton MA, Sekhon G, Waldman F. 1994. Long-term genome stability and minimal genotypic and phenotypic alterations in HPV16 E7-, but not E6-, immortalized human uroepithelial cells. Genes Dev 8:2227-2240.
49. Shair KH, Bendt KM, Edwards RH, Bedford EC, Nielsen JN, Raab-Traub N. 2007. EBV latent membrane protein 1 activates Akt, NFkappaB, and Stat3 in B cell lymphomas. PLoS Pathog 3:1669-1683.
50. Song LB, Zeng MS, Liao WT, Zhang L, Mo HY, Liu WL, Shao JY, Wu QL, Li MZ, Xia YF, Fu LW, Huang WL, Dimri GP, Band V, Zeng YX. 2006. Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells. Cancer Res 66:6225-6232.
51. Stevenson D, Charalambous C, Wilson JB. 2005. Epstein-Barr virus latent membrane protein 1 (CAO) up-regulates VEGF and TGF alpha concomitant with hyperlasia, with subsequent up-regulation of p16 and MMP9. Cancer Res 65:8826-8835.
52. Thornburg NJ, Kulwichit W, Edwards RH, Shair KH, Bendt KM, Raab-Traub N. 2006. LMP1 signaling and activation of NF-kappaB in LMP1 transgenic mice. Oncogene 25:288-297.
53. Tsao SW, Wong N, Wang X, Liu Y, Wan TS, Fung LF, Lancaster WD, Gregoire L, Wong YC. 2001. Nonrandom chromosomal imbalances in human ovarian surface epithelial cells immortalized by HPV16-E6E7 viral oncogenes. Cancer Genet Cytogenet 130:141-149.
54. Tsao SW, Tramoutanis G, Dawson CW, Lo AK, Huang DP. 2002a. The significance of LMP1 expression in nasopharyngeal carcinoma. Semin Cancer Biol 12:473-487.
55. Tsao SW, Wang X, Liu Y, Cheung YC, Feng H, Zheng Z, Wong N, Yuen PW, Lo AK, Wong YC, Huang DP. 2002b. Establishment of two immortalized nasopharyngeal epithelial cell lines using SV40 large T and HPV16E6/E7 viral oncogenes. Biochim Biophys Acta 1590:150-158.
56. Yang X, He Z, Xin B, Cao L. 2000a. LMP1 of Epstein-Barr virus suppresses cellular senescence associated with the inhibition of p16INK4a expression. Oncogene 19:2002-2013.
57. Yang X, Sham JS, Ng MH, Tsao SW, Zhang D, Lowe SW, Cao L. 2000b. LMP1 of Epstein-Barr virus induces proliferation of primary mouse embryonic fibroblasts and cooperatively transforms the cells with a p16-insensitive CDK4 oncogene. J Virol 74:883-891.
58. Yip YL, Tsao SW. 2008. Regulation of p63 expression in primary and immortalized nasopharyngeal epithelial cells. Int J Oncol 33:713-724.
59. Zheng X, Hu L, Chen F, Christensson B. 1994. Expression of Ki67 antigen, epidermal growth factor receptor and Epstein-Barr virus-encoded latent membrane protein (LMP1) in nasopharyngeal carcinoma. Eur J Cancer B Oral Oncol 30B:290-295.