LMP1 of Epstein-Barr virus induces proliferation of primary mouse embryonic fibroblasts and cooperatively transforms the cells with a p16- insensitive CDK4 oncogene

Journal of Virology

Volumn 74, Issue 2, 2000, Pages 883-891

  Yang, Xinhai ^a   Sham, Jonathan S T ^a   Ng, M H ^a   Tsao, Sai Wah ^a   Zhang, Dekai ^a   Lowe, Scott W ^b   Cao, Liang ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 4; LATENT MEMBRANE PROTEIN 1; PROTEIN P16;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EPSTEIN BARR VIRUS; HODGKIN DISEASE; MOUSE; NASOPHARYNX CARCINOMA; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; RETROVIRUS; VIRUS CARCINOGENESIS; VIRUS CELL TRANSFORMATION; VIRUS ONCOGENE; VIRUS RECOMBINANT;

ANIMALS; CARRIER PROTEINS; CELL DIVISION; CELL TRANSFORMATION, NEOPLASTIC; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASES; FIBROBLASTS; GENETIC VECTORS; HELA CELLS; HERPESVIRUS 4, HUMAN; HUMANS; MICE; ONCOGENE PROTEINS, VIRAL; PROTO-ONCOGENE PROTEINS; RETROVIRIDAE; TELOMERASE; VIRAL MATRIX PROTEINS;

EID: 0033986419     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.2.883-891.2000     Document Type: Article

References (53)

1. Ashkenazi, A., and V. M. Dixit. 1998. Death receptors: signaling and modulation. Science 281:1305-1308.
2. Baichwal, V. R., and B. Sugden. 1988. Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus. Oncogene 2:461-467.
3. Bartkova, J., J. Lukas, P. Guldberg, J. Alsner, A. F. Kirkin, J. Zeuthen, and J. Bartek. 1996. The p16-cyclin D/Cdk4-pRb pathway as a functional unit frequently altered in melanoma pathogenesis. Cancer Res. 56:5475-5483.
4. Boyd, J. M., S. Malstrom, T. Subramanian, L. K. Venkatesh, U. Schaeper, B. Elangovan, C. D'Sa-Eipper, and G. Chinnadurai. 1994. Adenovirus E1B 19 KDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 79:341-351.
5. Cao, L., B. Faha, M. Dembski, L. H. Tsai, E. Harlow, and N. Dyson. 1992. Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F. Nature 355:176-179.
6. Chen, H. F., S. Kevan-Jah, K. O. Suentzenich, F. A. Grasser, and N. Mueller-Lantzsch. 1992. Expression of the Epstein-Barr virus latent membrane protein (LMP) in insect cells and detection of antibodies in human sera against this protein. Virology 190:106-115.
7. Cheng, R. Y., P. W. Yuen, J. M. Nicholls, Z. Zheng, W. Wei, J. S. Sham, X. H. Yang, L. Cao, D. P. Huang, and S. W. Tsao. 1998. Telomerase activation in nasopharyngeal carcinomas. Br. J. Cancer 77:456-460.
8. Cohen, J. I., F. Wang, J. Mannick, and E. Kieff. 1989. Epstein-Barr virus nuclear protein 2 is a key determinant of lymphocyte transformation. Proc. Natl. Acad. Sci. USA 86:9558-9562.
9. Counter, C. M., F. M. Botelho, P. Wang, C. B. Harley, and S. Bacchetti. 1994. Stabilization of short telomeres and telomerase activity accompany immortalization of Epstein-Barr virus-transformed human B lymphocytes. J. Virol. 68:3410-3414.
10. Debbas, M., and E. White. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546-554.
11. Eliopoulos, A. G., and L. S. Young. 1998. Activation of the c-Jun N-terminal kinase (JNK) pathway by the Epstein-Barr virus-encoded latent membrane protein 1 (LMP1). Oncogene 16:1731-1742.
12. Fahraeus, R., L. Rymo, J. S. Rhim, and G. Klein. 1990. Morphological transformation of human keratinocytes expressing the LMP gene of Epstein-Barr virus. Nature 345:447-449.
13. Fries, K. L., W. E. Miller, and N. Raab-Traub. 1996. Epstein-Barr virus latent membrane protein 1 blocks p53-mediated apoptosis through the induction of the A20 gene. J. Virol. 70:8653-8659.
14. Gires, O., U. Zimber-Strobl, R. Gonnella, M. Ueffing, G. Marschall, R. Zeidler, D. Pich, and W. Hammerschmidt. 1997. Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J. 16:6131-6140.
15. Hammerschmidt, W., and B. Sugden. 1989. Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes. Nature 340: 393-397.
16. Hawley-Nelson, P., K. H. Vousden, N. L. Hubbert, D. R. Lowy, and J. T. Schiller. 1989. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J. 8:3905-3910.
17. Henderson, S., M. Rowe, C. Gregory, D. Croom-Carter, F. Wang, R. Longnecker, E. Kieff, and A. Rickinson. 1991. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 65:1107-1115.
18. Hu, L. F., F. Chen, X. Zheng, I. Ernberg, S. L. Cao, B. Christensson, G. Klein, and G. Winberg. 1993. Clonability and tumorigenicity of human epithelial cells expressing the EBV encoded membrane protein LMP1. Oncogene 8:1575-1583.
19. Huen, D. S., S. A. Henderson, D. Croom-Carter, and M. Rowe. 1995. The Epstein-Barr virus latent membrane protein-1 (LMP1) mediates activation of NF-Kappa B and cell surface phenotype via two effector regions in its carboxy-terminal cytoplasmic domain. Oncogene 10:549-560.
20. Izumi, K. M., K. M. Kaye, and E. D. Kieff. 1997. The Epstein-Barr virus LMP1 amino acid sequence that engages tumor necrosis factor receptor associated factors is critical for primary B lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA 94:1447-1452.
21. Izumi, K. M., and E. K. Kieff. 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.
22. Kaye, K. M., K. M. Izumi, and E. Kieff. 1993. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA 90:9150-9154.
23. Kempkes, B., D. Spitkovsky, P. Jansen-Durr, J. W. Ellwart, E. Kremmer, H. J. Delecluse, C. Rottenberger, G. W. Bornkamm, and W. Hammerschmidt. 1995. B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2. EMBO J. 14:88-96.
24. Kieff, E. 1996. Epstein-Barr virus and its replication, p. 2343-2396. In B. N. Fields, D. M. Knipe, P. M. Howley, et al. (ed.), Fields virology. 3rd ed., vol. 2. Lippincott-Raven Publishers, Philadelphia, Pa.
25. Kieser, A., E. Kilger, O. Gires, M. Ueffing, W. Kolch, and W. Hammerschmidt. 1997. Epstein-Barr virus latent membrane protein-1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade. EMBO J. 16:6478-6485.
26. Ko, L. J., and C. Prives. 1996. p53: puzzle and paradigm. Genes Dev. 10:1054-1072.
27. Laherty, C. D., H. M. Hu, H. M. Opipari, F. Wang, and V. M. Dixit. 1992. The Epstein-Barr virus LMP1 gene product induces A20 zinc finger protein expression by activating nuclear factor kappa B. J. Biol. Chem. 267:24157-24160.
28. Lavoie, J. N., G. L'Allemain, A. Brunet, R. Muller, and J. Pouyssegur. 1996. Cyclin D1 expression is regulated positively hy the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J. Biol. Chem. 271: 20608-20616.
29. Lowe, S. W., and H. E. Ruley. 1993. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 7:535-545.
30. Mann, K. P., D. Staunton, and D. A. Thorley-Lawson. 1985. Epstein-Barr virus-encoded protein found in plasma membranes of transformed cells. J. Virol. 55:710-720.
31. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-990.
32. Mitchell, T., and B. Sugden. 1995. Stimulation of NF-Κ B-mediated transcription by mutant derivatives of the latent membrane protein of Epstein-Barr virus. J. Virol. 69:2968-2976.
33. Moorthy, R. K., and D. A. Thorley-Lawson. 1993. All three domains of the Epstein-Barr virus-encoded latent membrane protein LMP-1 are required for transformation of Rat-1 fibroblasts. J. Virol. 67:1638-1646.
34. Mosialos, G., M. Birkenbach, R. Yalamanchili, T. VanArsdale, C. Ware, and E. Kieff. 1995. The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 80:389-399.
35. Mowat, M. R. 1998. p53 in tumor progression: life, death, and everything. Adv. Cancer Res. 74:25-48.
36. Nicholson, L. J., P. Hopwood, I. Johannessen, J. R. Salisbury, J. Codd, D. Thorley-Lawson, and D. H. Crawford. 1997. Epstein-Barr virus latent membrane protein does not inhibit differentiation and induces tumorigenicity of human epithelial cells. Oncogene 15:275-283.
37. Okan, I., Y. Wang, F. Chen, L. F. Hu, S. Imreh, G. Klein, and K. G. Wiman. 1995. The EBV-encoded LMP1 protein inhibits p53-triggered apoptosis but not growth arrest. Oncogene 11:1027-1031.
38. Raab-Traub, N., and K. Flynn. 1986. The structure of the termini of the Epstein-Barr virus as a marker of clonal cellular proliferation. Cell 47:883-889.
39. Rickinson, A. B., and E. Kieff. 1996. Epstein-Barr virus, p. 2397-2446. In B. N. Fields, D. M. Knipe, P. M. Howley, et al. (ed.), Fields virology, 3rd ed., vol. 2. Lippincott-Raven Publishers, Philadelphia, Pa.
40. Roberts, M. L., and N. R. Cooper. 1998. Activation of a ras-MAPK-dependent pathway by Epstein-Barr virus latent membrane protein 1 is essential for cellular transformation. Virology 240:93-99.
41. Roussel, M. F. 1998. Key effectors of signal transduction and G1 progression. Adv. Cancer Res. 74:1-24.
42. Rowe, M., H. S. Evans, L. S. Young, K. Hennessy, E. Kieff, and A. B. Rickinson. 1987. Monoclonal antibodies to the latent membrane protein of Epstein-Barr virus reveal heterogeneity of the protein and inducible expression in virus-transformed cells. J. Gen. Virol. 68:1575-1586.
43. Rowe, M., M. Peng-Pilon, D. S. Huen, R. Hardy, D. Croom-Carter, E. Lundgren, and A. B. Rickinson. 1994. Upregulation bcl-2 by the Epstein-Barr virus latent membrane protein LMP1: a B-cell-specific response that is delayed relative to NF-KB activation and to induction of cell surface markers. J. Virol. 68:5602-5612.
44. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
45. Serrano, M., H. Lee, L. Chin, C. Cordon-Cardo, D. Beach, and R. A. DePinho. 1996. Role of the INK4a locus in tumor suppression and cell mortality. Cell 85:27-37.
46. Serrano, M., A. W. Lin, M. E. McCurrach, D. Beach, and S. W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602.
47. Srinivasan, A., K. W. Peden, and J. M. Pipas. 1989. The large tumor antigen of simian virus 40 encodes at least two distinct transforming functions. J. Virol. 63:5459-5463.
48. Tomkinson, B., E. Robertson, and E. Kieff. 1993. Epslein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J. Virol. 67:2014-2025.
49. Wang, D., D. Liebowitz, and E. Kieff. 1985. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell 43:831-840.
50. Watanabe, S., T. Kanda, and K. Yoshiike. 1989. Human papillomavirus type 16 transformation of primary human embryonic fibroblasts requires expression of open reading frames E6 and E7. J. Virol. 63:965-969.
51. Wolfel, T., M. Hauer, J. Schneider, M. Serrano, C. Wolfel, E. Klehmann-Hieb, E. De Plaen, T. Hankeln, K. H. Meyer zum Buschenfelde, and D. Beach. 1995. A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science 269:1281-1284.
52. Yew, P. R., and A. J. Berk. 1992. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 357: 82-85.
53. Zhu, J., P. W. Rice, L. Gorsch, M. Abate, and C. N. Cole. 1992. Transformation of a continuous rat embryo fibroblast cell line requires three separate domains of simian virus 40 large T antigen. J. Virol. 66:2780-2791.