Identification of functional differences between prototype Epstein-Barr virus-encoded LMP1 and a nasopharyngeal carcinoma-derived LMP1 in human epithelial cells

Virology

Volumn 272, Issue 1, 2000, Pages 204-217

  Dawson, Christopher W ^a   Eliopoulos, Aristides G ^a   Blake, Sarah M ^a   Barker, Rachel ^a   Young, Lawrence S ^a  

^a UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; HERMES ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA; VIRUS ENVELOPE PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL PROTECTION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; NASOPHARYNX CARCINOMA; PRIORITY JOURNAL;

ALPHAVIRUS; DNA VIRUSES; HUMAN HERPESVIRUS 4;

EID: 0034691192     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.2000.0344     Document Type: Article

References (65)

1. Allen-Hoffmann B. L., Schlosser S. J., Rhim J. S. Use of RHEK-1 immortalized human keratinocytes for detection of induced mutation at the locus. Int. J. Oncol. 3:1993;619-625.
2. Chen M. L, Tsai C. N., Liang C. L., Shu C. H., Huang C. R., Sulitzeanu D., Liu S. T., Chang Y. S. Cloning and characterization of the latent membrane protein (LMP) of a specific Epstein-Barr virus variant derived from the nasopharyngeal carcinoma in the Taiwanese population. Oncogene. 7:1992;2131-2140.
3. Chen W. G., Chen Y. Y., Bacchi M. M., Bacchi C. E., Alvarenga M., Weiss L. M. Genotyping of Epstein-Barr virus in Brazilian Burkitt's lymphoma and reactive lymphoid tissue-type A with a high prevalence of deletions within the latent membrane protein gene. Am. J. Pathol. 148:1996;17-23.
4. Chen W. X., Bowden G. T. Activation of p38 MAP kinase and ERK are required for ultraviolet-B induced c-fos expression in human keratinocytes. Oncogene. 18:1999;7469-7476.
5. Cheung S. T., Leung S. F., Lo K. W., Chiu K. W., Tam J. S. L., Fok T. F., Johnson P. J., Lee J. C. K., Huang D. P. Specific latent membrane protein 1 gene sequences in type 1 and type 2 Epstein-Barr virus from nasopharyngeal carcinoma in Hong Kong. Int. J. Cancer. 76:1998;399-406.
6. Dawson C. W., Dawson J., Jones R., Ward K., Young L. S. Functional differences between BHRF1, the Epstein-Barr virus-encoded Bcl-2 homologue, and Bcl-2 in human epithelial cells. J. Virol. 72:1998;9016-9024.
7. Dawson C. W., Eliopoulos A. G., Dawson J., Young L. S. BHRF1, a viral homologue of the Bcl-2 oncogene, disturbs epithelial cell differentiation. Oncogene. 9:1995;69-77.
8. Dawson C. W., Rickinson A. B., Young L. S. Epstein-Barr virus latent membrane protein inhibits human epithelial cell differentiation. Nature. 344:1990;777-780.
9. Eliopoulos A. G., Blake S. M. S., Floettmann J. E., Rowe M., Young L. S. Epstein-Barr virus-encoded latent membrane protein 1 activates the JNK pathway through its extreme C-terminus via a mechanism involving TRADD and TRAF2. J. Virol. 73:1998;1023-1035.
10. Eliopoulos A. G., Stack M., Dawson C. W., Kaye K. M., Hodgkin L., Sihota S., Rowe M., Young L. S. Epstein-Barr virus-encoded LMP1 and CD40 mediate IL-6 production in epithelial cells via an NF-κB pathway involving TNF-receptor-associated factors. Oncogene. 14:1997;2899-2916.
11. Eliopoulos A. G, Young L. S. Activation of the c-jun N-terminal kinase (JNK) pathway by the Epstein-Barr virus-encoded latent membrane protein 1 (LMP1). Oncogene. 16:1998;1731-1742.
12. Eliopoulos A. G., Gallagher N. J., Blake S. M. S., Dawson C. W., Young L. S. Activation of the p38 mitogen-activated protein kinase pathway by Epstein-Barr virus-encoded latent membrane protein 1 coregulates interleukin-6 and interleukin-8 production. J. Biol. Chem. 274:1999;16085-16096.
13. Fahraeus R., Rymo L., Rhim J. S., Klein G. Morphological transformation of human keratinocytes expressing the LMP gene of Epstein-Barr virus. Nature. 345:1990;447-449.
14. Floettmann J. E., Eliopoulos A. G., Jones M., Young L. S., Rowe M. Epstein-Barr virus latent membrane protein-1 (LMP1) signalling is distinct from CD40 and involves physical cooperation of its two C- terminus functional regions. Oncogene. 17:1998;2383-2392.
15. Gires O., Kohlhuber F., Kilger E., Baumann M., Kieser A., Kaiser C., Zeidler R., Scheffer B., Ueffing M., Hammerschmidt W. Latent membrane protein 1 of Epstein-Barr virus interacts with JAK3 and activates STAT proteins. EMBO J. 18:1999;3064-3073.
16. Grimaldi J. C., Torres R., Kozak C. A., Chang R., Clark E. A., Howard M., Cockayne D. A. Genomic structure and chromosomal mapping of the murine CD40 gene. J. Immunol. 149:1991;3921-3926.
17. Henderson S., Rowe M., Gregory C., Croom-Carter D., Wang F., Longnecker R., Kieff E., Rickinson A. B. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell. 65:1991;1107-1115.
18. Hu L. F., Chen F., Zheng X., Ernberg I., CAO S. L., Christensson B., Klein G., Winberg G. Clonability and tumorigenicity of human epithelial cells expressing the EBV-encoded membrane-protein LMP1. Oncogene. 8:1993;1575-1583.
19. Hu L. F., Zabarovsky E. R., Chen F., CAO S. L., Ernberg I., Klein G., Winberg G. Isolation and sequencing of the Epstein-Barr virus BNLF-1 gene (LMP1) from a Chinese nasopharyngeal carcinoma. J. Gen. Virol. 72:1991;2399-2409.
20. Hu Y., Baud V., Delhase M., Zhang P., Deerinck T., Ellisman M., Johnson R. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKα subunit of the IκB kinase. Science. 284:1999;318-320.
21. Huen D. S., Henderson S. A., Croom-Carter D., Rowe M. The Epstein-Barr virus latent membrane protein 1 (LMP1) mediates activation of NF-κB and cell-surface phenotype via 2 effector regions in its carboxy terminal cytoplasmic domain. Oncogene. 10:1995;549-560.
22. Izumi K. M., Kieff E. D. The Epstein-Barr virus oncogene product latent membrane protein 1 engages the tumour necrosis factor receptor-associated death domain protein to mediate B lymphocyte growth transformation and activate NF-κB. Proc. Natl. Acad. Sci. USA. 94:1997a;12592-12597.
23. Izumi K. M., Kieff E. D. The Epstein-Barr virus LMP1 amino acid sequence that engages tumour necrosis factors is critical for primary B lymphocyte growth transformation. Proc. Natl. Acad Sci. USA. 94:1997b;1447-1452.
24. Johnson R. J., Stack M., Hazlewood S. A., Jones M., Blackmore C. G., Hu L. F., Rowe M. The 30-base-pair deletion in Chinese variants of the Epstein-Barr virus LMP1 gene is not the major effector of functional differences between variant LMP1 genes in human lymphocytes. J. Virol. 72:1998;4038-4048.
25. Kaye K. M., Izumi K. M., Kieff E. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA. 90:1993;9150-9154.
26. Kaye K. M., Izumi K. M., Li H., Johannsen E., Davidson D., Longnecker R., Kieff E. An Epstein-Barr virus that expresses only the first 231 LMP1 amino acids efficiently initiates primary B-lymphocyte growth transformation. J. Virol. 73:1999;10525-10530.
27. Kaye K. M., Izumi K. M., Mosialos G., Kieff E. The Epstein-Barr virus LMP-1 cytoplasmic carboxy terminus is essential for B-lymphocyte transformation: Fibroblast cocultivation complements a critical function within the last 155 residues. J. Virol. 69:1995;675-683.
28. Khanim F., Yao Q-Y., Niedobitek G., Sihota S., Rickinson A. B., Young L. S. Analysis of Epstein-Barr virus gene polymorphisms in normal donors and in virus-associated tumors from different geographical locations. Blood. 88:1996;3491-3501.
29. Kieff E. Epstein-Barr virus and its replication. Fields B. N., Knipe D. N., Howley P. M. Fields' Virology. 1996;2343-2396 Lippincott-Raven Publishers, Philadelphia.
30. Kieser A., Kilger E., Gires O., Ueffing M., Kolch W., Hammerschmidt W. Epstein-Barr virus latent membrane protein-1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade. EMBO J. 16:1997;6478-6485.
31. Knecht H., Bachmann E., Brousset P., Rothenberger S., Einsele H., Lestou V. S., Delsol G., Bachmann F., Ambros P. F., Odermatt B. F. Mutational hot-spots within the carboxy-terminal region of the LMP1 oncogene of Epstein-Barr virus are frequent in lymphoproliferative disorders. Oncogene. 10:1995;523-528.
32. Laherty C. D., Hu H. M., Opipari A. W., Wang F., Dixit V. M. The Epstein-Barr virus LMP1-gene product induces A20-zinc finger protein expression by activating nuclear factor-kappa-B. J. Biol. Chem. 267:1992;24157-24160.
33. Lee M. S., Yang J. H., Salehi Z., Arnstein P., Chen L. S., Jay G., Rhim J. S. Neoplastic transformation of a human keratinocyte cell-line by the v-Fos oncogene. Oncogene. 8:1993;387-393.
34. Li S.-N., Chang Y.-S., Liu S.-H. Effect of a 10-amino-acid deletion on the oncogenic activity of latent membrane protein-1 of Epstein-Barr virus. Oncogene. 12:1996;2129-2135.
35. Li Q., D. Van Antwerp D., Mercurio F., Lee K-F., Verma I. M. Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science. 284:1999;321-325.
36. May M. J., Ghosh S. IκB kinases: Kinsmen with different crafts. Science. 284:1999;271-272.
37. Miller W. E., Cheshire J. L., Raab-Traub N. Interaction of tumor necrosis factor receptor-associated factor signaling proteins with the latent membrane protein 1 PXQXT motif is essential for induction of epidermal growth factor receptor expression. Mol. Cell. Biol. 18:1998a;2835-2844.
38. Miller W. E, Cheshire J. L., Baldwin A. S., Raab-Traub N. The NPC derived C15 LMP1 protein confers enhanced activation of NF-κB and induction of the EGFR in epithelial cells. Oncogene. 16:1998b;1869-1877.
39. Miller W. E., Earp H. S., Raab-Traub N. The Epstein-Barr virus latent membrane protein 1 induces expression of the epidermal growth factor receptor. J. Virol. 69:1995;4390-4398.
40. Miller W. E., Edwards R. H., Walling D. M., Raab-Traub N. Sequence variation in the Epstein-Barr virus latent membrane protein-1. J. Gen. Virol. 75:1994;2729-2740.
41. Miller W. E., Mosialos G., Kieff E., Raab-Traub N. Epstein-Barr virus LMP1 induction of the epidermal growth factor receptor is mediated through a TRAF signaling pathway distinct from NF-κB activation. J. Virol. 71:1997;586-594.
42. Mosialos G., Birkenbach M., Yalamanchili R., VanArsdale T., Ware C., Kieff E. The Epstein-Barr virus transforming protein LMP 1 engages signalling proteins for the tumour necrosis factor receptor family. Cell. 80:1995;389-399.
43. Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65:1983;55-63.
44. Osato T., Imai S. Epstein-Barr virus and gastric carcinoma. Semin. Cancer. Biol. 7:1996;175-182.
45. Parkinson E. K., Grabham P., Emmerson A. A sub-population of cultured human keratinocytes which is resistant to the induction of terminal differentiation-related changes by phorbol, 12-myristate, 13-acetate: Evidence for an increase in the resistant population following transformation. Carcinogenesis. 4:1983;857-861.
46. Raab-Traub N. Pathogenesis of Epstein-Barr virus and its associated malignancies. Semin. Virol. 7:1996;315-323.
47. Razzzaque A., Williams O., Wang J. H., Rhim J. S. Neoplastic transformation of immortalized human epidermal keratinocytes by 2 HHV-6 DNA clones. Virology. 195:1993;113-120.
48. Rheinwald J. G., Beckett M. A. Tumourigenic keratinocyte lines requiring anchorage and fibroblast support cultured from human squamous cell carcinomas. Cancer Res. 41:1981;1657-1663.
49. Rickinson A. B., Kieff E. Epstein-Barr virus. Fields B. N., Knipe D. N., Howley P. M. Fields' Virology. 1996;2397-2446 Lippincott-Raven Publishers, Philadelphia.
50. Rowe M., Evans H. S., Young L. S., Hennessy K., Kieff E., Rickinson A. B. 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. 68:1987;1575-1586.
51. Rowe M., Pengpilon M., Huen D. S., Hardy R., Croom-Carter D., Lundgren E., Rickinson A. B. Up-regulation of Bcl-2 by the Epstein-Barr virus latent membrane protein LMP1: A B-cell-specific response that is delayed relative to NF-κB activation and to induction of cell-surface markers. J. Virol. 68:1994;5602-5612.
52. Sample J., Kieff E. F., Kieff E. D. Epstein-Barr virus type-1 and type-2 have nearly identical LMP1 transforming genes. J. Gen. Virol. 75:1994;2741-2746.
53. Seitz C. S, Lin Q., Deng H., Khavari P. A. Alterations in NF-κB function in transgenic epithelial tissue demonstrate a growth inhibitory role for NF-κB. Proc. Natl. Acad. Sci. USA. 95:1998;2307-2312.
54. Sung N. S., Edwards R. H., Seillier-Moiseiwitsch F., Perkins A. G., Zeng Y., Raab-Traub N. Epstein-Barr virus strain variation in nasopharyngeal carcinoma from the endemic and non-endemic regions of China. Int. J. Cancer. 76:1998;207-215.
55. Sylla B. S., Hung S. C., Davidson D. M., Hatzivassiliou E., Malinin N. L., Wallach D., Gilmore T. D., Kieff E., Mosialos G. Epstein-Barr virus-transforming protein latent infection membrane protein 1 activates transcription factor NF-κB through a pathway that includes the NF-κB-inducing kinase and the IκB kinases IKKα and IKKβ Proc. Natl. Acad. Sci. USA. 95:1998;10106-10111.
56. Takeda K., Takeuchi O., Tsujimura T., Itami S., Adachi O., Kawai T., Sanjo H., Yoshikawa K., Terada N., Akira S. Limb and skeletal abnormalities in mice lacking IKKα Science. 284:1999;313-316.
57. Voraberger G., Schafe R., Stratowa C. Cloning of the human gene for intercellular-adhesion molecule-1 and analysis of its 5′-regulatory region: Induction by cytokines and phorbol ester. J. Immunol. 147:1991;2777-2786.
58. Walling D. M., Shebib N, Weaver S. C., Nichols C. M., Flaitz C. M., Webster-Cyriaque J. The molecular epidemiology and evolution of Epstein-Barr virus: Sequence variation and genetic recombination in the latent membrane protein-1 gene. J. Infect. Dis. 179:1999;763-774.
59. Wang D, Liebowitz D., Wang F., Gregory C., Rickinson A. B., Larson R., Springer T., Kieff E. Epstein-Barr virus latent infection membrane protein alters the human B lymphocyte phenotype: Deletion of the amino terminus abolishes activity. J. Virol. 62:1988;4173-4184.
60. Wang F., Gregory C., Sample C., Rowe M., Liebowitz D., Murray R., Rickinson A. B., Kieff E. Epstein-Barr virus latent membrane protein (LMP1) and nuclear protein 2 and protein 3C are effectors of phenotypic changes in B lymphocytes: EBNA-2 and LMP1 cooperatively induced CD23. J. Virol. 64:1990;2309-2318.
61. Wang S., Rowe M., Lundgren E. Expression of the Epstein Barr virus transforming protein LMP1 causes a rapid and transient stimulation of the Bcl-2 homologue Mcl-1 levels in B-cell lines. Cancer Res. 56:1996;4610-4613.
62. Welter J. F., Eckert R. L. Differential expression of the Fos and Jun family members c-Fos, FosB, Fra-1, Fra-2, c-Jun, JunB, and JunD during human epidermal keratinocyte differentiation. Oncogene. 11:1995;2681-2687.
63. Wilson J. B., Weinberg W., .Johnson R., Yuspa S., Levine A. J. Expression of the BNLF1-1 oncogene of Epstein-Barr virus in the skin of transgenic mice induces hyperplasia and aberrant expression of keratin-6. Cell. 61:1990;1315-1327.
64. Yang J. H., Thraves P., Dritschilo A., Rhim J. S. Neoplastic transformation of immortalized human keratinocytes by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. Cancer Res. 52:1992;3478-3482.
65. Zheng X., Yuan F., Hu L. F., Klein G., Christensson B. Effect of B-lymphocyte- and NPC-derived EBV-LMP1 gene expression on in vitro growth and differentiation of human epithelial cells. Int. J. Cancer. 57:1994;747-753.