Epstein-Barr virus exploits BSAP/Pax5 to achieve the B-cell specificity of its growth-transforming program

Journal of Virology

Volumn 81, Issue 18, 2007, Pages 10092-10100

  Tierney, Rosemary ^a   Nagra, Jasdeep ^a   Hutchings, Isabel ^a   Shannon Lowe, Claire ^a   Altmann, Markus ^b   Hammerschmidt, Wolfgang ^b   Rickinson, Alan ^a   Bell, Andrew ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR PAX5; PAX5 PROTEIN, HUMAN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; B LYMPHOCYTE; EPSTEIN BARR VIRUS; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSCRIPTION; IMMUNOPRECIPITATION; MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS GENOME; VIRUS RECOMBINANT; ANTIBODY SPECIFICITY; BINDING SITE; CELL CULTURE; EPITHELIUM CELL; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; PROMOTER REGION; VIROLOGY; VIRUS CELL TRANSFORMATION;

HUMAN HERPESVIRUS 4;

B-CELL-SPECIFIC ACTIVATOR PROTEIN; B-LYMPHOCYTES; BINDING SITES; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; EPITHELIAL CELLS; GENE DELETION; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; ORGAN SPECIFICITY; PROMOTER REGIONS (GENETICS); TRANSCRIPTION, GENETIC; VIRAL REGULATORY PROTEINS;

EID: 35348905543     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00358-07     Document Type: Article

References (45)

1. Adams, B., P. Dorfler, A. Aguzzi, Z. Kozmik, P. Urbanek, I. Maurer-Fogy, and M. Busslinger. 1992. Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS, and adult testis. Genes Dev. 6:1589-1607.
2. Alfieri, C., M. Birkenbach, and E. Kieff. 1991. Early events in Epstein-Barr virus infection of human B lymphocytes. Virology 181:595-608.
3. Allan, G. J., and D. T. Rowe. 1989. Size and stability of the Epstein-Barr virus major internal repeat (IR-1) in Burkitt's lymphoma and lymphoblastoid cell lines. Virology 173:489-498.
4. Altmann, M., and W. Hammerschmidt. 2005. Epstein-Barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis. PLoS Biol. 3:e404.
5. Altmann, M., D. Pich, R. Ruiss, J. Wang, B. Sugden, and W. Hammerschmidt. 2006. Transcriptional activation by EBV nuclear antigen 1 is essential for the expression of EBV's transforming genes. Proc. Natl. Acad. Sci. USA 103:14188-14193.
6. Bell, A., J. Skinner, H. Kirby, and A. Rickinson. 1998. Characterisation of regulatory sequences at the Epstein-Barr virus BamHI W promoter. Virology 252:149-161.
7. Bell, A. I., K. Groves, G. L. Kelly, D. Croom-Carter, E. Hui, A. T. Chan, and A. B. Rickinson. 2006. Analysis of Epstein-Barr virus latent gene expression in endemic Burkitt's lymphoma and nasopharyngeal carcinoma tumour cells by using quantitative real-time PCR assays. J. Gen. Virol. 87:2885-2890.
8. Chau, C. M., and P. M. Lieberman. 2004. Dynamic chromatin boundaries delineate a latency control region of Epstein-Barr virus. J. Virol. 78:12308-12319.
9. Crawford, D. H., and I. Ando. 1986. EB virus induction is associated with B-cell maturation. Immunology 59:405-409.
10. Delecluse, H. J., S. Bartnizke, W. Hammerschmidt, J. Bullerdiek, and G. W. Bornkamm. 1993. Episomal and integrated copies of Epstein-Barr virus coexist in Burkitt lymphoma cell lines. J. Virol. 67:1292-1299.
11. Delecluse, H. J., T. Hilsendegen, D. Pich, R. Zeidler, and W. Hammerschmidt. 1998. Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc. Natl. Acad. Sci. USA 95:8245-8250.
12. Evans, T. J., P. J. Farrell, and S. Swaminathan. 1996. Molecular genetic analysis of Epstein-Barr virus Cp promoter function. J. Virol. 70:1695-1705.
13. Fu, S. M., J. N. Hurley, J. M. McCune, H. G. Kunkel, and R. A. Good. 1980. Pre-B cells and other possible precursor lymphoid cell lines derived from patients with X-linked agammaglobulinemia. J. Exp. Med. 152:1519-1526.
14. Fujiwara, S., and Y. Ono. 1995. Isolation of Epstein-Barr virus-infected clones of the human T-cell line MT-2: use of recombinant viruses with a positive selection marker. J. Virol. 69:3900-3903.
15. Hansson, M., K. Falk, and I. Ernberg. 1983. Epstein-Barr virus transformation of human pre-B cells. J. Exp. Med. 158:616.
16. Imai, S., J. Nishikawa, and K. Takada. 1998. Cell-to-cell contact as an efficient mode of Epstein-Barr virus infection of diverse human epithelial cells. J. Virol. 72:4371-4378.
17. Isobe, Y., K. Sugimoto, L. Yang, K. Tamayose, M. Egashira, T. Kaneko, K. Takada, and K. Oshimi. 2004. Epstein-Barr virus infection of human natural killer cell lines and peripheral blood natural killer cells. Cancer Res. 64: 2167-2174.
18. Jansson, A., M. Masucci, and L. Rymo. 1992. Methylation of discrete sites within the enhancer region regulates the activity of the Epstein-Barr virus BamHI W promoter in Burkitt lymphoma lines. J. Virol. 66:62-69.
19. Joseph, A. M., G. J. Babcock, and D. A. Thorley-Lawson. 2000. Cells expressing the Epstein-Barr virus growth program are present in and restricted to the naive B-cell subset of healthy tonsils. J. Virol. 74:9964-9971.
20. Katamine, S., M. Otsu, K. Tada, S. Tsuchiya, T. Sato, N. Ishida, T. Honjo, and Y. Ono. 1984. Epstein-Barr virus transforms precursor B cells even before immunoglobulin gene rearrangements. Nature 309:369-372.
21. Kempkes, B., D. Pich, R. Zeidler, and W. Hammerschmidt. 1995. Immortalization of human primary B lymphocytes in vitro with DNA. Proc. Natl. Acad. Sci. USA 92:5875-5879.
22. Kirby, H., A. Rickinson, and A. Bell. 2000. The activity of the Epstein-Barr virus BamHI W promoter in B cells is dependent on the binding of CREB/ ATF factors. J. Gen. Virol. 81:1057-1066.
23. Knox, P. G., Q. X. Li, A. B. Rickinson, and L. S. Young. 1996. In vitro production of stable Epstein-Barr virus-positive epithelial cell clones which resemble the virus: cell interaction observed in nasopharyngeal carcinoma. Virology 215:40-50.
24. Kozmik, Z., S. Wang, P. Dorfler, B. Adams, and M. Busslinger. 1992. The promoter of the CD19 gene is a target for the B-cell-specific transcription factor BSAP. Mol. Cell. Biol. 12:2662-2672.
25. Kurth, J., T. Spieker, J. Wustrow, G. J. Strickler, L. M. Hansmann, K. Rajewsky, and R. Kuppers. 2000. EBV-infected B cells in infectious mononucleosis: viral strategies for spreading in the B cell compartment and establishing latency. Immunity 13:485-495.
26. Li, Q. X., L. S. Young, G. Niedobitek, C. W. Dawson, M. Birkenbach, F. Wang, and A. B. Rickinson. 1992. Epstein-Barr virus infection and replication in a human epithelial cell system. Nature 356:347-350.
27. Matthias, P., and A. G. Rolink. 2005. Transcriptional networks in developing and mature B cells. Nat. Rev. Immunol. 5:497-508.
28. McCann, E. M., G. L. Kelly, A. B. Rickinson, and A. I. Bell. 2001. Genetic analysis of the Epstein-Barr virus-coded leader protein EBNA-LP as a coactivator of EBNA2 function. J. Gen. Virol. 82:3067-3079.
29. Peng, R., J. Tan, and P. D. Ling. 2000. Conserved regions in the Epstein-Barr virus leader protein define distinct domains required for nuclear localization and transcriptional cooperation with EBNA2. J. Virol. 74:9953-9963.
30. Puglielli, M. T., N. Desai, and S. H. Speck. 1997. Regulation of EBNA gene transcription in lymphoblastoid cell lines: characterization of sequences downstream of BCR2 (Cp). J. Virol. 71:120-128.
31. Rickinson, A. B., and E. Kieff. 2001. Epstein-Barr virus, p. 2575-2627. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
32. Ricksten, A., A. Olsson, T. Andersson, and L. Rymo. 1988. The 5′ flanking region of the gene for the Epstein-Barr virus-encoded nuclear antigen 2 contains a cell type specific cis-acting regulatory element that activates transcription in transfected B cells. Nucleic Acids Res. 16:8391.
33. Rivailler, P., H. Jiang, Y. G. Cho, C. Quink, and F. Wang. 2002. Complete nucleotide sequence of the rhesus lymphocryptovirus: genetic validation for an Epstein-Barr virus animal model. J. Virol. 76:421-426.
34. Rochford, R., M. V. Hobbs, J. L. Garnier, N. R. Cooper, and M. J. Cannon. 1993. Plasmacytoid differentiation of Epstein-Barr virus-transformed B cells in vivo is associated with reduced expression of viral latent genes. Proc. Natl. Acad. Sci. USA 90:352-356.
35. Sample, J., M. Hummel, D. Braun, M. Birkenbach, and E. Kieff. 1986. Nucleotide sequences of mRNAs encoding Epstein-Barr virus nuclear proteins: a probable transcriptional initiation site. Proc. Natl. Acad. Sci. USA 83:5096-5100.
36. Shannon-Lowe, C., G. Baldwin, R. Feederle, A. Bell, A. Rickinson, and H. J. Delecluse. 2005. Epstein-Barr virus-induced B-cell transformation: quantitating events from virus binding to cell outgrowth. J. Gen. Virol. 86:3009-3019.
37. Shannon-Lowe, C. D., B. Neuhierl, G. Baldwin, A. B. Rickinson, and H. J. Delecluse. 2006. Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells. Proc. Natl. Acad. Sci. USA 103:7065-7070.
38. Speck, S. H., A. Pfitzner, and J. L. Strominger. 1986. An Epstein-Barr virus transcript from a latently infected, growth-transformed B-cell line encodes a highly repetitive polypeptide. Proc. Natl. Acad. Sci. USA 83:9298-9302.
39. Sugano, N., W. P. Chen, M. L. Roberts, and N. R. Cooper. 1997. Epstein-Barr virus binding to CD21 activates the initial viral promoter via NF-kappa B induction. J. Exp. Med. 186:731-737.
40. Thorley-Lawson, D. A. 2001. Epstein-Barr virus: exploiting the immune system. Nat. Rev. Immunol. 1:75-82.
41. Tierney, R., H. Kirby, J. Nagra, A. Rickinson, and A. Bell. 2000. The Epstein-Barr virus promoter initiating B-cell transformation is activated by RFX proteins and the B-cell-specific activator protein BSAP/Pax5. J. Virol. 74: 10458-10467.
42. Woisetschlaeger, M., C. N. Yandava, L. A. Furmanski, J. L. Strominger, and S. H. Speck. 1990. Promoter switching in Epstein-Barr virus during the initial stages of infection of B lymphocytes. Proc. Natl. Acad. Sci. USA 87:1725-1729.
43. Yoo, L. I., J. Woloszynek, S. Templeton, and S. H. Speck. 2002. Deletion of Epstein-Barr virus regulatory sequences upstream of the EBNA gene promoter Wp1 is unfavorable for B-cell immortalization. J. Virol. 76:11763-11769.
44. Yoshiyama, H., S. Imai, N. Shimizu, and K. Takada. 1997. Epstein-Barr virus infection of human gastric carcinoma cells: implication of the existence of a new virus receptor different from CD21. J. Virol. 71:5688-5691.
45. Yoshiyama, H., N. Shimizu, and K. Takada. 1995. Persistent Epstein-Barr virus infection in a human T-cell line: unique program of latent virus expression. EMBO J. 14:3706-3711.