The Epstein-Barr virus nuclear antigen 2 (EBNA2), a protein required for B lymphocyte immortalization, induces the synthesis of type I interferon in Burkitt's lymphoma cell lines

Biological Chemistry

Volumn 380, Issue 2, 1999, Pages 213-221

  Kanda, Kayoko ^a,c   Kempkes, Bettina ^b   Bornkamm, Georg W ^b   Von Gabain, Alexander ^a   Decker, Thomas ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

B lymphocytes; Cellular proliferation; Cytokine; Gene regulation; Signal transduction

Indexed keywords

BETA INTERFERON; CELL NUCLEUS ANTIGEN; EPSTEIN BARR VIRUS ANTIGEN; GAMMA INTERFERON; INTERFERON; MESSENGER RNA;

ARTICLE; B LYMPHOCYTE; BURKITT LYMPHOMA; CELL IMMORTALIZATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA TRANSFECTION; GENE INDUCTION; HUMAN; HUMAN CELL; LYMPHOMA CELL LINE; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

DNA VIRUSES; HUMAN HERPESVIRUS 4;

EID: 0033053122     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/bc.1999.029     Document Type: Article

References (56)

1. Abbot, S. D., Rowe, M., Cadwallader, K., Ricksten, A., Gordon, J., Wang, F., Rymo, L., and Rickinson, A.B. (1990). Epstein-Barr virus nuclear antigen 2 induces expression of the virus-encoded latent membrane protein. J. Virol. 64, 2126-2134.
2. Ackrill, A.M., Foster, G.R., Laxton, C.D., Flavell, D.M., Stark, G.R., and Kerr, I.M. (1991). Inhibition of the cellular response to interferons by products of the adenovirus type 5 E1A oncogene. Nucl. Acids. Res. 19, 4387-4393.
3. Adams, A., Lidin, B., Strander, H., and Cantell, K. (1975a). Spontaneous interferon production and Epstein-Barr virus expression in human lymphoid cell lines. J. Gen. Virol. 28, 219-223.
4. Adams, A., Strander, H., and Cantell, K. (1975b). Sensitivity of the Epstein-Barr virus transformed human lymphoid cell lines to interferon. J. Gen. Virol. 28, 207-217.
5. Adolf, G.R., Haas, O., Fischer, P., and Swetly, R (1982). Spontaneous production of alpha-and beta Interferon in human lymphoblastoid and lymphoma cell lines. Arch. Virol. 72, 169-178.
6. Aman, P., and von Gabain, A. (1990). An Epstein-Barr virus immortalization associated gene segment interferes specifically with the interferon-induced antiproliferative response in human B lymphoid cell lines. EMBO J. 9, 147-152.
7. Bhattacharya, S., Eckner, R., Grossman, S., Oldread, E., Arany, Z., D'Andrea, A., and Livingston, D. M. (1996). Cooperation of Stat2 and p300/CBP in signalling induced by interferon-alpha. Nature 383, 344-347.
8. Bromberg, J.F., Horvath, C.M., Wen, Z., Schreiber, R.D., and Darnell, J.E., Jr. (1996). Transcriptionally active Stat1 is required for the antiproliferative effects of both interferon alpha and interferon gamma. Proc. Natl. Acad. Sci. USA 93, 7673-7678.
9. Chomczynski, R, and Sacchi, N. (1987). Single step method of RNA isolation by acid guanidin thiocyanate-pheno-chloroform extraction. Anal. Biochem. 762, 156-159.
10. Cohen, J.I., Wang, F., and Kieff, E. (1991). Epstein-Barr virus nuclear protein 2 mutations define essential domains for transformation and transactivation. J. Virol. 65, 2545-2554.
11. Cordier, M., Calender, A., Billaud, M., Zimber, U., Rousselet, G., Pavlish, O., Banchereau, J., Tursz, T., Bornkamm, G., and Lenoir, G.M. (1990). Stable transfection of Epstein-Barr virus (EBV) nuclear antigen 2 in lymphoma cells containing the EBV P3HR1 genome induces expression of B-cell activation molecules CD21 and CD23. J. Virol. 64, 1002-1013.
12. Darnell, J.E., Jr., Kerr, I.M., and Stark, G.R. (1994). Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421.
13. Decker, T. (1997). The Molecular Biology of Type I Interferons (Interferon-α/β) (Gene Activation, Promoters, Proteins Induced)., A.T. Reder, ed. (New York: Marcel Dekker, Inc.).
14. Decker, T., Lew, D.J., and Darnell, J.E., Jr. (1991). Two distinct alpha-interferon-dependent signal transduction pathways may contribute to activation of transcription of the guanylate-binding protein gene. Mol. Cell. Biol. 11, 5147-5153.
15. Decker, T., Kovarik, P., and Meinke, A. (1997). Gas elements: a few nucleotides with a major impact on cytokine-induced gene expression. J. Interferon and Cytokine Res. 17, 121-134.
16. Durbin, J.E., Hackenmiller, R., Simon, M.C., and Levy, D.E. (1996). Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84, 443-450.
17. Fahraeus, R., Jansson, A., Ricksten, A., Sjoblom, A., and Rymo, L. (1990). Epstein-Barr virus-encoded nuclear antigen 2 activates the viral latent membrane protein promoter by modulating the activity of a negative regulatory element. Proc. Natl. Acad. Sci. USA 87, 7390-7394.
18. Fahraeus, R., Jansson, A., Sjoblom, A., Nilsson, T., Klein, G., and Rymo, L. (1993). Cell phenotype-dependent control of Epstein-Barr virus latent membrane protein 1 gene regulatory sequences. Virology 195, 71-80.
19. Garner, J.G., Hirsch, M.S., and Schooley, R.T. (1983). Prevention of Epstein-Barr virus-induced B cell outgrowth by interferon alpha. Infect. Immunity 43, 920-924.
20. Grossmann, S.R., Johannsen, E., Tong, X., Yalamanchili, R., and Kieff, E. (1994). The Epstein-Barr virus nuclear antigen 2 trans-activator is directed to response elements by the Jk recombination signal binding protein. Proc. Natl. Acad. Sci. USA 97, 7568-7572.
21. Gutch, M.J., and Reich, N.C. (1991). Repression of the interferon signal transduction pathway by the adenovirus E1A oncogene. Proc. Natl. Acad. Sci. USA 88, 7913-7917.
22. Hammerschmidt, W., and Sugden, B. (1989). Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes. Nature 340, 393-397.
23. Henkel, T., Ling, P.D., Hayward, S.D., and Peterson, M.G. (1994). Mediation of Epstein-Barr virus EBNA2 transactivation by recombination signal-binding protein J kappa. Science 265, 92-95.
24. Hiscott, J., Wong, A., Alper, D., and Xanthoudakis, S. (1988). Transactivation of type I interferon promoters by Simian virus 40 T antigen. Mol. Cell. Biol. 8, 3397-3405.
25. Horvath, C.M., and Darnell, J.E., Jr. (1996). The antiviral state induced by alpha interferon and gamma interferon requires transcriptionally active Stat1 protein. J. Virol. 70, 647-650.
26. Hsieh, J.J., and Hayward, S.D. (1995). Masking of the CBF1/ RBPJ kappa transcriptional repression domain by Epstein-Barr virus EBNA2. Science 268, 560-563.
27. Kanda, K., Decker, T., Aman, P., Wahlstrom, M., von Gabain, A., and Kallin, B. (1992). The EBNA2-related resistance towards alpha interferon (IFN-alpha) in Burkitt's lymphoma cells effects induction of IFN-induced genes but not the activation of transcription factor ISGF-3 [published erratum appears in Mol Cell Biol 1993 Mar;13(3):1981]. Mol. Cell. Biol. 12, 4930-4936.
28. Kastenbauer, S., Wedel, A., Frankenberger, M., Wirth, T., and Ziegler-Heitbrock, H.W.L. (1996). Analysis of promoter activity by PCR amplification of reporter gene m-RNA. Anal. Biochem. 233, 137-139.
29. Kempkes, B., Pawlita, M., Zimber Strobl, U., Eissner, G., Laux, G., and Bornkamm, G.W. (1995a). Epstein-Barr virus nuclear antigen 2-estrogen receptor fusion proteins transactivate viral and cellular genes and interact with RBP-J kappa in a conditional fashion. Virology 214, 675-679.
30. Kempkes, B., Spitkovsky, D., Jansen Durr, P., Ellwart, J.W., Kremmer, E., Delecluse, H.J., Rottenberger, C., Bornkamm, G.W., and Hammerschmidt, W. (1995b). B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2. EMBO J. 14, 88-96.
31. Kempkes, B., Zimber Strobl, U., Eissner, G., Pawlita, M., Falk, M., Hammerschmidt, W., and Bornkamm, G.W. (1996). Epstein-Barr virus nuclear antigen 2 (EBNA2)-oestrogen receptor fusion proteins complement the EBNA2-deficient Epstein-Barr virus strain P3HR1 in transformation of primary B cells but suppress growth of human B cell lymphoma lines. J. Gen. Virol 77, 227-237.
32. Kessler, D. S., Pine, R., Pfeffer, L.M., Levy, D.E., and Darnell, J.E., Jr. (1988). Cells resistant to interferon are defective in activation of a promoter-binding factor. EMBO J. 7, 3779-3783.
33. Kessler, D.S., Veals, S.A., Fu, X.Y., and Levy, D.E. (1990). Interferon-alpha regulates nuclear translocation and DNA-binding affinity of ISGF3, a multimeric transcriptional activator. Genes Dev. 4, 1753-1765.
34. Knutsen, J.C. (1990). The level of c-fgr RNA is increased by EBNA2, an Epstein-Barr virus gene required for B-cell immortalization. J. Virol 64, 2530-2536.
35. Larner, A.C., Chaudhuri, A., and Darnell J.E., Jr. (1986). Transcriptional induction by interferon, new protein(s) determine the extent and length of induction. J. Biol. Chem. 267, 453-459.
36. Lotz, M., Tsoukas, C.D., Fong, S., Carson, D.A., and Vaughan, J.H. (1985). Regulation of Epstein-Barr virus infection by recombinant interferons. Selected sensitivity to interferon-γ. Eur. J. Immunol. 15, 520-525.
37. Masucci, M.G., and Ernberg, I. (1994). Epstein-Barr virus: adaptation to a life within the immune system. Trends Microbiol. 2, 125-130.
38. McKendry, R., Pellegrini, S., Kerr, I.M., and Stark, G.R. (1994). Constitutive production of alpha and beta interferons in mutant human cell lines. J. Virol. 68, 4057-4062.
39. Meraz, M.A., White, J.M., Sheehan, K.C., Bach, E.A., Rodig, S.J., Dighe, A.S., Kaplan, D.H., Riley, J.K., Greenlund, A.C., Campbell, D., Carver Moore, K., DuBois, R.N., Clark, R., Aguet, M., and Schreiber, R.D. (1996). Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431-442.
40. Nielsch, U., Pine, R., Zimmer, S.G., and Babiss, L.E. (1992). Induced expression of the endogenous beta interferon gene in adenovirus type 5-transformed rat fibroblasts. J. Virol 66, 1884-1890.
41. Nonkwelo, C., Ruf, I.K., and Sample, J. (1997). Interferon-independent and induced regulation of Epstein-Barr virus EBNA-1 gene transcription in Burkitt lymphoma. J. Virol. 71, 6887-6897.
42. Nourbaksh, M., Hoffmann, K., and Hauser, H.-J. (1993). Interferon-beta promoters contain a DNA element that acts as a position-independent silencer on the NF-κB site. EMBO J. 12, 451-459.
43. Pickering, L.A., Kronenberg, L.H., and Stewart, L.E., II. (1980). Spontaneous production of human interferon. Proc. Natl. Acad. Sci. USA 77, 5938-5942.
44. Porter, A. C., Chernajovsky, Y., Dale, T. C., Gilbert, C. S., Stark, G. R., and Kerr, I. M. (1988). Interferon response element of the human gene6-16. EMBO J. 7, 85-92.
45. Schaefer, B.C., Paulson, E., Strominger, J.L., and Speck, S.H. (1997). Constitutive activation of Epstein-Barr virus (EBV) nuclear antigen 1 gene transcription by IRF1 and IRF2 during restricted EBVlatency. Mol. Cell. Biol. 17, 873-886.
46. Strehlow, I., and Decker, T. (1992). Transcriptional induction of IFN-gamma-responsive genes is modulated by DNA surrounding the interferon stimulation response element. Nucl. Acids Res. 20, 3865-3872.
47. Swaminathan, S., Huneycutt, B.S., Reiss, C.S., and Kieff, E. (1992). Epstein-Barr virus-encoded small RNAs (EBERs) do not modulate interferon effects in infected lymphocytes. J. Virol. 66, 5133-5136.
48. Tsang, S.F., Wang, F., Izumi, K.M., and Kieff, E. (1991). Delineation of the cis-acting element mediating EBNA-2 transactivation of latent membrane protein expression. J. Virol. 65, 6765-6771.
49. Waltzer, L., Logeat, F., Brou, C., Israel, A., Sergeant, A., and Manet, E. (1994). The human J kappa recombination signal sequence binding protein (RBP-J kappa) targets the Epstein-Barr virus EBNA2 protein to its DNA responsive elements. EMBO J. 13, 5633-5638.
50. Waltzer, L., Bourillot, P.Y., Sergeant, A., and Manet, E. (1995). RBP-J kappa repression activity is mediated by a co-repressor and antagonized by the Epstein-Barr virus transcription factor EBNA2. Nucl. Acids. Res 23, 4939-4945.
51. Wang, F., Gregory, C.D., Rowe, M., Rickinson, A.B., Wang, D., Birkenbach, M., Kikutani, H.T.K., and Kieff, E. (1987). Epstein-Barr virus nuclear antigen 2 specifically induces expression of the B-cell activation antigen CD23. Proc. Natl. Acad. Sci USA 84, 3452-3456.
52. Wang, F., Gregory, C., Sample, C., Rowe, M., Liebowitz, D., Murray, R., Rikinson, A., and Kieff, E. (1990). Epstein-Barr virus latent membrane protein (LMP1) and nuclear proteins 2 and 3C are effectors of phenotypic changes in B lymphocytes: EBNA-2 and LMP1 cooperatively induce CD23. J. Virol. 64, 2309-2318.
53. Wang, F., Kikutani, H., Tsang, S.F., Kishimoto, T., and Kieff, E. (1991). Epstein-Barr virus nuclear protein 2 transactivates a cis-acting CD23 DNA element. J. Virol. 65, 4101-4106.
54. Zhang, L., and Pagano, J.S. (1997). IRF-7, a new interferon regulatory factor associated with Epstein-Barr virus latency. Mol. Cell. Biol. 17, 5748-5757.
55. Zimber Strobl, U., Suentzenich, K. O., Laux, G., Eick, D., Cordier, M., Calender, A., Billaud, M., Lenoir, G. M., and Bornkamm, G. W. (1991). Epstein-Barr virus nuclear antigen 2 activates transcription of the terminal protein gene. J. Virol. 65, 415-423.
56. Zimber Strobl, U., Kremmer, E., Grasser, F., Marschall, G., Laux, G., and Bornkamm, G. W. (1993). The Epstein-Barr virus nuclear antigen 2 interacts with an EBNA2 responsive cis-element of the terminal protein 1 gene promoter. EMBO J. 72, 167-175.