EBNA-3B- and EBNA-3C-regulated cellular genes in Epstein-Barr virus-immortalized lymphoblastoid cell lines

Journal of Virology

Volumn 80, Issue 20, 2006, Pages 10139-10150

  Chen, Adrienne ^a   Zhao, Bo ^a   Kieff, Elliott ^a   Aster, Jon C ^a   Wang, Fred ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b CHANNING LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN; CHEMOKINE RECEPTOR CXCR4; EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS NUCLEAR ANTIGEN 3B; EPSTEIN BARR VIRUS NUCLEAR ANTIGEN 3C; FILAMIN A; GAMMA SECRETASE; JAGGED1; KANAMYCIN; NEUROCALCIN; NOTCH RECEPTOR; OXIDOREDUCTASE; PYRIDOXAL KINASE; RNA POLYMERASE II; SULFOTRANSFERASE; UNCLASSIFIED DRUG; VIRUS RNA;

ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CELL IMMORTALIZATION; CELL MIGRATION; CONTROLLED STUDY; EPSTEIN BARR VIRUS; FLOW CYTOMETRY; GENE EXPRESSION; HOST CELL; IN VIVO STUDY; LATENT VIRUS INFECTION; LYMPHOBLASTOID CELL LINE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; VIRUS REACTIVATION; WESTERN BLOTTING;

ANTIGENS, VIRAL; CALCIUM-BINDING PROTEINS; CELL LINE; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HERPESVIRUS 4, HUMAN; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOCYTES; MEMBRANE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, CXCR4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA;

ANIMALIA; CERCOPITHECINE HERPESVIRUS 15; HUMAN HERPESVIRUS 4;

EID: 33749491637     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00854-06     Document Type: Article

References (56)

1. Babcock, G. J., L. L. Decker, M. Volk, and D. A. Thorley-Lawson. 1998. EBV persistence in memory B cells in vivo. Immunity 9:395-404.
2. Chen, A., M. Divisconte, X. Jiang, C. Quink, and F. Wang. 2005. Epstein-Barr virus with the latent infection nuclear antigen 3B completely deleted is still competent for B-cell growth transformation in vitro. J. Virol. 79:4506-4509.
3. Cludts, I., and P. J. Farrell. 1998. Multiple functions within the Epstein-Barr virus EBNA-3A protein. 72:1862-1869.
4. Cotter, M. A., II, and E. S. Robertson. 2000. Modulation of histone acetyltransferase activity through interaction of Epstein-Barr nuclear antigen 3C with prothymosin alpha. Mol. Cell. Biol. 20:5722-5735.
5. D'Apuzzo, M., A. Rolink, M. Loetscher, J. A. Hoxie, I. Clark-Lewis, F. Melchers, M. Baggiolini, and B. Moser. 1997. The chemokine SDF-1, stromal cell-derived factor 1, attracts early stage B cell precursors via the chemokine receptor CXCR4. Eur. J. Immunol. 27:1788-1793.
6. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
7. Ehlin-Henriksson, B., F. Mowafi, G. Klein, and A. Nilsson. 2006. Epstein-Barr virus infection negatively impacts the CXCR4-dependent migration of tonsillar B cells. Immunology 117:379-385.
8. Fedyk, E. R., D. H. Ryyan, I. Ritterman, and T. A. Springer. 1999. Maturation decreases responsiveness of human hone marrow B lineage cells to stromal-derived factor 1 (SDF-1). J. Leukoc. Biol. 66:667-673.
9. Finke, J., M. Rowe, B. Kallin, I. Ernberg, A. Rosen, J. Dillner, and G. Klein. 1987. Monoclonal and polyclonal antibodies against Epstein-Barr virus nuclear antigen 5 (EBNA-5) detect multiple protein species in Burkitt's lymphoma and lymphoblastoid cell lines. J. Virol. 61:3870-3878.
10. Gavioli, R., P. O. De Campos-Lima, M. G. Kurilla, E. Kieff, G. Klein, and M. G. Masucci. 1992. Recognition of the Epstein-Barr virus-encoded nuclear antigens EBNA-4 and EBNA-6 by HLA-A11-restricted cytotoxic T lymphocytes: implications for down-regulation of HLA-A11 in Burkitt lymphoma. Proc. Natl. Acad. Sci. USA 89:5862-5866.
11. Gordadze, A. V., R. Peng, J. Tan, G. Liu, R. Sutton, B. Kempkes, G. W. Bornkamm, and P. D. Ling. 2001. Notch11C partially replaces EBNA2 function in B cells immortalized by Epstein-Barr virus. J. Virol. 75:5899-5912.
12. Grillot-Courvalin, C., S. Goussard, F. Huetz, D. M. Ojcius, and P. Courvalin. 1998. Functional gene transfer from intracellular bacteria to mammalian cells. Nat. Biotechnol. 16:862-866.
13. Grossman, S. R., E. Johannsen, X. Tong, R. Yalamanchili, and E. Kieff. 1994. The Epstein-Barr virus nuclear antigen 2 transactivator is directed to response elements by the J kappa recombination signal binding protein. Proc. Natl. Acad. Sci. USA 91:7568-7572.
14. Henkel, T., P. D. Ling, S. D. Hayward, und M. G. Peterson. 1994. Mediation of Epstein-Barr virus EBNA2 transactivation by recombination signal-binding protein J kappa. Science 265:92-95.
15. Hickabottom, M., G. A. Parker, P. Freemont, T. Crook, and M. J. Allday. 2002. Two nonconsensus sites in the Epstein-Barr virus oncoprotein EBNA3A cooperate to bind the co-repressor carboxyl-terminal-binding protein (CtBP). J. Biol. Chem. 277:47197-47204.
16. Honczarenko, M., R. S. Douglas, C. Mathias, B. Lee, M. Z. Ratajczak, and L. E. Silberstein. 1999. SDF-1 responsiveness does not correlate with CXCR4 expression levels of developing human bone marrow B cells. Blood 94:2990-2998.
17. Hsieb, J. J., T. Henkel, P. Salmon, E. Robey, M. G. Peterson, and S. D. Hayward. 1996. Truncated mammalian Notch1 activates CBFI/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2. Mol. Cell. Biol. 16:952-959.
18. Jiang, H., Y. G. Cho, and F. Wang. 2000. Structural, functional, and genetic comparisons of Epstein-Barr virus nuclear antigen 3A, 3B, and 3C homologues encoded by the rhesus lymphocryptovirus. J. Virol. 74:5921-5932.
19. Khanna, R., S. R. Burrows, M. G. Kurilla, C. A. Jacob, I. S. Misko, T. B. Sculley, E. Kieff, and D. J. Moss. 1992. Localization of Epstein-Barr virus cytotoxic T cell epitopes using recombinant vaccinia: implications for vaccine development. J. Exp. Med. 176:169-176.
20. Kienzle, N., D. Young, S. L. Silins, and T. B. Sculley. 1996. Induction of pleckstrin by the Epstein-Barr virus nuclear antigen 3 family. Virology 224:167-174.
21. King, W., A. L. Thomas-Powell, N. Raab-Traub, M. Hawke, and E. Kieff. 1980. Epstein-Barr virus RNA. V. Viral RNA in a restringently infected, growth-transformed cell line. J. Virol. 36:506-518.
22. Kiss, C., J. Nishikawa, K. Takada, P. Trivedi, G. Klein, and L. Szekely. 2003. T cell leukemia 1 oncogene expression depends on the presence of Epstein-Barr virus in the virus-carrying Burkitt lymphoma lines. Proc. Natl. Acad. Sci. USA 100:4813-4818.
23. Knight, J. S., K. Lan, C. Subramanian, and E. S. Robertson. 2003. Epstein-Barr virus nuclear antigen 3C recruits histone deacetylase activity and associates with the compressors mSin3A and NCoR in human B-cell lines. J. Virol. 77:4261-4272.
24. Lin, J., E. Johannsen, E. Robertson, and E. Kieff. 2002. Epstein-Barr virus nuclear antigen 3C putative repression domain mediates coactivation of the LMP1 promoter with EBNA-2. J. Virol. 76:232-242.
25. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
26. Ma, Q., D. Jones, P. R. Borghesani, R. A. Segal, T. Nagasawa, T. Kishimoto, R. T. Bronson, and T. A. Springer. 1998. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. USA 95:9448-9453.
27. 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.
28. Marshall, D., and C. Sample. 1995. Epstein-Barr virus nuclear antigen 3C is a transcriptional regulator. J. Virol. 69:3624-3630.
29. Maruo, S., E. Johannsen, D. Illanes, A. Cooper, and E. Kieff. 2003 Epstein-Barr Virus nuclear protein EBNA3A is critical for maintaining lymphoblastoid cell line growth. J. Virol. 77:10437-10447.
30. Maunders, M. J., L. Petti, and M. Rowe. 1994. Precipitation of the Epstein-Barr virus protein EBNA 2 by an EBNA 3c-specific monoclonal antibody. J. Gen. Virol. 75:769-778.
31. McKenzie, G. J., M. Khan, E. Briend, Y. Stallwood, and K. R. Champion. 2005. Notch: a unique therapeutic target for immunomodulation. Expert Opin. Ther. Targets 9:395-410.
32. Moghaddam, A., M. Rosenzweig, D. Lee-Parritz, B. Annis, R. P. Johnson, and F. Wang. 1997. An animal model for acute and persistent Epstein-Barr virus infection. Science 276:2030-2033.
33. Morimura, T., R. Goitsuka, Y. Zhang, I. Saito, M. Reth, and D. Kitamura. 2000. Cell cycle arrest and apoptosis induced by Notch1 in B cells. J. Biol. Chem. 275:36523-36531.
34. Murray, R. J., M. G. Kurilla, J. M. Brooks, W. A. Thomas, M. Rowe, E. Kieff, and A. B. Rickinson. 1992. Identification of target antigens for the human cytotoxic T cell response to Epstein-Barr virus (EBV): implications for the immune control of EBV-positive malignancies. J. Exp. Med. 176:157-168.
35. Nagasawa, T., T. Nakajima, K. Tachihana, H. Iizasa, C. C. Bleul, O. Yoshie, K. Matsushima, N. Yoshida, T. A. Springer, and T. Kishimoto. 1996. Molecular cloning and characterization of a murine pre-B-cell growth-stimulating factor/stromal cell-derived factor 1 receptor, a murine homolog of the human immunodeficiency virus 1 entry coreceptor fusin. Proc. Natl. Acad. Sci. USA 93:14726-14729.
36. Nakayama, T., R. Fujisawa, D. Izawa, K. Hieshima, K. Takada, and O. Yoshie. 2002. Human B cells immortalized with Epstein-Barr virus upregulate CCR6 and CCR10 and downregulate CXCR4 and CXCR5. J. Virol. 76:3072-3077.
37. Nie, Y., J. Waite, F. Brewer, M. J. Sunshine, D. R. Littman, and Y. R. Zou. 2004. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J. Exp. Med. 200:1145-1156.
38. Petti, L., and E. Kieff. 1988. A sixth Epstein-Barr virus nuclear protein (EBNA3B) is expressed in latently infected growth-transformed lymphocytes. J. Virol. 62:2173-2178.
39. Radkov, S. A., M. Bain, P. J. Farrell, M. West, M. Rowe, and M. J. Allday. 1997. Epstein-Barr virus EBNA3C represses Cp, the major promoter for EBNA expression, but has no effect on the promoter of the cell gene CD21. J. Virol. 71:8552-8562.
40. Radkov, S. A., R. Touitou, A. Brehm, M. Rowe, M. West, T. Kouzarides, and M. J. Allday. 1999. Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription. J. Virol. 73:5688-5697.
41. 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.
42. Seiffert, D., J. D. Bradley, C. M. Rominger, D. H. Rominger, F. Yang, J. E. Meredith, Jr., Q. Wang, A. H. Roach, L. A. Thompson, S. M. Spitz, J. N. Higaki, S. R. Prakash, A. P. Combs, R. A. Copeland, S. P. Arneric, P. R. Hartig, D. W. Robertson, B. Cordell, A. M. Stern, R. E. Olson, and R. Zaczek. 2000. Presenilin-1 and -2 are molecular targets for gamma-secretase inhibitors. J. Biol. Chem. 275:34086-34091.
43. Silins, S. L., and T. B. Sculley. 1994. Modulation of vimentin, the CD40 activation antigen and Burkitt's lymphoma antigen (CD77) by the Epstein-Barr virus nuclear antigen EBNA-4. Virology 202:16-24.
44. Tachibana, K., S. Hirota, H. Iizasa, H. Yoshida, K. Kawabata, Y. Kataoka, Y. Kitamura, K. Matsushima, N. Yoshida, S. Nishikawa, T. Kishimoto, and T. Nagasawa. 1998. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393:591-594.
45. Tierney, R. J., N. Steven, L. S. Young, and A. B. Rickinson. 1994. Epstein-Barr virus latency in blood mononuclear cells: analysis of viral gene transcription during primary infection and in the carrier state. J. Virol. 68:7374-7385.
46. Tomkinson, B., and E. Kieff. 1992. Use of second-site homologous recombination to demonstrate that Epstein-Barr virus nuclear protein 3B is not important for lymphocyte infection or growth transformation in vitro. J. Virol. 66:2893-2903.
47. Tomkinson, B., E. Robertson, and E. Kieff. 1993. Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J. Virol. 67:2014-2025.
48. Touitou, R., M. Hickabottom, G. Parker, T. Crook, and M. J. Allday. 2001. Physical and functional interactions between the corepressor CtBP and the Epstein-Barr virus nuclear antigen EBNA3C. J. Virol. 75:7749-7755.
49. Vicente-Manzanares, M., M. C. Montoya, M. Mellado, J. M. Frade, M. A. del Pozo, M. Nieto, M. O. de Landazuri, A. C. Martinez, and F. Sanchez-Madrid. 1998. The chemokine SDF-1alpha triggers a chemotactic response and induces cell polarization in human B lymphocytes. Eur. J. Immunol. 28:2197-2207.
50. Vigouroux, S., E. Yvon, H. J. Wagner, E. Biagi, G. Dotti, U. Sili, C. Lira, C. M. Rooney, and M. K. Brenner. 2003. Induction of antigen-specific regulatory T cells following overexpression of a Notch ligand by human B lymphocytes. J. Virol. 77:10872-10880.
51. Wang, F. 2001. A new animal model for Epstein-Barr virus pathogenesis. Curr. Top. Microbiol. Immunol. 258:201-219.
52. Wang, F., C. Gregory, C. Sample, M. Rowe, D. Liebowitz, R. Murray, A. Rickinson, and E. Kieff. 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. Yasukawa, M., A. Hasegawa, I. Sakai, H. Ohminami, J. Arai, S. Kaneko, Y. Yakushijin, K. Maeyama, H. Nakashima, R. Arakaki, and S. Fujita. 1999. Down-regulation of CXCR4 by human herpesvirus 6 (HHV-6) and HHV-7. J. Immunol. 162:5417-5422.
54. Yvon, E. S., S. Vigouroux, R. F. Rousseau, E. Biagi, P. Amrolia, G. Dotti, H. J. Wagner, and M. K. Brenner. 2003. Overexpression of the Notch ligand, Jagged-1, induces alloantigen-specific human regulatory T cells. Blood 102:3815-3821.
55. Zhao, B., and C. E. Sample. 2000. Epstein-Barr virus nuclear antigen 3C activates the latent membrane protein 1 promoter in the presence of Epstein-Barr virus nuclear antigen 2 through sequences encompassing an Spi-1/Spi-B binding site. J. Virol. 74:5151-5160.
56. Zou, Y. R., A. H. Kottmann, M. Kuroda, I. Taniuchi, and D. R. Littman. 1998. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393:595-599.