Germinal center B cells latently infected with Epstein-Barr virus proliferate extensively but do not increase in number

Journal of Virology

Volumn 84, Issue 2, 2010, Pages 1158-1168

  Roughan, Jill E ^a,b   Torgbor, Charles ^a,c   Thorley Lawson, David A ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c KWAME NKRUMAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Ghana)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL 2; PROTEIN BCL 6; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL DIVISION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GERMINAL CENTER; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; TONSIL; VIRUS INFECTION;

ANIMALS; B-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GERMINAL CENTER; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOCYTE COUNT; MICE; PALATINE TONSIL; VIRAL MATRIX PROTEINS; VIRUS LATENCY;

HUMAN HERPESVIRUS 4; MUS MUSCULUS;

EID: 73849106679     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01780-09     Document Type: Article

References (58)

1. Allen, C. D., K. M. Ansel, C. Low, R. Lesley, H. Tamamura, N. Fujii, and J. G. Cyster. 2004. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol. 5:943-952.
2. Allen, C. D., T. Okada, and J. G. Cyster. 2007. Germinal-center organization and cellular dynamics. Immunity 27:190-202.
3. Allen, D., A. Cumano, R. Dildrop, C. Kocks, K. Rajewsky, N. Rajewsky, J. Roes, F. Sablitzky, and M. Siekevitz. 1987. Timing, genetic requirements and functional consequences of somatic hypermutation during B-cell development. Immunol. Rev. 96:5-22.
4. Arpin, C., J. Déchanet, C. Van Kooten, P. Merville, G. Grouard, F. Brière, J. Banchereau, and Y. J. Liu. 1995. Generation of memory B cells and plasma cells in vitro. Science 268:720-722.
5. 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.
6. Babcock, G. J., D. Hochberg, and A. D. Thorley-Lawson. 2000. The expression pattern of Epstein-Barr virus latent genes in vivo is dependent upon the differentiation stage of the infected B cell. Immunity 13:497-506.
7. Cai, X., A. Schafer, S. Lu, J. P. Bilello, R. C. Desrosiers, R. Edwards, N. Raab-Traub, and B. R. Cullen. 2006. Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2:e23.
8. Caldwell, R. G., J. B. Wilson, S. J. Anderson, and R. Longnecker. 1998. Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals. Immunity 9:405-411.
9. Callan, M. F., L. Tan, N. Annels, G. S. Ogg, J. D. Wilson, C. A. O'Callaghan, N. Steven, A. J. McMichael, and A. B. Rickinson. 1998. Direct visualization of antigen-specific CD8+ T cells during the primary immune response to Epstein-Barr virus in vivo. J. Exp. Med. 187:1395-1402.
10. Casola, S., K. L. Otipoby, M. Alimzhanov, S. Humme, N. Uyttersprot, J. L. Kutok, M. C. Carroll, and K. Rajewsky. 2004. B cell receptor signal strength determines B cell fate. Nat. Immunol. 5:317-327.
11. Collins, C. M., J. M. Boss, and S. H. Speck. 2009. Identification of infected B-cell populations by using a recombinant murine gammaherpesvirus 68 expressing a fluorescent protein. J. Virol. 83:6484-6493.
12. Cosmopoulos, K., M. Pegtel, J. Hawkins, H. Moffett, C. Novina, J. Middeldorp, and D. A. Thorley-Lawson. 2009. Comprehensive profiling of Epstein-Barr virus microRNAs in nasopharyngeal carcinoma. J. Virol. 83:2357-2367.
13. Dent, A. L., A. L. Shaffer, X. Yu, D. Allman, and L. M. Staudt. 1997. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 276:589-592.
14. Ganusov, V. V., and R. J. De Boer. 2007. Do most lymphocytes in humans really reside in the gut? Trends Immunol. 28:514-518.
15. Gerdes, J., U. Schwab, H. Lemke, and H. Stein. 1983. Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int. J. Cancer 31:13-20.
16. 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.
17. Grundhoff, A., C. S. Sullivan, and D. Ganem. 2006. A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 12:733-750.
18. Hadinoto, V., M. Shapiro, T. C. Greenough, J. L. Sullivan, K. Luzuriaga, and D. A. Thorley-Lawson. 2008. On the dynamics of acute EBV infection and the pathogenesis of infectious mononucleosis. Blood 111:1420-1427.
19. He, B., N. Raab-Traub, P. Casali, and A. Cerutti. 2003. EBV-encoded latent membrane protein 1 cooperates with BAFF/BLyS and APRIL to induce T cell-independent Ig heavy chain class switching. J. Immunol. 171:5215-5224.
20. 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.
21. Hislop, A. D., G. S. Taylor, D. Sauce, and A. B. Rickinson. 2007. Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu. Rev. Immunol. 25:587-617.
22. Hoagland, R. 1964. The incubation period of infectious mononucleosis. Am. J. Public Health Nations Health 54:1699-1704.
23. Hochberg, D., J. M. Middeldorp, M. Catalina, J. L. Sullivan, K. Luzuriaga, and D. A. Thorley-Lawson. 2004. Demonstration of the Burkitt's lymphoma Epstein-Barr virus phenotype in dividing latently infected memory cells in vivo. Proc. Natl. Acad. Sci. U. S. A. 101:239-244.
24. Hochberg, D., T. Souza, M. Catalina, J. L. Sullivan, K. Luzuriaga, and D. A. Thorley-Lawson. 2004. Acute infection with Epstein-Barr virus targets and overwhelms the peripheral memory B-cell compartment with resting, latently infected cells. J. Virol. 78:5194-5204.
25. Hudnall, S. D., Y. Ge, L. Wei, N. P. Yang, H. Q. Wang, and T. Chen. 2005. Distribution and phenotype of Epstein-Barr virus-infected cells in human pharyngeal tonsils. Mod. Pathol. 18:519-527.
26. Hurley, E. A., L. D. Klaman, S. Agger, J. B. Lawrence, and D. A. Thorley-Lawson. 1991. The prototypical Epstein-Barr virus-transformed lymphoblastoid cell line IB4 is an unusual variant containing integrated but no episomal viral DNA. J. Virol. 65:3958-3963.
27. Hurley, E. A., J. A. McNeil, J. B. Lawrence, and D. A. Thorley-Lawson. 1990. Genomic integration as a novel mechanism of EBV persistence. Curr. Top. Microbiol. Immunol. 166:367-374.
28. Hurley, E. A., and D. A. Thorley-Lawson. 1988. B cell activation and the establishment of Epstein-Barr virus latency. J. Exp. Med. 168:2059-2075.
29. Kelsoe, G. 1996. Life and death in germinal centers (redux). Immunity 4:107-111.
30. Klaman, L. D., E. A. Hurley, and D. A. Thorley-Lawson. 1991. Is there a unique episome in EBV transformed B cells? Virology 185:883-887.
31. Laichalk, L. L., D. Hochberg, G. J. Babcock, R. B. Freeman, and D. A. Thorley-Lawson. 2002. The dispersal of mucosal memory B cells: evidence from persistent EBV infection. Immunity 16:745-754.
32. Laichalk, L. L., and D. A. Thorley-Lawson. 2005. Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J. Virol. 79:1296-1307.
33. Leanderson, T., E. Kallberg, and D. Gray. 1992. Expansion, selection and mutation of antigen-specific B cells in germinal centers. Immunol. Rev. 126:47-61.
34. Lindner, S. E., and B. Sugden. 2007. The plasmid replicon of Epstein-Barr virus: mechanistic insights into efficient, licensed, extrachromosomal replication in human cells. Plasmid 58:1-12.
35. Liu, Y. J., and C. Arpin. 1997. Germinal center development. Immunol. Rev. 156:111-126.
36. Liu, Y. J., D. Y. Mason, G. D. Johnson, S. Abbot, C. D. Gregory, D. L. Hardie, J. Gordon, and I. C. MacLennan. 1991. Germinal center cells express bcl-2 protein after activation by signals which prevent their entry into apoptosis. Eur. J. Immunol. 21:1905-1910.
37. MacLennan, I. C. 1994. Germinal centers. Annu. Rev. Immunol. 12:117-139.
38. McKean, D., K. Huppi, M. Bell, L. Staudt, W. Gerhard, and M. Weigert. 1984. Generation of antibody diversity in the immune response of BALB/c mice to influenza virus hemagglutinin. Proc. Natl. Acad. Sci. U. S. A. 81: 3180-3184.
39. Muramatsu, M., K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553-563.
40. Nanbo, A., A. Sugden, and B. Sugden. 2007. The coupling of synthesis and partitioning of EBV's plasmid replicon is revealed in live cells. EMBO J. 26:4252-4262.
41. Niedobitek, G., H. Herbst, L. S. Young, L. Brooks, M. G. Masucci, J. Crocker, A. B. Rickinson, and H. Stein. 1992. Patterns of Epstein-Barr virus infection in non-neoplastic lymphoid tissue. Blood 79:2520-2526.
42. Panagopoulos, D., P. Victoratos, M. Alexiou, G. Kollias, and G. Mosialos. 2004. Comparative analysis of signal transduction by CD40 and the Epstein-Barr virus oncoprotein LMP1 in vivo. J. Virol. 78:13253-13261.
43. Pascual, V., Y. J. Liu, A. Magalski, O. de Bouteiller, J. Banchereau, and J. D. Capra. 1994. Analysis of somatic mutation in five B cell subsets of human tonsil. J. Exp. Med. 180:329-339.
44. Pfeffer, S., M. Zavolan, F. A. Grasser, M. Chien, J. J. Russo, J. Ju, B. John, A. J. Enright, D. Marks, C. Sander, and T. Tuschl. 2004. Identification of virus-encoded microRNAs. Science 304:734-736.
45. Rickinson, A. B., and E. Kieff. 2007. Epstein-Barr virus, p. 2655-2700. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
46. Roughan, J. E., and D. A. Thorley-Lawson. 2009. The intersection of Epstein-Barr virus with the germinal center. J. Virol. 83:3968-3976.
47. Rudikoff, S., M. Pawlita, J. Pumphrey, and M. Heller. 1984. Somatic diversification of immunoglobulins. Proc. Natl. Acad. Sci. U. S. A. 81:2162-2166.
48. Schwickert, T. A., R. L. Lindquist, G. Shakhar, G. Livshits, D. Skokos, M. H. Kosco-Vilbois, M. L. Dustin, and M. C. Nussenzweig. 2007. In vivo imaging of germinal centres reveals a dynamic open structure. Nature 446:83-87.
49. Shapiro, M., K. A. Duca, K. Lee, E. Delgado-Eckert, J. Hawkins, A. S. Jarrah, R. Laubenbacher, N. F. Polys, V. Hadinoto, and D. A. Thorley-Lawson. 2008. A virtual look at Epstein-Barr virus infection: simulation mechanism. J. Theor. Biol. 252:633-648.
50. Souza, T. A., B. D. Stollar, J. L. Sullivan, K. Luzuriaga, and D. A. Thorley-Lawson. 2007. Influence of EBV on the peripheral blood memory B cell compartment. J. Immunol. 179:3153-3160.
51. Souza, T. A., B. D. Stollar, J. L. Sullivan, K. Luzuriaga, and D. A. Thorley-Lawson. 2005. Peripheral B cells latently infected with Epstein-Barr virus display molecular hallmarks of classical antigen-selected memory B cells. Proc. Natl. Acad. Sci. U. S. A. 102:18093-18098.
52. Stewart, S., C. W. Dawson, K. Takada, J. Curnow, C. A. Moody, J. W. Sixbey, and L. S. Young. 2004. Epstein-Barr virus-encoded LMP2A regulates viral and cellular gene expression by modulation of the NF-kappaB transcription factor pathway. Proc. Natl. Acad. Sci. U. S. A. 101:15730-15735.
53. Swanson-Mungerson, M. A., R. G. Caldwell, R. Bultema, and R. Longnecker. 2005. Epstein-Barr virus LMP2A alters in vivo and in vitro models of B-cell anergy, but not deletion, in response to autoantigen. J. Virol. 79:7355-7362.
54. Thorley-Lawson, D. 2005. EBV persistence and latent infection in vivo, p. 309-349. In E. S. Robertson (ed.), Epstein-Barr virus, 1st ed. Caister Academic Press, Norfolk, England.
55. Thorley-Lawson, D. A. 2001. Epstein-Barr virus: exploiting the immune system. Nat. Rev. Immunol. 1:75-82.
56. Thorley-Lawson, D. A., and M. J. Allday. 2008. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat. Rev. Microbiol. 6:913-924.
57. Thorley-Lawson, D. A., and A. Gross. 2004. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N. Engl. J. Med. 350:1328-1337.
58. Ye, B. H., G. Cattoretti, Q. Shen, J. Zhang, N. Hawe, R. de Waard, C. Leung, M. Nouri-Shirazi, A. Orazi, R. S. Chaganti, P. Rothman, A. M. Stall, P. P. Pandolfi, and R. Dalla-Favera. 1997. The BCL-6 proto-oncogene controls germinal-centre formation and Th2-type inflammation. Nat. Genet. 16:161-170.