Epstein-barr virus lytic infection contributes to lymphoproliferative disease in a SCID mouse model

Journal of Virology

Volumn 79, Issue 22, 2005, Pages 13993-14003

  Hong, Gregory K ^a,b   Gulley, Margaret L ^b   Feng, Wen Hai ^a   Delecluse, Henri Jacques ^c   Holley Guthrie, Elizabeth ^a   Kenney, Shannon C ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACICLOVIR; B LYMPHOCYTE GROWTH FACTOR; BETA 2 MICROGLOBULIN; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 6; RNA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPSTEIN BARR VIRUS; FEMALE; GENE DELETION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LYMPHOBLASTOID CELL; LYMPHOPROLIFERATIVE DISEASE; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; VIRUS INFECTION; VIRUS LATENCY; VIRUS REPLICATION;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL DIVISION; DISEASE MODELS, ANIMAL; DNA PRIMERS; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HUMANS; LYMPHOPROLIFERATIVE DISORDERS; MICE; MICE, SCID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ANIMALIA; HUMAN HERPESVIRUS 4;

EID: 27644567614     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.22.13993-14003.2005     Document Type: Article

References (62)

1. Baiocchi, R. A., M. E. Ross, J. C. Tan, C. C. Chou, L. Sullivan, S. Haldar, M. Monne, M. V. Seiden, S. K. Narula, J. Sklar, et al. 1995. Lymphomagenesis in the SCID-hu mouse involves abundant production of human interleukin-10. Blood 85:1063-1074.
2. Bais, C., B. Santomasso, O. Coso, L. Arvanitakis, E. G. Raaka, J. S. Gutkind, A. S. Asch, E. Cesarman, M. C. Gershengorn, and E. A. Mesri. 1998. G-protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391:86-89.
3. Beatty, P. R., S. M. Krams, and O. M. Martinez. 1997. Involvement of IL-10 in the autonomous growth of EBV-transformed B cell lines. J. Immunol. 158:4045-4051.
4. Cayrol, C., and E. K. Flemington. 1995. Identification of cellular target genes of the Epstein-Barr virus transactivator Zta: activation of transforming growth factor beta igh3 (TGF-beta igh3) and TGF-beta 1. J. Virol. 69: 4206-4212.
5. Cordano, P., A. Lake, L. Shield, G. M. Taylor, F. E. Alexander, P. R. Taylor, J. White, and R. F. Jarrett. 2005. Effect of IL-6 promoter polymorphism on incidence and outcome in Hodgkin's lymphoma. Br. J. Haematol. 128: 493-495.
6. Dirmeier, U., B. Neuhierl, E. Kilger, G. Reisbach, M. L. Sandberg, and W. Hammerschmidt. 2003. Latent membrane protein 1 is critical for efficient growth transformation of human B cells by Epstein-Barr virus. Cancer Res. 63:2982-2989.
7. Durandy, A., D. Emilie, M. Peuchmaur, M. Forveille, C. Clement, J. Wijdenes, and A. Fischer. 1994. Role of IL-6 in promoting growth of human EBV-induced B-cell tumors in severe combined immunodeficient mice. J. Immunol. 152:5361-5367.
8. Eskdale, J., G. Gallagher, C. L. Verweij, V. Keijsers, R. G. Westendorp, and T. W. Huizinga. 1998. Interleukin 10 secretion in relation to human IL-10 locus haplotypes. Proc. Natl. Acad. Sci. USA 95:9465-9470.
9. Feederle, R. M. Kost, M. Baumann, A. Janz, E. Drouet, W. Hammerschmidt, and H. J. Delecluse. 2000. The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. EMBO J. 19:3080-3089.
10. Feng, W. H., J. I. Cohen, S. Fischer, L. Li, M. Sneller, R. Goldbach-Mansky, N. Raab-Traub, H. J. Delecluse, and S. C. Kenney. 2004. Reactivation of latent Epstein-Barr virus by methotrexate: a potential contributor to methotrexate-associated lymphomas. J. Natl. Cancer Inst. 96:1691-1702.
11. Glasgow, L. A., J. T. Richards, and E. R. Kern. 1982. Effect of acyclovir treatment on acute and chronic murine cytomegalovirus infection. Am. J. Med. 73:132-137,
12. Haddad, E., S. Paczesny, V. Leblond, J. M. Seigneurin, M. Stern, A. Achkar, M. Bauwens, V. Delwail, D. Debray, C. Duvoux, P. Hubert, B. Hurault de Ligny, J. Wijdenes, A. Durandy, and A. Fischer. 2001. Treatment of B-lymphoproliferative disorder with a monoclonal anti-interleukin-6 antibody in 12 patients: a multicenter phase 1-2 clinical trial. Blood 97:1590-1597.
13. Hayes, D. P., A. A. Brink, M. B. Vervoort, J. M. Middeldorp, C. J. Meijer, and A. J. van den Brule. 1999. Expression of Epstein-Barr virus (EBV) transcripts encoding homologues to important human proteins in diverse EBV associated diseases. Mol. Pathol. 52:97-103.
14. Hong, G. K., H. J. Delecluse, H. Gruffat, T. E. Morrison, W. H. Feng, A. Sergeant, and S. C. Kenney. 2004. The BRRF1 early gene of Epstein-Barr virus encodes a transcription factor that enhances induction of lytic infection by BRLF1. J. Virol. 78:4983-4992.
15. Hong, G. K., P. Kumar, L. Wang, B. Damania, M. L. Gulley, H.-J. Delecluse, P. J. Polverini, and S. C. Kenney. 2005. Epstein-Barr virus lytic infection is required for efficient production of the angiogenesis factor vascular endothelial growth factor in lymphoblastoid cell lines. J. Virol. 79:13984-13992.
16. Hsu, D. H., R. de Waal Malefyt, D. F. Fiorentino, M. N. Dang, P. Vieira, J. de Vries, H. Spits, T. R. Mosmann, and K. W. Moore. 1990. Expression of interleukin-10 activity by Epstein-Barr virus protein BCRF1. Science 250: 830-832.
17. Humme, S., G. Reisbach, R. Feederle, H. J. Delecluse, K. Bousset, W. Hammerschmidt, and A. Schepers. 2003. The EBV nuclear antigen 1 (EBNA1) enhances B cell immortalization several thousandfold. Proc. Natl. Acad. Sci. USA 100:10989-10994.
18. Izumi, K. M., E. D. Cahir McFarland, E. A. Riley, D. Rizzo, Y. Chen, and E. Kieff. 1999. The residues between the two transformation effector sites of Epstein-Barr virus latent membrane protein 1 are not critical for B-lymphocyte growth transformation. J. Virol. 73:9908-9916.
19. Izumi, K. M., K. M. Kaye, and E. D. Kieff. 1997. The Epstein-Barr virus LMP1 amino acid sequence that engages tumor necrosis factor receptor associated factors is critical for primary B lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA 94:1447-1452.
20. Izumi, K. M., and E. D. Kieff. 1997. The Epstein-Barr virus oncogene product latent membrane protein 1 engages the tumor necrosis factor receptor-associated death domain protein to mediate B lymphocyte growth transformation and activate NF-κB. Proc. Natl. Acad. Sci. USA 94:12592-12597.
21. Johannessen, I., T. Haque, J. N'Jie-Jobe, and D. H. Crawford. 1998. Non-correlation of in vivo and in vitro parameters of Epstein-Barr virus persistence suggests heterogeneity of B cell infection. J. Gen. Virol. 79:1631-1636.
22. Kaye, K. M., K. M. Izumi, and E. Kieff. 1993. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA 90:9150-9154.
23. Khatri, V. P., and M. A. Caligiuri. 1998. A review of the association between interleukin-10 and human B-cell malignancies. Cancer Immunol. Immunother. 46:239-244.
24. - RNA supports Burkitt's lymphoma growth through interleukin-10 induction. EMBO J. 19:6742-6750.
25. Kurzrock, R. 2001. Cytokine deregulation in cancer. Biomed. Pharmacother. 55:543-547.
26. Li, Y., N. P. Mahajan, J. Webster-Cyriaque, P. Bhende, G. K. Hong, H. S. Earp, and S. Kenney. 2004. The C-mer gene is induced by Epstein-Barr virus immediate-early protein BRLF1. J. Virol. 78:11778-11785.
27. Li, Y., J. Webster-Cyriaque, C. C. Tomlinson, M. Yohe, and S. Kenney. 2004. Fatty acid synthase expression is induced by the Epstein-Barr virus immediate-early protein BRLF1 and is required for lytic viral gene expression. J. Virol. 78:4197-4206.
28. Mahot, S., A. Sergeant, E. Drouet, and H. Gruffat. 2003. A novel function for the Epstein-Barr virus transcription factor EB1/Zta: induction of transcription of the hIL-10 gene. J. Gen. Virol. 84:965-974.
29. Marchini, A., B. Tomkinson, J. I. Cohen, and E. Kieff. 1991. BHRF1, the Epstein-Barr virus gene with homology to Bcl2, is dispensable for B-lymphocyte transformation and virus replication. J. Virol. 65:5991-6000.
30. Masood, R., Y. Zhang, M. W. Bond, D. T. Scadden, T. Moudgil, R. E. Law, M. H. Kaplan, B. Jung, B. M. Espina, Y. Lunardi-Iskandar, et al. 1995. Interleukin-10 is an autocrine growth factor for acquired immunodeficiency syndrome-related B-cell lymphoma. Blood 85:3423-3430.
31. Mauray, S., M. T. Fuzzati-Armentero, P. Trouillet, M. Ruegg, G. Nicoloso, M. Hart, L. Aarden, M. Schapira, and M. A. Duchosal. 2000. Epstein-Barr virus-dependent lymphoproliferative disease: critical role of IL-6. Eur. J. Immunol. 30:2065-2073.
32. Mauser, A., S. Saito, E. Appella, C. W. Anderson, W. T. Seaman, and S. Kenney. 2002. The Epstein-Barr virus immediate-early protein BZLF1 regulates p53 function through multiple mechanisms. J. Virol. 76:12503-12512.
33. McKendrick, M. W., J. I. McGill, J. E. White, and M. J. Wood. 1986. Oral acyclovir in acute herpes zoster. Br. Med. J. 293:1529-1532.
34. Miyazaki, I., R. K. Cheung, and H. M. Dosch. 1993. Viral interleukin 10 is critical for the induction of B cell growth transformation by Epstein-Barr virus. J. Exp. Med. 178:439-447.
35. Montaner, S., A. Sodhi, A. Molinolo, T. H. Bugge, E. T. Sawai, Y. He, Y. Li, P. E. Ray, and J. S. Gutkind. 2003. Endothelial infection with KSHV genes in vivo reveals that vGPCR initiates Kaposi's sarcomagenesis and can promote the tumorigenic potential of viral latent genes. Cancer Cell 3:23-36.
36. Montone, K. T., R. L. Hodinka, K. E. Salhany, E. Lavi, A. Rostami, and J. E. Tomaszewski. 1996. Identification of Epstein-Barr virus lytic activity in post-transplantation lymphoproliferative disease. Mod. Pathol. 9:621-630.
37. Moore, P. S., C. Boshoff, R. A. Weiss, and Y. Chang. 1996. Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science 274:1739-1744.
38. Mosier, D. E., G. R. Picchio, S. M. Baird, R. Kobayashi, and T. J. Kipps. 1992. Epstein-Barr virus-induced human B-cell lymphomas in SCID mice reconstituted with human peripheral blood leukocytes. Cancer Res. 52(19 Suppl.):5552s-5553s.
39. Nepomuceno, R. R., C. E. Balatoni, Y. Natkunam, A. L. Snow, S. M. Krams, and O. M. Martinez. 2003. Rapamycin inhibits the interleukin 10 signal transduction pathway and the growth of Epstein-Barr virus B-cell lymphomas. Cancer Res. 63:4472-4480.
40. Ogura, N., M. Tobe, H. Sakamaki, H. Kujiraoka, M. Akiba, Y. Abiko, and H. Nagura. 2002. Interleukin-1 beta induces interleukin-6 mRNA expression and protein production in synovial cells from human temporomandibular joint. J. Oral Pathol. Med. 31:353-360.
41. Pallesen, G., K. Sandvej, S. J. Hamilton-Dutoit, M. Rowe, and L. S. Young. 1991. Activation of Epstein-Barr virus replication in Hodgkin and Reed-Sternberg cells. Blood 78:1162-1165.
42. Picchio, G. R., R. Kobayashi, M. Kirven, S. M. Baird, T. J. Kipps, and D. E. Mosier. 1992. Heterogeneity among Epstein-Barr virus-seropositive donors in the generation of immunoblastic B-cell lymphomas in SCID mice receiving human peripheral blood leukocyte grafts. Cancer Res. 52:2468-2477.
43. Raju, J., B. McCarthy, and R. P. Bird. 2002. Steady state levels of transforming growth factor-beta1 and -beta2 mRNA and protein expression are elevated in colonic tumors in vivo irrespective of dietary lipids intervention. Int. J. Cancer 100:635-641.
44. Rickinson, A. B-, and E. Kieff. 2001. Epstein-Barr virus, p. 2575-2627. 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, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
45. Rickinson, A. B., and E. Kieff. 2001. Epstein-Barr virus and its replication, p. 2511-2553. 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, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
46. Rousset, F., E. Garcia, T. Defrance, C. Peronne, N. Vezzio, D. H. Hsu, R. Kastelein, K. W. Moore, and J. Banchereau. 1992. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc. Natl. Acad. Sci. USA 89:1890-1893.
47. Rowe, M., L. S. Young, J. Crocker, H. Stokes, S. Henderson, and A. B. Rickinson. 1991. Epstein-Barr virus (EBV)-associated lymphoproliferative disease in the SCID mouse model: implications for the pathogenesis of EBV-positive lymphomas in man. J. Exp. Med. 173:147-158.
48. Scala, G., I. Quinto, M. R. Ruocco, A. Arcucci, M. Mallardo, P. Caretto, G. Forni, and S. Venuta. 1990. Expression of an exogenous interleukin 6 gene in human Epstein-Barr virus B cells confers growth advantage and in vivo tumorigenicity. J. Exp. Med. 172:61-68.
49. Skare, J., J. Farley, J. L. Strominger, K. O. Fresen, M. S. Cho, and H. zur Hausen. 1985. Transformation by Epstein-Barr virus requires DNA sequences in the region of BamHI fragments Y and H. J. Virol. 55:286-297.
50. Speck, S. H., T. Chatila, and E. Flemington. 1997. Reactivation of Epstein-Barr virus: regulation and function of the BZLF1 gene. Trends Microbiol. 5:399-405.
51. Staskus, K. A., R. Sun, G. Miller, P. Racz, A. Jaslowski, C. Metroka, H. Brett-Smith, and A. T. Haase. 1999. Cellular tropism and viral interleukin-6 expression distinguish human herpesvirus 8 involvement in Kaposi's sarcoma, primary effusion lymphoma, and multicentric Castleman's disease. J. Virol. 73:4181-4187.
52. Steven, N. M., N. E. Annels, A. Kumar, A. M. Leese, M. G. Kurilla, and A. B. Rickinson. 1997. Immediate early and early lytic cycle proteins are frequent targets of the Epstein-Barr virus-induced cytotoxic T cell response. J. Exp. Med. 185:1605-1617.
53. Stuart, A. D., J. P. Stewart, J. R. Arrand, and M. Mackett. 1995. The Epstein-Barr virus encoded cytokine viral interleukin-10 enhances transformation of human B lymphocytes. Oncogene 11:1711-1719.
54. Swaminathan, S., R. Hesselton, J. Sullivan, and E. Kieff. 1993. Epstein-Barr virus recombinants with specifically mutated BCRF1 genes. J. Virol. 67: 7406-7413.
55. Tanner, J., and G. Tosato. 1991. Impairment of natural killer functions by interleukin 6 increases lymphoblastoid cell tumorigenicity in athymic mice. J. Clin. Investig. 88:239-247.
56. Thomas, J. A., N. A. Hotchin, M. J. Allday, P. Amlot, M. Rose, M. Yacoub, and D. H. Crawford. 1990. Immunohistology of Epstein-Barr virus-associated antigens in B cell disorders from immunocompromised individuals. Transplantation 49:944-953.
57. 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.
58. Tosato, G., J. Tanner, K. D. Jones, M. Revel, and S. E. Pike. 1990. Identification of interleukin-6 as an autocrine growth factor for Epstein-Barr virus-immortalized B cells. J. Virol. 64:3033-3041.
59. Tynell, E., E. Aurelius, A. Brandell, I. Julander, M. Wood, Q. Y. Yao, A. Rickinson, B. Akerlund, and J. Andersson. 1996. Acyclovir and prednisolone treatment of acute infectious mononucleosis: a multicenter, double-blind, placebo-controlled study. J. Infect. Dis. 174:324-331.
60. Vockerodt, M., B. Haier, P. Buttgereit, H. Tesch, and D. Kube. 2001. The Epstein-Barr virus latent membrane protein 1 induces interleukin-10 in Burkitt's lymphoma cells but not in Hodgkin's cells involving the p38/SAPK2 pathway. Virology 280:183-198.
61. Webster-Cyriaque, J., and N. Raab-Traub. 1998. Transcription of Epstein-Barr virus latent cycle genes in oral hairy leukoplakia. Virology 248:53-65.
62. Xue, S. A., L. G. Labrecque, Q. L. Lu, S. K. Ong, I. A. Lampert, P. Kazembe, E. Molyneux, R. L. Broadhead, E. Borgstein, and B. E. Griffin. 2002. Promiscuous expression of Epstein-Barr virus genes in Burkitt's lymphoma from the central African country Malawi. Int. J. Cancer 99:635-643.