Latency type-dependent modulation of Epstein-Barr virus-encoded latent membrane protein 1 expression by type I interferons in B cells

Journal of Virology

Volumn 86, Issue 8, 2012, Pages 4701-4707

  Salamon, Daniel ^a,b   Adori, Monika ^a   Ujvari, Dorina ^a   Wu, Liang ^a   Kis, Lorand L ^a   Madapura, Harsha S ^a   Nagy, Noemi ^a   Klein, George ^a   Klein, Eva ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL CENTER FOR EPIDEMIOLOGY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CRK LIKE PROTEIN; CYCLOHEXIMIDE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN RECEPTOR SUBSTRATE; JANUS KINASE; LATENT MEMBRANE PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PICEATANNOL; PROTEIN KINASE C; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; VIRUS MESSENGER RNA; WORTMANNIN;

ARTICLE; BURKITT LYMPHOMA; CELL PROLIFERATION; DAUDI CELL; DOWN REGULATION; EPSTEIN BARR VIRUS; GENE EXPRESSION REGULATION; GROWTH INHIBITION; HUMAN; IMMUNOMODULATION; MEMORY CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION; VIRUS CELL TRANSFORMATION; VIRUS GENE; VIRUS LATENCY;

B-LYMPHOCYTES; CELL LINE; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; INTERFERON TYPE I; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; VIRAL MATRIX PROTEINS; VIRUS LATENCY;

HUMAN HERPESVIRUS 4;

EID: 84861352748     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06829-11     Document Type: Article

References (49)

1. Altiok E, et al. 1992. Host-cell phenotype-dependent control of the BCR2/BWR1 promoter complex regulates the expression of Epstein-Barr virus nuclear antigens 2-6. Proc. Natl. Acad. Sci. U. S. A. 89:905-909.
2. Andersson JP, Andersson UG, Ernberg IT, Britton SF, DeLey M. 1985. Effects of pure interferons on Epstein-Barr virus infection in vitro. J. Virol. 54:615-618.
3. Bellan C, et al. 2005. Immunoglobulin gene analysis reveals 2 distinct cells of origin for EBV-positive and EBV-negative Burkitt lymphomas. Blood 106:1031-1036.
4. Bornkamm GW, Hudewentz J, Freese UK, Zimber U. 1982. Deletion of the nontransforming Epstein-Barr virus strain P3HR-1 causes fusion of the large internal repeat to the DSL region. J. Virol. 43:952-968.
5. Chang RS. 1984. Interferons on the transformation of non-T blood mononuclear leukocytes by Epstein-Barr virus. J. Interferon Res. 4:173-177.
6. Delcayre AX, Lotz M, Lernhardt W. 1993. Inhibition of Epstein-Barr virus-mediated capping of CD21/CR2 by alpha interferon (IFN-alpha): immediate antiviral activity of IFN-alpha during the early phase of infection. J. Virol. 67:2918-2921.
7. Ernberg I, et al. 1989. The role of methylation in the phenotype dependent modulation of Epstein-Barr nuclear antigen 2 and latent membrane protein genes in cells latently infected with Epstein-Barr virus. J. Gen. Virol. 70:2989-3002.
8. Exley R, Gordon J, Nathan P, Walker L, Clemens MJ. 1987. Antiproliferative effects of interferons on Daudi Burkitt lymphoma cells: induction of cell differentiation and loss of response to autocrine growth factors. Int. J. Cancer 40:53-57.
9. Fasler-Kan E, Pansky A, Wiederkehr M, Battegay M, Heim HM. 1998. Interferon-alpha activates signal transducers and activators of transcription 5 and 6 in Daudi cells. Eur. J. Biochem. 254:514-519.
10. Fensterl V, Sen GC. 2011. The ISG56/IFIT1 gene family. J. Interferon Cytokine Res. 31:71-78.
11. Garner JG, Hirsch MS, Schooley RT. 1984. Prevention of Epstein-Barr virus-induced B-cell outgrowth by interferon alpha. Infect. Immun. 43: 920-924.
12. Geiger TR, Martin JM. 2006. The Epstein-Barr virus-encoded LMP-1 oncoprotein negatively affects Tyk2 phosphorylation and interferon signaling in human B cells. J. Virol. 80:11638-11650.
13. Gross AJ, Hochberg D, Rand WM, Thorley-Lawson DA. 2005. EBV and systemic lupus erythematosus: a new perspective. J. Immunol. 174:6599-6607.
14. Gupta S, Jiang M, Pernis AB. 1999. IFN-alpha activates Stat6 and leads to the formation of Stat2:Stat6 complexes in B cells. J. Immunol. 163:3834-3841.
15. Harley JB, Harley IT, Guthridge JM, James JA. 2006. The curiously suspicious: a role for Epstein-Barr virus in lupus. Lupus 15:768-777.
16. He B, Raab-Traub N, Casali P, Cerutti A. 2003. EBV-encoded latent membrane protein 1 cooperates with BAFF/BLyS and APRIL to induce T cellindependent Ig heavy chain class switching. J. Immunol. 171:5215-5224.
17. Henderson EE, Doetsch PW, Charubala R, Pfleiderer W, Suhadolnik RJ. 1982. Inhibition of Epstein-Barr virus-associated nuclear antigen (EBNA) induction by (2',5')oligoadenylate and the cordycepin analog: mechanism of action for inhibition of EBV-induced transformation. Virology 122:198-201.
18. Hudson GS, Farrell PJ, Barrell BG. 1985. Two related but differentially expressed potential membrane proteins encoded by the EcoRI Dhet region of Epstein-Barr virus B95-8. J. Virol. 53:528-535.
19. Hurley EA, Thorley-Lawson DA. 1988. B cell activation and the establishment of Epstein-Barr virus latency. J. Exp. Med. 168:2059-2075.
20. Ishii H, et al. 2012. Monocytes enhance cell proliferation and LMP1 expression of nasal natural killer/T-cell lymphoma cells by cell contactdependent interaction through membrane-bound IL-15. Int. J. Cancer 130:48-58.
21. Iwakiri D, et al. 2009. Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J. Exp. Med. 206:2091-2099.
22. Jones MD, Foster L, Sheedy T, Griffin BE. 1984. The EB virus genome in Daudi Burkitt's lymphoma cells has a deletion similar to that observed in a non-transforming strain (P3HR-1) of the virus. EMBO J. 3:813-821.
23. Kelly G, Bell A, Rickinson A. 2002. Epstein-Barr virus-associated Burkitt lymphomagenesis selects for downregulation of the nuclear antigen EBNA2. Nat. Med. 8:1098-1104.
24. Kieff E, Rickinson AB. 2007. Epstein-Barr virus and its replication, p 2603-2654. In Fields BN, Knipe DM, HowleyPM(ed), Fields virology, 5th ed. Lippincott-Williams & Wilkins Publishers, Philadelphia, PA.
25. Kikuta H, Mizuno F, Yano S, Osato T. 1984. Interferon production by Epstein-Barr virus in human mononuclear leukocytes. J. Gen. Virol. 65: 837-841.
26. Kis LL, et al. 2011. STAT6 signaling pathway activated by the cytokines IL-4 and IL-13 induces expression of the Epstein-Barr virus-encoded protein LMP-1 in absence of EBNA-2: implications for the type II EBV latent gene expression in Hodgkin lymphoma. Blood 117:165-174.
27. Kis LL, et al. 2010. IL-21 imposes a type II EBV gene expression on type III and type I B cells by the repression of C-and activation of LMP-1-promoter. Proc. Natl. Acad. Sci. U. S. A. 107:872-877.
28. Kis LL, Takahara M, Nagy N, Klein G, Klein E. 2006. IL-10 can induce the expression of EBV-encoded latent membrane protein-1 (LMP-1) in the absence of EBNA-2 in B lymphocytes and in Burkitt lymphoma-and NK lymphoma-derived cell lines. Blood 107:2928-2935.
29. Klein E, et al. 1968. Surface IgM-kappa specificity on a Burkitt lymphoma cell in vivo and in derived culture lines. Cancer Res. 28:1300-1310.
30. Lotz M, Tsoukas CD, Fong S, Carson DA, Vaughan JH. 1985. Regulation of Epstein-Barr virus infection by recombinant interferons. Selected sensitivity to interferon-gamma. Eur. J. Immunol. 15:520-525.
31. Maher SG, Romero-Weaver AL, Scarzello AJ, Gamero AM. 2007. Interferon: cellular executioner or white knight? Curr. Med. Chem. 14: 1279-1289.
32. Masucci MG, et al. 1989. 5-Azacytidine up regulates the expression of Epstein-Barr virus nuclear antigen 2 (EBNA-2) through EBNA-6 and latent membrane protein in the Burkitt's lymphoma line Rael. J. Virol. 63: 3135-3141.
33. Minarovits J, Hu LF, Minarovits-Kormuta S, Klein G, Ernberg I. 1994. Sequence-specific methylation inhibits the activity of the Epstein-Barr virus LMP 1 and BCR2 enhancer-promoter regions. Virology 200:661-667.
34. Niller HH, Wolf H, Ay E, Minarovits J. 2011. Epigenetic dysregulation of Epstein-Barr virus latency and development of autoimmune disease. Adv. Exp. Med. Biol. 711:82-102.
35. Pfeffer LM. 2011. The role of nuclear factor κB in the interferon response. J. Interferon Cytokin Res. 31:553-559.
36. Pfeffer LM, et al. 1991. Transmembrane signaling by interferon alpha involves diacylglycerol production and activation of the epsilon isoform of protein kinase C in Daudi cells. Proc. Natl. Acad. Sci. U. S. A. 88:7988-7992.
37. Platanias LC. 2005. Mechanisms of type-I- and type-II-interferonmediated signaling. Nat. Rev. Immunol. 5:375-386.
38. Quan TE, Roman RM, Rudenga BJ, Holers VM, Craft JE. 2010. Epstein-Barr virus promotes interferon-alpha production by plasmacytoid dendritic cells. Arthritis Rheum. 62:1693-1701.
39. Rickinson AB, Kieff E. 2007. Epstein-Barr virus, p 2655-2700. In Fields BN, Knipe DM, Howley PM (ed), Fields virology, 5th ed. Lippincott-Williams & Wilkins Publishers, Philadelphia, PA.
40. Sadler RH, Raab-Traub N. 1995. The Epstein-Barr virus 3.5-kilobase latent membrane protein 1 mRNA initiates from a TATA-less promoter within the first terminal repeat. J. Virol. 69:4577-4581.
41. Salamon D, et al. 2012. Type I interferons directly down-regulate BCL-6 in primary and transformed germinal center B cells: differential regulation in B cell lines derived from endemic or sporadic Burkitt's lymphoma. Cytokine 57:360-371.
42. Schneider U, Schwenk HU, Bornkamm G. 1977. Characterization of EBV-genome negative "null" and "T" cell lines derived from children with acute lymphoblastic leukemia and leukemic transformed non-Hodgkin lymphoma. Int. J. Cancer 19:621-626.
43. Su L, David M. 2000. Distinct mechanisms of STAT phosphorylation via the interferon-alpha/beta receptor. Selective inhibition of STAT3 and STAT5 by piceatannol. J. Biol. Chem. 275:12661-12666.
44. Takacs M, et al. 2001. Epigenetics of latent Epstein-Barr virus genomes: high resolution methylation analysis of the bidirectional promoter region of latent membrane protein 1 and 2B genes. Biol. Chem. 382:699-705.
45. Takada K, et al. 1991. An Epstein-Barr virus-producer line Akata: establishment of the cell line and analysis of viral DNA. Virus Genes 5:147-156.
46. Theofilopoulos AN, Baccala R, Beutler B, Kono DH. 2005. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 23:307-336.
47. Thorley-Lawson DA. 1981. The transformation of adult but not newborn human lymphocytes by Epstein Barr virus and phytohemagglutinin is inhibited by interferon: the early suppression by T cells of Epstein Barr infection is mediated by interferon. J. Immunol. 126:829-833.
48. Thorley-Lawson DA, Allday MJ. 2008. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat. Rev. Microbiol. 6:913-924.
49. Yamamoto N, et al. 2003. The orally available spleen tyrosine kinase inhibitor 2-[7-(3,4-dimethoxyphenyl)-imidazo[1,2-c]pyrimidin-5-ylamino]-nicotinamide dihydrochloride (BAY 61-3606) blocks antigeninduced airway inflammation in rodents. J. Pharmacol. Exp. Ther. 306: 1174-1181.