Cellular differentiation regulator BLIMP1 induces epstein-barr virus lytic reactivation in epithelial and B cells by activating transcription from both the R and Z promoters

Journal of Virology

Volumn 89, Issue 3, 2015, Pages 1731-1743

  Reusch, Jessica A ^a   Nawandar, Dhananjay M ^a   Wright, Kenneth L ^b   Kenney, Shannon C ^a,c   Mertz, Janet E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BRLF1 PROTEIN, HUMAN HERPESVIRUS 4; BZLF1 PROTEIN, HERPESVIRUS 4, HUMAN; IMMEDIATE EARLY PROTEIN; PRDM1 PROTEIN, HUMAN; REPRESSOR PROTEIN; TRANSACTIVATOR PROTEIN;

ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; BINDING SITE; BRLF1 GENE; BZLF1 GENE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; EPITHELIUM CELL; EPSTEIN BARR VIRUS; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; IMMEDIATE EARLY GENE; KERATINOCYTE; MOLECULAR DYNAMICS; NASOPHARYNX CARCINOMA; NONHUMAN; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STOMACH CANCER; VIRUS GENE; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS REPLICATION; BIOSYNTHESIS; CELL LINE; GENETIC TRANSCRIPTION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS ACTIVATION;

HUMAN HERPESVIRUS 4;

B-LYMPHOCYTES; CELL LINE; EPITHELIAL CELLS; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84921480902     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02781-14     Document Type: Article

References (94)

1. Henle G, Henle W, Diehl V. 1968. Relation of Burkitt's tumor-associated herpes-ytpe virus to infectious mononucleosis. Proc Natl Acad Sci U S A 59:94-101. http://dx.doi.org/10.1073/pnas.59.1.94.
2. Cohen JI. 2000. Epstein-Barr virus infection. N Engl J Med 343:481-492. http://dx.doi.org/10.1056/NEJM200008173430707.
3. Lindahl T, Adams A, Bjursell G, Bornkamm GW, Kaschka-Dierich C, Jehn U. 1976. Covalently closed circular duplex DNA of Epstein-Barr virus in a human lymphoid cell line. J Mol Biol 102:511-530. http://dx.doi.org/10.1016/0022-2836(76)90331-4.
4. Epstein MA, Achong BG, Barr YM. 1964. Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet i:702-703.
5. zur Hausen H, Schulte-Holthausen H, Klein G, Henle W, Henle G, Clifford P, Santesson L. 1970. Epstein-Barr virus in Burkitt's lymphoma and nasopharyngeal carcinoma: EBV DNA in biopsies of Burkitt tumours and anaplastic carcinomas of the nasopharynx. Nature 228:1056-1058. http://dx.doi.org/10.1038/2281056a0.
6. Desgranges C, Wolf H, De-Thé G, Shanmugaratnam K, Cammoun N, Ellouz R, Klein G, Lennert K, Muñoz N, Zur Hausen H. 1975. Nasopharyngeal carcinoma. X. Presence of Epstein-Barr genomes in separated epithelial cells of tumours in patients from Singapore, Tunisia and Kenya. Int J Cancer 16:7-15.
7. Nalesnik MA, Jaffe R, Starzl TE, Demetris AJ, Porter K, Burnham JA, Makowka L, Ho M, Locker J. 1988. The pathology of posttransplant lymphoproliferative disorders occurring in the setting of cyclosporine Aprednisone immunosuppression. Am J Pathol 133:173-192.
8. Shibata D, Weiss LM. 1992. Epstein-Barr virus-associated gastric adenocarcinoma. Am J Pathol 140:769-774.
9. Paya CV, Fung JJ, Nalesnik MA, Kieff E, Green M, Gores G, Habermann TM, Wiesner PH, Swinnen JL, Woodle ES, Bromberg JS. 1999. Epstein-Barr virus-induced posttransplant lymphoproliferative disorders. ASTS/ASTP EBV-PTLD Task Force and The Mayo Clinic Organized International Consensus Development Meeting. Transplantation 68:1517-1525.
10. Kieff E, Rickinson AB. 2007. Epstein-Barr virus and its replication, p 1225-2654. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
11. Rickinson AB, Kieff E. 2007. Epstein-Barr virus, p 2655-2700. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams&Wilkins, Philadelphia, PA.
12. Kimura H, Kawada J, Ito Y. 2013. Epstein-Barr virus-associated lymphoid malignancies: the expanding spectrum of hematopoietic neoplasms. Nagoya J Med Sci 75:169-179. http://www.med.nagoya-u.ac.jp/medlib/nagoya_j_med_sci/7534/02_Kimura.pdf.
13. Feederle R, Kost M, Baumann M, Janz A, Drouet E, Hammerschmidt W, Delecluse H-J. 2000. The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. EMBO J 19:3080-3089. http://dx.doi.org/10.1093/emboj/19.12.3080.
14. Countryman J, Miller G. 1985. Activation of expression of latent Epstein-Barr herpesvirus after gene transfer with a small cloned subfragment of heterogeneous viral DNA. Proc Natl Acad Sci U S A 82:4085-4089. http://dx.doi.org/10.1073/pnas.82.12.4085.
15. Takada K, Shimizu N, Sakuma S, Ono Y. 1986. trans Activation of the latent Epstein-Barr virus (EBV) genome after transfection of the EBV DNA fragment. J Virol 57:1016-1022.
16. Chevallier-Greco A, Manet E, Chavrier P, Mosnier C, Daillie J, Sergeant A. 1986. Both Epstein-Barr virus (EBV)-encoded trans-acting factors, EB1 and EB2, are required to activate transcription from an EBV early promoter. EMBO J 5:3243-3249.
17. Countryman J, Jenson H, Seibl R, Wolf H, Miller G. 1987. Polymorphic proteins encoded within BZLF1 of defective and standard Epstein-Barr viruses disrupt latency. J Virol 61:3672-3679.
18. Flemington E, Speck SH. 1990. Autoregulation of Epstein-Barr virus putative lytic switch gene BZLF1. J Virol 64:1227-1232.
19. Sinclair AJ, Brimmell M, Shanahan F, Farrell PJ. 1991. Pathways of activation of the Epstein-Barr virus productive cycle. J Virol 65:2237-2244.
20. Zalani S, Holley-Guthrie E, Kenney S. 1996. Epstein-Barr viral latency is disrupted by the immediate-early BRLF1 protein through a cell-specific mechanism. Proc Natl Acad Sci U S A 93:9194-9199. http://dx.doi.org/10.1073/pnas.93.17.9194.
21. Ragoczy T, Heston L, Miller G. 1998. The Epstein-Barr virus Rta protein activates lytic cycle genes and can disrupt latency in B lymphocytes. J Virol 72:7978-7984.
22. Adamson AL, Darr D, Holley-Guthrie E, Johnson RA, Mauser A, Swenson J, Kenney S. 2000. Epstein-Barr virus immediate early proteins BZLF1 and BRLF1 activate the ATF2 transcription factor by increasing the levels of phosphorylated p38 and c-Jun N-terminal kinases. J Virol 74:1224-1233. http://dx.doi.org/10.1128/JVI.74.3.1224-1233.2000.
23. Lin T-Y, Chu Y-Y, Yang Y-C, Hsu S-W, Liu S-T, Chang L-K. 2014. MCAF1 and Rta-activated BZLF1 transcription in Epstein-Barr virus. PLoS One 9:e90698. http://dx.doi.org/10.1371/journal.pone.0090698.
24. Murata T, Narita Y, Sugimoto A, Kawashima D, Kanda T, Tsurumi T. 2013. Contribution of myocyte enhancer factor 2 family transcription factors to BZLF1 expression in Epstein-Barr virus reactivation from latency. J Virol 87:10148-10162. http://dx.doi.org/10.1128/JVI.01002-13.
25. Wille CK, Nawandar DM, Panfil AR, Ko MM, Hagemeier SR, Kenney SC. 2013. Viral genome methylation differentially affects the ability of BZLF1 versus BRLF1 to activate Epstein-Barr virus lytic gene expression and viral replication. J Virol 87:935-950. http://dx.doi.org/10.1128/JVI.01790-12.
26. Hardwick JM, Lieberman PM, Hayward SD. 1988. A new Epstein-Barr virus transactivator, R, induces expression of a cytoplasmic early antigen. J Virol 62:2274-2284.
27. Cox MA, Leahy J, Hardwick JM. 1990. An enhancer within the divergent promoter of Epstein-Barr virus responds synergistically to the R and Z transactivators. J Virol 64:313-321.
28. Ragoczy T, Miller G. 1999. Role of the Epstein-Barr virus RTA protein in activation of distinct classes of viral lytic cycle genes. J Virol 73:9858-9866.
29. Miller G, El-Guindy A, Countryman J, Ye J, Gradoville L. 2007. Lytic cycle switches of oncogenic human gammaherpesviruses. Adv Cancer Res 97:81-109. http://dx.doi.org/10.1016/S0065-230X(06)97004-3.
30. Speck SH, Chatila T, Flemington E. 1997. Reactivation of Epstein-Barr virus: regulation and function of the BZLF1 gene. Trends Microbiol 5:399-405. http://dx.doi.org/10.1016/S0966-842X(97)01129-3.
31. Murata T. 2014. Regulation of Epstein-Barr virus reactivation from latency. Microbiol Immunol 58:307-317. http://dx.doi.org/10.1111/1348-0421.12155.
32. Murata T, Tsurumi T. 2014. Switching of EBV cycles between latent and lytic states. Rev Med Virol 24:142-153. http://dx.doi.org/10.1002/rmv.1780.
33. Kenney SC, Mertz JE. 2014. Regulation of the latent-lytic switch in Epstein-Barr virus. Semin Cancer Biol 26:60-68. http://dx.doi.org/10.1016/j.semcancer.2014.01.002.
34. Ragoczy T, Miller G. 2001. Autostimulation of the Epstein-Barr virus BRLF1 promoter is mediated through consensus Sp1 and Sp3 binding sites. J Virol 75:5240-5251. http://dx.doi.org/10.1128/JVI.75.11.5240-5251.2001.
35. Liu P, Speck SH. 2003. Synergistic autoactivation of the Epstein-Barr virus immediate-early BRLF1 promoter by Rta and Zta. Virology 310:199-206. http://dx.doi.org/10.1016/S0042-6822(03)00145-4.
36. Laichalk LL, Thorley-Lawson DA. 2005. Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J Virol 79:1296-1307. http://dx.doi.org/10.1128/JVI.79.2.1296-1307.2005.
37. Young LS, Lau R, Rowe M, Niedobitek G, Packham G, Shanahan F, Rowe DT, Greenspan D, Greenspan JS, Rickinson AB. 1991. Differentiation-associated expression of the Epstein-Barr virus BZLF1 transactivator protein in oral hairy leukoplakia. J Virol 65:2868-2874.
38. Bhende PM, Dickerson SJ, Sun X, Feng W-H, Kenney SC. 2007. X-box-binding protein 1 activates lytic Epstein-Barr virus gene expression in combination with protein kinase D. J Virol 81:7363-7370. http://dx.doi.org/10.1128/JVI.00154-07.
39. Sun CC, Thorley-Lawson DA. 2007. Plasma cell-specific transcription factor XBP-1s binds to and transactivates the Epstein-Barr virus BZLF1 promoter. J Virol 81:13566-13577. http://dx.doi.org/10.1128/JVI.01055-07.
40. Turner CA, Jr, Mack DH, Davis MM. 1994. Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 77:297-306. http://dx.doi.org/10.1016/0092-8674(94)90321-2.
41. Shapiro-Shelef M, Lin K-I, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG, Calame K. 2003. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 19:607-620. http://dx.doi.org/10.1016/S1074-7613(03)00267-X.
42. Magnúsdóttir E, Kalachikov S, Mizukoshi K, Savitsky D, Ishida-Yamamoto A, Panteleyev AA, Calame K. 2007. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc Natl Acad Sci U S A 104:14988-14993. http://dx.doi.org/10.1073/pnas.0707323104.
43. Chiang M-F, Yang S-Y, Lin I-Y, Hong J-B, Lin S-J, Ying H-Y, Chen C-M, Wu S-Y, Liu F-T, Lin K-I. 2013. Inducible deletion of the Blimp-1 gene in adult epidermis causes granulocyte-dominated chronic skin inflammation in mice. Proc Natl Acad Sci U S A 110:6476-6481. http://dx.doi.org/10.1073/pnas.1219462110.
44. Keller AD, Maniatis T. 1992. Only two of the five zinc fingers of the eukaryotic transcriptional repressor PRDI-BF1 are required for sequencespecific DNA binding. Mol Cell Biol 12:1940-1949.
45. Kuo TC, Calame KL. 2004. B lymphocyte-induced maturation protein (Blimp)-1, IFN regulatory factor (IRF)-1, and IRF-2 can bind to the same regulatory sites. J Immunol 173:5556-5563. http://dx.doi.org/10.4049/jimmunol.173.9.5556.
46. Lin Y, Wong K, Calame K. 1997. Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation. Science 276:596-599. http://dx.doi.org/10.1126/science.276.5312.596.
47. Shaffer AL, Lin K-I, Kuo TC, Yu X, Hurt EM, Rosenwald A, Giltnane JM, Yang L, Zhao H, Calame K, Staudt LM. 2002. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17:51-62. http://dx.doi.org/10.1016/S1074-7613(02)00335-7.
48. Lin K-I, Angelin-Duclos C, Kuo TC, Calame K. 2002. Blimp-1-dependent repression of Pax-5 is required for differentiation of B cells to immunoglobulin M-secreting plasma cells. Mol Cell Biol 22:4771-4780. http://dx.doi.org/10.1128/MCB.22.13.4771-4780.2002.
49. Yan J, Jiang J, Lim CA, Wu Q, Ng H-H, Chin K-C. 2007. BLIMP1 regulates cell growth through repression of p53 transcription. Proc Natl Acad SciUSA 104:1841-1846. http://dx.doi.org/10.1073/pnas.0605562104.
50. Keller AD, Maniatis T. 1991. Identification and characterization of a novel repressor of beta-interferon gene expression. Genes Dev 5:868-879. http://dx.doi.org/10.1101/gad.5.5.868.
51. Ren B, Chee KJ, Kim TH, Maniatis T. 1999. PRDI-BF1/Blimp-1 repression is mediated by corepressors of the Groucho family of proteins. Genes Dev 13:125-137. http://dx.doi.org/10.1101/gad.13.1.125.
52. Chen G, Fernandez J, Mische S, Courey AJ. 1999. A functional interaction between the histone deacetylase Rpd3 and the corepressor Groucho in Drosophila development. Genes Dev 13:2218-2230. http://dx.doi.org/10.1101/gad.13.17.2218.
53. Yu J, Angelin-Duclos C, Greenwood J, Liao J, Calame K. 2000. Transcriptional repression by Blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase. Mol Cell Biol 20:2592-2603. http://dx.doi.org/10.1128/MCB.20.7.2592-2603.2000.
54. Gyory I, Wu J, Fejér G, Seto E, Wright KL. 2004. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat Immunol 5:299-308. http://dx.doi.org/10.1038/ni1046.
55. Robinson AR, Kwek SS, Kenney SC. 2012. The B-cell specific transcription factor, Oct-2, promotes Epstein-Barr virus latency by inhibiting the viral immediate-early protein, BZLF1. PLoS Pathog 8:e1002516. http://dx.doi.org/10.1371/journal.ppat.1002516.
56. Raver RM, Panfil AR, Hagemeier SR, Kenney SC. 2013. The B-cell-specific transcription factor and master regulator Pax5 promotes Epstein-Barr virus latency by negatively regulating the viral immediate early protein BZLF1. J Virol 87:8053-8063. http://dx.doi.org/10.1128/JVI.00546-13.
57. Nera K-P, Kohonen P, Narvi E, Peippo A, Mustonen L, Terho P, Koskela K, Buerstedde J-M, Lassila O. 2006. Loss of Pax5 promotes plasma cell differentiation. Immunity 24:283-293. http://dx.doi.org/10.1016/j.immuni.2006.02.003.
58. Vrzalikova K, Vockerodt M, Leonard S, Bell A, Wei W, Schrader A, Wright KL, Kube D, Rowe M, Woodman CB, Murray PG. 2011. Down-regulation of BLIMP1α by the EBV oncogene, LMP-1, disrupts the plasma cell differentiation program and prevents viral replication in B cells: implications for the pathogenesis of EBV-associated B-cell lymphomas. Blood 117:5907-5917. http://dx.doi.org/10.1182/blood-2010-09-307710.
59. Buettner M, Lang A, Tudor CS, Meyer B, Cruchley A, Barros MHM, Farrell PJ, Jäck H-M, Schuh W, Niedobitek G. 2012. Lytic Epstein-Barr virus infection in epithelial cells but not in B-lymphocytes is dependent on Blimp1. J Gen Virol 93:1059-1064. http://dx.doi.org/10.1099/vir.0.038661-0.
60. Park JG, Yang HK, Kim WH, Chung JK, Kang MS, Lee JH, Oh JH, Park HS, Yeo KS, Kang SH, Song SY, Kang YK, Bang YJ, Kim YH, Kim JP. 1997. Establishment and characterization of human gastric carcinoma cell lines. Int J Cancer 70:443-449. http://dx.doi.org/10.1002/(SICI)1097-0215(19970207)70:4<443::AID-IJC12>3.0.CO;2-G.
61. Strong MJ, Baddoo M, Nanbo A, Xu M, Puetter A, Lin Z. 2014. Comprehensive high-throughput RNA sequencing analysis reveals contamination of multiple nasopharyngeal carcinoma cell lines with HeLa cell genomes. J Virol 88:10696-10704. http://dx.doi.org/10.1128/JVI.01457-14.
62. 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. http://dx.doi.org/10.1038/nm758.
63. Kelly GL, Stylianou J, Rasaiyaah J, Wei W, Thomas W, Croom-Carter D, Kohler C, Spang R, Woodman C, Kellam P, Rickinson AB, Bell AI. 2013. Different patterns of Epstein-Barr virus latency in endemic Burkitt lymphoma (BL) lead to distinct variants within the BL-associated gene expression signature. J Virol 87:2882-2894. http://dx.doi.org/10.1128/JVI.03003-12.
64. Györy I, Fejér G, Ghosh N, Seto E, Wright KL. 2003. Identification of a functionally impaired positive regulatory domain I binding factor 1 transcription repressor in myeloma cell lines. J Immunol 170:3125-3133. http://dx.doi.org/10.4049/jimmunol.170.6.3125.
65. Ghosh N, Gyory I, Wright G, Wood J, Wright KL. 2001. Positive regulatory domain I binding factor 1 silences class II transactivator expression in multiple myeloma cells. J Biol Chem 276:15264-15268. http://dx.doi.org/10.1074/jbc.M100862200.
66. Sarisky RT, Gao Z, Lieberman PM, Fixman ED, Hayward GS, Hayward SD. 1996. A replication function associated with the activation domain of the Epstein-Barr virus Zta transactivator. J Virol 70:8340-8347.
67. Ghosh N, Piskurich JF, Wright G, Hassani K, Ting JP-Y, Wright KL. 1999. A novel element and a TEF-2-like element activate the major histocompatibility complex class II transactivator in B-lymphocytes. J Biol Chem 274:32342-32350. http://dx.doi.org/10.1074/jbc.274.45.32342.
68. Klug M, Rehli M. 2006. Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 1:127-130. http://dx.doi.org/10.4161/epi.1.3.3327.
69. Adamson AL, Kenney S. 2001. Epstein-Barr virus immediate-early protein BZLF1 is SUMO-1 modified and disrupts promyelocytic leukemia bodies. J Virol 75:2388-2399. http://dx.doi.org/10.1128/JVI.75.5.2388-2399.2001.
70. Altmann M, Hammerschmidt W. 2005. Epstein-Barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis. PLoS Biol 3:e404. http://dx.doi.org/10.1371/journal.pbio.0030404.
71. Gonzalez E, Kulkarni H, Bolivar H, Mangano A, Sanchez R, Catano G, Nibbs RJ, Freedman BI, Quinones MP, Bamshad MJ, Murthy KK, Rovin BH, Bradley W, Clark RA, Anderson SA, O'Connell RJ, Agan BK, Ahuja SS, Bologna R, Sen L, Dolan MJ, Ahuja SK. 2005. The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307:1434-1440. http://dx.doi.org/10.1126/science.1101160.
72. Schreiber E, Matthias P, Muller MM, Schaffner W. 1989. Rapid detection of octamer binding proteins with "mini-extracts," prepared from a small number of cells. Nucleic Acids Res 17:6419. http://dx.doi.org/10.1093/nar/17.15.6419.
73. Kraus RJ, Mirocha SJ, Stephany HM, Puchalski JR, Mertz JE. 2001. Identification of a novel element involved in regulation of the lytic switch BZLF1 gene promoter of Epstein-Barr virus. J Virol 75:867-877. http://dx.doi.org/10.1128/JVI.75.2.867-877.2001.
74. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098-1101. http://dx.doi.org/10.1126/science.1106148.
75. zur Hausen H, Bornkamm GW, Schmidt R, Hecker E. 1979. Tumor initiators and promoters in the induction of Epstein-Barr virus. Proc Natl Acad Sci U S A 76:782-785. http://dx.doi.org/10.1073/pnas.76.2.782.
76. Flemington E, Speck SH. 1990. Identification of phorbol ester response elements in the promoter of Epstein-Barr virus putative lytic switch gene BZLF1. J Virol 64:1217-1226.
77. Davies AH, Grand RJ, Evans FJ, Rickinson AB. 1991. Induction of Epstein-Barr virus lytic cycle by tumor-promoting and non-tumorpromoting phorbol esters requires active protein kinase C. J Virol 65:6838-6844.
78. Bhende PM, Seaman WT, Delecluse H-J, Kenney SC. 2004. The EBV lytic switch protein, Z, preferentially binds to and activates the methylated viral genome. Nat Genet 36:1099-1104. http://dx.doi.org/10.1038/ng1424.
79. Fernandez AF, Rosales C, Lopez-Nieva P, Graña O, Ballestar E, Ropero S, Espada J, Melo SA, Lujambio A, Fraga MF, Pino I, Javierre B, Carmona FJ, Acquadro F, Steenbergen RDM, Snijders PJF, Meijer CJ, Pineau P, Dejean A, Lloveras B, Capella G, Quer J, Buti M, Esteban J-I, Allende H, Rodriguez-Frias F, Castellsague X, Minarovits J, Ponce J, Capello D, Gaidano G, Cigudosa JC, Gomez-Lopez G, Pisano DG, Valencia A, Piris MA, Bosch FX, Cahir-McFarland E, Kieff E, Esteller M. 2009. The dynamic DNA methylomes of double-stranded DNA viruses associated with human cancer. Genome Res 19:438-451. http://dx.doi.org/10.1101/gr.083550.108.
80. Bergbauer M, Kalla M, Schmeinck A, Göbel C, Rothbauer U, Eck S, Benet-Pagès A, Strom TM, Hammerschmidt W. 2010. CpG-methylation regulates a class of Epstein-Barr virus promoters. PLoS Pathog 6:e1001114. http://dx.doi.org/10.1371/journal.ppat.1001114.
81. John SA, Garrett-Sinha LA. 2009. Blimp1: a conserved transcriptional repressor critical for differentiation of many tissues. Exp Cell Res 315:1077-1084. http://dx.doi.org/10.1016/j.yexcr.2008.11.015.
82. Vrzalikova K, Woodman CBJ, Murray PG. 2012. BLIMP1α, the master regulator of plasma cell differentiation is a tumor suppressor gene in B cell lymphomas. Biomed Pap Med Fac Univ Palackỳ Olomouc Czech Repub 156:1-6. http://dx.doi.org/10.5507/bp.2012.003.
83. Smith MA, Wright G, Wu J, Tailor P, Ozato K, Chen X, Wei S, Piskurich JF, Ting JP-Y, Wright KL. 2011. Positive regulatory domain I (PRDM1) and IRF8/PU.1 counter-regulate MHC class II transactivator (CIITA) expression during dendritic cell maturation. J Biol Chem 286:7893-7904. http://dx.doi.org/10.1074/jbc.M110.165431.
84. Terzaghi M, Klein-Szanto AJ. 1980. Differentiation of normal and cultured preneoplastic tracheal epithelial cells in rats: importance of epithelial mesenchymal interactions. J Natl Cancer Inst 65:1039-1048.
85. Tötterman TH, Nilsson K, Sundström C. 1980. Phorbol ester-induced differentiation of chronic lymphocytic leukaemia cells. Nature 288:176-178.
86. Hawley-Nelson P, Stanley JR, Schmidt J, Gullino M, Yuspa SH. 1982. The tumor promoter, 12-O-tetradecanoylphorbol-13-acetate accelerates keratinocyte differentiation and stimulates growth of an unidentified cell type in cultured human epidermis. Exp Cell Res 137:155-167.
87. Anisimová E, Prachová K, Roubal J, Vonka V. 1984. Effects of n-butyrate and phorbol ester (TPA) on induction of Epstein-Barr virus antigens and cell differentiation. Arch Virol 81:223-237.
88. 2+-mediated inositol lipid metabolism in normal and neoplastic epidermal cells. Carcinogenesis 9:1033-1038.
89. John SA, Clements JL, Russell LM, Garrett-Sinha LA. 2008. Ets-1 regulates plasma cell differentiation by interfering with the activity of the transcription factor Blimp-1. J Biol Chem 283:951-962. http://dx.doi.org/10.1074/jbc.M705262200.
90. John S, Russell L, Chin SS, Luo W, Oshima R, Garrett-Sinha LA. 2014. Transcription factor Ets1, but not the closely related factor Ets2, inhibits antibody-secreting cell differentiation. Mol Cell Biol 34:522-532. http://dx.doi.org/10.1128/MCB.00612-13.
91. Raghunandan R, Frissora FW, Muthusamy N. 2013. Modulation of Ets-1 expression in B lymphocytes is dependent on the antigen receptormediated activation signals and cell cycle status. Scand J Immunol 77:75-83. http://dx.doi.org/10.1111/sji.12012.
92. Luo W, Mayeux J, Gutierrez T, Russell L, Getahun A, Müller J, Tedder T, Parnes J, Rickert R, Nitschke L, Cambier J, Satterthwaite AB, Garrett-Sinha LA. 2014. A balance between B cell receptor and inhibitory receptor signaling controls plasma cell differentiation by maintaining optimal Ets1 levels. J Immunol 193:909-920. http://dx.doi.org/10.4049/jimmunol.1400666.
93. Vrzalikova K, Leonard S, Fan Y, Bell A, Vockerodt M, Flodr P, Wright KL, Rowe M, Tao Q, Murray PG. 2012. Hypomethylation and overexpression of the beta isoform of BLIMP1 is induced by Epstein-Barr virus infection of B cells; potential implications for the pathogenesis of EBVassociated lymphomas. Pathogens 1:83-101. http://dx.doi.org/10.3390/pathogens1020083.
94. Huang S, Shao G, Liu L. 1998. The PR domain of the Rb-binding zinc finger protein RIZ1 is a protein binding interface and is related to the SET domain functioning in chromatin-mediated gene expression. J Biol Chem 273:15933-15939.