CTCF prevents the epigenetic drift of EBV latency promoter Qp

PLoS Pathogens

Volumn 6, Issue 8, 2010, Pages 41-42

  Tempera, Italo ^a,b   Wiedmer, Andreas ^a   Dheekollu, Jayaraju ^a   Lieberman, Paul M ^a  

^a WISTAR INSTITUTE   (United States)

^b Pasteur Institute   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HYGROMYCIN; TRANSCRIPTION FACTOR CTCF; CCCTC-BINDING FACTOR; REPRESSOR PROTEIN;

ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; DNA MODIFICATION; EPSTEIN BARR VIRUS INFECTION; GENE MAPPING; GENE MUTATION; GENETIC DRIFT; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PROMOTER REGION; PROTEIN BINDING; QP GENE; TRANSCRIPTION INITIATION; VIRUS GENOME; VIRUS LATENCY; CELL LINE; CHROMATIN; CHROMOSOME MAP; EPSTEIN BARR VIRUS; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC TRANSFECTION; GENETICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS GENE;

HUMAN HERPESVIRUS 4;

CELL LINE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME MAPPING; DNA METHYLATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPIGENESIS, GENETIC; EPSTEIN-BARR VIRUS INFECTIONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, VIRAL; GENES, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION; VIRUS LATENCY;

EID: 77958134523     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001048     Document Type: Article

References (67)

1. Kieff E (2007) Epstein-Barr Virus and its replication.; Fields BN, Knipe DM, Howley PM, eds. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins, 2 v. (xix, 3091, 3086 p.) p.
2. Rickinson AB, Kieff E (2007) Epstein-Barr Virus.; Fields BN, Knipe DM, Howley PM, eds. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins, 2 v. (xix, 3091, 3086 p.) p.
3. Young LS, Rickinson AB (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4: 757-768.
4. Rowe M, Rowe DT, Gregory CD, Rickinson AB, et al. (1987) Differences in B- cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt's lymphoma cells. EMBO J 6: 2743-2751.
5. Babcock GJ, Hochberg D, Thorley-Lawson AD (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.
6. Thorley-Lawson DA (2001) Epstein-Barr virus: exploiting the immune system. Nat Rev Immunol 1: 75-82.
7. Miyashita EM, Yang B, Lam KM, Crawford DH, Thorley-Lawson DA (1995) A novel form of Epstein-Barr virus latency in normal B cells in vivo. Cell 80: 593-601.
8. Chen F, Zou JZ, di Renzo L, Winberg G, Hu LF, et al. (1995) A subpopulation of normal B cells latently infected with Epstein-Barr virus resembles Burkitt lymphoma cells in expressing EBNA-1 but not EBNA-2 or LMP1. J Virol 69: 3752-3758.
9. Qu L, Rowe DT (1992) Epstein-Barr virus latent gene expression in uncultured peripheral blood lymphocytes. J Virol 66: 3715-3724.
10. Tierney RJ, Steven N, Young LS, Rickinson AB (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.
11. Fahraeus R, Fu HL, Ernberg I, Finke J, Rowe M, et al. (1988) Expression of Epstein-Barr virus-encoded proteins in nasopharyngeal carcinoma. Int J Cancer 42: 329-338.
12. Shibata D, Weiss LM (1992) Epstein-Barr virus-associated gastric adenocarci-noma. Am J Pathol 140: 769-774.
13. Young LS, Dawson CW, Clark D, Rupani H, Busson P, et al. (1988) Epstein- Barr virus gene expression in nasopharyngeal carcinoma. J Gen Virol 69 (Pt 5): 1051-1065.
14. Farrell PJ (1995) Epstein-Barr virus immortalizing genes. Trends Microbiol 3: 105-109.
15. Thorley-Lawson DA, Gross A (2004) Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med 350: 1328-1337.
16. Woisetschlaeger M, Strominger JL, Speck SH (1989) Mutually exclusive use of viral promoters in Epstein-Barr virus latently infected lymphocytes. Proc Natl Acad Sci U S A 86: 6498-6502.
17. Woisetschlaeger M, Jin XW, Yandava CN, Furmanski LA, Strominger JL, et al. (1991) Role for the Epstein-Barr virus nuclear antigen 2 in viral promoter switching during initial stages of infection. Proc Natl Acad Sci U S A 88: 3942-3946.
18. Lina IY, Speck SH (2000) Regulation of EBNA gene expression. Epstein-Barr Virus Report 7: 175-185.
19. Rowe M, Lear AL, Croom-Carter D, Davies AH, Rickinson AB (1992) Three pathways of Epstein-Barr virus gene activation from EBNA1-positive latency in B lymphocytes. J Virol 66: 122-131.
20. Nonkwelo C, Skinner J, Bell A, Rickinson A, Sample J (1996) Transcription start sites downstream of the Epstein-Barr virus (EBV) Fp promoter in early-passage Burkitt lymphoma cells define a fourth promoter for expression of the EBV EBNA-1 protein. J Virol 70: 623-627.
21. Tierney R, Kirby H, Nagra J, Rickinson A, Bell A (2000) The Epstein-Barr virus promoter initiating B-cell transformation is activated by RFX proteins and the B-cell-specific activator protein BSAP/Pax5. J Virol 74: 10458-10467.
22. Yoo L, Speck SH (2000) Determining the role of the Epstein-Barr virus Cp EBNA2-dependent enhancer during the establishment of latency by using mutant and wild-type viruses recovered from cottontop marmoset lymphoblastoid cell lines. J Virol 74: 11115-11120.
23. Ling PD, Rawlins DR, Hayward SD (1993) The Epstein-Barr virus immortalizing protein EBNA2 is targeted to DNA by a cellular enhancer binding protein. Proc Natl Acad Sci, USA 90: 9237-9241.
24. Henkel T, Ling PD, Hayward SD, Peterson MG (1994) Mediation of Epstein-Barr virus EBNA2 transactivation by recombination signal-binding protein J kappa. Science 265: 92-95.
25. Abbot SD, Rowe M, Cadwallader K, Ricksten A, Gordon J, et al. (1990) Epstein-Barr virus nuclear antigen 2 induces expression of the virus-encoded latent membrane protein. J Virol 64: 2126-2134.
26. Ambinder RF, Robertson KD, Tao Q (1999) DNA methylation and the Epstein-Barr virus. Semin Cancer Biol 9: 369-375.
27. Falk KI, Szekely L, Aleman A, Ernberg I (1998) Specific methylation patterns in two control regions of Epstein-Barr virus latency: the LMP-1-coding upstream regulatory region and an origin of DNA replication (oriP). J Virol 72: 2969-2974.
28. Robertson KD, Manns A, Swinnen LJ, Zong JC, Gulley ML, et al. (1996) CpG methylation of the major Epstein-Barr virus latency promoter in Burkitt's lymphoma and Hodgkin's disease. Blood 88: 3129-3136.
29. Robertson KD, Hayward SD, Ling PD, Samid D, Ambinder RF (1995) Transcriptional activation of the Epstein-Barr virus latency C promoter after 5- azacytidine treatment: evidence that demethylation at a single CpG site is crucial. Mol Cell Biol 15: 6150-6159.
30. Jin XW, Speck SH (1992) Identification of critical cis elements involved in mediating Epstein-Barr virus nuclear antigen 2-dependent activity of an enhancer located upstream of the viral BamHI C promoter. J Virol 66: 2846-2852.
31. Woisetschlaeger M, Yandava CN, Furmanski LA, Strominger JL, Speck SH (1990) Promoter switching in Epstein-Barr virus during the initial stages of infection of B lymphocytes. Proc Natl Acad Sci U S A 87: 1725-1729.
32. Allday MJ, Kundu D, Finerty S, Griffin BE (1990) CpG methylation of viral DNA in EBV-associated tumours. Int J Cancer 45: 1125-1130.
33. Ernberg I, Falk K, Minarovits J, Busson P, Tursz T, 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 (Pt 11): 2989-3002.
34. Humme S, Reisbach G, Feederle R, Delecluse HJ, Bousset K, et al. (2003) The EBV nuclear antigen 1 (EBNA1) enhances B cell immortalization several thousandfold. Proc Natl Acad Sci U S A 100: 10989-10994.
35. Kennedy G, Sugden B (2003) EBNA-1, a Bifunctional Transcriptional Activator. Mol Cell Biol 23: 6901-6908.
36. Wang J, Lindner SE, Leight ER, Sugden B (2006) Essential elements of a licensed, mammalian plasmid origin of DNA synthesis. Mol Cell Biol 26: 1124-1134.
37. Lindner SE, Sugden B (2007) The plasmid replicon of Epstein-Barr virus: mechanistic insights into efficient, licensed, extrachromosomal replication in human cells. Plasmid 58: 1-12.
38. Schaefer BC, Strominger JL, Speck SH (1995) Redefining the Epstein-Barr virus-encoded nuclear antigen EBNA-1 gene promoter and transcription initiation site in group I Burkitt lymphoma cell lines. Proc Natl Acad Sci U S A 92: 10565-10569.
39. Tsai CN, Liu ST, Chang YS (1995) Identification of a novel promoter located within the Bam HI Q region of the Epstein-Barr virus genome for the EBNA 1 gene. DNA Cell Biol 14: 767-776.
40. Nonkwelo C, Ruf IK, Sample J (1997) The Epstein-Barr virus EBNA-1 promoter Qp requires an initiator-like element. J Virol 71: 354-361.
41. Yoshioka M, Crum MM, Sample JT (2008) Autorepression of Epstein-Barr virus nuclear antigen 1 expression by inhibition of pre-mRNA processing. J Virol 82: 1679-1687.
42. Ruf IK, Moghaddam A, Wang F, Sample J (1999) Mechanisms that regulate Epstein-Barr virus EBNA-1 gene transcription during restricted latency are conserved among lymphocryptoviruses of Old World primates. J Virol 73: 1980-1989.
43. Minarovits J (2006) Epigenotypes of latent herpesvirus genomes. Curr Top Microbiol Immunol 310: 61-80.
44. Alazard N, Gruffat H, Hiriart E, Sergeant A, Manet E (2003) Differential hyperacetylation of histones H3 and H4 upon promoter-specific recruitment of EBNA2 in Epstein-Barr virus chromatin. J Virol 77: 8166-8172.
45. Altmann M, Pich D, Ruiss R, Wang J, Sugden B, et al. (2006) Transcriptional activation by EBV nuclear antigen 1 is essential for the expression of EBV's transforming genes. Proc Natl Acad Sci U S A 103: 14188-14193.
46. Reisman D, Sugden B (1986) Trans activation of an Epstein-Barr viral transcriptional enhancer by the Epstein-Barr viral nuclear antigen 1. Mol Cell Biol 5: 3838-3846.
47. Puglielli MT, Woisetschlaeger M, Speck SH (1996) OriP is essential for EBNA gene promoter activity in Epstein-Barr virus-immortalized lymphoblastoid cell lines. J Virol 70: 5758-5768.
48. Bushey AM, Dorman ER, Corces VG (2008) Chromatin insulators: regulatory mechanisms and epigenetic inheritance. Mol Cell 32: 1-9.
49. West AG, Gaszner M, Felsenfeld G (2002) Insulators: many functions, many mechanisms. Genes Dev 16: 271-288.
50. Wallace JA, Felsenfeld G (2007) We gather together: insulators and genome organization. Curr Opin Genet Dev 17: 400-407.
51. Capelson M, Corces VG (2004) Boundary elements and nuclear organization. Biol Cell 96: 617-629.
52. Phillips JE, Corces VG (2009) CTCF: master weaver of the genome. Cell 137: 1194-1211.
53. Ohlsson R, Renkawitz R, Lobanenkov V (2001) CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 17: 520-527.
54. Day L, Chau CM, Nebozhyn M, Rennenkamp AJ, Showe M, et al. (2007) Chromatin Profiling Of Epstein-Barr Virus Latency Control Region. J Virol.
55. Chau CM, Zhang XY, McMahon SB, Lieberman PM (2006) Regulation of Epstein-Barr virus latency type by the chromatin boundary factor CTCF. J Virol 80: 5723-5732.
56. Copeland NG, Jenkins NA, Court DL (2001) Recombineering: a powerful new tool for mouse functional genomics. Nat Rev Genet 2: 769-779.
57. Paulson EJ, Fingeroth JD, Yates JL, Speck SH (2002) Methylation of the EBV genome and establishment of restricted latency in low-passage EBV-infected 293 epithelial cells. Virology 299: 109-121.
58. Trivedi P, Spinsanti P, Cuomo L, Volpe M, Takada K, et al. (2001) Differential regulation of Epstein-Barr virus (EBV) latent gene expression in Burkitt lymphoma cells infected with a recombinant EBV strain. J Virol 75: 4929-4935.
59. Li H, Minarovits J (2003) Host cell-dependent expression of latent Epstein-Barr virus genomes: regulation by DNA methylation. Adv Cancer Res 89: 133-156.
60. Chau CM, Lieberman PM (2004) Dynamic chromatin boundaries delineate a latency control region of Epstein-Barr virus. J Virol 78: 12308-12319.
61. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, et al. (2000) CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405: 486-489.
62. Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF, et al. (2000) Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr Biol 10: 853-856.
63. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447: 407-412.
64. Chernukhin I, Shamsuddin S, Kang SY, Bergstrom R, Kwon YW, et al. (2007) CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide. Mol Cell Biol 27: 1631-1648.
65. Delecluse HJ, Hilsendegen T, Pich D, Zeidler R, Hammerschmidt W (1998) Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc Natl Acad Sci U S A 95: 8245-8250.
66. Deng Z, Lezina L, Chen CJ, Shtivelband S, So W, et al. (2002) Telomeric proteins regulate episomal maintenance of Epstein-Barr virus origin of plasmid replication. Mol Cell 9: 493-503.
67. Hirt B (1967) Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol 26: 365-369.