Genome-wide DNA methylation as an epigenetic consequence of Epstein-Barr virus infection of immortalized keratinocytes

Journal of Virology

Volumn 88, Issue 19, 2014, Pages 11442-11458

  Birdwell, Christine E ^b   Queen, Krista J ^b,c   Kilgore, Phillip C S R ^a   Rollyson, Phoebe ^b   Trutschl, Marjan ^a   Cvek, Urska ^a   Scott, Rona S ^b  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ABC TRANSPORTER A1; AMYLOID BETA PROTEIN; CALCIUM; COLLAGEN TYPE 5; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; CXCL1 CHEMOKINE; CYTOCHROME B; CYTOGLOBIN; EPHRIN RECEPTOR; EPSTEIN BARR VIRUS ANTIGEN 1; IMMEDIATE EARLY PROTEIN BZLF1; INTERLEUKIN 21 RECEPTOR; LYMPHOID ENHANCER FACTOR 1; METHYLCELLULOSE; METHYLTRANSFERASE; MYOSIN V; NATRIURETIC PEPTIDE RECEPTOR B; NEUROFILAMENT PROTEIN; NEUROLIGIN 1; PLEXIN; PROTEIN KINASE SYK; SOMATOMEDIN BINDING PROTEIN; SYNAPTOTAGMIN; T BOX TRANSCRIPTION FACTOR; TOLL LIKE RECEPTOR 2; TRANSCRIPTION FACTOR RELA; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE; WNT5A PROTEIN; AZACITIDINE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DRUG DERIVATIVE; ENZYME INHIBITOR;

ARTICLE; CELL DIFFERENTIATION; COCULTURE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; ELECTRIC RESISTANCE; EPIGENETICS; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GENE EXPRESSION; GENE SEQUENCE; HUMAN; HUMAN CELL; IMMORTALIZED CELL LINE; KERATINOCYTE; MICROARRAY ANALYSIS; MOUTH CAVITY; NUCLEOTIDE SEQUENCE; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SEQUENCE ALIGNMENT; SOUTHERN BLOTTING; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; UPREGULATION; VIRUS GENOME; VIRUS REPLICATION; CHEMISTRY; CHROMATIN; DRUG ANTAGONISM; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; HOST PATHOGEN INTERACTION; HUMAN GENOME; METABOLISM; MOUTH MUCOSA; PROMOTER REGION; TRANSFORMED CELL LINE; VIROLOGY; VIRUS LATENCY;

AZACITIDINE; CELL LINE, TRANSFORMED; CHROMATIN; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ENZYME INHIBITORS; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENOME, HUMAN; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; KERATINOCYTES; MOUTH MUCOSA; PROMOTER REGIONS, GENETIC; VIRUS LATENCY;

EID: 84906969231     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00972-14     Document Type: Article

References (62)

1. Murray RJ, Kurilla MG, Brooks JM, Thomas WA, Rowe M, Kieff E, Rickinson AB. 1992. Identification of target antigens for the human cytotoxic T cell response to Epstein-Barr virus (EBV): implications for the immune control of EBV-positive malignancies. J. Exp. Med. 176:157-168. http://dx.doi.org/10.1084/jem.176.1.157.
2. Arvey A, Tempera I, Tsai K, Chen HS, Tikhmyanova N, Klichinsky M, Leslie C, Lieberman PM. 2012. An atlas of the Epstein-Barr virus transcriptome and epigenome reveals host-virus regulatory interactions. Cell Host Microbe 12:233-245. http://dx.doi.org/10.1016/j.chom.2012.06.008.
3. Tao Q, Robertson KD. 2003. Stealth technology: how Epstein-Barr virus utilizes DNAmethylationtocloakitselffromimmunedetection.Clin.Immunol.109:53-63. http://dx.doi.org/10.1016/S1521-6616(03)00198-0.
4. Tempera I, Lieberman PM. 2014. Epigenetic regulation of EBV persistence and oncogenesis. Semin. Cancer Biol. 26:22-29. http://dx.doi.org /10.1016/j.semcancer.2014.01.003.
5. Johannsen E, Luftig M, Chase MR, Weicksel S, Cahir-McFarland E, Illanes D, Sarracino D, Kieff E. 2004. Proteins of purified Epstein-Barr virus. Proc. Natl. Acad. Sci. U. S. A. 101:16286-16291. http://dx.doi.org /10.1073/pnas.0407320101.
6. Kalla M, Schmeinck A, Bergbauer M, Pich D, Hammerschmidt W. 2010. AP-1 homolog BZLF1 of Epstein-Barr virus has two essential functions dependent on the epigenetic state of the viral genome. Proc. Natl. Acad. Sci. U. S. A. 107:850 - 855. http://dx.doi.org/10.1073/pnas .0911948107.
7. Masucci MG, Contreras-Salazar B, Ragnar E, Falk K, Minarovits J, Ernberg I, Klein G. 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.
8. Schaefer BC, Woisetschlaeger M, Strominger JL, Speck SH. 1991. Exclusive expression of Epstein-Barr virus nuclear antigen 1 in Burkitt lymphoma arises from a third promoter, distinct from the promoters used in latently infected lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 88:6550- 6554. http://dx.doi.org/10.1073/pnas.88.15.6550.
9. Hino R, Uozaki H, Murakami N, Ushiku T, Shinozaki A, Ishikawa S, Morikawa T, Nakaya T, Sakatani T, Takada K, Fukayama M. 2009. Activation of DNA methyltransferase 1 by EBV latent membrane protein 2A leads to promoter hypermethylation of PTEN gene in gastric carcinoma. Cancer Res. 69:2766-2774. http://dx.doi.org/10.1158/0008-5472 .CAN-08-3070.
10. Tsai CN, Tsai CL, Tse KP, Chang HY, Chang YS. 2002. The Epstein-Barr virus oncogene product, latent membrane protein 1, induces the downregulation of E-cadherin gene expression via activation of DNA methyltransferases. Proc. Natl. Acad. Sci. U. S. A. 99:10084-10089. http://dx.doi .org/10.1073/pnas.152059399.
11. Bhende PM, Seaman WT, Delecluse HJ, 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.
12. Flower K, Thomas D, Heather J, Ramasubramanyan S, Jones S, Sinclair AJ. 2011. Epigenetic control of viral life-cycle by a DNA-methylation dependent transcription factor. PLoS One 6:e25922. http://dx.doi.org/10 .1371/journal.pone.0025922.
13. Tempera I, Wiedmer A, Dheekollu J, Lieberman PM. 2010. CTCF prevents the epigenetic drift of EBV latency promoter Qp. PLoS Pathog. 6:e1001048. http://dx.doi.org/10.1371/journal.ppat.1001048.
14. Niller HH, Wolf H, Minarovits J. 2011. Viral hit and run-oncogenesis: genetic and epigenetic scenarios. Cancer Lett. 305:200-217. http://dx.doi .org/10.1016/j.canlet.2010.08.007.
15. Iizasa H, Nanbo A, Nishikawa J, Jinushi M, Yoshiyama H. 2012. Epstein-Barr Virus (EBV)-associated gastric carcinoma. Viruses 4:3420- 3439. http://dx.doi.org/10.3390/v4123420.
16. Kim J, Lee HS, Bae SI, Lee YM, Kim WH. 2005. Silencing and CpG island methylation of GSTP1 is rare in ordinary gastric carcinomas but common in Epstein-Barr virus-associated gastric carcinomas. Anticancer Res. 25: 4013-4019.
17. Kwong J, Lo KW, To KF, Teo PM, Johnson PJ, Huang DP. 2002. Promoter hypermethylation of multiple genes in nasopharyngeal carcinoma. Clin. Cancer Res. 8:131-137.
18. Lo KW, Chung GT, To KF. 2012. Deciphering the molecular genetic basis of NPC through molecular, cytogenetic, and epigenetic approaches. Semin. Cancer Biol. 22:79-86. http://dx.doi.org/10.1016/j.semcancer.2011 .12.011.
19. Matsusaka K, Kaneda A, Nagae G, Ushiku T, Kikuchi Y, Hino R, Uozaki H, Seto Y, Takada K, Aburatani H, Fukayama M. 2011. Classification of Epstein-Barr virus-positive gastric cancers by definition of DNA methylation epigenotypes. Cancer Res. 71:7187-7197. http://dx.doi .org/10.1158/0008-5472.CAN-11-1349.
20. Saito M, Nishikawa J, Okada T, Morishige A, Sakai K, Nakamura M, Kiyotoki S, Hamabe K, Okamoto T, Oga A, Sasaki K, Suehiro Y, Hinoda Y, Sakaida I. 2013. Role of DNA methylation in the development of Epstein-Barr virus-associated gastric carcinoma. J. Med. Virol. 85:121-127. http://dx.doi.org/10.1002/jmv.23405.
21. Tsao SW, Tsang CM, Pang PS, Zhang G, Chen H, Lo KW. 2012. The biology of EBV infection in human epithelial cells. Semin. Cancer Biol. 22:137-143. http://dx.doi.org/10.1016/j.semcancer.2012.02.004.
22. Tsai CL, Li HP, Lu YJ, Hsueh C, Liang Y, Chen CL, Tsao SW, Tse KP, Yu JS, Chang YS. 2006. Activation of DNA methyltransferase 1 by EBV LMP1 Involves c-Jun NH(2)-terminal kinase signaling. Cancer Res. 66: 11668-11676. http://dx.doi.org/10.1158/0008-5472.CAN-06-2194.
23. Paschos K, Parker GA, Watanatanasup E, White RE, Allday MJ. 2012. BIM promoter directly targeted by EBNA3C in polycomb-mediated repression by EBV. Nucleic Acids Res. 40:7233-7246. http://dx.doi.org/10 .1093/nar/gks391.
24. Skalska L, White RE, Franz M, Ruhmann M, Allday MJ. 2010. Epigenetic repression of p16(INK4A) by latent Epstein-Barr virus requires the interaction of EBNA3A and EBNA3C with CtBP. PLoS Pathog. 6:e1000951. http://dx.doi.org/10.1371/journal.ppat.1000951.
25. White RE, Groves IJ, Turro E, Yee J, Kremmer E, Allday MJ. 2010. Extensive co-operation between the Epstein-Barr virus EBNA3 proteins in the manipulation of host gene expression and epigenetic chromatin modification. PLoS One 5:e13979. http://dx.doi.org/10.1371/journal.pone .0013979.
26. Hansen KD, Sabunciyan S, Langmead B, Nagy N, Curley R, Klein G, Klein E, Salamon D, Feinberg AP. 2014. Large-scale hypomethylated blocks associated with Epstein-Barr virus-induced B-cell immortalization. Genome Res. 24:177-184. http://dx.doi.org/10.1101/gr.157743.113.
27. Hernando H, Shannon-Lowe C, Islam AB, Al-Shahrour F, Rodriguez- Ubreva J, Rodriguez-Cortez VC, Javierre BM, Mangas C, Fernandez AF, Parra M, Delecluse HJ, Esteller M, Lopez-Granados E, Fraga MF, Lopez-Bigas N, Ballestar E. 2013. The B cell transcription program mediates hypomethylation and overexpression of key genes in Epstein-Barr virus-associated proliferative conversion. Genome Biol. 14:R3. http://dx .doi.org/10.1186/gb-2013-14-1-r3.
28. Anderton JA, Bose S, Vockerodt M, Vrzalikova K, Wei W, Kuo M, Helin K, Christensen J, Rowe M, Murray PG, Woodman CB. 2011. The H3K27me3 demethylase, KDM6B, is induced by Epstein-Barr virus and over-expressed in Hodgkin's lymphoma. Oncogene 30:2037-2043. http: //dx.doi.org/10.1038/onc.2010.579.
29. Leonard S, Wei W, Anderton J, Vockerodt M, Rowe M, Murray PG, Woodman CB. 2011. Epigenetic and transcriptional changes which follow Epstein-Barr virus infection of germinal center B cells and their relevance to the pathogenesis of Hodgkin's lymphoma. J. Virol. 85:9568- 9577. http://dx.doi.org/10.1128/JVI.00468-11.
30. Queen KJ, Shi M, Zhang F, Cvek U, Scott RS. 2013. Epstein-Barr virus-induced epigenetic alterations following transient infection. Int. J. Cancer 132:2076-2086. http://dx.doi.org/10.1002/ijc.27893.
31. Molesworth SJ, Lake CM, Borza CM, Turk SM, Hutt-Fletcher LM. 2000. Epstein-Barr virus gH is essential for penetration of B cells but also plays a role in attachment of virus to epithelial cells. J. Virol. 74:6324- 6332. http://dx.doi.org/10.1128/JVI.74.14.6324-6332.2000.
32. Dirks W, Dexler H. 2004. Authentication of cancer cell lines by DNA fingerprinting. Methods Mol. Med. 88:43-55.
33. Repic AM, Shi M, Scott RS, Sixbey JW. 2010. Augmented latent membrane protein 1 expression from Epstein-Barr virus episomes with minimal terminal repeats. J. Virol. 84:2236-2244. http://dx.doi.org/10.1128 /JVI.01972-09.
34. Morrison JA, Raab-Traub N. 2005. Roles of the ITAM and PY motifs of Epstein-Barr virus latent membrane protein 2A in the inhibition of epithelial cell differentiation and activation of β-catenin signaling. J. Virol. 79:2375-2382. http://dx.doi.org/10.1128/JVI.79.4.2375-2382.2005.
35. Lin Z, Wang X, Strong MJ, Concha M, Baddoo M, Xu G, Baribault C, Fewell C, Hulme W, Hedges D, Taylor CM, Flemington EK. 2013. Whole-genome sequencing of the Akata and Mutu Epstein-Barr virus strains. J. Virol. 87:1172-1182. http://dx.doi.org/10.1128/JVI.02517-12.
36. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19:1639-1645. http://dx.doi.org/10.1101/gr .092759.109.
37. Imai S, Koizumi S, Sugiura M, Tokunaga M, Uemura Y, Yamamoto N, Tanaka S, Sato E, Osato T. 1994. Gastric carcinoma: monoclonal epithelial malignant cells expressing Epstein-Barr virus latent infection protein. Proc. Natl. Acad. Sci. U. S. A. 91:9131-9135. http://dx.doi.org/10.1073 /pnas.91.19.9131.
38. Feederle R, Neuhierl B, Bannert H, Geletneky K, Shannon-Lowe C, Delecluse HJ. 2007. Epstein-Barr virus B95.8 produced in 293 cells shows marked tropism for differentiated primary epithelial cells and reveals interindividual variation in susceptibility to viral infection. Int. J. Cancer 121:588-594. http://dx.doi.org/10.1002/ijc.22727.
39. Pegtel DM, Middeldorp J, Thorley-Lawson DA. 2004. Epstein-Barr virus infection in ex vivo tonsil epithelial cell cultures of asymptomatic carriers. J. Virol. 78:12613-12624. http://dx.doi.org/10.1128/JVI.78.22 .12613-12624.2004.
40. Dawson CW, Dawson J, Jones R, Ward K, Young LS. 1998. Functional differences between BHRF1, the Epstein-Barr virus-encoded Bcl-2 homologue, and Bcl-2 in human epithelial cells. J. Virol. 72:9016-9024.
41. Dawson CW, Rickinson AB, Young LS. 1990. Epstein-Barr virus latent membrane protein inhibits human epithelial cell differentiation. Nature 344:777-780. http://dx.doi.org/10.1038/344777a0.
42. Scholle F, Bendt KM, Raab-Traub N. 2000. Epstein-Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt. J. Virol. 74:10681-10689. http://dx.doi.org/10.1128/JVI.74.22.10681-10689 .2000.
43. Boyce ST, Ham RG. 1983. Calcium-regulated differentiation of normal human epidermal keratinocytes in chemically defined clonal culture and serum-free serial culture. J. Investig. Dermatol. 81:33s-40s. http://dx.doi .org/10.1111/1523-1747.ep12540422.
44. Matter K, Aijaz S, Tsapara A, Balda MS. 2005. Mammalian tight junctions in the regulation of epithelial differentiation and proliferation. Curr. Opin. Cell Biol. 17:453-458. http://dx.doi.org/10.1016/j.ceb.2005.08.003.
45. Green H, Rheinwald JG, Sun TT. 1977. Properties of an epithelial cell type in culture: the epidermal keratinocyte and its dependence on products of the fibroblast. Prog. Clin. Biol. Res. 17:493-500.
46. Krebs A, Frontini M, Tora L. 2008. GPAT: retrieval of genomic annotation from large genomic position datasets. BMC Bioinformatics 9:533. http://dx.doi.org/10.1186/1471-2105-9-533.
47. Kwok WK, Pang JC, Lo KW, Ng HK. 2009. Role of the RARRES1 gene in nasopharyngeal carcinoma. Cancer Genet. Cytogenet. 194:58-64. http: //dx.doi.org/10.1016/j.cancergencyto.2009.06.005.
48. 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.
49. Han J, Kamber M. 2001. Data mining: concepts and techniques. Academic Press, London, United Kingdom.
50. Pearson K. 1901. On lines and planes of closest fit to systems of points in space. Philos. Mag. 2:559-572. http://dx.doi.org/10.1080/14786440109462720.
51. Wullaert A, Bonnet MC, Pasparakis M. 2011. NF-κB in the regulation of epithelial homeostasis and inflammation. Cell Res. 21:146-158. http://dx .doi.org/10.1038/cr.2010.175.
52. Barbieri CE, Pietenpol JA. 2006. p63 and epithelial biology. Exp. Cell Res. 312:695-706. http://dx.doi.org/10.1016/j.yexcr.2005.11.028.
53. Candi E, Cipollone R, Rivetti di Val Cervo P, Gonfloni S, Melino G, Knight R. 2008. p63 in epithelial development. Cell. Mol. Life Sci. 65: 3126-3133. http://dx.doi.org/10.1007/s00018-008-8119-x.
54. Israel A. 2010. The IKK complex, a central regulator of NF-κB activation. Cold Spring Harb. Perspect. Biol. 2:a000158. http://dx.doi.org/10.1101 /cshperspect.a000158.
55. Fotheringham JA, Mazzucca S, Raab-Traub N. 2010. Epstein-Barr virus latent membrane protein-2A-induced ΔNp63α expression is associated with impaired epithelial-cell differentiation. Oncogene 29:4287-4296. http://dx.doi.org/10.1038/onc.2010.175.
56. Jones PA. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13:484-492. http://dx.doi.org/10 .1038/nrg3230.
57. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, Ji H, Potash JB, Sabunciyan S, Feinberg AP. 2009. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 41:178-186. http://dx.doi.org/10.1038/ng.298.
58. Dihal AA, Boot A, van Roon EH, Schrumpf M, Farina-Sarasqueta A, Fiocco M, Zeestraten EC, Kuppen PJ, Morreau H, van Wezel T, Boer JM. 2013. The homeobox gene MEIS1 is methylated in BRAF (p.V600E) mutated colon tumors. PLoS One 8:e79898. http://dx.doi.org/10.1371 /journal.pone.0079898.
59. Oleksiewicz U, Liloglou T, Tasopoulou KM, Daskoulidou N, Bryan J, Gosney JR, Field JK, Xinarianos G. 2013. Cytoglobin has bimodal: tumour suppressor and oncogene functions in lung cancer cell lines. Hum. Mol. Genet. 22:3207-3217. http://dx.doi.org/10.1093/hmg/ddt174.
60. Li L, Su X, Choi GC, Cao Y, Ambinder RF, Tao Q. 2012. Methylation profiling of Epstein-Barr virus immediate-early gene promoters, BZLF1 and BRLF1 in tumors of epithelial, NK- and B-cell origins. BMC Cancer 12:125. http://dx.doi.org/10.1186/1471-2407-12-125.
61. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, Mohammad HP, Chen W, Daniel VC, Yu W, Berman DM, Jenuwein T, Pruitt K, Sharkis SJ, Watkins DN, Herman JG, Baylin SB. 2007. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 39:237-242. http://dx.doi.org/10.1038/ng1972.
62. Kulis M, Queiros AC, Beekman R, Martin-Subero JI. 2013. Intragenic DNA methylation in transcriptional regulation, normal differentiation and cancer. Biochim. Biophys. Acta 1829:1161-1174. http://dx.doi.org/10 .1016/j.bbagrm.2013.08.001.