CTCF binding to the first intron of the major immediate early (MIE) gene of human cytomegalovirus (HCMV) negatively regulates MIE gene expression and HCMV replication

Journal of Virology

Volumn 88, Issue 13, 2014, Pages 7389-7401

  Martínez, Francisco Puerta ^a   Cruz, Ruth ^a   Lu, Fang ^b   Plasschaert, Robert ^c   Deng, Zhong ^b   Rivera Molina, Yisel A ^a   Bartolomei, Marisa S ^c   Lieberman, Paul M ^b   Tang, Qiyi ^a  

^a PONCE SCHOOL OF MEDICINE   (Puerto Rico)

^b WISTAR INSTITUTE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RECOMBINANT ALPHA2B INTERFERON; RNA POLYMERASE II; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR CTCF; CCCTC-BINDING FACTOR; IE1 PROTEIN, CYTOMEGALOVIRUS; IE2 PROTEIN, CYTOMEGALOVIRUS; IMMEDIATE EARLY PROTEIN; REPRESSOR PROTEIN; TRANSACTIVATOR PROTEIN;

ARTICLE; BINDING SITE; CHROMATIN; CONTROLLED STUDY; DNA REPLICATION; DNA SEQUENCE; EMBRYO; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MIE GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN INTERACTION; PROTEIN MOTIF; RNA ANALYSIS; RNA SPLICING; VIRUS GENE; VIRUS REPLICATION; VIRUS TRANSCRIPTION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; IMMUNOBLOTTING; INTRON; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; VIROLOGY;

BASE SEQUENCE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, VIRAL; HEK293 CELLS; HUMANS; IMMEDIATE-EARLY PROTEINS; IMMUNOBLOTTING; INTRONS; MOLECULAR SEQUENCE DATA; REPRESSOR PROTEINS; TRANS-ACTIVATORS; VIRUS REPLICATION;

EID: 84901981495     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00845-14     Document Type: Article

References (55)

1. Landolfo S, Gariglio M, Gribaudo G, Lembo D. 2003. The human cytomegalovirus. Pharmacol. Ther. 98:269-297. http://dx.doi.org/10 .1016/S0163-7258(03)00034-2.
2. Mocarski ES, Jr, Shenk T, Pass RF. 2006. Cytomegaloviruses, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
3. Sweet C. 1999. The pathogenicity of cytomegalovirus. FEMS Microbiol. Rev. 23:457-482. http://dx.doi.org/10.1111/j.1574-6976.1999.tb00408.x.
4. Ahn JH, Hayward GS. 1997. The major immediate-early proteins IE1 and IE2 of human cytomegalovirus colocalize with and disrupt PMLassociated nuclear bodies at very early times in infected permissive cells. J. Virol. 71:4599-4613.
5. Awasthi S, Isler JA, Alwine JC. 2004. Analysis of splice variants of the immediate-early 1 region of human cytomegalovirus. J. Virol. 78:8191-8200. http://dx.doi.org/10.1128/JVI.78.15.8191-8200.2004.
6. Hagemeier C, Walker SM, Sissons PJ, Sinclair JH. 1992. The 72K IE1 and 80K IE2 proteins of human cytomegalovirus independently transactivate the c-fos, c-myc and hsp70 promoters via basal promoter elements. J. Gen. Virol. 73(Pt 9):2385-2393. http://dx.doi.org/10.1099/0022-1317-73-9-2385.
7. Liu B, Hermiston TW, Stinski MF. 1991. A cis-acting element in the major immediate-early (IE) promoter of human cytomegalovirus is required for negative regulation by IE2. J. Virol. 65:897-903.
8. Meier JL, Stinski MF. 1997. Effect of a modulator deletion on transcription of the human cytomegalovirus major immediate-early genes in infected undifferentiated and differentiated cells. J. Virol. 71:1246-1255.
9. Sadanari H, Yamada R, Yamagoshi T, Ohnishi K, Matsubara K, Fukuda S, Tanaka J. 2000. The major immediate-early genes of human cytomegalovirus induce two novel proteins with molecular weights of 91 and 102 kilodaltons. Arch. Virol. 145:1257-1266. http://dx.doi.org/10.1007 /s007050070125.
10. Scully AL, Sommer MH, Schwartz R, Spector DH. 1995. The human cytomegalovirus IE2 86-kilodalton protein interacts with an early gene promoter via site-specific DNA binding and protein-protein associations. J. Virol. 69:6533-6540.
11. Stenberg RM. 1996. The human cytomegalovirus major immediate-early gene. Intervirology 39:343-349.
12. Stenberg RM, Thomsen DR, Stinski MF. 1984. Structural analysis of the major immediate early gene of human cytomegalovirus. J. Virol. 49:190-199.
13. Tang Q, Li L, Maul GG. 2005. Mouse cytomegalovirus early M112/113 proteins control the repressive effect of IE3 on the major immediate-early promoter. J. Virol. 79:257-263. http://dx.doi.org/10.1128/JVI.79.1.257-263.2005.
14. Tang Q, Maul GG. 2005. Immediate early interactions and epigenetic defense mechanisms, p 131-150. In Reddehase MJ (ed), Cytomegaloviruses: molecular biology and immunology. Caister Academic Press, Norwich, United Kingdom.
15. Meier JL, Stinski MF. 2006. Major immediate-early enhancer and its gene products. Caister Academic Press, Norfolk, United Kingdom.
16. Murphy JC, Fischle W, Verdin E, Sinclair JH. 2002. Control of cytomegalovirus lytic gene expression by histone acetylation. EMBO J. 21: 1112-1120. http://dx.doi.org/10.1093/emboj/21.5.1112.
17. Nevels M, Paulus C, Shenk T. 2004. Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc. Natl. Acad. Sci. U. S. A. 101:17234-17239. http://dx .doi.org/10.1073/pnas.0407933101.
18. Woodhall DL, Groves IJ, Reeves MB, Wilkinson G, Sinclair JH. 2006. Human Daxx-mediated repression of human cytomegalovirus gene expression correlates with a repressive chromatin structure around the major immediate early promoter. J. Biol. Chem. 281:37652-37660. http://dx .doi.org/10.1074/jbc.M604273200.
19. Kim YE, Lee JH, Kim ET, Shin HJ, Gu SY, Seol HS, Ling PD, Lee CH, Ahn JH. 2011. Human cytomegalovirus infection causes degradation of Sp100 proteins that suppress viral gene expression. J. Virol. 85:11928-11937. http://dx.doi.org/10.1128/JVI.00758-11.
20. Saffert RT, Kalejta RF. 2007. Human cytomegalovirus gene expression is silenced by Daxx-mediated intrinsic immune defense in model latent infections established in vitro. J. Virol. 81:9109-9120. http://dx.doi.org/10 .1128/JVI.00827-07.
21. Tavalai N, Adler M, Scherer M, Riedl Y, Stamminger T. 2011. Evidence for a dual antiviral role of the major nuclear domain 10 component Sp100 during the immediate-early and late phases of the human cytomegalovirus replication cycle. J. Virol. 85:9447-9458. http://dx.doi.org/10.1128/JVI .00870-11.
22. Tavalai N, Papior P, Rechter S, Leis M, Stamminger T. 2006. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 80:8006-8018. http://dx.doi.org/10.1128/JVI.00743-06.
23. Cosme RS, Yamamura Y, Tang Q. 2009. Roles of polypyrimidine tract binding proteins in major immediate-early gene expression and viral replication of human cytomegalovirus. J. Virol. 83:2839-2850. http://dx.doi .org/10.1128/JVI.02407-08.
24. Phillips JE, Corces VG. 2009. CTCF: master weaver of the genome. Cell 137:1194-1211. http://dx.doi.org/10.1016/j.cell.2009.06.001.
25. Sun FL, Elgin SC. 1999. Putting boundaries on silence. Cell 99:459-462. http://dx.doi.org/10.1016/S0092-8674(00)81534-2.
26. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S. 2011. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479:74-79. http://dx.doi.org/10.1038/nature10442.
27. Barkess G, West AG. 2012. Chromatin insulator elements: establishing barriers to set heterochromatin boundaries. Epigenomics 4:67-80. http: //dx.doi.org/10.2217/epi.11.112.
28. Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF, Wolffe A, Ohlsson R, Lobanenkov VV. 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. http://dx.doi.org/10.1016 /S0960-9822(00)00597-2.
29. Kim TH, Abdullaev ZK, Smith AD, Ching KA, Loukinov DI, Green RD, Zhang MQ, Lobanenkov VV, Ren B. 2007. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128: 1231-1245. http://dx.doi.org/10.1016/j.cell.2006.12.048.
30. 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.
31. Kang H, Wiedmer A, Yuan Y, Robertson E, Lieberman PM. 2011. Coordination of KSHV latent and lytic gene control by CTCF-cohesin mediated chromosome conformation. PLoS Pathog. 7:e1002140. http: //dx.doi.org/10.1371/journal.ppat.1002140.
32. Stedman W, Kang H, Lin S, Kissil JL, Bartolomei MS, Lieberman PM.2008. Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J. 27:654-666. http: //dx.doi.org/10.1038/emboj.2008.1.
33. Amelio AL, McAnany PK, Bloom DC. 2006. A chromatin insulator-like element in the herpes simplex virus type 1 latency-associated transcript region binds CCCTC-binding factor and displays enhancer-blocking and silencing activities. J. Virol. 80:2358-2368. http://dx.doi.org/10.1128/JVI .80.5.2358-2368.2006.
34. Chen Q, Lin L, Smith S, Huang J, Berger SL, Zhou J. 2007. CTCFdependent chromatin boundary element between the latency-associated transcript and ICP0 promoters in the herpes simplex virus type 1 genome. J. Virol. 81:5192-5201. http://dx.doi.org/10.1128/JVI.02447-06.
35. Chapman BS, Thayer RM, Vincent KA, Haigwood NL. 1991. Effect of intron A from human cytomegalovirus (Towne) immediate-early gene on heterologous expression in mammalian cells. Nucleic Acids Res. 19:3979-3986. http://dx.doi.org/10.1093/nar/19.14.3979.
36. Mariati Ng YK, Chao SH, Yap MG, Yang Y. 2010. Evaluating regulatory elements of human cytomegalovirus major immediate early gene for enhancing transgene expression levels in CHO K1 and HEK293 cells. J. Biotechnol. 147:160-163. http://dx.doi.org/10.1016/j.jbiotec.2010.02.022.
37. Xia W, Bringmann P, McClary J, Jones PP, Manzana W, Zhu Y, Wang S, Liu Y, Harvey S, Madlansacay MR, McLean K, Rosser MP, MacRobbie J, Olsen CL, Cobb RR. 2006. High levels of protein expression using different mammalian CMV promoters in several cell lines. Protein Expr. Purif. 45:115-124. http://dx.doi.org/10.1016/j.pep.2005.07.008.
38. Hennighausen L, Fleckenstein B. 1986. Nuclear factor 1 interacts with five DNA elements in the promoter region of the human cytomegalovirus major immediate early gene. EMBO J. 5:1367-1371.
39. de Bruyn Kops A, Knipe DM. 1988. Formation of DNA replication structures in herpes virus-infected cells requires a viral DNA binding protein. Cell 55:857-868. http://dx.doi.org/10.1016/0092-8674(88)90141-9.
40. Cosme-Cruz R, Martinez FP, Perez KJ, Tang Q. 2011. H2B homology region of major immediate-early protein 1 is essential for murine cytomegalovirus to disrupt nuclear domain 10, but is not important for viral replication in cell culture. J. Gen. Virol. 92:2006-2019. http://dx.doi.org /10.1099/vir.0.033225-0.
41. Stenberg RM, Fortney J, Barlow SW, Magrane BP, Nelson JA, Ghazal P.1990. Promoter-specific trans activation and repression by human cytomegalovirus immediate-early proteins involves common and unique protein domains. J. Virol. 64:1556-1565.
42. Keil GM, Ebeling-Keil A, Koszinowski UH. 1987. Immediate-early genes of murine cytomegalovirus: location, transcripts, and translation products. J. Virol. 61:526-533.
43. Borst EM, Hahn G, Koszinowski UH, Messerle M. 1999. Cloning of the human cytomegalovirus (HCMV) genome as an infectious bacterial artificial chromosome in Escherichia coli: a new approach for construction of HCMV mutants. J. Virol. 73:8320-8329.
44. Warden, C., Tang Q, and Zhu H. 2011. Herpesvirus BACs: past, present, and future. J. Biomed. Biotechnol. 2011:124595. http://dx.doi.org/10 .1155/2011/124595.
45. Moerke NJ. 2009. Fluorescence polarization (FP) assays for monitoring peptide-protein or nucleic acid-protein binding. Curr. Protoc. Chem. Biol. 1:1-15. http://dx.doi.org/10.1002/9780470559277.ch090102.
46. Bao L, Zhou M, Cui Y. 2008. CTCFBSDB: a CTCF-binding site database for characterization of vertebrate genomic insulators. Nucleic Acids Res. 36(Database Issue):D83-D87. http://dx.doi.org/10.1093/nar/gkm875.
47. Plasschaert RN, Vigneau S, Tempera I, Gupta R, Maksimoska J, Everett L, Davuluri R, Mamorstein R, Lieberman PM, Schultz D, Hannenhalli S, Bartolomei MS. 2014. CTCF binding site sequence differences are associated with unique regulatory and functional trends during embryonic stem cell differentiation. Nucleic Acids Res. 42:774-789. http://dx .doi.org/10.1093/nar/gkt910.
48. Deng Z, Wang Z, Stong N, Plasschaert R, Moczan A, Chen HS, Hu S, Wikramasinghe P, Davuluri RV, Bartolomei MS, Riethman H, Lieberman PM. 2012. A role for CTCF and cohesin in subtelomere chromatin organization, TERRA transcription, and telomere end protection. EMBO J. 31:4165-4178. http://dx.doi.org/10.1038/emboj.2012.266.
49. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, Cobb BS, Yokomori K, Dillon N, Aragon L, Fisher AG, Merkenschlager M. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422-433. http://dx.doi.org/10.1016/j.cell.2008.01.011.
50. Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN, Baliga NS, Aebersold R, Ranish JA, Krumm A. 2008. CTCF physically links cohesin to chromatin. Proc. Natl. Acad. Sci. U. S. A. 105:8309-8314. http://dx.doi .org/10.1073/pnas.0801273105.
51. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796-801. http://dx.doi.org/10 .1038/nature06634.
52. Merkenschlager M, Odom DT. 2013. CTCF and cohesin: linking gene regulatory elements with their targets. Cell 152:1285-1297. http://dx.doi .org/10.1016/j.cell.2013.02.029.
53. Guo Y, Monahan K, Wu H, Gertz J, Varley KE, Li W, Myers RM, Maniatis T, Wu Q. 2012. CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice. Proc. Natl. Acad. Sci. U. S. A. 109:21081-21086. http://dx.doi.org/10.1073/pnas.1219280110.
54. 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.
55. Herold M, Bartkuhn M, Renkawitz R. 2012. CTCF: insights into insulator function during development. Development 139:1045-1057. http: //dx.doi.org/10.1242/dev.065268.