Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators

EMBO Journal

Volumn 27, Issue 4, 2008, Pages 654-666

  Stedman, William ^a   Kang, Hyojeung ^a   Lin, Shu ^a   Kissil, Joseph L ^a   Bartolomei, Marisa S ^a   Lieberman, Paul M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

c myc; Cohesin; CTCF; KSHV; Latency

Indexed keywords

COHESIN; DNA BINDING PROTEIN; PROTEIN CTCF; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; EPISOME; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; LATENT PERIOD; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRAL GENETICS;

CELL CYCLE PROTEINS; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; HELA CELLS; HERPESVIRUS 8, HUMAN; HUMANS; INSULIN-LIKE GROWTH FACTOR II; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-MYC; REPRESSOR PROTEINS; RNA, UNTRANSLATED; VIRUS LATENCY;

HUMAN HERPESVIRUS 8; MAMMALIA;

EID: 39449111307     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.1     Document Type: Article

References (72)

1. 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
2. Bais C, Santomasso B, Coso O, Arvanitakis L, Raaka EG, Gutkind JS, Asch AS, Cesarman E, Gerhengorn MC, Mesri EA (1998) G-protein coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391: 86-89
3. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837
4. Bell AC, Felsenfeld G (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405: 482-485
5. Blat Y, Kleckner N (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98: 249-259
6. Boshoff C, Schulz TF, Kennedy MM, Graham AK, Fisher C, Thomas A, McGee JO, Weiss RA, O'Leary JJ (1995) Kaposi's sarcoma-asociated herpesvirus infects endothelial and spindle cells. Nat Med 1: 1274-1278
7. Burysek L, Pitha PM (2001) Latently expressed human herpesvirus 8-encoded interferon regulatory factor 2 inhibits double-stranded RNA-activated protein kinase. J Virol 75: 2345-2352
8. Cai X, Cullen BR (2006) Transcriptional origin of Kaposi's sarcoma-associated herpesvirus microRNAs. J Virol 80: 2234-2242
9. Capelson M, Corces VG (2004) Boundary elements and nuclear organization. Biol Cell 96: 617-629
10. Cesarman E (2002) The role of Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) in lymphoproliferative diseases. Recent Results Cancer Res 159: 27-37
11. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 332: 1186-1191
12. Cesarman E, Nador RG, Bai F, Bohenzky RA, Russo JJ, Moore PS, Chang Y, Knowles DM (1996) Kaposi's sarcoma-associated herpesvirus contains G protein-coupled receptor and cyclin D homologs which are expressed in Kaposi's sarcoma and malignant lymphoma. J Virol 70: 8218-8223
13. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, Moore PS (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865-1869
14. Chau CM, Lieberman PM (2004) Dynamic chromatin boundaries delineate a latency control region of Epstein-Barr virus. J Virol 78: 12308-12319
15. 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
16. Chen Q, Lin L, Smith S, Huang J, Berger SL, Zhou J (2007) CTCF-dependent chromatin boundary element between the latency-associated transcript and ICP0 promoters in the herpes simplex virus type 1 genome. J Virol 81: 5192-5201
17. Chernukhin I, Shamsuddin S, Kang SY, Bergstrom R, Kwon YW, Yu W, Whitehead J, Mukhopadhyay R, Docquier F, Farrar D, Morrison I, Vigneron M, Wu SY, Chiang CM, Loukinov D, Lobanenkov V, Ohlsson R, Klenova E (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
18. Copeland NG, Jenkins NA, Court DL (2001) Recombineering: a powerful new tool for mouse functional genomics. Nat Rev Genet 2: 769-779
19. Cotter II MA, Robertson ES (2002) Molecular biology of Kaposi's sarcoma-associated herpesvirus. Front Biosci 7: d358-d375
20. Day L, Chau CM, Nebozhyn M, Rennenkamp AJ, Showe M, Lieberman PM (2007) Chromatin profiling of Epstein-Barr virus latency control region. J Virol 81: 6389-6401
21. Dittmer D, Lagunoff M, Renne R, Staskus K, Haase A, Ganem D (1998) A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J Virol 72: 8309-8315
22. Dorsett D (2004) Adherin: key to the cohesin ring and Cornelia de Lange syndrome. Curr Biol 14: R834-R836
23. Dorsett D (2007) Roles of the sister chromatid cohesion apparatus in gene expression, development, and human syndromes. Chromosoma 116: 1-13
24. Engel N, Thorvaldsen JL, Bartolomei MS (2006) CTCF binding sites promote transcription initiation and prevent DNA methylation on the maternal allele at the imprinted H19/Igf2 locus. Hum Mol Genet 15: 2945-2954
25. Farris SD, Rubio ED, Moon JJ, Gombert WM, Nelson BH, Krumm A (2005) Transcription-induced chromatin remodeling at the c-myc gene involves the local exchange of histone H2A.Z. J Biol Chem 280: 25298-25303
26. Fedoriw AM, Stein P, Svoboda P, Schultz RM, Bartolomei MS (2004) Transgenic RNAi reveals essential function for CTCF in H19 gene imprinting. Science 303: 238-240
27. Gaszner M, Felsenfeld G (2006) Insulators: exploiting transcriptional and epigenetic mechanisms. Nat Rev Genet 7: 703-713
28. Gelmann EP, Psallidopoulos MC, Papas TS, Dalla-Favera R (1983) Identification of reciprocal translocation sites within the c-myc oncogene and immunoglobulin mu locus in a Burkitt lymphoma. Nature 306: 799-803
29. Gerasimova TI, Corces VG (2001) Chromatin insulators and boundaries: effects on transcription and nuclear organization. Annu Rev Genet 35: 193-208
30. Gerbi SA, Strezoska Z, Waggener JM (2002) Initiation of DNA replication in multicellular eukaryotes. J Struct Biol 140: 17-30
31. Gillis LA, McCallum J, Kaur M, DeScipio C, Yaeger D, Mariani A, Kline AD, Li HH, Devoto M, Jackson LG, Krantz ID (2004) NIPBL mutational analysis in 120 individuals with Cornelia de Lange syndrome and evaluation of genotype-phenotype correlations. Am J Hum Genet 75: 610-623
32. Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, Koshland DE, DeRisi JL, Gerton JL (2004) Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol 2: E259
33. Gombert WM, Farris SD, Rubio ED, Morey-Rosler KM, Schubach WH, Krumm A (2003) The c-myc insulator element and matrix attachment regions define the c-myc chromosomal domain. Mol Cell Biol 23: 9338-9348
34. Guo HG, Sadowska M, Reid W, Tschachler E, Hayward G, Reitz M (2003) Kaposi's sarcoma-like tumors in a human herpesvirus 8 ORF74 transgenic mouse. J Virol 77: 2631-2639
35. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM (2000) CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405: 486-489
36. Hayward GS (2003) Initiation of angiogenic Kaposi's sarcoma lesions. Cancer Cell 3: 1-3
37. Hirano T (2006) At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 7: 311-322
38. Ishihara K, Oshimura M, Nakao M (2006) CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell 23: 733-742
39. Jeong J, Papin J, Dittmer D (2001) Differential regulation of the overlapping Kaposi's sarcoma-associated herpesvirus vGCR (orf74) and LANA (orf73) promoters. J Virol 75: 1798-1807
40. Kanda T, Kamiya M, Maruo S, Iwakiri D, Takada K (2007) Symmetrical localization of extrachromosomally replicating viral genomes on sister chromatids. J Cell Sci 120: 1529-1539
41. 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
42. Kedes DH, Lagunoff M, Renne R, Ganem D (1997) Identification of the gene encoding the major latency-associated nuclear antigen of the Kaposi's sarcoma-associated herpesvirus. J Clin Invest 100: 2606-2610
43. 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
44. Komatsu T, Ballestas ME, Barbera AJ, Kaye KM (2002) The KSHV latency-associated nuclear antigen: a multifunctional protein. Front Biosci 7: d726-d730
45. Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, Yaeger D, Jukofsky L, Wasserman N, Bottani A, Morris CA, Nowaczyk MJ, Toriello H, Bamshad MJ, Carey JC, Rappaport E, Kawauchi S, Lander AD, Calof AL, Li HH, Devoto M et al (2004) Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped-B. Nat Genet 36: 631-635
46. Kurukuti S, Tiwari VK, Tavoosidana G, Pugacheva E, Murrell A, Zhao Z, Lobanenkov V, Reik W, Ohlsson R (2006) CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc Natl Acad Sci USA 103: 10684-10689
47. Liang Y, Ganem D (2004) RBP-J (CSL) is essential for activation of the K14/vGPCR promoter of Kaposi's sarcoma-associated herpesvirus by the lytic switch protein RTA. J Virol 78: 6818-6826
48. Lin Q, Chen Q, Lin L, Zhou J (2004) The promoter targeting sequence mediates epigenetically heritable transcription memory. Genes Dev 18: 2639-2651
49. Ling JQ, Li T, Hu JF, Vu TH, Chen HL, Qiu XW, Cherry AM, Hoffman AR (2006) CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 312: 269-272
50. Losada A (2007) Cohesin regulation: fashionable ways to wear a ring. Chromosoma 116: 321-329
51. Montaner S, Sodhi A, Molinolo A, Bugge TH, Sawai ET, He Y, Li Y, Ray PE, Gutkind JS (2003) Endothelial infection with KSHV genes in vivo reveals that vGPCR initiates Kaposi's sarcomagenesis and can promote the tumorigenic potential of viral latent genes. Cancer Cell 3: 23-36
52. Muralidhar S, Pumfery AM, Hassani M, Sadaie MR, Kishishita M, Brady JN, Doniger J, Medveczky P, Rosenthal LJ (1998) Identification of kaposin (open reading frame K12) as a human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus) transforming gene. J Virol 72: 4980-4988
53. Mutlu AD, Cavallin LE, Vincent L, Chiozzini C, Eroles P, Duran EM, Asgari Z, Hooper AT, La Perle KM, Hilsher C, Gao SJ, Dittmer DP, Rafii S, Mesri EA (2007) In vivo restricted and reversible malignancy induced by human herpesvirus-8 KSHV: a cell and animal model of virally induced Kaposi's sarcoma. Cancer Cell 11: 245-258
54. Nador RG, Milligan LL, Flore O, Wang X, Arvanitakis L, Knowles DM, Cesarman E (2001) Expression of Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor monocistronic and bicistronic transcripts in primary effusion lymphomas. Virology 287: 62-70
55. Nanbo A, Sugden A, Sugden B (2007) The coupling of synthesis and partitioning of EBV's plasmid replicon is revealed in live cells. EMBO J 26: 4252-4262
56. Nasmyth K, Haering CH (2005) The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74: 595-648
57. Nasmyth K, Schleiffer A (2004) From a single double helix to paired double helices and back. Philos Trans R Soc Lond B Biol Sci 359: 99-108
58. Ohlsson R, Renkawitz R, Lobanenkov V (2001) CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 17: 520-527
59. Pearce M, Matsumura S, Wilson AC (2005) Transcripts encoding K12, v-FLIP, v-cyclin, and the microRNA cluster of Kaposi's sarcoma-associated herpesvirus originate from a common promoter. J Virol 79: 14457-14464
60. Rainbow L, Platt GM, Simpson GR, Sarid R, Gao SJ, Stoiber H, Herrington CS, Moore PS, Schulz TF (1997) The 222- to 234-kilodalton latent nuclear protein (LNA) of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) is encoded by orf73 and is a component of the latency-associated nuclear antigen. J Virol 71: 5915-5921
61. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, Parry JP, Peruzzi D, Edelman IS, Chang Y, Moore PS (1996) Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci USA 93: 14862-14867
62. Sadler R, Wu L, Forghani B, Renne R, Zhong W, Herndier B, Ganem D (1999) A complex translational program generates multiple novel proteins from the latently expressed kaposin (K12) locus of Kaposi's sarcoma-associated herpesvirus. J Virol 73: 5722-5730
63. Samols MA, Hu J, Skalsky RL, Renne R (2005) Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. J Virol 79: 9301-9305
64. Sarid R, Wiezorek JS, Moore PS, Chang Y (1999) Characterization and cell cycle regulation of the major Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) latent genes and their promoter. J Virol 73: 1438-1446
65. Sodhi A, Montaner S, Gutkind JS (2004) Does dysregulated expression of a deregulated viral GPCR trigger Kaposi's sarcomagenesis? FASEB J 18: 422-427
66. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, Babinet P, d'Agay MF, Clauvel JP, Raphael M, Degos L, Sigaux F (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86: 1276-1280
67. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, Galjart N, de Laat W (2006) CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev 20: 2349-2354
68. Stedman W, Deng Z, Lu F, Lieberman PM (2004) ORC, MCM, and histone hyperacetylation at the Kaposi's sarcoma-associated herpesvirus latent replication origin. J Virol 78: 12566-12575
69. Szabo PE, Tang SH, Silva FJ, Tsark WM, Mann JR (2004) Role of CTCF binding sites in the Igf2/H19 imprinting control region. Mol Cell Biol 24: 4791-4800
70. Talbot SJ, Weiss RA, Kellam P, Boshoff C (1999) Transcriptional analysis of human herpesvirus-8 open reading frames 71, 72, 73, K14, and 74 in a primary effusion lymphoma cell line. Virology 257: 84-94
71. Yusufzai TM, Tagami H, Nakatani Y, Felsenfeld G (2004) CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol Cell 13: 291-298
72. Zhou FC, Zhang YJ, Deng JH, Wang XP, Pan HY, Hettler E, Gao SJ (2002) Efficient infection by a recombinant Kaposi's sarcoma-associated herpesvirus cloned in a bacterial artificial chromosome: application for genetic analysis. J Virol 76: 6185-6196