A role for CTCF and cohesin in subtelomere chromatin organization, TERRA transcription, and telomere end protection

EMBO Journal

Volumn 31, Issue 21, 2012, Pages 4165-4178

  Deng, Zhong ^a   Wang, Zhuo ^a   Stong, Nick ^a   Plasschaert, Robert ^b   Moczan, Aliah ^a   Chen, Horng Shen ^a   Hu, Sufeng ^a,b   Wikramasinghe, Priyankara ^a   Davuluri, Ramana V ^a   Bartolomei, Marisa S ^a   Riethman, Harold ^b   Lieberman, Paul M ^a  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

histone; RNA polymerase; shelterin; subtelomere; telomere

Indexed keywords

COHESIN; DNA; NUCLEIC ACID BINDING PROTEIN; RAD21 PROTEIN; RNA POLYMERASE; TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR TERRA; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA DAMAGE; GENE MUTATION; HUMAN; HUMAN CELL; NUCLEOTIDE BINDING SITE; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN SUBUNIT; SUBTELOMERE; TELOMERE; TRANSCRIPTION REGULATION;

CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL PROTEINS, NON-HISTONE; CPG ISLANDS; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HUMANS; LUCIFERASES; NEOPLASMS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA POLYMERASE II; RNA, MESSENGER; TELOMERE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84868534644     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.266     Document Type: Article

References (87)

1. Ambrosini A, Paul S, Hu S, Riethman H (2007) Human subtelomeric duplicon structure and organization. Genome Biol 8: R151
2. Arora R, Brun CM, Azzalin CM (2011) TERRA: long noncoding RNA at eukaryotic telomeres. Prog Mol Subcell Biol 51: 65-94
3. Azzalin CM, Lingner J (2008) Telomeres: the silence is broken. Cell Cycle 7: 1161-1165 (Pubitemid 351749267)
4. Azzalin CM, Reichenback P, Khoriauli L, Giulotto E, Lingner J (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318: 798-801 (Pubitemid 351411771)
5. Bah A, Wischnewski H, Shchepachev V, Azzalin CM (2011) The telomeric transcriptome of Schizosaccharomyces pombe. Nucleic Acids Res 40: 2995-3005
6. Blasco MA (2007) The epigenetic regulation of mammalian telomeres. Nat Rev Genet 8: 299-309 (Pubitemid 46439289)
7. Bushey AM, Dorman ER, Corces VG (2008) Chromatin insulators: regulatory mechanisms and epigenetic inheritance. Mol Cell 32: 1-9
8. Canudas S, Houghtaling BR, Bhanot M, Sasa G, Savage SA, Bertuch AA, Smith S (2011) A role for heterochromatin protein 1gamma at human telomeres. Genes Dev 25: 1807-1819
9. Canudas S, Smith S (2009) Differential regulation of telomere and centromere cohesion by the Scc3 homologues SA1 and SA2, respectively, in human cells. J Cell Biol 187: 165-173
10. Caslini C, Connelly JA, Serna A, Broccoli D, Hess JL (2009) MLL associates with telomeres and regulates telomeric repeat-containing RNA transcription. Mol Cell Biol 29: 4519-4526
11. Chakraborty A, Shen Z, Prasanth SG (2011) 'ORCanization' on heterochromatin: linking DNA replication initiation to chromatin organization. Epigenetics 6: 665-670
12. 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 (Pubitemid 43849150)
13. 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
14. Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, Zhao K (2009) Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res 19: 24-32
15. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, Saretzki G, Carter NP, Jackson SP (2003) A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198 (Pubitemid 37442589)
16. de Lange T (2004) T-loops and the origin of telomeres. Nat Rev 5: 323-329 (Pubitemid 38480613)
17. de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110 (Pubitemid 41330312)
18. Deng Y, Chan SS, Chang S (2008) Telomere dysfunction and tumour suppression: the senescence connection. Nat Rev 8: 450-458 (Pubitemid 351744962)
19. Deng Z, Campbell AE, Lieberman PM (2010) TERRA, CpG methylation and telomere heterochromatin: lessons from ICF syndrome cells. Cell Cycle 9: 69-74
20. Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM (2009) TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol Cell 35: 403-413
21. Deng Z, Wang Z, Xiang C, Molczan A, Baubet V, Conejo-Garcia J, Xu X, Lieberman PM, Dahmane N (2012) Formation of telomeric repeat-containing RNA (TERRA) foci in highly proliferating mouse cerebellar neuronal progenitors and medulloblastoma. J Cell Sci (advance online publication 28 May 2012; doi:10.1242/jcs.108118)
22. Descipio C, Spinner NB, Kaur M, Yaeger D, Conlin LK, Ambrosini A, Hu S, Shan S, Krantz ID, Riethman H (2008) Fine-mapping subtelomeric deletions and duplications by comparative genomic hybridization in 42 individuals. Am J Med Genet A 146A: 730-739 (Pubitemid 351354148)
23. Dimitrova N, de Lange T (2006) MDC1 accelerates nonhomologous end-joining of dysfunctional telomeres. Genes Dev 20: 3238-3243 (Pubitemid 44904845)
24. Dorsett D (2011) Cohesin: genomic insights into controlling gene transcription and development. Curr Opin Genet Dev 21: 199-206
25. Ehrlich M, Jackson K, Weemaes C (2006) Immunodeficiency, centromeric region instability, facial anomalies syndrome (ICF). Orphanet J Rare Dis 1: 2
26. Fan Y, Newman T, Linardopoulou E, Trask BJ (2002) Gene content and function of the ancestral chromosome fusion site in human chromosome 2q13-2q14.1 and paralogous regions. Genome Res 12: 1663-1672 (Pubitemid 35363670)
27. Faulkner GJ, Forrest AR, Chalk AM, Schroder K, Hayashizaki Y, Carninci P, Hume DA, Grimmond SM (2008) A rescue strategy for multimapping short sequence tags refines surveys of transcriptional activity by CAGE. Genomics 91: 281-288
28. Fay A, Misulovin Z, Li J, Schaaf CA, Gause M, Gilmour DS, Dorsett D (2011) Cohesin selectively binds and regulates genes with paused RNA polymerase. Curr Biol 21: 1624-1634
29. Galati A, Magdinier F, Colasanti V, Bauwens S, Pinte S, Ricordy R, Giraud-Panis MJ, Pusch MC, Savino M, Cacchione S, Gilson E (2012) TRF2 controls telomeric nucleosome organization in a cell cycle phase-dependent manner. PLoS One 7: e34386
30. Garcia-Cao M, O'Sullivan R, Peters AH, Jenuwein T, Blasco MA (2004) Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 36: 94-99 (Pubitemid 38056214)
31. Gonzalo S, Jaco I, Fraga MF, Chen T, Li E, Esteller M, Blasco MA (2006) DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat Cell Biol 8416-424
32. Greenwood J, Cooper JP (2011) Non-coding telomeric and subtelomeric transcripts are differentially regulated by telomeric and heterochromatin assembly factors in fission yeast. Nucleic Acids Res 40: 2956-2963
33. Grunstein M (1997) Molecular model for telomeric heterochromatin in yeast. Curr Opin Cell Biol 9: 383-387 (Pubitemid 27263180)
34. Hirano T (2006) At the heart of the chromosome: SMC proteins in action. Nat Rev 7: 311-322
35. Jain D, Cooper JP (2011) Telomeric strategies: means to an end. Annu Rev Genet 44: 243-269
36. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-435
37. Kang H, Lieberman PM (2009) Cell cycle control of Kaposi's sarcoma-associated herpesvirus latency transcription by CTCFcohesin interactions. J Virol 83: 6199-6210
38. Kang H, Lieberman PM (2011) Mechanism of glycyrrhizic acid inhibition of Kaposi's sarcoma-associated herpesvirus: disruption of CTCF-cohesin-mediated RNA polymerase II pausing and sister chromatid cohesion. J Virol 85: 11159-11169
39. Karlseder J (2003) Telomere repeat binding factors: keeping the ends in check. Cancer Lett 194: 189-197 (Pubitemid 36577330)
40. Karlseder J, Smogorzewska A, de Lange T (2002) Senescence induced by altered telomere state, not telomere loss. Science 295: 2446-2449 (Pubitemid 34270257)
41. Kasowski M, Grubert F, Heffelfinger C, Hariharan M, Asabere A, Waszak SM, Habegger L, Rozowsky J, Shi M, Urban AE, Hong MY, Karczewski KJ, Huber W, Weissman SM, Gerstein MB, Korbel JO, Snyder M (2010) Variation in transcription factor binding among humans. Science 328: 232-235
42. 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 (Pubitemid 46427876)
43. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25
44. Lee BK, Bhinge AA, Battenhouse A, McDaniell RM, Liu Z, Song L, Ni Y, Birney E, Lieb JD, Furey TS, Crawford GE, Iyer VR (2012) Cell-type specific and combinatorial usage of diverse transcription factors revealed by genome-wide binding studies in multiple human cells. Genome Res 22: 9-24
45. Linardopoulou EV, Parghi SS, Friedman C, Osborn GE, Parkhurst SM, Trask BJ (2007) Human subtelomeric WASH genes encode a new subclass of the WASP family. PLoS Genet 3: e237
46. Linardopoulou EV, Williams EM, Fan Y, Friedman C, Young JM, Trask BJ (2005) Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437: 94-100 (Pubitemid 41613430)
47. Liu D, O'Connor MS, Qin J, Songyang Z (2004) Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J Biol Chem 279: 51338-51342 (Pubitemid 40017880)
48. Loo S, Rine J (1995) Silencing and heritable domains of gene expression. Annu Rev Cell Dev Biol 11: 519-548
49. Lu F, Tsai K, Chen HS, Wikramasinghe P, Davuluri RV, Showe L, Domsic J, Marmorstein R, Lieberman PM (2012) Identification of host-chromosome binding sites and candidate gene targets for KSHV LANA. J Virol 86: 5752-5762
50. Luke B, Lingner J (2009) TERRA: telomeric repeat-containing RNA. EMBO J 28: 2503-2510
51. Murnane JP (2011) Telomere dysfunction and chromosome instability. Mutat Res 730: 28-36
52. Nasmyth K, Haering CH (2005) The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74: 595-648 (Pubitemid 40995519)
53. Nechaev S, Adelman K (2011) Pol II waiting in the starting gates: regulating the transition from transcription initiation into productive elongation. Biochim Biophys Acta 1809: 34-45
54. Nergadze SG, Farnung BO, Wischnewski H, Khoriauli L, Vitelli V, Chawla R, Giulotto E, Azzalin CM (2009) CpG-island promoters drive transcription of human telomeres. RNA 15: 2186-2194
55. Ohlsson R, Lobanenkov V, Klenova E (2010) Does CTCF mediate between nuclear organization and gene expression? Bioessays 32: 37-50
56. Ottaviani A, Rival-Gervier S, Boussouar A, Foerster AM, Rondier D, Sacconi S, Desnuelle C, Gilson E, Magdinier F (2009a) The D4Z4 macrosatellite repeat acts as a CTCF and A-type lamins-dependent insulator in facio-scapulo-humeral dystrophy. PLoS Genet 5: e1000394
57. Ottaviani A, Schluth-Bolard C, Gilson E, Magdinier F (2011) D4Z4 as a prototype of CTCF and lamins-dependent insulator in human cells. Nucleus 1: 30-36
58. Ottaviani A, Schluth-Bolard C, Rival-Gervier S, Boussouar A, Rondier D, Foerster AM, Morere J, Bauwens S, Gazzo S, Callet-Bauchu E, Gilson E, Magdinier F (2009b) Identification of a perinuclear positioning element in human subtelomeres that requires A-type lamins and CTCF. EMBO J 28: 2428-2436
59. Palm W, de Lange T (2008) How Shelterin protects mammalian telomeres. Annu Rev Genet 42: 301-334
60. 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
61. Perrini B, Piacentini L, Fanti L, Altieri F, Chichiarelli S, Berloco M, Turano C, Ferraro A, Pimpinelli S (2004) HP1 controls telomere capping, telomere elongation, and telomere silencing by two different mechanisms in Drosophila. Mol Cell 15: 467-476 (Pubitemid 39092761)
62. Perrod S, Gasser SM (2003) Long-range silencing and position effects at telomeres and centromeres: parallels and differences. Cell Mol Life Sci 60: 2303-2318 (Pubitemid 37487252)
63. Phillips JE, Corces VG (2009) CTCF: master weaver of the genome. Cell 137: 1194-1211
64. Remeseiro S, Cuadrado A, Carretero M, Martinez P, Drosopoulos WC, Canamero M, Schildkraut CL, Blasco MA, Losada A (2012) Cohesin-SA1 deficiency drives aneuploidy and tumourigenesis in mice due to impaired replication of telomeres. EMBO J 31: 2076-2089
65. Rhee HS, Pugh BF (2012) Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483: 295-301
66. Riethman H (2008a) Human subtelomeric copy number variations. Cytogenet Genome Res 123: 244-252
67. Riethman H (2008b) Human telomere structure and biology. Annu Rev Genomics Hum Genet 9: 1-19
68. Riethman H, Ambrosini A, Castaneda C, Finklestein J, Hu XL, Mudunuri U, Paul S, Wei J (2004) Mapping and initial analysis of human subtelomeric sequence assemblies. Genome Res 14: 18-28 (Pubitemid 38088521)
69. Riethman H, Ambrosini A, Paul S (2005) Human subtelomere structure and variation. Chromosome Res 13: 505-515 (Pubitemid 41205633)
70. 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 USA 105: 8309-8314 (Pubitemid 351904752)
71. Rusche LN, Kirchmaier AL, Rine J (2003) The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72: 481-516 (Pubitemid 36930453)
72. Schoeftner S, Blasco MA (2008) Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 10228-236
73. Schoeftner S, Blasco MA (2009) A 'higher order' of telomere regulation: telomere heterochromatin and telomeric RNAs. EMBO J 28: 2323-2336
74. Selth LA, Sigurdsson S, Svejstrup JQ (2010) Transcript elongation by RNA polymerase II. Annu Rev Biochem 79: 271-293
75. StedmanW, 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 (Pubitemid 351273124)
76. Stewart JA, Chaiken MF, Wang F, Price CM (2012) Maintaining the end: roles of telomere proteins in end-protection, telomere replication and length regulation. Mutat Res 730: 12-19
77. Sugiyama T, Cam HP, Sugiyama R, Noma K, Zofall M, Kobayashi R, Grewal SI (2007) SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128: 491-504 (Pubitemid 46198892)
78. Sun H, Wu J, Wickramasinghe P, Pal S, Gupta R, Bhattacharyya A, Agosto-Perez FJ, Showe LC, Huang TH, Davuluri RV (2011) Genome-wide mapping of RNA Pol-II promoter usage in mouse tissues by ChIP-seq. Nucleic Acids Res 39: 190-201
79. Takai H, Smogorzewska A, de Lange T (2003) DNA damage foci at dysfunctional telomeres. Curr Biol 13: 1549-1556 (Pubitemid 37078413)
80. Teixeira MT, Arneric M, Sperisen P, Lingner J (2004) Telomere length homeostasis is achieved via a switch between telomerase-extendible and-nonextendible states. Cell 117: 323-335 (Pubitemid 38534539)
81. Wada Y, Ohta Y, Xu M, Tsutsumi S, Minami T, Inoue K, Komura D, Kitakami J, Oshida N, Papantonis A, Izumi A, Kobayashi M, Meguro H, Kanki Y, Mimura I, Yamamoto K, Mataki C, Hamakubo T, Shirahige K, Aburatani H et al (2009) A wave of nascent transcription on activated human genes. Proc Natl Acad Sci USA 106: 18357-18361
82. 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 (Pubitemid 351253176)
83. Wu P, de Lange T (2008) No overt nucleosome eviction at deprotected telomeres. Mol Cell Biol 28: 5724-5735
84. Xiao T,Wallace J, Felsenfeld G (2011) Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Mol Cell Biol 31: 2174-2183
85. Ye J, Wu Y, Gilson E (2010) Dynamics of telomeric chromatin at the crossroads of aging and cancer. Essays Biochem 48: 147-164
86. Yehezkel S, Segev Y, Viegas-Pequignot E, Skorecki K, Selig S (2008) Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum Mol Genet 17: 2776-2789
87. Zakian VA (2012) Telomeres: the beginnings and ends of eukaryotic chromosomes. Exp Cell Res 318: 1456-1460