Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA

Genes and Development

Volumn 24, Issue 22, 2010, Pages 2543-2555

  Yao, Hongjie ^a   Brick, Kevin ^a   Evrard, Yvonne ^a,b   Xiao, Tiaojiang ^a   Camerini Otero, R Daniel ^a   Felsenfeld, Gary ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

CTCF; Insulator function; Noncoding RNA; RNA binding protein

Indexed keywords

COHESIN; DEAD BOX PROTEIN; PROTEIN P68; SOMATOMEDIN B; STEROID RECEPTOR RNA ACTIVATOR; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ARTICLE; BINDING SITE; COMPLEX FORMATION; HUMAN; HUMAN CELL; INSULATOR ELEMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALLELES; ANIMALS; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME MAPPING; DEAD-BOX RNA HELICASES; FEMALE; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; HELA CELLS; HUMANS; INSULIN-LIKE GROWTH FACTOR II; MICE; MICE, INBRED C57BL; NIH 3T3 CELLS; PROTEIN BINDING; REPRESSOR PROTEINS; RNA;

EID: 78349252731     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1967810     Document Type: Article

References (62)

1. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histonemethylations in the human genome. Cell 129: 823-837.
2. Bartolomei MS, Zemel S, Tilghman SM. 1991. Parental imprinting of the mouse H19 gene. Nature 351: 153-155.
3. Bates GJ, Nicol SM,Wilson BJ, Jacobs A-MF, Bourdon J-C,Wardrop J, Gregory DJ, Lane DP, Perkins ND, Fuller-Pace FV. 2005. The DEAD box protein p68: A novel transcriptional coactivator of the p53 tumour suppressor. EMBO J 24: 543-553.
4. Bell AC, Felsenfeld G. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405: 482-485.
5. Bell AC, West AG, Felsenfeld G. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98: 387-396.
6. Bushey AM, Dorman ER, Corces VG. 2008. Chromatin insulators: Regulatory mechanisms and epigenetic inheritance. Mol Cell 32: 1-9.
7. Caretti G, Schiltz RL, Dilworth FJ, Di Padova M, Zhao P, Ogryzko V, Fuller-Pace FV, Hoffman EP, Tapscott SJ, Sartorelli V. 2006. The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell 11: 547-560.
8. Caretti G, Lei EP, Sartorelli V. 2007. The DEAD-box p68/p72 proteins and the noncoding RNA steroid receptor activator SRA: Eclectic regulators of disparate biological functions. Cell Cycle 6: 1172-1176.
9. Chao W, Huynh KD, Spencer RJ, Davidow LS, Lee JT. 2002. CTCF, a candidate trans-acting factor for X-inactivation choice. Science 295: 345-347.
10. Chooniedass-Kothari S, Emberley E, Hamedani MK, Troup S, Wang X, Czosnek A, Hube F, Mutawe M,Watson PH, Leygue E. 2004. The steroid receptor RNA activator is the first functional RNA encoding a protein. FEBS Lett 566: 43-47.
11. Chooniedass-Kothari S, Hamedani MK, Wang X, Carascossa S, Yan Y, Cooper C, Vincett D, Myal Y, Jalaguier S, Cavailles V, et al. 2010a. The steroid receptor RNA activator protein is recruited to promoter regions and acts as a transcriptional repressor. FEBS Lett 584: 2218-2224.
12. Chooniedass-Kothari S, Vincett D, Yan Y, Cooper C, Hamedani MK, Myal Y, Leygue E. 2010b. The protein encoded by the functional steroid receptor RNA activator is a new modulator of ERa transcriptional activity. FEBS Lett 584: 1174-1180.
13. Chung JH, Whiteley M, Felsenfeld G. 1993. A 5′ element of the chicken β-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell 74: 505-514.
14. Colley SM, Leedman PJ. 2009. SRA and its binding partners: An expanding role for RNA-binding coregulators in nuclear receptor-mediated gene regulation. Crit Rev Biochem Mol Biol 44: 25-33.
15. Colley SM, Iyer KR, Leedman PJ. 2008. The RNA coregulator SRA, its binding proteins and nuclear receptor signaling activity. IUBMB Life 60: 159-164.
16. 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.
17. DeChiara TM, Robertson EJ, Efstratiadis A. 1991. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64: 849-859.
18. Endoh H, Maruyama K, Masuhiro Y, Kobayashi Y, Goto M, Tai H, Yanagisawa J, Metzger D, Hashimoto S, Kato S. 1999. Purification and identification of p68 RNA helicase acting as a transcriptional coactivator specific for the activation function 1 of human estrogen receptor a. Mol Cell Biol 19: 5363-5372.
19. Engel N, Raval AK, Thorvaldsen JL, Bartolomei SM. 2008. Three-dimensional conformation at the H19/Igf2 locus supports a model of enhancer tracking. Hum Mol Genet 17: 3021-3029.
20. Filippova GN, Fagerlie S, Klenova EM, Myers C, Dehner Y, Goodwin G, Neiman PE, Collins SJ, Lobanenkov VV. 1996. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol Cell Biol 16: 2802-2813.
21. Fukuda T, Yamagata K, Fujiyama S, Matsumoto T, Koshida I, Yoshimura K, Mihara M, Naitou M, Endoh H, Nakamura T, et al. 2007. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nat Cell Biol 9: 604-611.
22. Fuller-Pace FV, Ali S. 2008. The DEAD box RNA helicases p68 (Ddx5) and p72 (Ddx17): Novel transcriptional co-regulators. Biochem Soc Trans 36: 609-612.
23. Gaszner M, Felsenfeld G. 2006. Insulators: Exploiting transcriptional and epigenetic mechanisms. Nat Rev Genet 7: 703-713.
24. Georgiev P, Kozycina M. 1996. Interaction between mutations in the suppressor of Hairy wing and modifier of mdg4 genes of Drosophila melanogaster affecting the phenotype of gypsyinduced mutations. Genetics 142: 425-436.
25. Geyer PK, Corces VG. 1992. DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev 6: 1865-1873.
26. Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T, Fraser P, Fisher AG, Merkenschlager M. 2009. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460: 410-413.
27. 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.
28. Holmgren C, Kanduri C, Dell G, Ward A, Mukhopadhya R, Kanduri M, Lobanenkov V, Ohlsson R. 2001. CpG methylation regulates the Igf2/H19 insulator. Curr Biol 11: 1128-1130.
29. Hou C, Dale R, Dean A. 2010. Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc Natl Acad Sci 107: 3651-3656.
30. Hube F, Guo JM, Chooniedass-Kothari S, Cooper C, Hamedani MK, Dibrov AA, Blanchard AAA, Wang XM, Deng G, Myal Y, et al. 2006. Alternative splicing of the first intron of the steroid receptor RNA activator (SRA) participates in the generation of coding and noncoding RNA isoforms in breast cancer cell lines. DNA Cell Biol 25: 418-428.
31. Ishihara K, Oshimura M, Nakao M. 2006. CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell 23: 733-742.
32. Jalal C, Uhlmann-Schiffler H, Stahl H. 2007. Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Res 35: 3590-3601.
33. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, et al. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-435.
34. 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.
35. Kellum R, Schedl P. 1991. A position-effect assay for boundaries of higher order chromosomal domains. Cell 64: 941-950.
36. 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.
37. Lanz RB, MeKenna NJ, Onate SA, Albrecht U, Wong J, Tsai SY, Tsai MJ, O'Malley BW. 1999. A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 97: 17-27.
38. Lei EP, Corces VG. 2006. RNA interference machinery influences the nuclear organization of a chromatin insulator. Nat Genet 38: 936-941.
39. Leygue E. 2007. Steroid receptor RNA activator (SRA1): Unusual bi-faceted gene products with suspected relevance to breast cancer. Nuclear Recept Signal 5: e006. doi: 10.1621/nrs.05006.
40. Li T, Hu JF, Qiu X, Ling J, Chen H, Wang S, Hou A, Vu TH, Hoffman AR. 2008. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop. Mol Cell Biol 28: 6473-6482.
41. Lin C, Yang L, Yang JJ, Huang Y, Liu ZR. 2005. ATPase/helicase activities of p68 RNA helicase are required for pre-mRNA splicing but not for assembly of the spliceosome. Mol Cell Biol 25: 7484-7493.
42. Métivier R, Penot G, Hübner MR, Reid G, Brand H, Kos M, Gannon F. 2003. Estrogen receptor-a directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115: 751-763.
43. Moon H, Filippova G, Loukinov D, Pugacheva E, Chen Q, Smith ST, Munhall A, Grewe B, Bartkuhn M, Arnold R, et al. 2005. CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep 6: 165-170.
44. Nativio R, Wendt KS, Ito Y, Huddleston JE, Uribe-Lewis S, Woodfine K, Krueger C, Reik W, Peters JM, Murrell A. 2009. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet 5: e1000739. doi: 10.1371/journal.pgen.1000739.
45. Ohlsson R, Renkawitz R, Lobanenkov V. 2001. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 17: 520-527.
46. Pai CY, Lei EP, Ghosh D, Corces VG. 2004. The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol Cell 16: 737-748.
47. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, et al. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132: 422-433.
48. Phillips JE, Corces VG. 2009. CTCF: Master weaver of the genome. Cell 137: 1194-1211.
49. Recillas-Targa F, Bell AC, Felsenfeld G. 1999. Positional enhancer-blocking activity of the chicken β-globin insulator in transiently transfected cells. Proc Natl Acad Sci 96: 14354-14359.
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 105: 8309-8314.
51. Salzman DW, Shubert-Coleman J, Furneaux H. 2007. P68 RNA helicase unwinds the human let-7 microRNA precursor duplex and is required for let-7-directed silencing of gene expression. J Biol Chem 282: 32773-32779.
52. Sandhu KS, Shi C, Sjölinder M, Zhao Z, Göndör A, Liu L, Tiwari VK, Guibert S, Emilsson L, Imreh MP, et al. 2009. Nonallelic transvection of multiple imprinted loci is organized by the H19 imprinting control region during germline development. Genes Dev 23: 2598-2603.
53. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD, Carroll JS, Flicek P, Odom DT. 2010. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20: 578-588.
54. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K. 2009. Modulation of microRNA processing by p53. Nature 460: 529-533.
55. Vostrov AA, Quitschke WW. 1997. The zinc finger protein CTCF binds to the APBb domain of the amyloid β-protein precursor promoter. Evidence for a role in transcriptional activation. J Biol Chem 272: 33353-33359.
56. Wallace JA, Felsenfeld G. 2007. We gather together: Insulators and genome organization. Curr Opin Genet Dev 17: 400-407.
57. Watanabe M, Yanagisawa J, Kitagawa H, Takeyama K, Ogawa S, Arao Y, Suzawa M, Kobayashi Y, Yano T, Yoshikawa H, et al. 2001. A subfamily of RNA-binding DEAD-box proteins acts as an estrogen receptor α coactivator through the N-terminal activation domain (AF-1) with an RNA coactivator, SRA. EMBO J 20: 1341-1352.
58. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, et al. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451: 796-801.
59. Xie X,Mikkelsen TS, Gnirke A, Lindblad-Toh K, Kellis M, Lander ES. 2007. Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites. Proc Natl Acad Sci 104: 7145-7150.
60. Yoon YS, Jeong S, Rong Q, Park KY, Chung JH, Pfeifer K. 2007. Analysis of the H19ICR insulator. Mol Cell Biol 27: 3499-3510.
61. 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.
62. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. 2008. Model-based analysis of ChIP-seq (MACS). Genome Biol 9: R137. doi: 10.1186/gb-2008-9-9-r137.