Functional interactions between NURF and Ctcf regulate gene expression

Molecular and Cellular Biology

Volumn 35, Issue 1, 2015, Pages 224-237

  Qiu, Zhijun ^a   Song, Carolyn ^a   Malakouti, Navid ^a   Murray, Daniel ^a   Hariz, Aymen ^a   Zimmerman, Mark ^a   Gygax, Derek ^a   Alhazmi, Aiman ^a   Landry, Joseph W ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROMODOMAIN PHD FINGER CONTAINING TRANSCRIPTION FACTOR; COHESIN; HISTONE H2AZ; HISTONE H3; KRUPPEL LIKE FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; CCCTC-BINDING FACTOR; CELL NUCLEUS ANTIGEN; CHROMATIN; FETAL ALZHEIMER ANTIGEN; HISTONE; HISTONE DEACETYLASE; NERVE PROTEIN; NUCLEOSOME; PROTEIN BINDING; REPRESSOR PROTEIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL RENEWAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; LOXP SITE; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; NUCLEOSOME; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION TERMINATION; ANIMAL; CHROMATIN; CYTOLOGY; DNA MICROARRAY; EMBRYONIC STEM CELL; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; ANTIGENS, NUCLEAR; BINDING SITES; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; HISTONES; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NUCLEOSOMES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84920053940     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00553-14     Document Type: Article

References (47)

1. Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273-304. http://dx.doi.org/10.1146/annurev.biochem.77.062706.153223.
2. Ho L, Crabtree GR. 2010. Chromatin remodelling during development. Nature 463:474-484. http://dx.doi.org/10.1038/nature08911.
3. Barak O, Lazzaro MA, Lane WS, Speicher DW, Picketts DJ, Shiekhattar R. 2003. Isolation of human NURF: a regulator of Engrailed gene expression. EMBO J 22:6089-6100. http://dx.doi.org/10.1093/emboj/cdg582.
4. Xiao H, Sandaltzopoulos R, Wang HM, Hamiche A, Ranallo R, Lee KM, Fu D, Wu C. 2001. Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol Cell 8:531-543. http://dx.doi.org/10.1016/S1097-2765(01)00345-8.
5. Alkhatib SG, Landry JW. 2011. The nucleosome remodeling factor. FEBS Lett 585:3197-3207. http://dx.doi.org/10.1016/j.febslet.2011.09.003.
6. Euskirchen GM, Auerbach RK, Davidov E, Gianoulis TA, Zhong G, Rozowsky J, Bhardwaj N, Gerstein MB, Snyder M. 2011. Diverse roles and interactions of the SWI/SNF chromatin remodeling complex revealed using global approaches. PLoS Genet 7:e1002008. http://dx.doi.org/10.1371/journal.pgen.1002008.
7. Ishihara K, Oshimura M, Nakao M. 2006. CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell 23:733-742. http://dx.doi.org/10.1016/j.molcel.2006.08.008.
8. Lai AY, Wade PA. 2011. Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat Rev Cancer 11:588-596. http://dx.doi.org/10.1038/nrc3091.
9. Trotter KW, Archer TK. 2008. The BRG1 transcriptional coregulator. Nucl Recept Signal 6:e004. http://dx.doi.org/10.1621/nrs.06004.
10. 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.
11. 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.
12. Faure AJ, Schmidt D, Watt S, Schwalie PC, Wilson MD, Xu H, Ramsay RG, Odom DT, Flicek P. 2012. Cohesin regulates tissue-specific expression by stabilizing highly occupied cis-regulatory modules. Genome Res 22:2163-2175. http://dx.doi.org/10.1101/gr.136507.111.
13. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD, Carroll J S, Flicek P, Odom DT. 2010. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20:578-588. http://dx.doi.org/10.1101/gr.100479.109.
14. Zuin J, Dixon JR, van der Reijden MI, Ye Z, Kolovos P, Brouwer RW, van de Corput MP, van de Werken HJ, Knoch TA, van Ijcken WF, Grosveld FG, Ren B, Wendt KS. 2014. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc Natl Acad Sci U S A 111:996-1001. http://dx.doi.org/10.1073/pnas.1317788111.
15. Fu Y, Sinha M, Peterson CL, Weng Z. 2008. The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet 4:e1000138. http://dx.doi.org/10.1371/journal.pgen.1000138.
16. Weth O, Renkawitz R. 2011. CTCF function is modulated by neighboring DNAbinding factors. Biochem Cell Biol 89:459-468. http://dx.doi.org/10.1139/o11-033.
17. Landry J, Sharov AA, Piao Y, Sharova LV, Xiao H, Southon E, Matta J, Tessarollo L, Zhang YE, Ko MS, Kuehn MR, Yamaguchi TP, Wu C. 2008. Essential role of chromatin remodeling protein Bptf in early mouse embryos and embryonic stem cells. PLoS Genet 4:e1000241. http://dx.doi.org/10.1371/journal.pgen.1000241.
18. Landry JW, Banerjee S, Taylor B, Aplan PD, Singer A, Wu C. 2011. Chromatin remodeling complex NURF regulates thymocyte maturation. Genes Dev 25:275-286. http://dx.doi.org/10.1101/gad.2007311.
19. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, Wagner U, Dixon J, Lee L, Lobanenkov VV, Ren B. 2012. A map of the cis-regulatory sequences in the mouse genome. Nature 488:116-120. http://dx.doi.org/10.1038/nature11243.
20. Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N. 2010. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 20:90-100. http://dx.doi.org/10.1101/gr.098509.109.
21. Jiang C, Pugh BF. 2009. Nucleosome positioning and gene regulation: advances through genomics. Nat Rev Genet 10:161-172. http://dx.doi.org/10.1038/nrg2522.
22. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, Loh YH, Yeo HC, Yeo ZX, Narang V, Govindarajan KR, Leong B, Shahab A, Ruan Y, Bourque G, Sung WK, Clarke ND, Wei CL, Ng HH. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133:1106-1117. http://dx.doi.org/10.1016/j.cell.2008.04.043.
23. Ebert A, McManus S, Tagoh H, Medvedovic J, Salvagiotto G, Novatchkova M, Tamir I, Sommer A, Jaritz M, Busslinger M. 2011. The distal V(H) gene cluster of the Igh locus contains distinct regulatory elements with Pax5 transcription factor-dependent activity in pro-B cells. Immunity 34:175-187. http://dx.doi.org/10.1016/j.immuni.2011.02.005.
24. 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. http://dx.doi.org/10.1038/nature09380.
25. Nitzsche A, Paszkowski-Rogacz M, Matarese F, Janssen-Megens EM, Hubner NC, Schulz H, de Vries I, Ding L, Huebner N, Mann M, Stunnenberg HG, Buchholz F. 2011. RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity. PLoS One 6:e19470. http://dx.doi.org/10.1371/journal.pone.0019470.
26. 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. http://dx.doi.org/10.1128/MCB.05093-11.
27. 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.
28. Hartley PD, Madhani HD. 2009. Mechanisms that specify promoter nucleosome location and identity. Cell 137:445-458. http://dx.doi.org/10.1016/j.cell.2009.02.043.
29. Ranjan A, Mizuguchi G, FitzGerald PC, Wei D, Wang F, Huang Y, Luk E, Woodcock CL, Wu C. 2013. Nucleosome-free region dominates histone acetylation in targeting SWR1 to promoters for H2A.Z replacement. Cell 154:1232-1245. http://dx.doi.org/10.1016/j.cell.2013.08.005.
30. Bell AC, West AG, Felsenfeld G. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98:387-396. http://dx.doi.org/10.1016/S0092-8674(00)81967-4.
31. Arcellana-Panlilio MY, Schultz GA. 1994. Temporal and spatial expression of major histocompatibility complex class I H-2K in the early mouse embryo. Biol Reprod 51:169-183. http://dx.doi.org/10.1095/biolreprod5 1.2.169.
32. Hedley ML, Drake BL, Head J R, Tucker PW, Forman J. 1989. Differential expression of the class I MHC genes in the embryo and placenta during midgestational development in the mouse. J Immunol 142:4046-4053.
33. Madeja Z, Yadi H, Apps R, Boulenouar S, Roper SJ, Gardner L, Moffett A, Colucci F, Hemberger M. 2011. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc Natl Acad Sci U S A 108:4012-4017. http://dx.doi.org/10.1073/pnas.1005342108.
34. Goller T, Vauti F, Ramasamy S, Arnold HH. 2008. Transcriptional regulator BPTF/FAC1 is essential for trophoblast differentiation during early mouse development. Mol Cell Biol 28:6819-6827. http://dx.doi.org/10.1128/MCB.01058-08.
35. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, KlingenhoffA, Frisch M, Bayerlein M, Werner T. 2005. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21:2933-2942. http://dx.doi.org/10.1093/bioinformatics/bti473.
36. Yamanaka S. 2007. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 1:39-49. http://dx.doi.org/10.1016/j.stem.2007.05.012.
37. Armstrong JA, Papoulas O, Daubresse G, Sperling AS, Lis JT, Scott MP, Tamkun JW. 2002. The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J 21:5245-5254. http://dx.doi.org/10.1093/emboj/cdf517.
38. Wilson CJ, Chao DM, Imbalzano AN, Schnitzler GR, Kingston RE, Young RA. 1996. RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling. Cell 84:235-244. http://dx.doi.org/10.1016/S0092-8674(00)80978-2.
39. Wu J I, Lessard J, Crabtree GR. 2009. Understanding the words of chromatin regulation. Cell 136:200-206. http://dx.doi.org/10.1016/j.cell.2009.01.009.
40. Tsukiyama T, Wu C. 1995. Purification and properties of an ATPdependent nucleosome remodeling factor. Cell 83:1011-1020. http://dx.doi.org/10.1016/0092-8674(95)90216-3.
41. Sala A, Toto M, Pinello L, Gabriele A, Di Benedetto V, Ingrassia AM, Lo Bosco G, Di Gesu V, Giancarlo R, Corona DF. 2011. Genome-wide characterization of chromatin binding and nucleosome spacing activity of the nucleosome remodelling ATPase ISWI. EMBO J 30:1766-1777. http://dx.doi.org/10.1038/emboj.2011.98.
42. Whitehouse I, Rando OJ, Delrow J, Tsukiyama T. 2007. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450: 1031-1035. http://dx.doi.org/10.1038/nature06391.
43. Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF. 2012. Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149:1461-1473. http://dx.doi.org/10.1016/j.cell.2012.04.036.
44. Moshkin YM, Chalkley GE, Kan TW, Reddy BA, Ozgur Z, van Ijcken WF, Dekkers DH, Demmers J A, Travers AA, Verrijzer CP. 2012. Remodelers organize cellular chromatin by counteracting intrinsic histone- DNA sequence preferences in a class-specific manner. Mol Cell Biol 32:675-688. http://dx.doi.org/10.1128/MCB.06365-11.
45. Hakimi MA, Bochar DA, Schmiesing J A, Dong Y, Barak OG, Speicher DW, Yokomori K, Shiekhattar R. 2002. A chromatin remodelling complex that loads cohesin onto human chromosomes. Nature 418:994-998. http://dx.doi.org/10.1038/nature01024.
46. Wang H, Maurano MT, Qu H, Varley KE, Gertz J, Pauli F, Lee K, Canfield T, Weaver M, Sandstrom R, Thurman RE, Kaul R, Myers RM, Stamatoyannopoulos JA. 2012. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res 22:1680-1688. http://dx.doi.org/10.1101/gr.136101.111.
47. Ross-Innes CS, Brown GD, Carroll JS. 2011. A co-ordinated interaction between CTCF and ER in breast cancer cells. BMCGenomics 12:593. http://dx.doi.org/10.1186/1471-2164-12-593.