Skip to main content
Log in

Regulation of ISWI chromatin remodelling activity

  • Mini-Review
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

The packaging of the eukaryotic genome into chromatin facilitates the storage of the genetic information within the nucleus, but prevents the access to the underlying DNA sequences. Structural changes in chromatin are mediated by several mechanisms. Among them, ATP-dependent remodelling complexes belonging to ISWI family provides one of the best examples that eukaryotic cells evolved to finely regulate these changes. ISWI-containing complexes use the energy derived from ATP hydrolysis to rearrange nucleosomes on chromatin in order to favour specific nuclear reactions. The combination of regulatory nuclear factors associated with the ATPase subunit as well as its modulation by specific histone modifications, specializes the nuclear function of each ISWI-containing complex. Here we review the different ways by which ISWI enzymatic activity can be modulated and regulated in the nucleus of eukaryotic cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aasland R, Gibson TJ, Stewart AF (1995) The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem Sci 20(2):56–59

    Article  PubMed  CAS  Google Scholar 

  • Angelov D, Molla A, Perche PY, Hans F, Cote J, Khochbin S, Bouvet P, Dimitrov S (2003) The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. Mol Cell 11(4):1033–1041

    Article  PubMed  CAS  Google Scholar 

  • Arancio W, Onorati MC, Burgio G, Collesano M, Ingrassia AM, Genovese SI, Fanto M, Corona DF (2010) The nucleosome remodeling factor ISWI functionally interacts with an evolutionarily conserved network of cellular factors. Genetics 185(1):129–140. doi:10.1534/genetics.110.114256

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21(3):381–395. doi:10.1038/cr.2011.22

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Becker PB, Horz W (2002) ATP-dependent nucleosome remodeling. Annu Rev Biochem 71:247–273

    Article  PubMed  CAS  Google Scholar 

  • Berger SL (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12(2):142–148

    Article  PubMed  CAS  Google Scholar 

  • Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P, Boyle PJ, Cao H, Carter NP, Clelland GK, Davis S, Day N, Dhami P, Dillon SC, Dorschner MO, Fiegler H, Giresi PG, Goldy J, Hawrylycz M, Haydock A, Humbert R, James KD, Johnson BE, Johnson EM, Frum TT, Rosenzweig ER, Karnani N, Lee K, Lefebvre GC, Navas PA, Neri F, Parker SC, Sabo PJ, Sandstrom R, Shafer A, Vetrie D, Weaver M, Wilcox S, Yu M, Collins FS, Dekker J, Lieb JD, Tullius TD, Crawford GE, Sunyaev S, Noble WS, Dunham I, Denoeud F, Reymond A, Kapranov P, Rozowsky J, Zheng D, Castelo R, Frankish A, Harrow J, Ghosh S, Sandelin A, Hofacker IL, Baertsch R, Keefe D, Dike S, Cheng J, Hirsch HA, Sekinger EA, Lagarde J, Abril JF, Shahab A, Flamm C, Fried C, Hackermuller J, Hertel J, Lindemeyer M, Missal K, Tanzer A, Washietl S, Korbel J, Emanuelsson O, Pedersen JS, Holroyd N, Taylor R, Swarbreck D, Matthews N, Dickson MC, Thomas DJ, Weirauch MT, Gilbert J, Drenkow J, Bell I, Zhao X, Srinivasan KG, Sung WK, Ooi HS, Chiu KP, Foissac S, Alioto T, Brent M, Pachter L, Tress ML, Valencia A, Choo SW, Choo CY, Ucla C, Manzano C, Wyss C, Cheung E, Clark TG, Brown JB, Ganesh M, Patel S, Tammana H, Chrast J, Henrichsen CN, Kai C, Kawai J, Nagalakshmi U, Wu J, Lian Z, Lian J, Newburger P, Zhang X, Bickel P, Mattick JS, Carninci P, Hayashizaki Y, Weissman S, Hubbard T, Myers RM, Rogers J, Stadler PF, Lowe TM, Wei CL, Ruan Y, Struhl K, Gerstein M, Antonarakis SE, Fu Y, Green ED, Karaoz U, Siepel A, Taylor J, Liefer LA, Wetterstrand KA, Good PJ, Feingold EA, Guyer MS, Cooper GM, Asimenos G, Dewey CN, Hou M, Nikolaev S, Montoya-Burgos JI, Loytynoja A, Whelan S, Pardi F, Massingham T, Huang H, Zhang NR, Holmes I, Mullikin JC, Ureta-Vidal A, Paten B, Seringhaus M, Church D, Rosenbloom K, Kent WJ, Stone EA, Batzoglou S, Goldman N, Hardison RC, Haussler D, Miller W, Sidow A, Trinklein ND, Zhang ZD, Barrera L, Stuart R, King DC, Ameur A, Enroth S, Bieda MC, Kim J, Bhinge AA, Jiang N, Liu J, Yao F, Vega VB, Lee CW, Ng P, Yang A, Moqtaderi Z, Zhu Z, Xu X, Squazzo S, Oberley MJ, Inman D, Singer MA, Richmond TA, Munn KJ, Rada-Iglesias A, Wallerman O, Komorowski J, Fowler JC, Couttet P, Bruce AW, Dovey OM, Ellis PD, Langford CF, Nix DA, Euskirchen G, Hartman S, Urban AE, Kraus P, Van Calcar S, Heintzman N, Kim TH, Wang K, Qu C, Hon G, Luna R, Glass CK, Rosenfeld MG, Aldred SF, Cooper SJ, Halees A, Lin JM, Shulha HP, Xu M, Haidar JN, Yu Y, Iyer VR, Green RD, Wadelius C, Farnham PJ, Ren B, Harte RA, Hinrichs AS, Trumbower H, Clawson H, Hillman-Jackson J, Zweig AS, Smith K, Thakkapallayil A, Barber G, Kuhn RM, Karolchik D, Armengol L, Bird CP, de Bakker PI, Kern AD, Lopez-Bigas N, Martin JD, Stranger BE, Woodroffe A, Davydov E, Dimas A, Eyras E, Hallgrimsdottir IB, Huppert J, Zody MC, Abecasis GR, Estivill X, Bouffard GG, Guan X, Hansen NF, Idol JR, Maduro VV, Maskeri B, McDowell JC, Park M, Thomas PJ, Young AC, Blakesley RW, Muzny DM, Sodergren E, Wheeler DA, Worley KC, Jiang H, Weinstock GM, Gibbs RA, Graves T, Fulton R, Mardis ER, Wilson RK, Clamp M, Cuff J, Gnerre S, Jaffe DB, Chang JL, Lindblad-Toh K, Lander ES, Koriabine M, Nefedov M, Osoegawa K, Yoshinaga Y, Zhu B, de Jong PJ (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447(7146):799–816. doi:10.1038/nature05874

    Article  PubMed  CAS  Google Scholar 

  • Bonaldi T, Langst G, Strohner R, Becker PB, Bianchi ME (2002) The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding. Embo J 21(24):6865–6873

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Boyer LA, Langer MR, Crowley KA, Tan S, Denu JM, Peterson CL (2002) Essential role for the SANT domain in the functioning of multiple chromatin remodeling enzymes. Mol Cell Mol Cell 10(4):935–942

    Article  Google Scholar 

  • Boyer LA, Latek RR, Peterson CL (2004) The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol 5(2):158–163. doi:10.1038/nrm1314

    Article  PubMed  CAS  Google Scholar 

  • Brehm A, Langst G, Kehle J, Clapier CR, Imhof A, Eberharter A, Muller J, Becker PB (2000) dMi-2 and ISWI chromatin remodelling factors have distinct nucleosome binding and mobilization properties. Embo J 19(16):4332–4341. doi:10.1093/emboj/19.16.4332

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Burgio G, La Rocca G, Sala A, Arancio W, Di Gesu D, Collesano M, Sperling AS, Armstrong JA, van Heeringen SJ, Logie C, Tamkun JW, Corona DF (2008) Genetic identification of a network of factors that functionally interact with the nucleosome remodeling ATPase ISWI. PLoS Genet 4(6):e1000089. doi:10.1371/journal.pgen.1000089

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chadwick BP, Willard HF (2001) Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant. Hum Mol Genet 10(10):1101–1113

    Article  PubMed  CAS  Google Scholar 

  • Chang EY, Ferreira H, Somers J, Nusinow DA, Owen-Hughes T, Narlikar GJ (2008) MacroH2A allows ATP-dependent chromatin remodeling by SWI/SNF and ACF complexes but specifically reduces recruitment of SWI/SNF. Biochemistry 47(51):13726–13732. doi:10.1021/bi8016944

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273–304. doi:10.1146/annurev.biochem.77.062706.153223

    Article  PubMed  CAS  Google Scholar 

  • Clapier CR, Cairns BR (2012) Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes. Nature 492(7428):280–284. doi:10.1038/nature11625

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Clapier CR, Langst G, Corona DF, Becker PB, Nightingale KP (2001) Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol Cell Biol 21(3):875–883. doi:10.1128/MCB.21.3.875-883.2001

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Clapier CR, Nightingale KP, Becker PB (2002) A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res 30(3):649–655

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Coleman-Derr D, Zilberman D (2012) Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet 8(10):e1002988

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Corona DF, Tamkun JW (2004a) Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim Biophys Acta 1677(1–3):113–119. doi:10.1016/j.bbaexp.2003.09.018

    Article  PubMed  CAS  Google Scholar 

  • Corona DF, Tamkun JW (2004b) Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim Biophys Acta 1677(1–3):113–119

    Article  PubMed  CAS  Google Scholar 

  • Corona DF, Langst G, Clapier CR, Bonte EJ, Ferrari S, Tamkun JW, Becker PB (1999) ISWI is an ATP-dependent nucleosome remodeling factor. Mol Cell 3(2):239–245

    Article  PubMed  CAS  Google Scholar 

  • Corona DF, Clapier CR, Becker PB, Tamkun JW (2002) Modulation of ISWI function by site-specific histone acetylation. EMBO Rep 3(3):242–247. doi:10.1093/embo-reports/kvf056

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dang W, Bartholomew B (2007) Domain architecture of the catalytic subunit in the ISW2–nucleosome complex. Mol Cell Biol 27(23):8306–8317. doi:10.1128/MCB.01351-07

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dang W, Kagalwala MN, Bartholomew B (2006) Regulation of ISW2 by concerted action of histone H4 tail and extranucleosomal DNA. Mol Cell Biol 26(20):7388–7396. doi:10.1128/MCB.01159-06

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Deuring R, Fanti L, Armstrong JA, Sarte M, Papoulas O, Prestel M, Daubresse G, Verardo M, Moseley SL, Berloco M, Tsukiyama T, Wu C, Pimpinelli S, Tamkun JW (2000) The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol Cell 5(2):355–365

    Article  PubMed  CAS  Google Scholar 

  • Dirscherl SS, Krebs JE (2004) Functional diversity of ISWI complexes. Biochem Cell Biol 82(4):482–489

    Article  PubMed  CAS  Google Scholar 

  • Doyen CM, Montel F, Gautier T, Menoni H, Claudet C, Delacour-Larose M, Angelov D, Hamiche A, Bednar J, Faivre-Moskalenko C, Bouvet P, Dimitrov S (2006) Dissection of the unusual structural and functional properties of the variant H2A.B.bd nucleosome. EMBO J 25(18):4234–4244. doi:10.1038/sj.emboj.7601310

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Eberharter A, Ferrari S, Langst G, Straub T, Imhof A, Varga-Weisz P, Wilm M, Becker PB (2001) Acf1, the largest subunit of CHRAC, regulates ISWI-induced nucleosome remodelling. Embo J 20(14):3781–3788. doi:10.1093/emboj/20.14.3781

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Eberharter A, Vetter I, Ferreira R, Becker PB (2004) ACF1 improves the effectiveness of nucleosome mobilization by ISWI through PHD-histone contacts. Embo J 23(20):4029–4039. doi:10.1038/sj.emboj.7600382

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Emelyanov AV, Vershilova E, Ignatyeva MA, Pokrovsky DK, Lu X, Konev AY, Fyodorov DV (2012) Identification and characterization of ToRC, a novel ISWI-containing ATP-dependent chromatin assembly complex. Genes Dev 26(6):603–614. doi:10.1101/gad.180604.111

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Erdel F, Krug J, Langst G, Rippe K (2011) Targeting chromatin remodelers: signals and search mechanisms. Biochim Biophys Acta 1809(9):497–508. doi:10.1016/j.bbagrm.2011.06.005

    Article  PubMed  CAS  Google Scholar 

  • Ferreira H, Flaus A, Owen-Hughes T (2007a) Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J Mol Biol 374(3):563–579. doi:10.1016/j.jmb.2007.09.059

    Article  CAS  Google Scholar 

  • Ferreira R, Eberharter A, Bonaldi T, Chioda M, Imhof A, Becker PB (2007b) Site-specific acetylation of ISWI by GCN5. BMC Mol Biol 8:73. doi:1471-2199-8-73 [pii] 10.1186/1471-2199-8-73

    Google Scholar 

  • Fyodorov DV, Kadonaga JT (2002) Binding of Acf1 to DNA involves a WAC motif and is important for ACF-mediated chromatin assembly. Mol Cell Biol 22(18):6344–6353

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Goldman JA, Garlick JD, Kingston RE (2010) Chromatin remodeling by imitation switch (ISWI) class ATP-dependent remodelers is stimulated by histone variant H2A.Z. J Biol Chem 285(7):4645–4651. doi:10.1074/jbc.M109.072348

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Greaves IK, Rangasamy D, Ridgway P, Tremethick DJ (2007) H2A.Z contributes to the unique 3D structure of the centromere. Proc Natl Acad Sci U S A 104(2):525–530. doi:10.1073/pnas.0607870104

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Grune T, Brzeski J, Eberharter A, Clapier CR, Corona DF, Becker PB, Muller CW (2003a) Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol Cell 12(2):449–460

    Article  Google Scholar 

  • Hamiche A, Kang JG, Dennis C, Xiao H, Wu C (2001) Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. Proc Natl Acad Sci U S A 98(25):14316–14321. doi:10.1073/pnas.251421398 251421398

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hanai K, Furuhashi H, Yamamoto T, Akasaka K, Hirose S (2008) RSF governs silent chromatin formation via histone H2Av replacement. PLoS Genet 4(2):e1000011. doi:10.1371/journal.pgen.1000011

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hartlepp KF, Fernandez-Tornero C, Eberharter A, Grune T, Muller CW, Becker PB (2005) The histone fold subunits of Drosophila CHRAC facilitate nucleosome sliding through dynamic DNA interactions. Mol Cell Biol 25(22):9886–9896. doi:10.1128/MCB.25.22.9886-9896.2005

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • He X, Fan HY, Garlick JD, Kingston RE (2008) Diverse regulation of SNF2h chromatin remodeling by noncatalytic subunits. Biochemistry 47(27):7025–7033. doi:10.1021/bi702304p

    Article  PubMed  CAS  Google Scholar 

  • Hota SK, Bartholomew B (2011) Diversity of operation in ATP-dependent chromatin remodelers. Biochim Biophys Acta 1809(9):476–487. doi:10.1016/j.bbagrm.2011.05.007

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hota SK, Bhardwaj SK, Deindl S, Lin YC, Zhuang X, Bartholomew B (2013) Nucleosome mobilization by ISW2 requires the concerted action of the ATPase and SLIDE domains. Nat Struct Mol Biol 20(2):222–229. doi:10.1038/nsmb.2486

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Iizuka M, Smith MM (2003) Functional consequences of histone modifications. Curr Opin Genet Dev 13(2):154–160

    Article  PubMed  CAS  Google Scholar 

  • Ito T, Levenstein ME, Fyodorov DV, Kutach AK, Kobayashi R, Kadonaga JT (1999) ACF consists of two subunits, Acf1 and ISWI, that function cooperatively in the ATP-dependent catalysis of chromatin assembly. Genes Dev 13(12):1529–1539

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kagalwala MN, Glaus BJ, Dang W, Zofall M, Bartholomew B (2004) Topography of the ISW2-nucleosome complex: insights into nucleosome spacing and chromatin remodeling. Embo J 23(10):2092–2104. doi:10.1038/sj.emboj.7600220

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Konev AY, Tribus M, Park SY, Podhraski V, Lim CY, Emelyanov AV, Vershilova E, Pirrotta V, Kadonaga JT, Lusser A, Fyodorov DV (2007) CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 317(5841):1087–1090. doi:10.1126/science.1145339

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kukimoto I, Elderkin S, Grimaldi M, Oelgeschlager T, Varga-Weisz PD (2004) The histone-fold protein complex CHRAC-15/17 enhances nucleosome sliding and assembly mediated by ACF. Mol Cell 13(2):265–277

    Article  PubMed  CAS  Google Scholar 

  • Lakhotia SC (2011) Forty years of the 93D puff of Drosophila melanogaster. J Biosci 36(3):399–423

    Article  PubMed  CAS  Google Scholar 

  • Lan L, Ui A, Nakajima S, Hatakeyama K, Hoshi M, Watanabe R, Janicki SM, Ogiwara H, Kohno T, Kanno S, Yasui A (2010) The ACF1 complex is required for DNA double-strand break repair in human cells. Mol Cell 40(6):976–987. doi:10.1016/j.molcel.2010.12.003

    Article  PubMed  CAS  Google Scholar 

  • Langst G, Bonte EJ, Corona DF, Becker PB (1999) Nucleosome movement by CHRAC and ISWI without disruption or trans-displacement of the histone octamer. Cell 97(7):843–852

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Hao Y, Dong X, Gong Q, Chen J, Zhang J, Tian W (2012) Molecular mechanisms and function prediction of long noncoding RNA. ScientificWorldJournal 2012:541786. doi:10.1100/2012/541786

    PubMed Central  PubMed  Google Scholar 

  • MacCallum DE, Losada A, Kobayashi R, Hirano T (2002) ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B. Mol Biol Cell 13(1):25–39. doi:10.1091/mbc.01-09-0441

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Manning BJ, Peterson CL (2013) Releasing the brakes on a chromatin-remodeling enzyme. Nat Struct Mol Biol 20(1):5–7. doi:10.1038/nsmb.2482

    Article  PubMed  CAS  Google Scholar 

  • Martens JA, Winston F (2003) Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr Opin Genet Dev 13(2):136–142

    Article  PubMed  CAS  Google Scholar 

  • Mayer C, Neubert M, Grummt I (2008) The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep 9(8):774–780. doi:10.1038/embor.2008.109

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • McConnell AD, Gelbart ME, Tsukiyama T (2004) Histone fold protein Dls1p is required for Isw2-dependent chromatin remodeling in vivo. Mol Cell Biol 24(7):2605–2613

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303(5656):343–348. doi:10.1126/science.1090701 1090701

    Article  PubMed  CAS  Google Scholar 

  • Moshkin YM, Chalkley GE, Kan TW, Reddy BA, Ozgur Z, van Ijcken WF, Dekkers DH, Demmers JA, 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(3):675–688. doi:10.1128/MCB.06365-11

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mueller-Planitz F, Klinker H, Ludwigsen J, Becker PB (2013) The ATPase domain of ISWI is an autonomous nucleosome remodeling machine. Nat Struct Mol Biol 20(1):82–89. doi:10.1038/nsmb.2457

    Article  PubMed  CAS  Google Scholar 

  • Okada M, Okawa K, Isobe T, Fukagawa T (2009) CENP-H-containing complex facilitates centromere deposition of CENP-A in cooperation with FACT and CHD1. Mol Biol Cell 20(18):3986–3995. doi:10.1091/mbc.E09-01-0065

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Onorati MC, Lazzaro S, Mallik M, Ingrassia AM, Carreca AP, Singh AK, Chaturvedi DP, Lakhotia SC, Corona DF (2011) The ISWI chromatin remodeler organizes the hsromega ncRNA-containing omega speckle nuclear compartments. PLoS Genet 7(5):e1002096. doi:10.1371/journal.pgen.1002096

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Partensky PD, Narlikar GJ (2009) Chromatin remodelers act globally, sequence positions nucleosomes locally. J Mol Biol 391(1):12–25. doi:10.1016/j.jmb.2009.04.085

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Perpelescu M, Nozaki N, Obuse C, Yang H, Yoda K (2009) Active establishment of centromeric CENP-A chromatin by RSF complex. J Cell Biol 185(3):397–407. doi:10.1083/jcb.200903088

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Prasanth KV, Rajendra TK, Lal AK, Lakhotia SC (2000) Omega speckles — a novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila. J Cell Sci 113(Pt 19):3485–3497

    PubMed  CAS  Google Scholar 

  • Pusarla RH, Bhargava P (2005) Histones in functional diversification. Core histone variants. Febs J 272(20):5149–5168. doi:10.1111/j.1742-4658.2005.04930.x

    Article  PubMed  CAS  Google Scholar 

  • Raisner RM, Madhani HD (2006) Patterning chromatin: form and function for H2A.Z variant nucleosomes. Curr Opin Genet Dev 16(2):119–124. doi:10.1016/j.gde.2006.02.005

    Article  PubMed  CAS  Google Scholar 

  • Rangasamy D, Greaves I, Tremethick DJ (2004) RNA interference demonstrates a novel role for H2A.Z in chromosome segregation. Nat Struct Mol Biol 11(7):650–655. doi:10.1038/nsmb786

    Article  PubMed  CAS  Google Scholar 

  • Rippe K, Schrader A, Riede P, Strohner R, Lehmann E, Langst G (2007) DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes. Proc Natl Acad Sci U S A 104(40):15635–15640. doi:10.1073/pnas.0702430104

    Article  PubMed Central  PubMed  Google Scholar 

  • Sala A, La Rocca G, Burgio G, Kotova E, Di Gesu D, Collesano M, Ingrassia AM, Tulin AV, Corona DF (2008) The nucleosome-remodeling ATPase ISWI is regulated by poly-ADP-ribosylation. PLoS Biol 6(10):e252. doi:10.1371/journal.pbio.0060252

    Article  PubMed  CAS  Google Scholar 

  • 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(9):1766–1777. doi:10.1038/emboj.2011.98

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Santos-Rosa H, Schneider R, Bernstein BE, Karabetsou N, Morillon A, Weise C, Schreiber SL, Mellor J, Kouzarides T (2003) Methylation of histone H3 K4 mediates association of the Isw1p ATPase with chromatin. Mol Cell 12(5):1325–1332

    Article  PubMed  CAS  Google Scholar 

  • Sheu JJ, Choi JH, Yildiz I, Tsai FJ, Shaul Y, Wang TL, Shih Ie M (2008) The roles of human sucrose nonfermenting protein 2 homologue in the tumor-promoting functions of Rsf-1. Cancer Res 68(11):4050–4057. doi:10.1158/0008-5472.CAN-07-3240

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stockdale C, Flaus A, Ferreira H, Owen-Hughes T (2006) Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J Biol Chem 281(24):16279–16288. doi:10.1074/jbc.M600682200

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stopka T, Skoultchi AI (2003) The ISWI ATPase Snf2h is required for early mouse development. Proc Natl Acad Sci U S A 100(24):14097–14102

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403(6765):41–45. doi:10.1038/47412

    Article  PubMed  CAS  Google Scholar 

  • Strohner R, Wachsmuth M, Dachauer K, Mazurkiewicz J, Hochstatter J, Rippe K, Langst G (2005) A 'loop recapture' mechanism for ACF-dependent nucleosome remodeling. Nat Struct Mol Biol 12(8):683–690. doi:10.1038/nsmb966

    Article  PubMed  CAS  Google Scholar 

  • van Vugt JJ, Ranes M, Campsteijn C, Logie C (2007) The ins and outs of ATP-dependent chromatin remodeling in budding yeast: biophysical and proteomic perspectives. Biochim Biophys Acta 1769(3):153–171

    Article  PubMed  CAS  Google Scholar 

  • Vasicova P, Stradalova V, Halada P, Hasek J, Malcova I (2013) Nuclear import of chromatin remodeler Isw1 is mediated by atypical bipartite cNLS and classical import pathway. Traffic 14(2):176–193. doi:10.1111/tra.12025

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Mizzen C, Ying C, Candau R, Barlev N, Brownell J, Allis CD, Berger SL (1997) Histone acetyltransferase activity is conserved between yeast and human GCN5 and is required for complementation of growth and transcriptional activation. Mol Cell Biol 17(1):519–527

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wu J, Grunstein M (2000) 25 years after the nucleosome model: chromatin modifications. Trends Biochem Sci 25(12):619–623

    Article  PubMed  CAS  Google Scholar 

  • Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, Wu C, Allis CD (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442(7098):86–90. doi:10.1038/nature04815

    PubMed  CAS  Google Scholar 

  • 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(3):531–543

    Article  PubMed  CAS  Google Scholar 

  • Xiao A, Li H, Shechter D, Ahn SH, Fabrizio LA, Erdjument-Bromage H, Ishibe-Murakami S, Wang B, Tempst P, Hofmann K, Patel DJ, Elledge SJ, Allis CD (2009) WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457(7225):57–62. doi:10.1038/nature07668

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yadon AN, Tsukiyama T (2011) SnapShot: chromatin remodeling: ISWI. Cell 144(3):453–453. doi:10.1016/j.cell.2011.01.019, e451

    Article  PubMed  CAS  Google Scholar 

  • Yamada K, Frouws TD, Angst B, Fitzgerald DJ, DeLuca C, Schimmele K, Sargent DF, Richmond TJ (2011) Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472(7344):448–453. doi:10.1038/nature09947

    Article  PubMed  CAS  Google Scholar 

  • Yang JG, Madrid TS, Sevastopoulos E, Narlikar GJ (2006) The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat Struct Mol Biol 13(12):1078–1083. doi:10.1038/nsmb1170

    Article  PubMed  CAS  Google Scholar 

  • Zentner GE, Tsukiyama T, Henikoff S (2013) ISWI and CHD chromatin remodelers bind promoters but act in gene bodies. PLoS Genet 9(2):e1003317. doi:10.1371/journal.pgen.1003317

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhou BR, Feng H, Ghirlando R, Kato H, Gruschus J, Bai Y (2012) Histone H4 K16Q mutation, an acetylation mimic, causes structural disorder of its N-terminal basic patch in the nucleosome. J Mol Biol 421(1):30–37. doi:10.1016/j.jmb.2012.04.032

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zofall M, Persinger J, Bartholomew B (2004) Functional role of extranucleosomal DNA and the entry site of the nucleosome in chromatin remodeling by ISW2. Mol Cell Biol 24(22):10047–10057. doi:10.1128/MCB.24.22.10047-10057.2004

    Article  PubMed Central  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank our colleagues Giosalba Burgio, Roberta Sanfilippo, Maria Cristina Onorati, Luca Lo Piccolo and Vincenzo Cavalieri for their critical reading of the manuscript. We also acknowlege the support of Fondazione Telethon, AIRC, MIUR-CNR EPIGEN and EMBO YIP to DFVC. MT was supported by a FIRC Fellowship. Finally, we apologize to all our colleagues whose work was not properly cited due to space restriction.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Davide F. V. Corona.

Additional information

M. Toto and G. D'Angelo contributed equally to this review.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Toto, M., D’Angelo, G. & Corona, D.F.V. Regulation of ISWI chromatin remodelling activity. Chromosoma 123, 91–102 (2014). https://doi.org/10.1007/s00412-013-0447-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-013-0447-4

Keywords

Navigation