Chromatin remodeling motors play essential roles in all DNA-based processes. These motors catalyze diverse outcomes ranging from sliding the smallest units of chromatin, known as nucleosomes, to completely disassembling chromatin. The broad range of actions carried out by these motors on the complex template presented by chromatin raises many stimulating mechanistic questions. Other well-studied nucleic acid motors provide examples of the depth of mechanistic understanding that is achievable from detailed biophysical studies. We use these studies as a guiding framework to discuss the current state of knowledge of chromatin remodeling mechanisms and highlight exciting open questions that would continue to benefit from biophysical analyses.


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Literature Cited

  1. Aalfs JD, Narlikar GJ, Kingston RE. 1.  2001. Functional differences between the human ATP-dependent nucleosome remodeling proteins BRG1 and SNF2H. J. Biol. Chem. 276:3634270–78 [Google Scholar]
  2. Adamkewicz JI, Mueller CG, Hansen KE, Prud'homme WA, Thorner J. 2.  2000. Purification and enzymic properties of Mot1 ATPase, a regulator of basal transcription in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 275:2821158–68 [Google Scholar]
  3. Anderson JD, Widom J. 3.  2000. Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. J. Mol. Biol. 296:4979–87 [Google Scholar]
  4. Andrews AJ, Chen X, Zevin A, Stargell LA, Luger K. 4.  2010. The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol. Cell 37:6834–42 [Google Scholar]
  5. Andrews AJ, Luger K. 5.  2011. Nucleosome structure(s) and stability: variations on a theme. Annu. Rev. Biophys. 40:99–117 [Google Scholar]
  6. Aoyagi S, Narlikar G, Zheng C, Sif S, Kingston RE, Hayes JJ. 6.  2002. Nucleosome remodeling by the human SWI/SNF complex requires transient global disruption of histone-DNA interactions. Mol. Cell. Biol. 22:113653–62 [Google Scholar]
  7. Auble DT, Hahn S. 7.  1993. An ATP-dependent inhibitor of TBP binding to DNA. Genes Dev. 7:5844–56 [Google Scholar]
  8. Auble DT, Hansen KE, Mueller CG, Lane WS, Thorner J, Hahn S. 8.  1994. Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism. Genes Dev. 8:161920–34 [Google Scholar]
  9. Badenhorst P, Voas M, Rebay I, Wu C. 9.  2002. Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev. 30:23186–98 [Google Scholar]
  10. Bartholomew B.10.  2014. Regulating the chromatin landscape: structural and mechanistic perspectives. Annu. Rev. Biochem. 83:671–96 [Google Scholar]
  11. Bazett-Jones DP, Côté J, Landel CC, Peterson CL, Workman JL. 11.  1999. The SWI/SNF complex creates loop domains in DNA and polynucleosome arrays and can disrupt DNA-histone contacts within these domains. Mol. Cell. Biol. 19:21470–78 [Google Scholar]
  12. Blosser TR, Yang JG, Stone MD, Narlikar GJ, Zhuang X. 12.  2009. Dynamics of nucleosome remodelling by individual ACF complexes. Nature 462:72761022–27 [Google Scholar]
  13. Böhm V, Hieb AR, Andrews AJ, Gansen A, Rocker A. 13.  et al. 2011. Nucleosome accessibility governed by the dimer/tetramer interface. Nucleic Acids Res. 39:83093–102 [Google Scholar]
  14. Bruno M, Flaus A, Stockdale C, Rencurel C, Ferreira H, Owen-Hughes T. 14.  2003. Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodeling activities. Mol. Cell 12:61599–606 [Google Scholar]
  15. Butryn A, Schuller JM, Stoehr G, Runge-Wollmann P, Förster F. 15.  et al. 2015. Structural basis for recognition and remodeling of the TBP:DNA:NC2 complex by Mot1. eLife 4:1–56 [Google Scholar]
  16. Canzio D, Larson A, Narlikar GJ. 16.  2014. Mechanisms of functional promiscuity by HP1 proteins. Trends Cell Biol. 24:6377–86 [Google Scholar]
  17. Chen L, Conaway RC, Conaway JW. 17.  2013. Multiple modes of regulation of the human Ino80 SNF2 ATPase by subunits of the INO80 chromatin-remodeling complex. PNAS 110:5120497–502 [Google Scholar]
  18. Chen Z, Yang H, Pavletich NP. 18.  2008. Mechanism of homologous recombination from the RecA–ssDNA/dsDNA structures. Nature 453:7194489–94 [Google Scholar]
  19. Clapier CR, Cairns BR. 19.  2009. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78:273–304 [Google Scholar]
  20. Clapier CR, Cairns BR. 20.  2012. Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes. Nature 492:7428280–84 [Google Scholar]
  21. Clapier CR, Längst G, Corona DF, Becker PB, Nightingale KP. 21.  2001. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 21:3875–83 [Google Scholar]
  22. Clapier CR, Nightingale KP, Becker PB. 22.  2002. A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res. 30:3649–55 [Google Scholar]
  23. Cloutier TE, Widom J. 23.  2004. Spontaneous sharp bending of double-stranded DNA. Mol. Cell 14:3355–62 [Google Scholar]
  24. Corona DF, Längst G, Clapier CR, Bonte EJ, Ferrari S. 24.  et al. 1999. ISWI is an ATP-dependent nucleosome remodeling factor. Mol. Cell 3:2239–45 [Google Scholar]
  25. Corona DFV, Tamkun JW. 25.  2004. Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim. Biophys. Acta. 1677:1–3113–19 [Google Scholar]
  26. Cox MM.26.  2007. Motoring along with the bacterial RecA protein. Nat. Rev. Mol. Cell Biol. 8:2127–38 [Google Scholar]
  27. Dang W, Bartholomew B. 27.  2007. Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol. Cell. Biol. 27:238306–17 [Google Scholar]
  28. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ. 28.  2002. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319:51097–113 [Google Scholar]
  29. Dechassa ML, Hota SK, Sen P, Chatterjee N, Prasad P, Bartholomew B. 29.  2012. Disparity in the DNA translocase domains of SWI/SNF and ISW2. Nucleic Acids Res. 40:104412–21 [Google Scholar]
  30. Dechassa ML, Sabri A, Pondugula S, Kassabov SR, Chatterjee N. 30.  et al. 2010. SWI/SNF has intrinsic nucleosome disassembly activity that is dependent on adjacent nucleosomes. Mol. Cell 38:4590–602 [Google Scholar]
  31. Deindl S, Hwang WL, Hota SK, Blosser TR, Prasad P. 31.  et al. 2013. ISWI remodelers slide nucleosomes with coordinated multi-base-pair entry steps and single-base-pair exit steps. Cell 152:3442–52 [Google Scholar]
  32. Del Campo M, Lambowitz AM. 32.  2009. Structure of the yeast DEAD box protein Mss116p reveals two wedges that crimp RNA. Mol. Cell 35:5598–609 [Google Scholar]
  33. Dorigo B, Schalch T, Bystricky K, Richmond TJ. 33.  2003. Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J. Mol. Biol. 327:185–96 [Google Scholar]
  34. Eberharter A, Ferrari S, Längst G, Straub T, Imhof A. 34.  et al. 2001. Acf1, the largest subunit of CHRAC, regulates ISWI-induced nucleosome remodelling. EMBO J. 20:143781–88 [Google Scholar]
  35. Eissenberg JC, Elgin SCR. 35.  2014. HP1a: a structural chromosomal protein regulating transcription. Trends Genet. 30:3103–10 [Google Scholar]
  36. Euskirchen G, Auerbach RK, Snyder M. 36.  2012. SWI/SNF chromatin-remodeling factors: multiscale analyses and diverse functions. J. Biol. Chem. 287:3730897–905 [Google Scholar]
  37. Fairman-Williams ME, Guenther U-P, Jankowsky E. 37.  2010. SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol. 20:3313–24 [Google Scholar]
  38. Fan H-Y, He X, Kingston RE, Narlikar GJ. 38.  2003. Distinct strategies to make nucleosomal DNA accessible. Mol. Cell 11:51311–22 [Google Scholar]
  39. Flaus A, Martin DMA, Barton GJ, Owen-Hughes T. 39.  2006. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res. 34:102887–905 [Google Scholar]
  40. Flaus A, Owen-Hughes T. 40.  2003. Dynamic properties of nucleosomes during thermal and ATP-driven mobilization. Mol. Cell. Biol. 23:217767–79 [Google Scholar]
  41. Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT. 41.  2004. Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev. 18:2170–83 [Google Scholar]
  42. Garraway LA, Lander ES. 42.  2013. Lessons from the cancer genome. Cell 153:117–37 [Google Scholar]
  43. Gerhold C-B, Hauer MH, Gasser SM. 43.  2015. INO80-C and SWR-C: guardians of the genome. J. Mol. Biol. 427:3637–51 [Google Scholar]
  44. Gerhold CB, Gasser SM. 44.  2014. INO80 and SWR complexes: relating structure to function in chromatin remodeling. Trends Cell Biol. 24:11619–31 [Google Scholar]
  45. Gkikopoulos T, Havas KM, Dewar H, Owen-Hughes T. 45.  2009. SWI/SNF and Asf1p cooperate to displace histones during induction of the Saccharomyces cerevisiae HO promoter. Mol. Cell. Biol. 29:154057–66 [Google Scholar]
  46. Gkikopoulos T, Schofield P, Singh V, Pinskaya M, Mellor J. 46.  et al. 2011. A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333:60501758–60 [Google Scholar]
  47. Guyon JR, Narlikar GJ, Sullivan EK, Kingston RE. 47.  2001. Stability of a human SWI-SNF remodeled nucleosomal array. Mol. Cell. Biol. 21:41132–44 [Google Scholar]
  48. Hamiche A, Kang JG, Dennis C, Xiao H, Wu C. 48.  2001. Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. PNAS 98:2514316–21 [Google Scholar]
  49. Hamiche A, Sandaltzopoulos R, Gdula DA, Wu C. 49.  1999. ATP-dependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell 97:7833–42 [Google Scholar]
  50. Harada BT, Hwang WL, Deindl S, Chatterjee N, Bartholomew B, Zhuang X. 50.  2016. Stepwise nucleosome translocation by RSC remodeling complexes. eLife 5:e10051 [Google Scholar]
  51. Harshman SW, Young NL, Parthun MR. 51.  2013. H1 histones: current perspectives and challenges. Nucleic Acids Res. 41:219593–609 [Google Scholar]
  52. Hartley PD, Madhani HD. 52.  2009. Mechanisms that specify promoter nucleosome location and identity. Cell 137:3445–58 [Google Scholar]
  53. He X, Fan H-Y, Narlikar GJ, Kingston RE. 53.  2006. Human ACF1 alters the remodeling strategy of SNF2h. J. Biol. Chem. 281:3928636–47 [Google Scholar]
  54. Hong J, Feng H, Wang F, Ranjan A, Chen J. 54.  et al. 2014. The catalytic subunit of the SWR1 remodeler is a histone chaperone for the H2A.Z-H2B dimer. Mol. Cell 53:3498–505 [Google Scholar]
  55. Hopfner K-P, Gerhold C-B, Lakomek K, Wollmann P. 55.  2012. Swi2/Snf2 remodelers: hybrid views on hybrid molecular machines. Curr. Opin. Struct. Biol. 22:2225–33 [Google Scholar]
  56. Horn PJ, Carruthers LM, Logie C, Hill DA, Solomon MJ. 56.  et al. 2002. Phosphorylation of linker histones regulates ATP-dependent chromatin remodeling enzymes. Nat. Struct. Mol. Biol. 9:4263–67 [Google Scholar]
  57. Huang H-R, Rowe CE, Mohr S, Jiang Y, Lambowitz AM, Perlman PS. 57.  2005. The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. PNAS 102:1163–68 [Google Scholar]
  58. Hwang WL, Deindl S, Harada BT, Zhuang X. 58.  2014. Histone H4 tail mediates allosteric regulation of nucleosome remodelling by linker DNA. Nature 512:7513213–17 [Google Scholar]
  59. Imbalzano AN, Schnitzler GR, Kingston RE. 59.  1996. Nucleosome disruption by human SWI/SNF is maintained in the absence of continued ATP hydrolysis. J. Biol. Chem. 271:3420726–33 [Google Scholar]
  60. Ito T, Bulger M, Pazin MJ, Kobayashi R, Kadonaga JT. 60.  1997. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90:1145–55 [Google Scholar]
  61. Jarmoskaite I, Russell R. 61.  2014. RNA helicase proteins as chaperones and remodelers. Annu. Rev. Biochem. 83:697–725 [Google Scholar]
  62. Kadam S, Emerson BM. 62.  2003. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol. Cell 11:2377–89 [Google Scholar]
  63. Kadoch C, Crabtree GR. 63.  2015. Mammalian SWI/SNF chromatin remodeling complexes and cancer: mechanistic insights gained from human genomics. Sci. Adv. 1:5e1500447 [Google Scholar]
  64. Kagalwala MN, Glaus BJ, Dang W, Zofall M, Bartholomew B. 64.  2004. Topography of the ISW2-nucleosome complex: insights into nucleosome spacing and chromatin remodeling. EMBO J. 23:102092–104 [Google Scholar]
  65. Kassabov SR, Zhang B, Persinger J, Bartholomew B. 65.  2003. SWI/SNF unwraps, slides, and rewraps the nucleosome. Mol. Cell 11:2391–403 [Google Scholar]
  66. Klinker H, Mueller-Planitz F, Yang R, Forné I, Liu C-F. 66.  et al. 2014. ISWI remodelling of physiological chromatin fibres acetylated at lysine 16 of histone H4. PLOS ONE 9:2e88411 [Google Scholar]
  67. Kornberg RD.67.  1974. Chromatin structure: a repeating unit of histones and DNA. Science 184:4139868–71 [Google Scholar]
  68. Kornberg RD, Lorch Y. 68.  1992. Chromatin structure and transcription. Annu. Rev. Cell Biol. 8:563–87 [Google Scholar]
  69. Längst G, Becker PB. 69.  2001. ISWI induces nucleosome sliding on nicked DNA. Mol. Cell 8:51085–92 [Google Scholar]
  70. Längst G, Bonte EJ, Corona DF, Becker PB. 70.  1999. Nucleosome movement by CHRAC and ISWI without disruption or trans-displacement of the histone octamer. Cell 97:7843–52 [Google Scholar]
  71. Leonard JD, Narlikar GJ. 71.  2015. A nucleotide-driven switch regulates flanking DNA length sensing by a dimeric chromatin remodeler. Mol. Cell 57:5850–59 [Google Scholar]
  72. Li G, Levitus M, Bustamante C, Widom J. 72.  2005. Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 12:146–53 [Google Scholar]
  73. Li M, Hada A, Sen P, Olufemi L, Hall MA. 73.  et al. 2015. Dynamic regulation of transcription factors by nucleosome remodeling. eLife 4:e06249 [Google Scholar]
  74. Lia G, Praly E, Ferreira H, Stockdale C, Tse-Dinh YC. 74.  et al. 2006. Direct observation of DNA distortion by the RSC complex. Mol. Cell 21:3417–25 [Google Scholar]
  75. Lieleg C, Ketterer P, Nueble J, Ludwigsen J, Gerland U. 74.  et al. 2015. Nucleosome spacing generated by ISWI and CHD1 remodelers is constant regardless of nucleosome density. Mol. Cell. Biol. 35:91588–605 [Google Scholar]
  76. Liu N, Peterson CL, Hayes JJ. 75.  2011. SWI/SNF- and RSC-catalyzed nucleosome mobilization requires internal DNA loop translocation within nucleosomes. Mol. Cell. Biol. 31:204165–75 [Google Scholar]
  77. Lorch Y, Cairns BR, Zhang M, Kornberg RD. 76.  1998. Activated RSC-nucleosome complex and persistently altered form of the nucleosome. Cell 94:129–34 [Google Scholar]
  78. Lorch Y, Maier-Davis B, Kornberg RD. 77.  2006. Chromatin remodeling by nucleosome disassembly in vitro. PNAS 103:93090–93 [Google Scholar]
  79. Lorch Y, Maier-Davis B, Kornberg RD. 78.  2014. Role of DNA sequence in chromatin remodeling and the formation of nucleosome-free regions. Genes Dev. 28:222492–97 [Google Scholar]
  80. Lorch Y, Zhang M, Kornberg RD. 79.  1999. Histone octamer transfer by a chromatin-remodeling complex. Cell 96:3389–92 [Google Scholar]
  81. Lorch Y, Zhang M, Kornberg RD. 80.  2001. RSC unravels the nucleosome. Mol. Cell 7:189–95 [Google Scholar]
  82. Lowary PT, Widom J. 81.  1998. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276:119–42 [Google Scholar]
  83. Ludwigsen J, Klinker H, Mueller-Planitz F. 82.  2013. No need for a power stroke in ISWI-mediated nucleosome sliding. EMBO Rep. 14:121092–97 [Google Scholar]
  84. Luger K, Dechassa ML, Tremethick DJ. 83.  2012. New insights into nucleosome and chromatin structure: an ordered state or a disordered affair?. Nat. Rev. Mol. Cell Biol. 13:7436–47 [Google Scholar]
  85. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 84.  1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:6648251–60 [Google Scholar]
  86. Luger K, Rechsteiner TJ, Flaus AJ, Waye MM, Richmond TJ. 85.  1997. Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 272:3301–11 [Google Scholar]
  87. Luk E, Ranjan A, FitzGerald PC, Mizuguchi G, Huang Y. 86.  et al. 2010. Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome. Cell 143:5725–36 [Google Scholar]
  88. Mallam AL, Del Campo M, Gilman B, Sidote DJ, Lambowitz AM. 87.  2012. Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature 490:7418121–25 [Google Scholar]
  89. McKnight JN, Jenkins KR, Nodelman IM, Escobar T, Bowman GD. 88.  2011. Extranucleosomal DNA binding directs nucleosome sliding by Chd1. Mol. Cell. Biol. 31:234746–59 [Google Scholar]
  90. Mizuguchi G, Shen X, Landry J, Wu W-H, Sen S, Wu C. 89.  2004. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:5656343–48 [Google Scholar]
  91. Morrison AJ, Shen X. 90.  2009. Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat. Rev. Mol. Cell Biol. 10:6373–84 [Google Scholar]
  92. Moyle-Heyrman G, Viswanathan R, Widom J, Auble DT. 91.  2012. Two-step mechanism for modifier of transcription 1 (Mot1) enzyme-catalyzed displacement of TATA-binding protein (TBP) from DNA. J. Biol. Chem. 287:129002–12 [Google Scholar]
  93. Narlikar GJ, Phelan ML, Kingston RE. 92.  2001. Generation and interconversion of multiple distinct nucleosomal states as a mechanism for catalyzing chromatin fluidity. Mol. Cell 8:61219–30 [Google Scholar]
  94. Narlikar GJ, Sundaramoorthy R, Owen-Hughes T. 93.  2013. Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154:3490–503 [Google Scholar]
  95. Nguyen VQ, Ranjan A, Stengel F, Wei D, Aebersold R. 94.  et al. 2013. Molecular architecture of the ATP-dependent chromatin-remodeling complex SWR1. Cell 154:61220–31 [Google Scholar]
  96. Nodelman IM, Bowman GD. 95.  2013. Nucleosome sliding by Chd1 does not require rigid coupling between DNA-binding and ATPase domains. EMBO Rep. 14:121098–103 [Google Scholar]
  97. Owen-Hughes T, Whitehouse I, Flaus A, Cairns BR, White MF, Workman JL. 96.  1999. Nucleosome mobilization catalysed by the yeast SWI/SNF complex. Nature 400:6746784–87 [Google Scholar]
  98. Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL. 97.  2011. Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144:2200–13 [Google Scholar]
  99. Partensky PD, Narlikar GJ. 98.  2009. Chromatin remodelers act globally, sequence positions nucleosomes locally. J. Mol. Biol. 391:112–25 [Google Scholar]
  100. Patel A, Chakravarthy S, Morrone S, Nodelman IM, McKnight JN, Bowman GD. 99.  2013. Decoupling nucleosome recognition from DNA binding dramatically alters the properties of the Chd1 chromatin remodeler. Nucleic Acids Res. 41:31637–48 [Google Scholar]
  101. Perez-Howard GM, Weil PA, Beechem JM. 100.  1995. Yeast TATA binding protein interaction with DNA: fluorescence determination of oligomeric state, equilibrium binding, on-rate, and dissociation kinetics. Biochemistry 34:258005–17 [Google Scholar]
  102. Phelan ML, Schnitzler GR, Kingston RE. 101.  2000. Octamer transfer and creation of stably remodeled nucleosomes by human SWI-SNF and its isolated ATPases. Mol. Cell. Biol. 20:176380–89 [Google Scholar]
  103. Phelan ML, Sif S, Narlikar GJ, Kingston RE. 102.  1999. Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol. Cell 3:2247–53 [Google Scholar]
  104. Polach KJ, Widom J. 103.  1995. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254:2130–49 [Google Scholar]
  105. Racki LR, Naber N, Pate E, Leonard JD, Cooke R, Narlikar GJ. 104.  2014. The histone H4 tail regulates the conformation of the ATP-binding pocket in the SNF2h chromatin remodeling enzyme. J. Mol. Biol. 426:102034–44 [Google Scholar]
  106. Racki LR, Yang JG, Naber N, Partensky PD, Acevedo A. 105.  et al. 2009. The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 462:72761016–21 [Google Scholar]
  107. Ranjan A, Mizuguchi G, FitzGerald PC, Wei D, Wang F. 106.  et al. 2013. Nucleosome-free region dominates histone acetylation in targeting SWR1 to promoters for H2A. Z replacement Cell 154:61232–45 [Google Scholar]
  108. Ranjan A, Wang F, Mizuguchi G, Wei D, Huang Y, Wu C. 107.  2015. H2A histone-fold and DNA elements in nucleosome activate SWR1-mediated H2A.Z replacement in budding yeast. eLife 4:e06845 [Google Scholar]
  109. Rowe CE, Narlikar GJ. 108.  2010. The ATP-dependent remodeler RSC transfers histone dimers and octamers through the rapid formation of an unstable encounter intermediate. Biochemistry 49:459882–90 [Google Scholar]
  110. Saha A, Wittmeyer J, Cairns BR. 109.  2002. Chromatin remodeling by RSC involves ATP-dependent DNA translocation. Genes Dev. 16:162120–34 [Google Scholar]
  111. Saha A, Wittmeyer J, Cairns BR. 110.  2005. Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat. Struct. Mol. Biol. 12:9747–55 [Google Scholar]
  112. Saha A, Wittmeyer J, Cairns BR. 111.  2006. Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 7:6437–47 [Google Scholar]
  113. Saikrishnan K, Griffiths SP, Cook N, Court R, Wigley DB. 112.  2008. DNA binding to RecD: role of the 1B domain in SF1B helicase activity. EMBO J. 27:162222–29 [Google Scholar]
  114. Schnitzler G, Sif S, Kingston RE. 113.  1998. Human SWI/SNF interconverts a nucleosome between its base state and a stable remodeled state. Cell 94:117–27 [Google Scholar]
  115. Schwanbeck R, Xiao H, Wu C. 114.  2004. Spatial contacts and nucleosome step movements induced by the NURF chromatin remodeling complex. J. Biol. Chem. 279:3839933–41 [Google Scholar]
  116. Segal E, Widom J. 115.  2009. What controls nucleosome positions?. Trends Genet. 25:8335–43 [Google Scholar]
  117. Sen P, Vivas P, Dechassa ML, Mooney AM, Poirier MG, Bartholomew B. 116.  2013. The SnAC domain of SWI/SNF is a histone anchor required for remodeling. Mol. Cell. Biol. 33:2360–70 [Google Scholar]
  118. Shen X, Ranallo R, Choi E, Wu C. 117.  2003. Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 12:1147–55 [Google Scholar]
  119. Shrader TE, Crothers DM. 118.  1990. Effects of DNA sequence and histone-histone interactions on nucleosome placement. J. Mol. Biol. 216:169–84 [Google Scholar]
  120. Simon JA, Kingston RE. 119.  2013. Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol. Cell 49:5808–24 [Google Scholar]
  121. Singleton MR, Dillingham MS, Gaudier M, Kowalczykowski SC, Wigley DB. 120.  2004. Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432:7014187–93 [Google Scholar]
  122. Singleton MR, Dillingham MS, Wigley DB. 121.  2007. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76:23–50 [Google Scholar]
  123. Sirinakis G, Clapier CR, Gao Y, Viswanathan R, Cairns BR, Zhang Y. 122.  2011. The RSC chromatin remodelling ATPase translocates DNA with high force and small step size. EMBO J. 30:122364–72 [Google Scholar]
  124. Spain MM, Ansari SA, Pathak R, Palumbo MJ, Morse RH, Govind CK. 123.  2014. The RSC complex localizes to coding sequences to regulate Pol II and histone occupancy. Mol. Cell 56:5653–66 [Google Scholar]
  125. Stockdale C, Flaus A, Ferreira H, Owen-Hughes T. 124.  2006. Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J. Biol. Chem. 281:2416279–88 [Google Scholar]
  126. Story RM, Steitz TA. 125.  1992. Structure of the recA protein-ADP complex. Nature 355:6358374–76 [Google Scholar]
  127. Strohner R, Wachsmuth M, Dachauer K, Mazurkiewicz J, Hochstatter J. 126.  et al. 2005. A ‘loop recapture’ mechanism for ACF-dependent nucleosome remodeling. Nat. Struct. Mol. Biol. 12:8683–90 [Google Scholar]
  128. Subramanian V, Fields PA, Boyer LA. 127.  2015. H2A.Z: a molecular rheostat for transcriptional control. F1000Prime Rep. 7:1 [Google Scholar]
  129. Suto RK, Clarkson MJ, Tremethick DJ, Luger K. 128.  2000. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat. Struct. Mol. Biol. 7:121121–24 [Google Scholar]
  130. Swygert SG, Peterson CL. 129.  2014. Chromatin dynamics: interplay between remodeling enzymes and histone modifications. Biochim. Biophys. Acta 1839:8728–36 [Google Scholar]
  131. Torigoe SE, Urwin DL, Ishii H, Smith DE, Kadonaga JT. 130.  2011. Identification of a rapidly formed nonnucleosomal histone-DNA intermediate that is converted into chromatin by ACF. Mol. Cell 43:4638–48 [Google Scholar]
  132. Tosi A, Haas C, Herzog F, Gilmozzi A, Berninghausen O. 131.  et al. 2013. Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex. Cell 154:61207–19 [Google Scholar]
  133. Tsukiyama T, Wu C. 132.  1995. Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 83:61011–20 [Google Scholar]
  134. Tsukuda T, Fleming AB, Nickoloff JA, Osley MA. 133.  2005. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438:379–83 [Google Scholar]
  135. Udugama M, Sabri A, Bartholomew B. 134.  2011. The INO80 ATP-dependent chromatin remodeling complex is a nucleosome spacing factor. Mol. Cell. Biol. 31:4662–73 [Google Scholar]
  136. Wallrath LL, Elgin SC. 135.  1995. Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev. 9:101263–77 [Google Scholar]
  137. Wang AY, Schulze JM, Skordalakes E, Gin JW, Berger JM. 136.  et al. 2009. Asf1-like structure of the conserved Yaf9 YEATS domain and role in H2A.Z deposition and acetylation. PNAS 106:5121573–78 [Google Scholar]
  138. Watanabe S, Radman-Livaja M, Rando OJ, Peterson CL. 137.  2013. A histone acetylation switch regulates H2A.Z deposition by the SWR-C remodeling enzyme. Science 340:6129195–99 [Google Scholar]
  139. Whitehouse I, Stockdale C, Flaus A, Szczelkun MD, Owen-Hughes T. 138.  2003. Evidence for DNA translocation by the ISWI chromatin-remodeling enzyme. Mol. Cell. Biol. 23:61935–45 [Google Scholar]
  140. Widom J.139.  2001. Role of DNA sequence in nucleosome stability and dynamics. Q. Rev. Biophys. 34:3269–324 [Google Scholar]
  141. Wigley DB.140.  2013. Bacterial DNA repair: recent insights into the mechanism of RecBCD, AddAB and AdnAB. Nat. Rev. Microbiol. 11:19–13 [Google Scholar]
  142. Wollmann P, Cui S, Viswanathan R, Berninghausen O, Wells MN. 141.  et al. 2011. Structure and mechanism of the Swi2/Snf2 remodeller Mot1 in complex with its substrate TBP. Nature 475:7356403–7 [Google Scholar]
  143. Wu W-H, Alami S, Luk E, Wu C-H, Sen S. 142.  et al. 2005. Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat. Struct. Mol. Biol. 12:121064–71 [Google Scholar]
  144. Wu W-H, Wu C-H, Ladurner A, Mizuguchi G, Wei D. 143.  et al. 2009. N terminus of Swr1 binds to histone H2AZ and provides a platform for subunit assembly in the chromatin remodeling complex. J. Biol. Chem. 284:106200–7 [Google Scholar]
  145. Yang JG, Madrid TS, Sevastopoulos E, Narlikar GJ. 144.  2006. The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat. Struct. Mol. Biol. 13:121078–83 [Google Scholar]
  146. Yang X, Zaurin R, Beato M, Peterson CL. 145.  2007. Swi3p controls SWI/SNF assembly and ATP-dependent H2A-H2B displacement. Nat. Struct. Mol. Biol. 14:6540–47 [Google Scholar]
  147. Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF. 146.  2012. Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149:71461–73 [Google Scholar]
  148. Yu M, Souaya J, Julin DA. 147.  1998. The 30-kDa C-terminal domain of the RecB protein is critical for the nuclease activity, but not the helicase activity, of the RecBCD enzyme from Escherichia coli. PNAS 95:3981–86 [Google Scholar]
  149. Zentner GE, Henikoff S. 148.  2013. Mot1 redistributes TBP from TATA-containing to TATA-less promoters. Mol. Cell. Biol. 33:244996–5004 [Google Scholar]
  150. Zhang Y, Smith CL, Saha A, Grill SW, Mihardja S. 149.  et al. 2006. DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. Mol. Cell 24:4559–68 [Google Scholar]
  151. Zhang Z, Wippo CJ, Wal M, Ward E, Korber P, Pugh BF. 150.  2011. A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332:6032977–80 [Google Scholar]
  152. Zhou J, Fan JY, Rangasamy D, Tremethick DJ. 151.  2007. The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat. Struct. Mol. Biol. 14:111070–76 [Google Scholar]
  153. Zofall M, Persinger J, Kassabov SR, Bartholomew B. 152.  2006. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat. Struct. Mol. Biol. 13:4339–46 [Google Scholar]

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