Multiple aspects of ATP-dependent nucleosome translocation by RSC and Mi-2 are directed by the underlying DNA sequence

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  van Vugt, Joke J F A ^a,b   de Jager, Martijn ^b   Murawska, Magdalena ^c   Brehm, Alexander ^c   van Noort, John ^b   Logie, Colin ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; AUTOANTIGEN; DROSOPHILA PROTEIN; FUNGAL PROTEIN; MI 2 PROTEIN, DROSOPHILA; MI-2 PROTEIN, DROSOPHILA;

ARTICLE; BINDING AFFINITY; CELL INTERACTION; CELL KINETICS; CELL SPECIFICITY; CONTROLLED STUDY; DNA BINDING; DNA SEQUENCE; GENE TRANSLOCATION; HYDROLYSIS; MOLECULAR MODEL; NONHUMAN; NUCLEOSOME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PURIFICATION; STRUCTURE ANALYSIS; ANIMAL; ATOMIC FORCE MICROSCOPY; BASE PAIRING; BIOCATALYSIS; METABOLISM; MONTE CARLO METHOD; NUCLEOTIDE SEQUENCE; TRANSPORT AT THE CELLULAR LEVEL;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; AUTOANTIGENS; BASE PAIRING; BASE SEQUENCE; BIOCATALYSIS; BIOLOGICAL TRANSPORT; DROSOPHILA PROTEINS; FUNGAL PROTEINS; MICROSCOPY, ATOMIC FORCE; MONTE CARLO METHOD; NUCLEOSOMES;

EID: 67749086828     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006345     Document Type: Article

References (82)

1. Logie C, Tse C, Hansen JC, Peterson C (1999) The core histone N-terminal domains are required for multiple rounds of catalytic chromatin remodelling by the SWI/SNF and RSC complexes. Biochemistry 38: 2514-2522.
2. Eisen JA, Sweder KS, Hanawalt PC (1995) Nucleic Acids Res 23: 2715-2723.
3. Hassan AH, Prochasson P, Neely KE, Galasinski SC, Chandy M, et al. (2002) Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111: 369-379.
4. Singh M, Popowicz GM, Krajewski M, Holak TA (2007) Structural ramification for acetyl-lysine recognition by the bromodomain of human BRG1 protein, a central ATPase of the SWI/SNF remodelling complex. Chembiochem 8: 1308-1316.
5. Awad S, Hassan AH (2008) The Swi2/Snf2 bromodomain is important for the full binding and remodelling activity of the SWI/SNF complex on H3- and H4-acetylated nucleosomes. Ann N Y Acad Sci 1138: 366-375.
6. Peterson CL, Herskowitz I (1992) Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell 68: 573-583.
7. Carey M, Li B, Workman JL (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Molecular Cell 24: 481-487.
8. Mas G, de Nadal E, Dechant R, de la Concepcion ML, Logie C, et al. (2009) Recruitment of a chromatin remodelling complex by the Hog1 MAP kinase to stress genes. The EMBO Journal 28: 326-336.
9. Gao X, Tate P, Hu P, Tjian R, Skarnes WC, et al. (2008) ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodelling component BAF250a. Proc Natl Acad Sci U S A 105: 6656-6661.
10. Yan Z, Wang Z, Sharova L, Sharov AA, Ling C, et al. (2008) BAF250B-associated SWI/SNF chromatin-remodelling complex is required to maintain undifferentiated mouse embryonic stem cells. Stem Cells 26: 1155-1165.
11. Baetz KK, Krogan NJ, Emili A, Greenblatt J, Hieter P (2004) The ctf13-30/ CTF13 genomic haploinsufficiency modifier screen identifies the yeast chromatin remodelling complex RSC, which is required for the establishment of sister chromatid cohesion. Mol Cell Biol 24: 1232-1244.
12. Chai B, Huang J, Cairns BR, Laurent BC (2005) Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes and Development 19: 1656-1661.
13. Vries RG, Bezrookove V, Zuijderduijn LM, Kia SK, Houweling A, et al. (2005) Cancer-associated mutations in chromatin remodeler hSNF5 promote chromosomal instability by compromising the mitotic checkpoint. Genes and Development 19: 665-670.
14. Campsteijn C, Wijnands-Collin AM, Logie C (2007) Reverse genetic analysis of the yeast RSC chromatin remodeler reveals a role for RSC3 and SNF5 homolog 1 in ploidy maintenance. PLoS Genet 3: 947-957.
15. Bochar DA, Wang L, Beniya H, Kinev A, Xue Y, et al. (2000) BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodelling to breast cancer. Cell 102: 257-265.
16. Otsuki T, Furukawa Y, Ikeda K, Endo H, Yamashita T, et al. (2001) Fanconi anemia protein, FANCA, associates with BRG1, a component of the human SWI/SNF complex. Hum Mol Genet 10: 2651-2660.
17. Yu Y, Waters R (2005) Histone acetylation, chromatin remodelling and nucleotide excision repair: hint from the study on MFA2 in Saccharomyces cerevisiae. Cell Cycle 4: 1043-1045.
18. Shim EY, Hong SJ, Oum JH, Yanez Y, Zhang Y, et al. (2006) RSC Mobilizes Nucleosomes to Improve Accessibility of Repair Machinery to the Damaged Chromatin. Mol Cell Biol 27: 1602-1613.
19. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER 3rd, Hurov KE, et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316: 1160-1166.
20. Gong F, Fahy D, Liu H, Wang W, Smerdon MJ (2008) Role of the mammalian SWI/SNF chromatin remodelling complex in the cellular response to UV damage. Cell Cycle 7: 1067-1074.
21. Osley MA, Tsukuda T, Nickoloff JA (2007) ATP-dependent chromatin remodelling factors and DNA damage repair. Mutat Res 618: 65-80.
22. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, et al. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124.
23. Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, et al. (2005) Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438: 1181-1185.
24. Bouazoune K, Mitterweger A, Langst G, Imhof A, Akhtar A, et al. (2002) The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. The EMBO Journal 21: 2430-2440.
25. Marfella CG, Imbalzano AN (2007) The Chd family of chromatin remodelers. Mutat Res 618: 30-40.
26. Xue Y, Wong J, Moreno GT, Young MK, Cote J, et al. (1998) NURD, a novel complex with both ATP-dependent chromatin-remodelling and histone deacetylase activities. Molecular Cell 2: 851-861.
27. Brehm A, Nielsen SJ, Miska EA, McCance DJ, Reid JL, et al. (1999) The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth. The EMBO Journal 18: 2449-2458.
28. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, et al. (1999) Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes and Development 13: 1924-1935.
29. Stielow B, Sapetschnig A, Kruger I, Kunert N, Brehm A, et al. (2008) Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. Molecular Cell 29: 742-754.
30. Kunert N, Wagner E, Murawska M, Klinker H, Kremmer E, et al. (2009) dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression. The EMBO Journal 28: 533-544.
31. Van Vugt JJFA, Ranes M, Campsteijn C, Logie C (2007) The ins and outs of ATP-dependent chromatin remodelling in budding yeast: biophysical and proteomic perspectives. Biochim Biophys Acta Gene Structure and Expression 1769: 153-171.
32. Boyer LA, Logie C, Bonte E, Becker PB, Wade PA, et al. (2000) Functional delineation of three groups of the ATP-dependent family of chromatin remodelling enzymes. The Journal of Biological Chemistry 275: 18864-18870.
33. Kagalwala MN, Glaus BJ, Dang W, Zofall M, Bartholomew B (2004) Topography of the ISW2-nucleosome complex: insights into nucleosome spacing and chromatin remodelling. The EMBO Journal 23: 2092-2104.
34. Zofall M, Persinger J, Kassabov SR, Bartholomew B (2006) Chromatin remodelling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat Struct Mol Biol 13: 339-346.
35. Chaban Y, Ezeokonkwo C, Chung WH, Zhang F, Kornberg RD, et al. (2008) Structure of a RSC-nucleosome complex and insights into chromatin remodelling. Nat Struct Mol Biol 15: 1272-1277.
36. Dechassa ML, Zhang B, Horowitz-Scherer R, Persinger J, Woodcock CL, et al. (2008) Architecture of the SWI/SNF-nucleosome complex. Mol Cell Biol 28: 6010-6021.
37. Cairns BR (2007) Chromatin remodelling: insights and intrigue from single-molecule studies. Nat Struct Mol Biol 14: 989-996.
38. Flaus A, Owen-Hughes T (2003) Dynamic properties of nucleosomes during thermal and ATP-driven mobilization. Mol Cell Biol 23: 7767-7779.
39. Rippe K, Schrader A, Riede P, Strohner R, Lehmann E, et al. (2007) DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodelling complexes. Proc Natl Acad Sci U S A 104: 15635-15640.
40. Sims HI, Lane JM, Ulyanova NP, Schnitzler GR (2007) Human SWI/SNF drives sequence-directed repositioning of nucleosomes on C-myc promoter DNA minicircles. Biochemistry 46: 11377-11388.
41. Partensky PD, Narlikar GJ (2009) Chromatin remodelers act globally, sequence positions nucleosomes locally. J Mol Biol doi: 10.1016/ j.jmb.2009.04.085.
42. Brehm A, Langst G, Kehle J, Clapier CR, Imhof A, et al. (2000) dMi-2 and ISWI chromatin remodelling factors have distinct nucleosome binding and mobilization properties. The EMBO Journal 19: 4332-4341.
43. Jaskelioff M, Gavin IM, Peterson CL, Logie C (2000) SWI-SNF-mediated nucleosome remodelling: Role of the histone octamer mobility in the persistance of the remodelled state. Mol Cell Biol 20: 3058-3068.
44. Schwanbeck R, Xiao H, Wu C (2004) Spatial contacts and nucleosome step movement induced by the NURF chromatin remodelling complex. The Journal of Biological Chemistry 279: 39933-39941.
45. Lowary PT, Widom J (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276: 19-42.
46. Edsall JT (1953) Some comments on proteins and protein structure. Proc R Soc Lond B Biol Sci 141: 97-103.
47. Wyman C, Grotkopp E, Bustamante C, Nelson HC (1995) Determination of heat-shock transcription factor 2 stoichiometry at looped DNA complexes using scanning force microscopy. The EMBO Journal 14: 117-123.
48. Willemsen OH, Snel MM, van Noort SJ, van der Werf KO, de Grooth BG, et al. (1999) Optimization of adhesion mode atomic force microscopy resolves individual molecules in topography and adhesion. Ultramicroscopy 80: 133-144.
49. Sorel I, Piétrement O, Hamon L, Baconnais S, Cam EL, et al. (2006) The EcoRI-DNA complex as a model for investigating protein-DNA interactions by atomic force microscopy. Biochemistry 45: 14675-14682.
50. Bash R, Wang H, Anderson C, Yodh J, Hager G, et al. (2006) AFM imaging of protein movements: Histone H2A-H2B release during nucleosome remodelling. Federation of European Biochemical Societies Letters 580: 4757-61.
51. Engeholm M, De Jager M, Flaus A, Brenk R, Van Noort J, et al. (2009) Nucleosomes can invade DNA territories occupied by their neighbors. Nat Struct Mol Biol 16: 151-158.
52. Bruno M, Flaus A, Stockdale C, Rencurel C, Ferreira H, et al. (2003) Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodelling activities. Molecular Cell 12: 1599-1606.
53. Kassabov SR, Zhang B, Persinger J, Bartholomew B (2003) SWI/SNF unwraps, slides and rewraps the nucleosome. Molecular Cell 11: 391-403.
54. Lia G, Praly E, Ferreira H, Stockdale C, Ching Tse-Dinh Y, et al. (2006) Direct observation of DNA distortion by the RSC complex. Molecular Cell 21: 417-425.
55. Van Noort J, van der Heijden T, Dutta CF, Firman K, Dekker C (2004) Initiation of translocation by Type I restriction-modification enzymes is associated with a short DNA extrusion. Nucleic Acids Res 32: 6540-6547.
56. Cairns BR, Lorch Y, Li Y, Zhang M, Lacomis L, et al. (1996) RSC, an essential, abundant chromatin-remodelling complex. Cell 87: 1249-1260.
57. Quinn J, Fyrberg AM, Ganster RW, Schmidt MC, Peterson CL (1996) DNA-binding properties of the yeast SWI/SNF complex. Nature 379: 844-847.
58. Logie C, Peterson CL (1997) Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays. The EMBO Journal 16: 6772-6782.
59. Saha A, Wittmeyer J, Cairns BR (2005) Chromatin remodelling through directional DNA translocation from an internal nucleosomal site. Nat Struct Mol Biol 12: 747-755.
60. Sims HI, Baughman CB, Schnitzler GR (2008) Human SWI/SNF directs sequence-specific chromatin changes on promoter polynucleosomes. Nucleic Acids Res 36: 6118-6131.
61. Cairns BR, Schlichter A, Erdjument-Bromage H, Tempst P, Kornberg RD, et al. (1999) Two functionally distinct forms of the RSC nucleosome-remodelling complex, containing essential AT hook, BAH, and bromodomains. Molecular Cell 4: 715-723.
62. Van Attikum H, Gasser SM (2005) The histone code at DNA breaks: A guide to repair? Nature Reviews Molecular Cell Biology 6: 757-765.
63. Zhang Y, Smith CL, Saha A, Grill SW, Mihardja S, et al. (2006) DNA translocation and loop formation mechanism of chromatin remodelling by SWI/SNF and RSC. Mol Cell 24: 559-568.
64. Fischer CJ, Saha A, Cairns BR (2007) Kinetic model for the ATP-dependent translocation of Saccharomyces cerevisiae RSC along double-stranded DNA. Biochemistry 46: 12416-12426.
65. Ulyanova NP, Schnitzler GR (2005) Human SWI/SNF generates abundant, structurally altered dinucleosomes on polynucleosomal templates. Mol Cell Biol 25: 11156-11170.
66. Fernandez AG, Anderson JN (2007) Nucleosome positioning determinants. J Mol Biol 371: 649-668.
67. Bash R, Wang H, Yodh J, Hager G, Lindsay SM, et al. (2003) Nucleosomal arrays can be salt-reconstituted on a single-copy MMTV promoter DNA template: their properties differ in several ways from those of comparable 5S concatameric arrays. Biochemistry 42: 4681-4690.
68. Thastrom A, Lowary PT, Widom J (2004) Measurement of histone-DNA interaction free energy in nucleosomes. Methods 33: 33-44.
69. Simpson RT, Stafford DW (1983) Structural features of a phased nucleosome core particle. Proc Natl Acad Sci U S A 80: 51-55.
70. Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, et al. (2006) A genomic code for nucleosome positioning. Nature 442: 772-778.
71. Hall M, Shundrovsky A, Bai L, Fulbright RM, Lis JT, et al. (2009) High-resolution dynamic mapping of histone-DNA interactions in a nucleosome. Nat Struct Mol Biol 16: 124-129.
72. Shundrovsky A, Smith CL, Lis JT, Peterson CL, Wang MD (2006) Probing SWI/ SNF remodelling of the nucleosome by unzipping single DNA molecules. Nat Struct Mol Biol 13: 549-554.
73. Saha A, Wittmeyer J, Cairns BR (2002) Chromatin remodelling by RSC involves ATP-dependent DNA translocation. Genes and Development 16: 2120-2134.
74. Velankar SS, Soultanas P, Dillingham MS, Subramanya HS, Wigley DB (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97: 75-84.
75. Cote J, Quinn J, Workman JL, Peterson DL (1994) Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265: 53-60.
76. Yudkovsky N, Logie C, Hahn S, Peterson CL (1999) Recruitment of the SWI/ SNF chromatin remodelling complex by transcriptional activators. Genes and Development 13: 2369-2374.
77. Lorch Y, Maier-Davis B, Kornberg RD (2006) Chromatin remodelling by nucleosome disassembly in vitro. Proc Natl Acad Sci U S A 103: 3090-3093.
78. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737-741.
79. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691.
80. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, et al. (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24: 218-229.
81. Logie C, Peterson CL (1999) Purification and biochemical properties of yeast SWI/SNF complex. In: Wolffe AP, ed. Chromatin remodelling complexes Academic Press. pp 726-727.
82. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.