ISWI remodelling of physiological chromatin fibres acetylated at lysine 16 of histone H4

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Klinker, Henrike ^a,b   Mueller Planitz, Felix ^a   Yang, Renliang ^c   Forné, Ignasi ^a,b   Liu, Chuan Fa ^c   Nordenskiöld, Lars ^c   Becker, Peter B ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b Munich Center for Integrated Protein Science   (Germany)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HISTONE H4; LYSINE; PROTEIN ISWI; UNCLASSIFIED DRUG; CHROMATIN; HISTONE; ISWI PROTEIN; MULTIPROTEIN COMPLEX; NUCLEOSOME; TRANSCRIPTION FACTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; ENZYME SUBSTRATE; HISTONE ACETYLATION; IN VITRO STUDY; NONHUMAN; NUCLEOSOME; PROTEIN INTERACTION; ACETYLATION; ANIMAL; CHROMATIN; DROSOPHILA MELANOGASTER; METABOLISM;

ACETYLATION; ADENOSINE TRIPHOSPHATASES; ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DROSOPHILA MELANOGASTER; HISTONES; LYSINE; MULTIPROTEIN COMPLEXES; NUCLEOSOMES; TRANSCRIPTION FACTORS;

EID: 84895514809     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088411     Document Type: Article

References (79)

1. Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304.
2. Flaus A, Martin DM, Barton GJ, Owen-Hughes T (2006) Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res 34: 2887-2905. (Pubitemid 44540417)
3. Becker PB, Workman JL (2013) Nucleosome remodeling and epigenetics. Cold Spring Harb Perspect Biol 5.
4. Yadon AN, Tsukiyama T (2011) SnapShot: Chromatin remodeling: ISWI. Cell 144: 453-453 e451.
5. Mueller-Planitz F, Klinker H, Becker PB (2013) Nucleosome sliding mechanisms: new twists in a looped history. Nat Struct Mol Biol 20: 1026-1032.
6. Narlikar GJ, Sundaramoorthy R, Owen-Hughes T (2013) Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154: 490-503.
7. Corona DF, Langst G, Clapier CR, Bonte EJ, Ferrari S, et al. (1999) ISWI is an ATP-dependent nucleosome remodeling factor. Mol Cell 3: 239-245. (Pubitemid 29292624)
8. Gelbart ME, Rechsteiner T, Richmond TJ, Tsukiyama T (2001) Interactions of Isw2 chromatin remodeling complex with nucleosomal arrays: analyses using recombinant yeast histones and immobilized templates. Mol Cell Biol 21: 2098-2106. (Pubitemid 32479631)
9. He X, Fan HY, Narlikar GJ, Kingston RE (2006) Human ACF1 alters the remodeling strategy of SNF2h. J Biol Chem 281: 28636-28647. (Pubitemid 44507006)
10. Ito T, Bulger M, Pazin MJ, Kobayashi R, Kadonaga JT (1997) ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90: 145-155. (Pubitemid 28009426)
11. Torigoe SE, Urwin DL, Ishii H, Smith DE, Kadonaga JT (2011) Identification of a rapidly formed nonnucleosomal histone-DNA intermediate that is converted into chromatin by ACF. Mol Cell 43: 638-648.
12. Varga-Weisz PD, Wilm M, Bonte E, Dumas K, Mann M, et al. (1997) Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388: 598-602. (Pubitemid 27340011)
13. Corona DF, Tamkun JW (2004) Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim Biophys Acta 1677: 113-119. (Pubitemid 38327095)
14. Erdel F, Rippe K (2011) Chromatin remodelling in mammalian cells by ISWI-type complexes-where, when and why? FEBS J 278: 3608-3618.
15. Zofall M, Persinger J, Kassabov SR, Bartholomew B (2006) Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat Struct Mol Biol 13: 339-346. (Pubitemid 43873505)
16. Dang W, Kagalwala MN, Bartholomew B (2006) Regulation of ISW2 by concerted action of histone H4 tail and extranucleosomal DNA. Mol Cell Biol 26: 7388-7396. (Pubitemid 44547691)
17. Schwanbeck R, Xiao H, Wu C (2004) Spatial contacts and nucleosome step movements induced by the NURF chromatin remodeling complex. J Biol Chem 279: 39933-39941. (Pubitemid 39258266)
18. Racki LR, Yang JG, Naber N, Partensky PD, Acevedo A, et al. (2009) The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 462: 1016-1021.
19. 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. (Pubitemid 27406632)
20. 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: 875-883. (Pubitemid 32104735)
21. 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: 14316-14321. (Pubitemid 33121389)
22. Eberharter A, Ferrari S, Langst G, Straub T, Imhof A, et al. (2001) Acf1, the largest subunit of CHRAC, regulates ISWI-induced nucleosome remodelling. EMBO J 20: 3781-3788. (Pubitemid 32691789)
23. Clapier CR, Nightingale KP, Becker PB (2002) A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res 30: 649-655. (Pubitemid 34679629)
24. Fazzio TG, Gelbart ME, Tsukiyama T (2005) Two distinct mechanisms of chromatin interaction by the Isw2 chromatin remodeling complex in vivo. Mol Cell Biol 25: 9165-9174. (Pubitemid 41507820)
25. Pepenella S, Murphy KJ, Hayes JJ (2013) Intra- and inter-nucleosome interactions of the core histone tail domains in higher-order chromatin structure. Chromosoma.
26. Gordon F, Luger K, Hansen JC (2005) The core histone N-terminal tail domains function independently and additively during salt-dependent oligomerization of nucleosomal arrays. J Biol Chem 280: 33701-33706. (Pubitemid 41443087)
27. Dorigo B, Schalch T, Bystricky K, Richmond TJ (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J Mol Biol 327: 85-96. (Pubitemid 36293304)
28. Kan PY, Caterino TL, Hayes JJ (2009) The H4 tail domain participates in intra-and internucleosome interactions with protein and DNA during folding and oligomerization of nucleosome arrays. Mol Cell Biol 29: 538-546.
29. Wang X, Hayes JJ (2008) Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol Cell Biol 28: 227-236.
30. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, et al. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311: 844-847. (Pubitemid 43228847)
31. Robinson PJ, An W, Routh A, Martino F, Chapman L, et al. (2008) 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J Mol Biol 381: 816-825.
32. Allahverdi A, Yang R, Korolev N, Fan Y, Davey CA, et al. (2011) The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association. Nucleic Acids Res 39: 1680-1691.
33. McBryant SJ, Lu X, Hansen JC (2010) Multifunctionality of the linker histones: an emerging role for protein-protein interactions. Cell Res 20: 519-528.
34. Bell O, Schwaiger M, Oakeley EJ, Lienert F, Beisel C, et al. (2010) Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nat Struct Mol Biol 17: 894-900.
35. Shia WJ, Pattenden SG, Workman JL (2006) Histone H4 lysine 16 acetylation breaks the genome's silence. Genome Biol 7: 217.
36. Conrad T, Akhtar A (2011) Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nat Rev Genet 13: 123-134.
37. Ferreira H, Flaus A, Owen-Hughes T (2007) Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J Mol Biol 374: 563-579. (Pubitemid 350018763)
38. Corona DF, Clapier CR, Becker PB, Tamkun JW (2002) Modulation of ISWI function by site-specific histone acetylation. EMBO Rep 3: 242-247. (Pubitemid 34269517)
39. Nightingale KP, Baumann M, Eberharter A, Mamais A, Becker PB, et al. (2007) Acetylation increases access of remodelling complexes to their nucleosome targets to enhance initiation of V(D)J recombination. Nucleic Acids Res 35: 6311-6321. (Pubitemid 350018591)
40. Deuring R, Fanti L, Armstrong JA, Sarte M, Papoulas O, et al. (2000) The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol Cell 5: 355-365. (Pubitemid 30628092)
41. Corona DF, Siriaco G, Armstrong JA, Snarskaya N, McClymont SA, et al. (2007) ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol 5: e232.
42. Lusser A, Urwin DL, Kadonaga JT (2005) Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat Struct Mol Biol 12: 160-166.
43. Maier VK, Chioda M, Rhodes D, Becker PB (2008) ACF catalyses chromatosome movements in chromatin fibres. EMBO J 27: 817-826. (Pubitemid 351417165)
44. Huynh VA, Robinson PJ, Rhodes D (2005) A method for the in vitro reconstitution of a defined "30 nm" chromatin fibre containing stoichiometric amounts of the linker histone. J Mol Biol 345: 957-968. (Pubitemid 40092217)
45. Becker PB, Wu C (1992) Cell-free system for assembly of transcriptionally repressed chromatin from Drosophila embryos. Mol Cell Biol 12: 2241-2249.
46. Oppikofer M, Kueng S, Martino F, Soeroes S, Hancock SM, et al. (2011) A dual role of H4K16 acetylation in the establishment of yeast silent chromatin. EMBO J 30: 2610-2621.
47. Routh A, Sandin S, Rhodes D (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc Natl Acad Sci U S A 105: 8872-8877.
48. Ner SS, Travers AA (1994) HMG-D, the Drosophila melanogaster homologue of HMG 1 protein, is associated with early embryonic chromatin in the absence of histone H1. EMBO J 13: 1817-1822. (Pubitemid 24124514)
49. Lu X, Simon MD, Chodaparambil JV, Hansen JC, Shokat KM, et al. (2008) The effect of H3K79 dimethylation and H4K20 trimethylation on nucleosome and chromatin structure. Nat Struct Mol Biol 15: 1122-1124.
50. Simon MD, Chu F, Racki LR, de la Cruz CC, Burlingame AL, et al. (2007) The site-specific installation of methyl-lysine analogs into recombinant histones. Cell 128: 1003-1012. (Pubitemid 46341408)
51. 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. (Pubitemid 28085408)
52. 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: 82-89.
53. Schwarz PM, Hansen JC (1994) Formation and stability of higher order chromatin structures. Contributions of the histone octamer. J Biol Chem 269: 16284-16289.
54. Clapier CR, Cairns BR (2012) Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes. Nature 492: 280-284.
55. Ludwigsen J, Klinker H, Mueller-Planitz F (2013) No need for a power stroke in ISWI-mediated nucleosome sliding. EMBO Rep.
56. van Holde KE (1989) Chromatin. New York: Springer.
57. Georgel PT, Tsukiyama T, Wu C (1997) Role of histone tails in nucleosome remodeling by Drosophila NURF. EMBO J 16: 4717-4726. (Pubitemid 27326609)
58. Bednar J, Horowitz RA, Grigoryev SA, Carruthers LM, Hansen JC, et al. (1998) Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. Proc Natl Acad Sci U S A 95: 14173-14178. (Pubitemid 28549340)
59. Pennings S, Meersseman G, Bradbury EM (1994) Linker histones H1 and H5 prevent the mobility of positioned nucleosomes. Proc Natl Acad Sci U S A 91: 10275-10279. (Pubitemid 24328979)
60. Ura K, Hayes JJ, Wolffe AP (1995) A positive role for nucleosome mobility in the transcriptional activity of chromatin templates: restriction by linker histones. EMBO J 14: 3752-3765.
61. 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: 1078-1083. (Pubitemid 44885917)
62. 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: 10047-10057. (Pubitemid 39458828)
63. 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: 2092-2104. (Pubitemid 38737736)
64. Yamada K, Frouws TD, Angst B, Fitzgerald DJ, DeLuca C, et al. (2011) Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472: 448-453.
65. 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: 16279-16288.
66. Nelson PP, Albright SC, Wiseman JM, Garrard WT (1979) Reassociation of histone H1 with nucleosomes. J Biol Chem 254: 11751-11760.
67. Nightingale KP, Pruss D, Wolffe AP (1996) A single high affinity binding site for histone H1 in a nucleosome containing the Xenopus borealis 5 S ribosomal RNA gene. J Biol Chem 271: 7090-7094. (Pubitemid 26104146)
68. Rodriguez-Campos A, Shimamura A, Worcel A (1989) Assembly and properties of chromatin containing histone H1. J Mol Biol 209: 135-150.
69. Rando OJ (2012) Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr Opin Genet Dev 22: 148-155.
70. Ruthenburg AJ, Li H, Patel DJ, Allis CD (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8: 983-994. (Pubitemid 350174643)
71. Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT (2004) Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev 18: 170-183. (Pubitemid 38141785)
72. Forne I, Ludwigsen J, Imhof A, Becker PB, Mueller-Planitz F (2012) Probing the conformation of the ISWI ATPase domain with genetically encoded photoreactive crosslinkers and mass spectrometry. Mol Cell Proteomics 11: M111 012088.
73. Hamiche A, Sandaltzopoulos R, Gdula DA, Wu C (1999) ATP-dependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell 97: 833-842. (Pubitemid 29375043)
74. Ito T, Levenstein ME, Fyodorov DV, Kutach AK, Kobayashi R, et al. (1999) ACF consists of two subunits, Acf1 and ISWI, that function cooperatively in the ATP-dependent catalysis of chromatin assembly. Genes Dev 13: 1529-1539. (Pubitemid 29297921)
75. Villar-Garea A, Israel L, Imhof A (2008) Analysis of histone modifications by mass spectrometry. Curr Protoc Protein Sci Chapter 14: Unit 14 10.
76. Luger K, Rechsteiner TJ, Flaus AJ, Waye MM, Richmond TJ (1997) Characterization of nucleosome core particles containing histone proteins made in bacteria. J Mol Biol 272: 301-311. (Pubitemid 27410045)
77. Croston GE, Kerrigan LA, Lira LM, Marshak DR, Kadonaga JT (1991) Sequence-specific antirepression of histone H1-mediated inhibition of basal RNA polymerase II transcription. Science 251: 643-649. (Pubitemid 21916885)
78. Routh A, Rhodes D (2009) In vitro reconstitution of nucleosome arrays with a stoichiometric content of histone octamer and linker histone (PROT42).
79. Tal M, Silberstein A, Nusser E (1985) Why does Coomassie Brilliant Blue R interact differently with different proteins? A partial answer. J Biol Chem 260: 9976-9980. (Pubitemid 16244080)