Remodelers organize cellular chromatin by counteracting intrinsic histone-DNA sequence preferences in a class-specific manner

Molecular and Cellular Biology

Volumn 32, Issue 3, 2012, Pages 675-688

  Moshkin, Yuri M ^a   Chalkley, Gillian E ^a   Kan, Tsung Wai ^a   Reddy, B Ashok ^a   Ozgur, Zeliha ^a   van Ijcken, Wilfred F J ^a   Dekkers, Dick H W ^a   Demmers, Jeroen A ^a   Travers, Andrew A ^b   Verrijzer, C Peter ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BAP PROTEIN; DNA FRAGMENT; DOUBLE STRANDED RNA; PBAP PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA HISTONE INTERACTION; DNA SEQUENCE; DROSOPHILA; GENETIC ASSOCIATION; MICROARRAY ANALYSIS; NUCLEIC ACID IMMOBILIZATION; NUCLEOSOME; PRIORITY JOURNAL; RNA ISOLATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BINDING SITES; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENOME; HISTONES; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; NUCLEOSOMES; TRANSCRIPTION FACTORS;

EUKARYOTA;

EID: 84856806926     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06365-11     Document Type: Article

References (65)

1. Badis G, et al. 2008. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell 32:878-887.
2. Caserta M, et al. 2009. A translational signature for nucleosome positioning in vivo. Nucleic Acids Res. 37:5309 -5321.
3. Chaban Y, et al. 2008. Structure of a RSC-nucleosome complex and insights into chromatin remodeling. Nat. Struct. Mol. Biol. 15:1272-1277.
4. Chalkley GE, et al. 2008. The transcriptional coactivator SAYP is a trithorax group signature subunit of the PBAP chromatin remodeling complex. Molecular Cell. Biol. 28:2920 -2929.
5. Chalkley GE, Verrijzer CP. 2004. Immuno-depletion and purification strategies to study chromatin-remodeling factors in vitro. Methods Enzymol. 377:421- 442.
6. Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78:273-304.
7. Deal RB, Henikoff JG, Henikoff S. 2010. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328:1161-1164.
8. Dechassa ML, et al. 2010. SWI/SNF has intrinsic nucleosome disassembly activity that is dependent on adjacent nucleosomes. Mol. Cell 38: 590-602.
9. Drew HR, Travers AA. 1985. DNA bending and its relation to nucleosome positioning. J. Mol. Biol. 186:773-790.
10. Engeholm M, et al. 2009. Nucleosomes can invade DNA territories occupied by their neighbors. Nat. Struct. Mol. Biol. 16:151-158.
11. Floer M, et al. 2010. A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell 141:407- 418.
12. Fuda NJ, Ardehali MB, Lis JT. 2009. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461:186 -192.
13. 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.
14. Ghaemmaghami S, et al. 2003. Global analysis of protein expression in yeast. Nature 425:737-741.
15. Giresi PG, Kim J, McDaniell RM, Iyer VR, Lieb JD. 2007. FAIRE (formaldehyde-assisted isolation of regulatory elements) isolates active regulatory elements from human chromatin. Genome Res. 17: 877- 885.
16. Gkikopoulos T, et al. 2011. A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333:1758- 1760.
17. Goh WS, Orlov Y, Li J, Clarke ND. 2010. Blurring of high-resolution data shows that the effect of intrinsic nucleosome occupancy on transcription factor binding is mostly regional, not local. PLoS Comp. Biol. 6:e1000649.
18. Goodsell DS, Dickerson RE. 1994. Bending and curvature calculations in B-DNA. Nucleic Acids Res. 22:5497-5503.
19. Gracey LE, et al. 2010. An in vitro-identified high-affinity nucleosomepositioning signal is capable of transiently positioning a nucleosome in vivo. Epigenet. Chromatin 3:13.
20. Hargreaves DC, Crabtree GR. 2011. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21:396-420.
21. Hartley PD, Madhani HD. 2009. Mechanisms that specify promoter nucleosome location and identity. Cell 137:445- 458.
22. Henikoff S. 2008. Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. 9:15-26.
23. Ho L, Crabtree GR. 2010. Chromatin remodelling during development. Nature 463:474-484.
24. Horz W, Altenburger W. 1981. Sequence specific cleavage of DNA by micrococcal nuclease. Nucleic Acids Res. 9:2643-2658.
25. Jiang C, Pugh BF. 2009. Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. 10:161-172.
26. Kaeser MD, Aslanian A, Dong MQ, Yates JR, 3rd, Emerson BM. 2008. BRD7, a novel PBAF-specific SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells. J. Biol. Chem. 283: 32254-32263.
27. Kal AJ, Mahmoudi T, Zak NB, Verrijzer CP. 2000. The Drosophila brahma complex is an essential coactivator for the trithorax group protein zeste. Genes Dev. 14:1058 -1071.
28. Kaplan N, et al. 2009. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458:362-366.
29. Kornberg RD. 1977. Structure of chromatin. Annu. Rev. Biochem. 46: 931-954.
30. Kornberg RD, Stryer L. 1988. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res. 16: 6677-6690.
31. Kristjuhan A, Svejstrup JQ. 2004. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 23:4243- 4252.
32. Kunert N, Brehm A. 2009. Novel Mi-2 related ATP-dependent chromatin remodelers. Epigenetics 4:209 -211.
33. Lange M, et al. 2008. Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex. Genes Dev. 22:2370 -2384.
34. Locke G, Tolkunov D, Moqtaderi Z, Struhl K, Morozov AV. 2010. High-throughput sequencing reveals a simple model of nucleosome energetics. Proc. Natl. Acad. Sci. U. S. A. 107:20998 -21003.
35. Lorch Y, Maier-Davis B, Kornberg RD. 2010. Mechanism of chromatin remodeling. Proc. Natl. Acad. Sci. U. S. A. 107:3458 -3462.
36. 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.
37. Mohd-Sarip A, et al. 2006. Architecture of a polycomb nucleoprotein complex. Mol. Cell 24:91-100.
38. Mohrmann L, et al. 2004. Differential targeting of two distinct SWI/SNFrelated Drosophila chromatin-remodeling complexes. Mol. Cell. Biol. 24: 3077-3088.
39. Moshkin YM, Mohrmann L, van Ijcken WF, Verrijzer CP. 2007. Functional differentiation of SWI/SNF remodelers in transcription and cell cycle control. Mol. Cell. Biol. 27:651- 661.
40. Ng HH, Robert F, Young RA, Struhl K. 2002. Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev. 16:806-819.
41. Parnell TJ, Huff JT, Cairns BR. 2008. RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes. EMBO J. 27:100 -110.
42. Pham CD, He X, Schnitzler GR. 2010. Divergent human remodeling complexes remove nucleosomes from strong positioning sequences. Nucleic Acids Res. 38:400-413.
43. Protozanova E, Yakovchuk P, Frank-Kamenetskii MD. 2004. Stacked-unstacked equilibrium at the nick site of DNA. J. Mol. Biol. 342:775-785.
44. Quinn J, Fyrberg AM, Ganster RW, Schmidt MC, Peterson CL. 1996. DNA-binding properties of the yeast SWI/SNF complex. Nature 379: 844-847.
45. Rando OJ, Chang HY. 2009. Genome-wide views of chromatin structure. Annu. Rev. Biochem. 78:245-271.
46. Reddy BA, et al. 2010. Drosophila transcription factor Tramtrack69 binds MEP1 to recruit the chromatin remodeler NuRD. Mol. Cell. Biol. 30: 5234-5244.
47. Rippe K, et al. 2007. DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes. Proc. Natl. Acad. Sci. U. S. A. 104:15635-15640.
48. Sala A, et al. 2011. Genome-wide characterization of chromatin binding and nucleosome spacing activity of the nucleosome remodelling ATPase ISWI. EMBO J. 30:1766 -1777.
49. Segal E, et al. 2006. A genomic code for nucleosome positioning. Nature 442:772-778.
50. Segal E, Widom J. 2009. What controls nucleosome positions? Trends Genet. 25:335-343.
51. Shukla MS, et al. 2010. Remosomes: RSC generated non-mobilized particles with approximately 180 bp DNA loosely associated with the histone octamer. Proc. Natl. Acad. Sci. U. S. A. 107:1936 -1941.
52. Simonis M, et al. 2006. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-onchip (4C). Nat. Genet. 38:1348 -1354.
53. Stein A, Takasuka TE, Collings CK. 2010. Are nucleosome positions in vivo primarily determined by histone-DNA sequence preferences? Nucleic Acids Res. 38:709 -719.
54. Travers A, Hiriart E, Churcher M, Caserta M, Di Mauro E. 2010. The DNA sequence-dependence of nucleosome positioning in vivo and in vitro. J. Biomol. Struct. Dynamics 27:713-724.
55. Valouev A, et al. 2008. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res. 18:1051-1063.
56. Weake VM, Workman JL. 2010. Inducible gene expression: diverse regulatory mechanisms. Nat. Rev. 11:426-437.
57. 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.
58. Whitehouse I, Tsukiyama T. 2006. Antagonistic forces that position nucleosomes in vivo. Nat. Struct. Mol. Biol. 13:633- 640.
59. Worby CA, Simonson-Leff N, Dixon JE. 2001. RNA interference of gene expression (RNAi) in cultured Drosophila cells. Sci. STKE 2001:PL1.
60. Wu C, Travers A. 2005. Relative affinities of DNA sequences for the histone octamer depend strongly upon both the temperature and octamer concentration. Biochemistry 44:14329 -14334.
61. Xi Y, Yao J, Chen R, Li W, He X. 2011. Nucleosome fragility reveals novel functional states of chromatin and poises genes for activation. Genome Res. 21:718 -724.
62. Yamada K, et al. 2011. Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472:448-453.
63. Zaret KS, et al. 2008. Pioneer factors, genetic competence, and inductive signaling: programming liver and pancreas progenitors from the endoderm. Cold Spring Harbor Symp. Quant. Biol. 73:119 -126.
64. Zhang Y, et al. 2009. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat. Struct. Mol. Biol. 16:847-852.
65. Zhang Z, et al. 2011. A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332:977-980.