Chromatin Modification by PSC Occurs at One PSC per Nucleosome and Does Not Require the Acidic Patch of Histone H2A

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Lo, Stanley M ^a,b   McElroy, Kyle A ^a   Francis, Nicole J ^a  

^a HARVARD UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; DROSOPHILA PROTEIN PCG; HISTONE H2A; POSTERIOR SEX COMB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; ELECTRON MICROSCOPY; HETEROZYGOSITY; HISTONE MODIFICATION; NONHUMAN; NUCLEOSOME; OLIGOMERIZATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MODIFICATION; STOICHIOMETRY;

ANIMALS; BINDING SITES; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA; DNA-BINDING PROTEINS; HELA CELLS; HISTONES; HUMANS; MICROSCOPY, ELECTRON, SCANNING TRANSMISSION; MODELS, GENETIC; NUCLEOSOMES; POLYCOMB-GROUP PROTEINS; SF9 CELLS; SPODOPTERA; XENOPUS LAEVIS;

EID: 84867423907     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047162     Document Type: Article

References (76)

1. McBryant SJ, Adams VH, Hansen JC, (2006) Chromatin architectural proteins. Chromosome Res 14(1): 39-51.
2. McBryant SJ, Krause C, Woodcock CL, Hansen JC, (2008) The silent information regulator 3 protein, SIR3p, binds to chromatin fibers and assembles a hypercondensed chromatin architecture in the presence of salt. Mol Cell Biol 28(11): 3563-3572.
3. Ghosh RP, Horowitz-Scherer RA, Nikitina T, Shlyakhtenko LS, Woodcock CL, (2010) MeCP2 binds cooperatively to its substrate and competes with histone H1 for chromatin binding sites. Mol Cell Biol 30(19): 4656-4670.
4. Canzio D, Chang EY, Shankar S, Kuchenbecker KM, Simon MD, et al. (2011) Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol Cell 41(1): 67-81.
5. Lewis EB, (1978) A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
6. Jurgens G, (1985) A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature 316: 153-155.
7. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G, (2007) Genome regulation by polycomb and trithorax proteins. Cell 128(4): 735-745.
8. Butenko Y, Ohad N, (2011) Polycomb-group mediated epigenetic mechanisms through plant evolution. Biochim Biophys Acta 1809(8): 395-406.
9. Ringrose L, Paro R, (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38: 413-443.
10. Heard E, Disteche CM, (2006) Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 20(14): 1848-1867.
11. Delaval K, Feil R, (2004) Epigenetic regulation of mammalian genomic imprinting. Curr Opin Genet Dev 14(2): 188-195.
12. Schwartz YB, Pirrotta V, (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8(1): 9-22.
13. Li X, Han Y, Xi R, (2010) Polycomb group genes Psc and Su(z)2 restrict follicle stem cell self-renewal and extrusion by controlling canonical and noncanonical Wnt signaling. Genes Dev 24(9): 933-946.
14. Richly H, Aloia L, Di Croce L, (2011) Roles of the Polycomb group proteins in stem cells and cancer. Cell Death Dis 2: e204.
15. Francis NJ, Kingston RE, Woodcock CL, (2004) Chromatin compaction by a Polycomb Group Protein Complex. Science 306: 1574-1577.
16. Margueron R, Li G, Sarma K, Blais A, Zavadil J, et al. (2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol Cell 32(4): 503-518.
17. Mohd-Sarip A, van der Knaap JA, Wyman C, Kanaar R, Schedl P, et al. (2006) Architecture of a polycomb nucleoprotein complex. Mol Cell 24(1): 91-100.
18. Muller M, Hagstrom K, Gyurkovics H, Pirrotta V, Schedl P, (1999) The mcp element from the Drosophila melanogaster bithorax complex mediates long-distance regulatory interactions. Genetics 153(3): 1333-1356.
19. Kassis JA, (2002) Pairing-sensitive silencing, polycomb group response elements, and transposon homing in Drosophila. Adv Genet 46: 421-438.
20. Fauvarque M-O, Dura J-M, (1993) polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila. Genes Dev 7: 1508-1520.
21. Bantignies F, Grimaud C, Lavrov S, Gabut M, Cavalli G, (2003) Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev 17(19): 2406-2420.
22. Lanzuolo C, Roure V, Dekker J, Bantignies F, Orlando V, (2007) Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat Cell Biol 9(10): 1167-1174.
23. Fedorova E, Sadoni N, Dahlsveen IK, Koch J, Kremmer E, et al. (2008) The nuclear organization of Polycomb/Trithorax group response elements in larval tissues of Drosophila melanogaster. Chromosome Res 16(4): 649-673.
24. Bantignies F, Cavalli G, (2011) Polycomb group proteins: repression in 3D. Trends Genet 27: 454-464.
25. Bantignies F, Roure V, Comet I, Leblanc B, Schuettengruber B, et al. (2011) Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 144(2): 214-226.
26. Tolhuis B, Blom M, Kerkhoven RM, Pagie L, Teunissen H, et al. (2011) Interactions among Polycomb domains are guided by chromosome architecture. PLoS Genet 7(3): e1001343.
27. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, et al. (2012) Three-Dimensional Folding and Functional Organization Principles of the Drosophila Genome. Cell.
28. Comet I, Schuettengruber B, Sexton T, Cavalli G, (2011) A chromatin insulator driving three-dimensional Polycomb response element (PRE) contacts and Polycomb association with the chromatin fiber. Proc Natl Acad Sci U S A 108(6): 2294-2299.
29. Li HB, Muller M, Bahechar IA, Kyrchanova O, Ohno K, et al. (2011) Insulators, not Polycomb response elements, are required for long-range interactions between Polycomb targets in Drosophila melanogaster. Mol Cell Biol 31(4): 616-625.
30. Terranova R, Yokobayashi S, Stadler MB, Otte AP, van Lohuizen M, et al. (2008) Polycomb Group Proteins Ezh2 and Rnf2 Direct Genomic Contraction and Imprinted Repression in Early Mouse Embryos. Dev Cell.
31. Chambeyron S, Da Silva NR, Lawson KA, Bickmore WA, (2005) Nuclear re-organisation of the Hoxb complex during mouse embryonic development. Development 132(9): 2215-2223.
32. Chambeyron S, Bickmore WA, (2004) Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev 18(10): 1119-1130.
33. Eskeland R, Leeb M, Grimes GR, Kress C, Boyle S, et al. (2010) Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol Cell 38(3): 452-464.
34. Mahmoudi T, Katsani KR, Verrijzer CP, (2002) GAGA can mediate enhancer function in trans by linking two separate DNA molecules. Embo J 21(7): 1775-1781.
35. Lavigne M, Francis NJ, King IF, Kingston RE, (2004) Propagation of silencing: recruitment and repression of naive chromatin in trans by Polycomb repressed chromatin. Mol Cell 13: 415-425.
36. Shao Z, Raible F, Mollaaghababa R, Guyon JR, Wu C-t, et al. (1999) Stabilization of chromatin structure by PRC1, a polycomb complex. Cell 98: 37-46.
37. Lagarou A, Mohd-Sarip A, Moshkin YM, Chalkley GE, Bezstarosti K, et al. (2008) dKDM2 couples histone H2A ubiquitylation to histone H3 demethylation during Polycomb group silencing. Genes Dev 22(20): 2799-2810.
38. Mohd-Sarip A, Lagarou A, Doyen CM, van der Knaap JA, Aslan U, et al. (2012) Transcription-independent function of Polycomb group protein PSC in cell cycle control. Science 336(6082): 744-747.
39. Francis NJ, Saurin AJ, Shao Z, Kingston RE, (2001) Reconstitution of a functional core Polycomb repressive complex. Mol Cell 8: 545-556.
40. King IFG, Francis NJ, Kingston RE, (2002) Native and recombinant Polycomb-Group complexes establish a selective block to template accessibility to repress transcription in vitro. Mol Cell Biol 22: 7919-7928.
41. King IF, Emmons RB, Francis NJ, Wild B, Muller J, et al. (2005) Analysis of a polycomb group protein defines regions that link repressive activity on nucleosomal templates to in vivo function. Mol Cell Biol 25(15): 6578-6591.
42. Gutierrez L, Oktaba K, Scheuermann JC, Gambetta MC, Ly-Hartig N, et al. (2012) The role of the histone H2A ubiquitinase Sce in Polycomb repression. Development 139(1): 117-127.
43. Lo SM, Follmer NE, Lengsfeld BM, Madamba EV, Seong S, et al. (2012) A Bridging Model for Persistence of a Polycomb Group Protein Complex through DNA Replication In Vitro. Mol Cell 46(6): 784-796.
44. Schwarz PM, Hansen JC, (1994) Formation and stability of higher order chromatin structures. Contributions of the histone octamer. J Biol Chem 269: 16284-16289.
45. Wall JS, Hainfeld JF, Simon MN, (1998) Scanning transmission electron microscopy of nuclear structures. Methods in Cell Biology 53: 139-162.
46. Emmons RB, Genetti H, Filandrinos S, Lokere J, Wu CT, (2009) Molecular genetic analysis of Suppressor 2 of zeste identifies key functional domains. Genetics 182(4): 999-1013.
47. Beh LY, Colwell LJ, Francis NJ (2012) A core subunit of Polycomb repressive complex 1 is broadly conserved in function but not primary sequence. PNAS 109.
48. Lo SM, Francis NJ, (2010) Inhibition of chromatin remodeling by polycomb group protein posterior sex combs is mechanistically distinct from nucleosome binding. Biochemistry 49(44): 9438-9448.
49. Dorigo B, Schalch T, Bystricky K, Richmond TJ, (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J Mol Biol 327(1): 85-96.
50. 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(5762): 844-847.
51. Zhou J, Fan JY, Rangasamy D, Tremethick DJ, (2007) The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat Struct Mol Biol 14(11): 1070-1076.
52. Wyrick JJ, Kyriss MN, Davis WB, (2012) Ascending the nucleosome face: Recognition and function of structured domains in the histone H2A-H2B dimer. Biochim Biophys Acta 1819(8): 892-901.
53. Dyer PN, Edayathumangalam RS, White CL, Bao Y, Chakravarthy S, et al. (2004) Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol 375: 23-44.
54. Utley RT, Ikeda K, Grant PA, Cote J, Steger DJ, et al. (1998) Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 394: 498-502.
55. Schwarz PM, Felthauser A, Fletcher TM, Hansen JC, (1996) Reversible oligonucleosome self-association: dependence on divalent cations and core histone tail domains. Biochemistry 35(13): 4009-4015.
56. McBryant SJ, Klonoski J, Sorensen TC, Norskog SS, Williams S, et al. (2009) Determinants of histone H4 N-terminal domain function during nucleosomal array oligomerization: roles of amino acid sequence, domain length, and charge density. J Biol Chem 284(25): 16716-16722.
57. Polach KJ, Widom J, (1995) Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J Mol Biol 254: 130-149.
58. Logie C, Peterson CL, (1997) Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays. EMBO J 16: 6772-6782.
59. Trojer P, Li G, Sims RJ, 3rd, Vaquero A, Kalakonda N, et al (2007) L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129(5): 915-928.
60. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, et al. (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301(5636): 1090-1093.
61. Papp B, Muller J, (2006) Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 20(15): 2041-2054.
62. Mito Y, Henikoff JG, Henikoff S, (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315(5817): 1408-1411.
63. Georgel PT, Horowitz-Scherer RA, Adkins N, C.L W, Wade PA, et al. (2003) Chromatin compaction by human MeCP2. Assembly of novel secondary chromatin structures in the absence of DNA methylation. J Biol Chem 278: 32181-328188.
64. Adkins NL, McBryant SJ, Johnson CN, Leidy JM, Woodcock CL, et al. (2009) Role of nucleic acid binding in Sir3p-dependent interactions with chromatin fibers. Biochemistry 48(2): 276-288.
65. Armache KJ, Garlick JD, Canzio D, Narlikar GJ, Kingston RE, (2011) Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 A resolution. Science 334(6058): 977-982.
66. Gambetta MC, Oktaba K, Muller J, (2009) Essential role of the glycosyltransferase sxc/Ogt in polycomb repression. Science 325(5936): 93-96.
67. Sinclair DA, Syrzycka M, Macauley MS, Rastgardani T, Komljenovic I, et al. (2009) Drosophila O-GlcNAc transferase (OGT) is encoded by the Polycomb group (PcG) gene, super sex combs (sxc). Proc Natl Acad Sci U S A 106(32): 13427-13432.
68. Workman JL, Taylor IC, Kingston RE, Roeder RG, (1991) Control of class II gene transcription during in vitro nucleosome assembly. Methods Cell Biol 35: 419-447.
69. Luger K, Rechsteiner TJ, Richmond TJ, (1999) Preparation of nucleosome core particle from recombinant histones. Methods Enzymol 304: 3-19.
70. Sif S, Stukenberg PT, Kirschner MW, Kingston RE, (1998) Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev 12: 2842-2851.
71. Wong I, Lohman TM, (1993) A double-filter method for nitrocellulose-filter binding: Application to protein-nucleic acid interactions. Proc Natl Acad Sci USA 90: 5428-5432.
72. Francis NJ, Follmer NE, Simon MD, Aghia G, Butler JD (2009) Polycomb Proteins Remain Bound to Chromatin and DNA during DNA Replication In Vitro. Cell: 110-122.
73. Carruthers LM, Tse C, Walker KP, Hansen JC, (1999) Assembly of defined nucleosomal and chromatin arrays from pure components. Methods Enzymol 304: 19-35.
74. Lee KM, Narlikar G (2001) Assembly of nucleosomal templates by salt dialysis. Curr Protoc Mol Biol Chapter 21: Unit 21 26.
75. Woodcock CL, Horowitz RA, (1998) Electron microscopic imaging of chromatin with nucleosome resolution. Methods in Cell Biology 53: 167-186.
76. Yang JG, Narlikar GJ, (2007) FRET-based methods to study ATP-dependent changes in chromatin structure. Methods 41(3): 291-295.