Progressive polycomb assembly on H3K27me3 compartments generates Polycomb bodies with developmentally regulated motion

PLoS Genetics

Volumn 8, Issue 1, 2012, Pages

  Cheutin, Thierry ^a   Cavalli, Giacomo ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HISTONE H3; HYBRID PROTEIN; POLYCOMB GROUP PROTEIN; POLYHOMEOTIC PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; LYSINE; MULTIPROTEIN COMPLEX; NUCLEOPROTEIN; POLYCOMB PROTEIN, DROSOPHILA; POLYHOMEOTIC PROTEIN, DROSOPHILA;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; EUCHROMATIN; FLUORESCENCE IN SITU HYBRIDIZATION; GENE SILENCING; GENETIC ASSOCIATION; HISTONE METHYLATION; IMMUNOHISTOCHEMISTRY; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN LOCALIZATION; TIME LAPSE IMAGING; ANIMAL; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; CELL COMPARTMENTATION; CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMES; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EUCHROMATIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; IN SITU HYBRIDIZATION, FLUORESCENCE; LYSINE; MULTIPROTEIN COMPLEXES; NUCLEOPROTEINS; TIME-LAPSE IMAGING;

EID: 84857467274     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002465     Document Type: Article

References (56)

1. Jenuwein T, Allis CD, (2001) Translating the histone code. Science 293: 1074-1080.
2. Shao Z, Raible F, Mollaaghababa R, Guyon JR, Wu CT, et al. (1999) Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98: 37-46.
3. Simon JA, Kingston RE, (2009) Mechanisms of Polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol.
4. Schwartz YB, Pirrotta V, (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8: 9-22.
5. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G, (2007) Genome regulation by polycomb and trithorax proteins. Cell 128: 735-745.
6. Negre N, Hennetin J, Sun LV, Lavrov S, Bellis M, et al. (2006) Chromosomal distribution of PcG proteins during Drosophila development. PLoS Biol 4: e170 doi:10.1371/journal.pbio.0040170.
7. Schuettengruber B, Ganapathi M, Leblanc B, Portoso M, Jaschek R, et al. (2009) Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol 7: e13 doi:10.1371/journal.pbio.1000013.
8. Muller J, Verrijzer P, (2009) Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr Opin Genet Dev 19: 150-158.
9. 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: 1167-1174.
10. 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: 214-226.
11. 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: e1001343 doi:10.1371/journal.pgen.1001343.
12. Bantignies F, Grimaud C, Lavrov S, Gabut M, Cavalli G, (2003) Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev 17: 2406-2420.
13. Vazquez J, Muller M, Pirrotta V, Sedat JW, (2006) The Mcp element mediates stable long-range chromosome-chromosome interactions in Drosophila. Mol Biol Cell 17: 2158-2165.
14. Li HB, Muller M, Bahechar IA, Kyrchanova O, Ohno K, et al. (2010) Insulators, not Polycomb Response Elements, are required for long-range interactions between Polycomb targets in Drosophila. Mol Cell Biol.
15. Grimaud C, Bantignies F, Pal-Bhadra M, Ghana P, Bhadra U, et al. (2006) RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 124: 957-971.
16. Buchenau P, Hodgson J, Strutt H, Arndt-Jovin DJ, (1998) The distribution of polycomb-group proteins during cell division and development in Drosophila embryos: impact on models for silencing. J Cell Biol 141: 469-481.
17. Messmer S, Franke A, Paro R, (1992) Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev 6: 1241-1254.
18. 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: 452-464.
19. 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 15: 668-679.
20. Ficz G, Heintzmann R, Arndt-Jovin DJ, (2005) Polycomb group protein complexes exchange rapidly in living Drosophila. Development 132: 3963-3976.
21. Ren X, Vincenz C, Kerppola TK, (2008) Changes in the distributions and dynamics of polycomb repressive complexes during embryonic stem cell differentiation. Mol Cell Biol 28: 2884-2895.
22. Marshall WF, Straight A, Marko JF, Swedlow J, Dernburg A, et al. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol 7: 930-939.
23. Vazquez J, Belmont AS, Sedat JW, (2001) Multiple regimes of constrained chromosome motion are regulated in the interphase Drosophila nucleus. Curr Biol 11: 1227-1239.
24. Chubb JR, Boyle S, Perry P, Bickmore WA, (2002) Chromatin motion is constrained by association with nuclear compartments in human cells. Curr Biol 12: 439-445.
25. Heun P, Laroche T, Shimada K, Furrer P, Gasser SM, (2001) Chromosome dynamics in the yeast interphase nucleus. Science 294: 2181-2186.
26. Thakar R, Csink AK, (2005) Changing chromatin dynamics and nuclear organization during differentiation in Drosophila larval tissue. J Cell Sci 118: 951-960.
27. Chuang CH, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P, et al. (2006) Long-range directional movement of an interphase chromosome site. Curr Biol 16: 825-831.
28. Dundr M, Ospina JK, Sung MH, John S, Upender M, et al. (2007) Actin-dependent intranuclear repositioning of an active gene locus in vivo. J Cell Biol 179: 1095-1103.
29. Platani M, Goldberg I, Lamond AI, Swedlow JR, (2002) Cajal body dynamics and association with chromatin are ATP-dependent. Nat Cell Biol 4: 502-508.
30. Gorisch SM, Wachsmuth M, Ittrich C, Bacher CP, Rippe K, et al. (2004) Nuclear body movement is determined by chromatin accessibility and dynamics. Proc Natl Acad Sci U S A 101: 13221-13226.
31. Alkema MJ, Bronk M, Verhoeven E, Otte A, van 't Veer LJ, et al. (1997) Identification of Bmi1-interacting proteins as constituents of a multimeric mammalian polycomb complex. Genes Dev 11: 226-240.
32. Saurin AJ, Shiels C, Williamson J, Satijn DP, Otte AP, et al. (1998) The human polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J Cell Biol 142: 887-898.
33. Netter S, Faucheux M, Theodore L, (2001) Developmental dynamics of a polyhomeotic-EGFP fusion in vivo. DNA Cell Biol 20: 483-492.
34. Dietzel S, Niemann H, Bruckner B, Maurange C, Paro R, (1999) The nuclear distribution of Polycomb during Drosophila melanogaster development shown with a GFP fusion protein. Chromosoma 108: 83-94.
35. Schwartz YB, Kahn TG, Nix DA, Li XY, Bourgon R, et al. (2006) Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38: 700-705.
36. Tolhuis B, de Wit E, Muijrers I, Teunissen H, Talhout W, et al. (2006) Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38: 694-699.
37. Manak JR, Dike S, Sementchenko V, Kapranov P, Biemar F, et al. (2006) Biological function of unannotated transcription during the early development of Drosophila melanogaster. Nat Genet 38: 1151-1158.
38. Kosman D, Mizutani CM, Lemons D, Cox WG, McGinnis W, et al. (2004) Multiplex detection of RNA expression in Drosophila embryos. Science 305: 846.
39. Jagla K, Jagla T, Heitzler P, Dretzen G, Bellard F, et al. (1997) ladybird, a tandem of homeobox genes that maintain late wingless expression in terminal and dorsal epidermis of the Drosophila embryo. Development 124: 91-100.
40. Rieckhof GE, Casares F, Ryoo HD, Abu-Shaar M, Mann RS, (1997) Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 91: 171-183.
41. Kerber B, Fellert S, Hoch M, (1998) Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. Genes & development 12: 1781-1786.
42. Swaminathan J, Baxter EM, Corces VG, (2005) The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev 19: 65-76.
43. Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, et al. (2008) Nucleosome organization in the Drosophila genome. Nature 453: 358-362.
44. Leach TJ, Mazzeo M, Chotkowski HL, Madigan JP, Wotring MG, et al. (2000) Histone H2A.Z is widely but nonrandomly distributed in chromosomes of Drosophila melanogaster. J Biol Chem 275: 23267-23272.
45. Cmarko D, Verschure PJ, Otte AP, van Driel R, Fakan S, (2003) Polycomb group gene silencing proteins are concentrated in the perichromatin compartment of the mammalian nucleus. J Cell Sci 116: 335-343.
46. Francis NJ, Kingston RE, Woodcock CL, (2004) Chromatin compaction by a polycomb group protein complex. Science 306: 1574-1577.
47. 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: 503-518.
48. Fitzgerald DP, Bender W, (2001) Polycomb group repression reduces DNA accessibility. Mol Cell Biol 21: 6585-6597.
49. Levi V, Ruan Q, Plutz M, Belmont AS, Gratton E, (2005) Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys J 89: 4275-4285.
50. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, et al. (2006) Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 38: 1348-1354.
51. Wachsmuth M, Caudron-Herger M, Rippe K, (2008) Genome organization: balancing stability and plasticity. Biochim Biophys Acta 1783: 2061-2079.
52. Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, et al. (2006) Chromosome territories-a functional nuclear landscape. Curr Opin Cell Biol 18: 307-316.
53. Thakar R, Gordon G, Csink AK, (2006) Dynamics and anchoring of heterochromatic loci during development. J Cell Sci 119: 4165-4175.
54. Misteli T, (2001) Protein dynamics: implications for nuclear architecture and gene expression. Science 291: 843-847.
55. Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, et al. (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143: 212-224.
56. Langevin J, Le Borgne R, Rosenfeld F, Gho M, Schweisguth F, et al. (2005) Lethal giant larvae controls the localization of notch-signaling regulators numb, neuralized, and Sanpodo in Drosophila sensory-organ precursor cells. Curr Biol 15: 955-962.