A Vertebrate Polycomb Response Element Governs Segmentation of the Posterior Hindbrain

Cell

Volumn 138, Issue 5, 2009, Pages 885-897

  Sing, Angela ^a,c   Pannell, Dylan ^b,c   Karaiskakis, Angelo ^b,c   Sturgeon, Kendra ^a,c   Djabali, Malek ^d   Ellis, James ^b,c   Lipshitz, Howard D ^b,c   Cordes, Sabine P ^a,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d CNRS   (France)

Author keywords

DEVBIO; DNA

Indexed keywords

POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 1 PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2 PROTEIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAFB; TRITHORAX GROUP PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; EMBRYO; EMBRYO SEGMENTATION; GENE EXPRESSION REGULATION; GENE REPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RHOMBENCEPHALON; VERTEBRATE;

INVERTEBRATA; MAMMALIA; METAZOA; VERTEBRATA;

EID: 69449086947     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.08.020     Document Type: Article

References (71)

1. Artzt K., Dubois P., Bennett D., Condamine H., Babinet C., and Jacob F. Surface antigens common to mouse cleavage embryos and primitive teratocarcinoma cells in culture. Proc. Natl. Acad. Sci. USA 70 (1973) 2988-2992
2. Atchison L., Ghias A., Wilkinson F., Bonini N., and Atchison M.L. Transcription factor YY1 functions as a PcG protein in vivo. EMBO J. 22 (2003) 1347-1358
3. Beisel C., Buness A., Roustan-Espinosa I.M., Koch B., Schmitt S., Haas S.A., Hild M., Katsuyama T., and Paro R. Comparing active and repressed expression states of genes controlled by the Polycomb/Trithorax group proteins. Proc. Natl. Acad. Sci. USA 104 (2007) 16615-16620
4. Bel-Vialar S., Core N., Terranova R., Goudot V., Boned A., and Djabali M. Altered retinoic acid sensitivity and temporal expression of Hox genes in polycomb-M33-deficient mice. Dev. Biol. 224 (2000) 238-249
5. Boyer L.A., Plath K., Zeitlinger J., Brambrink T., Medeiros L.A., Lee T.I., Levine S.S., Wernig M., Tajonar A., Ray M.K., et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441 (2006) 349-353
6. Bracken A.P., Dietrich N., Pasini D., Hansen K.H., and Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20 (2006) 1123-1136
7. Brown J.L., Mucci D., Whiteley M., Dirksen M.L., and Kassis J.A. The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1. Mol. Cell 1 (1998) 1057-1064
8. Brown J.L., Fritsch C., Mueller J., and Kassis J.A. The Drosophila pho-like gene encodes a YY1-related DNA binding protein that is redundant with pleiohomeotic in homeotic gene silencing. Development 130 (2003) 285-294
9. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., and Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298 (2002) 1039-1043
10. Cavalli G., and Paro R. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell 93 (1998) 505-518
11. Chamberlain S.J., Yee D., and Magnuson T. Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 26 (2008) 1496-1505
12. Chan C.S., Rastelli L., and Pirrotta V. A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J. 13 (1994) 2553-2564
13. Cordes S.P., and Barsh G.S. The mouse segmentation gene kr encondes a novel basic domain-leucine zipper transcription factor. Cell 79 (1994) 1025-1034
14. Courel M., Friesenhahn L., and Lees J.A. E2f6 and Bmi1 cooperate in axial skeletal development. Dev. Dyn. 237 (2008) 1232-1242
15. Crosby M.A., Miller C., Alon T., Watson K.L., Verrijzer C.P., Goldman-Levi R., and Zak N.B. The trithorax group gene moira encodes a brahma-associated putative chromatin-remodeling factor in Drosophila melanogaster. Mol. Cell. Biol. 19 (1999) 1159-1170
16. Czermin B., Melfi R., McCabe D., Seitz V., Imhof A., and Pirrotta V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111 (2002) 185-196
17. Dietrich N., Bracken A.P., Trinh E., Schjerling C.K., Koseki H., Rappsilber J., Helin K., and Hansen K.H. Bypass of senescence by the polycomb group protein CBX8 through direct binding to the INK4A-ARF locus. EMBO J. 26 (2007) 1637-1648
18. Eden E., Lipson D., Yogev S., and Yakhini Z. Discovering motifs in ranked lists of DNA sequences. PLoS Comput. Biol. 3 (2007) e39 10.1371/journal.pcbi.0030039
19. Frohman M.A., Martin G.R., Cordes S.P., Halamek L.P., and Barsh G.S. Altered rhombomere-specific gene expression and hyoid bone differentiation in the mouse segmentation mutant, kreisler (kr). Development 117 (1993) 925-936
20. Gavalas A., Studer M., Lumsden A., Rijli F.M., Krumlauf R., and Chambon P. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 125 (1998) 1123-1136
21. Gee H. Evolutionary biology: the amphioxus unleashed. Nature 453 (2008) 999-1000
22. Gellon G., Harding K.W., McGinnis N., Martin M.M., and McGinnis W. A genetic screen for modifiers of Deformed homeotic function identifies novel genes required for head development. Development 124 (1997) 3321-3331
23. Gil J., Bernard D., Martinez D., and Beach D. Polycomb CBX7 has a unifying role in cellular lifespan. Nat. Cell Biol. 6 (2004) 67-72
24. Giudicelli F., Gilardi-Hebenstreit P., Mechta-Grigoriou F., Poquet C., and Charnay P. Novel activities of MafB underlie its dual role in hindbrain segmentation and regional specification. Dev. Biol. 253 (2003) 150-162
25. Grimaud C., Negre N., and Cavalli G. From genetics to epigenetics: the tale of Polycomb group and trithorax group genes. Chromosome Res. 14 (2006) 363-375
26. Guthrie S., and Lumsden A. Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. Development 112 (1991) 221-229
27. Hauenschild A., Ringrose L., Altmutter C., Paro R., and Rehmsmeier M. Evolutionary plasticity of polycomb/trithorax response elements in Drosophila species. PLoS Biol. 6 (2008) e261 10.1371/journal.pbio.0060261
28. Ho L., Jothi R., Ronan J.L., Cui K., Zhao K., and Crabtree G.R. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc. Natl. Acad. Sci. USA 106 (2009) 5187-5191
29. Holland L.Z., Albalat R., Azumi K., Benito-Gutierrez E., Blow M.J., Bronner-Fraser M., Brunet F., Butts T., Candiani S., Dishaw L.J., et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 18 (2008) 1100-1111
30. Huang D.H., Chang Y.L., Yang C.C., Pan I.C., and King B. pipsqueak encodes a factor essential for sequence-specific targeting of a polycomb group protein complex. Mol. Cell. Biol. 22 (2002) 6261-6271
31. John R.M., Aparicio S.A., Ainscough J.F., Arney K.L., Khosla S., Hawker K., Hilton K.J., Barton S.C., and Surani M.A. Imprinted expression of neuronatin from modified BAC transgenes reveals regulation by distinct and distant enhancers. Dev. Biol. 236 (2001) 387-399
32. Kahn T.G., Schwartz Y.B., Dellino G.I., and Pirrotta V. Polycomb complexes and the propagation of the methylation mark at the Drosophila ubx gene. J. Biol. Chem. 281 (2006) 29064-29075
33. Karakuzu O., Wang D.P., and Cameron S. MIG-32 and SPAT-3A are PRC1 homologs that control neuronal migration in Caenorhabditis elegans. Development 136 (2009) 943-953
34. Kirmizis A., Bartley S.M., Kuzmichev A., Margueron R., Reinberg D., Green R., and Farnham P.J. Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev. 18 (2004) 1592-1605
35. Kim F.A., Sing A., Kaneko T., Bieman M., Stallwood N., Sadl V.S., and Cordes S.P. The vHNF1 homeodomain protein establishes early rhombomere identity by direct regulation of Kreisler expression. Mech. Dev. 122 (2005) 1300-1309
36. King I.F., Francis N.J., and Kingston R.E. Native and recombinant polycomb group complexes establish a selective block to template accessibility to repress transcription in vitro. Mol. Cell. Biol. 22 (2002) 7919-7928
37. Ku M., Koche R.P., Rheinbay E., Mendenhall E.M., Endoh M., Mikkelsen T.S., Presser A., Nusbaum C., Xie X., Chi A.S., et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4 (2008) e1000242 10.1371/journal.pgen.1000242
38. Lanzuolo C., Roure V., Dekker J., Bantignies F., and Orlando V. Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat. Cell Biol. 9 (2007) 1167-1174
39. Lavrov S., Déjardin J., and Cavalli G. Combined immunostaining and FISH analysis of polytene chromosomes. Methods Mol. Biol. 247 (2004) 289-303
40. Lee T.I., Jenner R.G., Boyer L.A., Guenther M.G., Levine S.S., Kumar R.M., Chevalier B., Johnstone S.E., Cole M.F., Isono K., et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125 (2006) 301-313
41. Levine S.S., Weiss A., Erdjument-Bromage H., Shao Z., Tempst P., and Kingston R.E. The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol. Cell. Biol. 22 (2002) 6070-6078
42. Liu J., Cao L., Chen J., Song S., Lee I.H., Quijano C., Liu H., Keyvanfar K., Chen H., Cao L.Y., et al. Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 459 (2009) 387-392
43. Lumsden A., and Krumlauf R. Patterning the vertebrate neuraxis. Science 274 (1996) 1109-1115
44. Lyko F., Brenton J.D., Surani M.A., and Paro R. An imprinting element from the mouse H19 locus functions as a silencer in Drosophila. Nat. Genet. 16 (1997) 171-173
45. Marson A., Levine S.S., Cole M.F., Frampton G.M., Brambrink T., Johnstone S., Guenther M.G., Johnston W.K., Wernig M., Newman J., et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134 (2008) 521-533
46. Mihaly J., Mishra R.K., and Karch F. A conserved sequence motif in Polycomb-response elements. Mol. Cell 1 (1998) 1065-1066
47. Montgomery N.D., Yee D., Chen A., Kalantry S., Chamberlain S.J., Otte A.P., and Magnuson T. The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr. Biol. 15 (2005) 942-947
48. Müller J., Hart C.M., Francis N.J., Vargas M.L., Sengupta A., Wild B., Miller E.L., O'Connor M.B., Kingston R.E., and Simon J.A. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111 (2002) 197-208
49. Nekrasov M., Klymenko T., Fraterman S., Papp B., Oktaba K., Kocher T., Cohen A., Stunnenberg H.G., Wilm M., and Muller J. Pcl-PRC2 is needed to generate high levels of H3-K27 trimethylation at Polycomb target genes. EMBO J. 26 (2007) 4078-4088
50. Papp B., and Muller J. Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev. 20 (2006) 2041-2054
51. Pasini D., Bracken A.P., Hansen J.B., Capillo M., and Helin K. The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 27 (2007) 3769-3779
52. Puschendorf M., Terranova R., Boutsma E., Mao X., Isono K., Brykczynska U., Kolb C., Otte A.P., Koseki H., Orkin S.H., et al. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 40 (2008) 411-420
53. Ringrose L., Rehmsmeier M., Dura J.M., and Paro R. Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev. Cell 5 (2003) 759-771
54. Rivkin E., and Cordes S.P. Generation of a transgenic mouse line expressing GFP-Cre protein from a Hoxb4 neural enhancer. Genesis 46 (2008) 119-124
55. Rusch D.B., and Kaufman T.C. Regulation of proboscipedia in Drosophila by homeotic selector genes. Genetics 156 (2000) 183-194
56. Sadl V.S., Sing A., Mar L., Jin F., and Cordes S.P. Analysis of hindbrain patterning defects caused by the kreisler enu mutation reveals multiple roles of Kreisler in hindbrain segmentation. Dev. Dyn. 227 (2003) 134-142
57. Schoeftner S., Sengupta A.K., Kubicek S., Mechtler K., Spahn L., Koseki H., Jenuwein T., and Wutz A. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 25 (2006) 3110-3122
58. Schuettengruber B., Ganapathi M., Leblanc B., Portoso M., Jaschek R., Tolhuis B., van Lohuizen M., Tanay A., and Cavalli G. Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol. 7 (2009) e13 10.1371/journal.pbio.1000013
59. Schwartz Y.B., and Pirrotta V. Polycomb complexes and epigenetic states. Curr. Opin. Cell Biol. 20 (2008) 266-273
60. Schwartz Y.B., Kahn T.G., Nix D.A., Li X.Y., Bourgon R., Biggin M., and Pirrotta V. Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat. Genet. 38 (2006) 700-705
61. Shi J., Levinson D.F., Duan J., Sanders A.R., Zheng Y., Pe'er I., Dudbridge F., Holmans P.A., Whittemore A.S., Mowry B.J., et al. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 460 (2009) 753-757
62. Simon J., Chiang A., Bender W., Shimell M.J., and O'Connor M. Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev. Biol. 158 (1993) 131-144
63. Sparmann A., and van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 6 (2006) 846-856
64. Squazzo S.L., O'Geen H., Komashko V.M., Krig S.R., Jin V.X., Jang S.W., Margueron R., Reinberg D., Green R., and Farnham P.J. Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res. 16 (2006) 890-900
65. Swaminathan J., Baxter E.M., and Corces V.G. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev. 19 (2005) 65-76
66. Tamkun J.W., Deuring R., Scott M.P., Kissinger M., Pattatucci A.M., Kaufman T.C., and Kennison J.A. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68 (1992) 561-572
67. Tanay A., O'Donnell A.H., Damelin M., and Bestor T.H. Hyperconserved CpG domains underlie Polycomb-binding sites. Proc. Natl. Acad. Sci. USA 104 (2007) 5521-5526
68. Voncken J.W., Roelen B.A., Roefs M., de Vries S., Verhoeven E., Marino S., Deschamps J., and van Lohuizen M. Rnf2 (Ring1b) deficiency causes gastrulation arrest and cell cycle inhibition. Proc. Natl. Acad. Sci. USA 100 (2003) 2468-2473
69. Wang L., Brown J.L., Cao R., Zhang Y., Kassis J.A., and Jones R.S. Hierarchical recruitment of polycomb group silencing complexes. Mol. Cell 14 (2004) 637-646
70. Wijnholds J., Chowdhury K., Wehr R., and Gruss P. Segment-specific expression of the neuronatin gene during early hindbrain development. Dev. Biol. 171 (1995) 73-84
71. Wu J.I., Lessard J., Olave I.A., Qiu Z., Ghosh A., Graef I.A., and Crabtree G.R. Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56 (2007) 94-108