Identification of regulators of the three-dimensional polycomb organization by a microscopy-based genome-wide RNAi screen

Molecular Cell

Volumn 54, Issue 3, 2014, Pages 485-499

  Gonzalez, Inma ^a   Mateos Langerak, Julio ^a   Thomas, Aubin ^a   Cheutin, Thierry ^a   Cavalli, Giacomo ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCOMB GROUP PROTEIN; SUMO PROTEIN;

ARTICLE; CHROMATIN; CONTROLLED STUDY; MICROSCOPY; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; RNA ANALYSIS; RNA INTERFERENCE; SUMOYLATION;

ANIMALS; CELL LINE; CELL NUCLEUS; CHROMATIN; CLUSTER ANALYSIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE KNOCKDOWN TECHNIQUES; GENE ONTOLOGY; IMAGINAL DISCS; PHENOTYPE; POLYCOMB-GROUP PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RNA INTERFERENCE; SUMOYLATION;

EID: 84899922567     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.03.004     Document Type: Article

References (63)

1. Bantignies F., Cavalli G. Polycomb group proteins: repression in 3D. Trends Genet. 2011, 27:454-464.
2. Bantignies F., Roure V., Comet I., Leblanc B., Schuettengruber B., Bonnet J., Tixier V., Mas A., Cavalli G. Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 2011, 144:214-226.
3. Berdnik D., Favaloro V., Luo L. The SUMO protease Verloren regulates dendrite and axon targeting in olfactory projection neurons. J.Neurosci. 2012, 32:8331-8340.
4. Brideau C., Gunter B., Pikounis B., Liaw A. Improved statistical methods for hit selection in high-throughput screening. J.Biomol. Screen 2003, 8:634-647.
5. Cabrera C.V., Botas J., Garcia-Bellido A. Distribution of Ultrabithorax proteins in mutants of Drosophila bithorax complex and its transregulatory genes. Nature 1985, 318:569-571.
6. Capelson M., Corces V.G. SUMO conjugation attenuates the activity of the gypsy chromatin insulator. EMBO J. 2006, 25:1906-1914.
7. Carpenter A.E., Jones T.R., Lamprecht M.R., Clarke C., Kang I.H., Friman O., Guertin D.A., Chang J.H., Lindquist R.A., Moffat J., et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 2006, 7:R100.
8. Chalkiadaki A., Talianidis I. SUMO-dependent compartmentalization in promyelocytic leukemia protein nuclear bodies prevents the access of LRH-1 to chromatin. Mol. Cell. Biol. 2005, 25:5095-5105.
9. Cheutin T., Cavalli G. Progressive polycomb assembly on H3K27me3 compartments generates polycomb bodies with developmentally regulated motion. PLoS Genet. 2012, 8:e1002465.
10. Czermin B., Melfi R., McCabe D., Seitz V., Imhof A., Pirrotta V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 2002, 111:185-196.
11. Duncan I.M. Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene complexes of Drosophila melanogaster. Genetics 1982, 102:49-70.
12. Franke A., Messmer S., Paro R. Mapping functional domains of the polycomb protein of Drosophila melanogaster. Chromosome Res. 1995, 3:351-360.
13. Georlette D., Ahn S., MacAlpine D.M., Cheung E., Lewis P.W., Beall E.L., Bell S.P., Speed T., Manak J.R., Botchan M.R. Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. Genes Dev. 2007, 21:2880-2896.
14. Golovnin A., Volkov I., Georgiev P. SUMO conjugation is required for the assembly of Drosophila Su(Hw) and Mod(mdg4) into insulator bodies that facilitate insulator complex formation. J.Cell Sci. 2012, 125:2064-2074.
15. Grimaud C., Nègre N., Cavalli G. From genetics to epigenetics: the tale of Polycomb group and trithorax group genes. Chromosome Res. 2006, 14:363-375.
16. Hari K.L., Cook K.R., Karpen G.H. The Drosophila Su(var)2-10 locus regulates chromosome structure and function and encodes a member of the PIAS protein family. Genes Dev. 2001, 15:1334-1348.
17. Hay R.T. SUMO: a history of modification. Mol. Cell 2005, 18:1-12.
18. Hou C., Li L., Qin Z.S., Corces V.G. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol. Cell 2012, 48:471-484.
19. Huang H.W., Tsoi S.C., Sun Y.H., Li S.S. Identification and characterization of the SMT3 cDNA and gene encoding ubiquitin-like protein from Drosophila melanogaster. Biochem. Mol. Biol. Int. 1998, 46:775-785.
20. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
21. Ismail I.H., Gagné J.P., Caron M.C., McDonald D., Xu Z., Masson J.Y., Poirier G.G., Hendzel M.J. CBX4-mediated SUMO modification regulates BMI1 recruitment at sites of DNA damage. Nucleic Acids Res. 2012, 40:5497-5510.
22. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 2004, 73:355-382.
23. Joyce E.F., Williams B.R., Xie T., Wu C.T. Identification of genes that promote or antagonize somatic homolog pairing using a high-throughput FISH-based screen. PLoS Genet. 2012, 8:e1002667.
24. Jürgens G. A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature 1985, 316:153-155.
25. Kagey M.H., Melhuish T.A., Wotton D. The polycomb protein Pc2 is a SUMO E3. Cell 2003, 113:127-137.
26. Kang X., Qi Y., Zuo Y., Wang Q., Zou Y., Schwartz R.J., Cheng J., Yeh E.T. SUMO-specific protease 2 is essential for suppression of polycomb group protein-mediated gene silencing during embryonic development. Mol. Cell 2010, 38:191-201.
27. Klymenko T., Papp B., Fischle W., Köcher T., Schelder M., Fritsch C., Wild B., Wilm M., Müller J. A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev. 2006, 20:1110-1122.
28. Korenjak M., Taylor-Harding B., Binné U.K., Satterlee J.S., Stevaux O., Aasland R., White-Cooper H., Dyson N., Brehm A. Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 2004, 119:181-193.
29. Krumova P., Meulmeester E., Garrido M., Tirard M., Hsiao H.H., Bossis G., Urlaub H., Zweckstetter M., Kügler S., Melchior F., et al. Sumoylation inhibits alpha-synuclein aggregation and toxicity. J.Cell Biol. 2011, 194:49-60.
30. Li S.J., Hochstrasser M. The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell. Biol. 2000, 20:2367-2377.
31. Li B., Zhou J., Liu P., Hu J., Jin H., Shimono Y., Takahashi M., Xu G. Polycomb protein Cbx4 promotes SUMO modification of de novo DNA methyltransferase Dnmt3a. Biochem. J. 2007, 405:369-378.
32. Lima C.D., Reverter D. Structure of the human SENP7 catalytic domain and poly-SUMO deconjugation activities for SENP6 and SENP7. J.Biol. Chem. 2008, 283:32045-32055.
33. MacPherson M.J., Beatty L.G., Zhou W., Du M., Sadowski P.D. The CTCF insulator protein is posttranslationally modified by SUMO. Mol. Cell. Biol. 2009, 29:714-725.
34. Maison C., Romeo K., Bailly D., Dubarry M., Quivy J.P., Almouzni G. The SUMO protease SENP7 is a critical component to ensure HP1 enrichment at pericentric heterochromatin. Nat. Struct. Mol. Biol. 2012, 19:458-460.
35. Marblestone J.G., Edavettal S.C., Lim Y., Lim P., Zuo X., Butt T.R. Comparison of SUMO fusion technology with traditional gene fusion systems: enhanced expression and solubility with SUMO. Protein Sci. 2006, 15:182-189.
36. McKeon J., Slade E., Sinclair D.A., Cheng N., Couling M., Brock H.W. Mutations in some Polycomb group genes of Drosophila interfere with regulation of segmentation genes. Mol. Gen. Genet. 1994, 244:474-483.
37. Mendjan S., Taipale M., Kind J., Holz H., Gebhardt P., Schelder M., Vermeulen M., Buscaino A., Duncan K., Mueller J., et al. Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol. Cell 2006, 21:811-823.
38. Mukhopadhyay D., Arnaoutov A., Dasso M. The SUMO protease SENP6 is essential for inner kinetochore assembly. J.Cell Biol. 2010, 188:681-692.
39. Nayak A., Glöckner-Pagel J., Vaeth M., Schumann J.E., Buttmann M., Bopp T., Schmitt E., Serfling E., Berberich-Siebelt F. Sumoylation of the transcription factor NFATc1 leads to its subnuclear relocalization and interleukin-2 repression by histone deacetylase. J.Biol. Chem. 2009, 284:10935-10946.
40. Neyret-Kahn H., Benhamed M., Ye T., Le Gras S., Cossec J.C., Lapaquette P., Bischof O., Ouspenskaia M., Dasso M., Seeler J., et al. Sumoylation at chromatin governs coordinated repression of a transcriptional program essential for cell growth and proliferation. Genome Res. 2013, 23:1563-1579.
41. Okulski H., Druck B., Bhalerao S., Ringrose L. Quantitative analysis of polycomb response elements (PREs) at identical genomic locations distinguishes contributions of PRE sequence and genomic environment. Epigenetics Chromatin 2011, 4:4.
42. Otte A.P., Kwaks T.H. Gene repression by Polycomb group protein complexes: a distinct complex for every occasion?. Curr. Opin. Genet. Dev. 2003, 13:448-454.
43. Panavas T., Sanders C., Butt T.R. SUMO fusion technology for enhanced protein production in prokaryotic and eukaryotic expression systems. Methods Mol. Biol. 2009, 497:303-317.
44. Ramadan N., Flockhart I., Booker M., Perrimon N., Mathey-Prevot B. Design and implementation of high-throughput RNAi screens in cultured Drosophila cells. Nat. Protoc. 2007, 2:2245-2264.
45. Rodriguez-Jato S., Busturia A., Herr W. Drosophila melanogaster dHCF interacts with both PcG and TrxG epigenetic regulators. PLoS ONE 2011, 6:e27479.
46. Rosa S., De Lucia F., Mylne J.S., Zhu D., Ohmido N., Pendle A., Kato N., Shaw P., Dean C. Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization. Genes Dev. 2013, 27:1845-1850.
47. Ross S., Best J.L., Zon L.I., Gill G. SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol. Cell 2002, 10:831-842.
48. Sabate R., Espargaro A., Graña-Montes R., Reverter D., Ventura S. Native structure protects SUMO proteins from aggregation into amyloid fibrils. Biomacromolecules 2012, 13:1916-1926.
49. Schuettengruber B., Cavalli G. Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 2009, 136:3531-3542.
50. Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007, 128:735-745.
51. Schuettengruber B., Ganapathi M., Leblanc B., Portoso M., Jaschek R., Tolhuis B., van Lohuizen M., Tanay A., Cavalli G. Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol. 2009, 7:e13.
52. Schwartz Y.B., Kahn T.G., Stenberg P., Ohno K., Bourgon R., Pirrotta V. Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet. 2010, 6:e1000805.
53. Seeler J.S., Dejean A. Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell Biol. 2003, 4:690-699.
54. Sexton T., Yaffe E., Kenigsberg E., Bantignies F., Leblanc B., Hoichman M., Parrinello H., Tanay A., Cavalli G. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 2012, 148:458-472.
55. Shao Z., Raible F., Mollaaghababa R., Guyon J.R., Wu C.T., Bender W., Kingston R.E. Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 1999, 98:37-46.
56. Shen T.H., Lin H.K., Scaglioni P.P., Yung T.M., Pandolfi P.P. The mechanisms of PML-nuclear body formation. Mol. Cell 2006, 24:331-339.
57. Smith M., Mallin D.R., Simon J.A., Courey A.J. Small ubiquitin-like modifier (SUMO) conjugation impedes transcriptional silencing by the polycomb group repressor Sex Comb on Midleg. J.Biol. Chem. 2011, 286:11391-11400.
58. Stielow B., Sapetschnig A., Krüger I., Kunert N., Brehm A., Boutros M., Suske G. Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. Mol. Cell 2008, 29:742-754.
59. Strübbe G., Popp C., Schmidt A., Pauli A., Ringrose L., Beisel C., Paro R. Polycomb purification by invivo biotinylation tagging reveals cohesin and Trithorax group proteins as interaction partners. Proc. Natl. Acad. Sci. USA 2011, 108:5572-5577.
60. Tolhuis B., Blom M., Kerkhoven R.M., Pagie L., Teunissen H., Nieuwland M., Simonis M., de Laat W., van Lohuizen M., van Steensel B. Interactions among Polycomb domains are guided by chromosome architecture. PLoS Genet. 2011, 7:e1001343.
61. Ulrich H.D. SUMO protocols. Preface. Methods Mol. Biol. 2009, 497:v-vi.
62. Vaquerizas J.M., Suyama R., Kind J., Miura K., Luscombe N.M., Akhtar A. Nuclear pore proteins nup153 and megator define transcriptionally active regions in the Drosophila genome. PLoS Genet. 2010, 6:e1000846.
63. Zhang H., Smolen G.A., Palmer R., Christoforou A., van den Heuvel S., Haber D.A. SUMO modification is required for invivo Hox gene regulation by the Caenorhabditis elegans Polycomb group protein SOP-2. Nat. Genet. 2004, 36:507-511.