Cause and Consequence of Tethering a SubTAD to Different Nuclear Compartments

Molecular Cell

Volumn 61, Issue 3, 2016, Pages 461-473

  Wijchers, Patrick J ^a   Krijger, Peter H L ^a   Geeven, Geert ^a   Zhu, Yun ^a   Denker, Annette ^a   Verstegen, Marjon J A M ^a   Valdes Quezada, Christian ^a   Vermeulen, Carlo ^a   Janssen, Mark ^a   Teunissen, Hans ^a   Anink Groenen, Lisette C M ^b   Verschure, Pernette J ^b   de Laat, Wouter ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE METHYLTRANSFERASE; LAC REPRESSOR; LACO PROTEIN; PROTEIN; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; CHROMATIN; EZH2 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; METHYLTRANSFERASE; NANOG PROTEIN, MOUSE; POLYCOMB REPRESSIVE COMPLEX 2; REPRESSOR PROTEIN; SUV39H1 PROTEIN, MOUSE;

ALLELE; ARTICLE; CELL NUCLEUS; CHROMATIN; GENE EXPRESSION; HISTONE MODIFICATION; NUCLEOTIDE SEQUENCE; PROTEIN LOCALIZATION; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME SEGREGATION; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSFECTION; GENETICS; LACTOSE OPERON; METABOLISM;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME SEGREGATION; EMBRYONIC STEM CELLS; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; GENE EXPRESSION REGULATION; GENETIC LOCI; HOMEODOMAIN PROTEINS; LAC OPERON; LAC REPRESSORS; METHYLTRANSFERASES; MICE, 129 STRAIN; MICE, INBRED C57BL; NANOG HOMEOBOX PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; REPRESSOR PROTEINS; TRANSFECTION;

EID: 84957665004     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.01.001     Document Type: Article

References (50)

1. Aagaard L., Laible G., Selenko P., Schmid M., Dorn R., Schotta G., Kuhfittig S., Wolf A., Lebersorger A., Singh P.B., et al. Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J. 1999, 18:1923-1938.
2. Akhtar W., Pindyurin A.V., de Jong J., Pagie L., Ten Hoeve J., Berns A., Wessels L.F., van Steensel B., van Lohuizen M. Using TRIP for genome-wide position effect analysis in cultured cells. Nat. Protoc. 2014, 9:1255-1281.
3. 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.
4. Bickmore W.A., van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell 2013, 152:1270-1284.
5. Blackledge N.P., Farcas A.M., Kondo T., King H.W., McGouran J.F., Hanssen L.L., Ito S., Cooper S., Kondo K., Koseki Y., et al. Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell 2014, 157:1445-1459.
6. Bolzer A., Kreth G., Solovei I., Koehler D., Saracoglu K., Fauth C., Müller S., Eils R., Cremer C., Speicher M.R., Cremer T. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol. 2005, 3:e157.
7. Brown K.E., Guest S.S., Smale S.T., Hahm K., Merkenschlager M., Fisher A.G. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 1997, 91:845-854.
8. Brown J.M., Green J., das Neves R.P., Wallace H.A., Smith A.J., Hughes J., Gray N., Taylor S., Wood W.G., Higgs D.R., et al. Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J. Cell Biol. 2008, 182:1083-1097.
9. Cheutin T., Cavalli G. Polycomb silencing: from linear chromatin domains to 3D chromosome folding. Curr. Opin. Genet. Dev. 2014, 25:30-37.
10. Chuang C.H., Carpenter A.E., Fuchsova B., Johnson T., de Lanerolle P., Belmont A.S. Long-range directional movement of an interphase chromosome site. Curr. Biol. 2006, 16:825-831.
11. Chubb J.R., Boyle S., Perry P., Bickmore W.A. Chromatin motion is constrained by association with nuclear compartments in human cells. Curr. Biol. 2002, 12:439-445.
12. de Wit E., de Laat W. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 2012, 26:11-24.
13. de Wit E., Bouwman B.A., Zhu Y., Klous P., Splinter E., Verstegen M.J., Krijger P.H., Festuccia N., Nora E.P., Welling M., et al. The pluripotent genome in three dimensions is shaped around pluripotency factors. Nature 2013, 501:227-231.
14. Deng W., Lee J., Wang H., Miller J., Reik A., Gregory P.D., Dean A., Blobel G.A. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 2012, 149:1233-1244.
15. Denholtz M., Bonora G., Chronis C., Splinter E., de Laat W., Ernst J., Pellegrini M., Plath K. Long-range chromatin contacts in embryonic stem cells reveal a role for pluripotency factors and polycomb proteins in genome organization. Cell Stem Cell 2013, 13:602-616.
16. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
17. Dixon J.R., Jung I., Selvaraj S., Shen Y., Antosiewicz-Bourget J.E., Lee A.Y., Ye Z., Kim A., Rajagopal N., Xie W., et al. Chromatin architecture reorganization during stem cell differentiation. Nature 2015, 518:331-336.
18. Dubarry M., Loïodice I., Chen C.L., Thermes C., Taddei A. Tight protein-DNA interactions favor gene silencing. Genes Dev. 2011, 25:1365-1370.
19. Francis N.J., Kingston R.E., Woodcock C.L. Chromatin compaction by a polycomb group protein complex. Science 2004, 306:1574-1577.
20. Geeven G., Zhu Y., Kim B.J., Bartholdy B.A., Yang S.M., Macfarlan T.S., Gifford W.D., Pfaff S.L., Verstegen M.J., Pinto H., et al. Local compartment changes and regulatory landscape alterations in histone H1-depleted cells. Genome Biol. 2015, 16:289.
21. Grewal S.I., Jia S. Heterochromatin revisited. Nat. Rev. Genet. 2007, 8:35-46.
22. Guelen L., Pagie L., Brasset E., Meuleman W., Faza M.B., Talhout W., Eussen B.H., de Klein A., Wessels L., de Laat W., van Steensel B. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 2008, 453:948-951.
23. Hakim O., Sung M.H., Voss T.C., Splinter E., John S., Sabo P.J., Thurman R.E., Stamatoyannopoulos J.A., de Laat W., Hager G.L. Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res. 2011, 21:697-706.
24. Hawkins R.D., Hon G.C., Lee L.K., Ngo Q., Lister R., Pelizzola M., Edsall L.E., Kuan S., Luu Y., Klugman S., et al. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 2010, 6:479-491.
25. Kind J., Pagie L., Ortabozkoyun H., Boyle S., de Vries S.S., Janssen H., Amendola M., Nolen L.D., Bickmore W.A., van Steensel B. Single-cell dynamics of genome-nuclear lamina interactions. Cell 2013, 153:178-192.
26. Krijger P.H., de Laat W. Identical cells with different 3D genomes; cause and consequences?. Curr. Opin. Genet. Dev. 2013, 23:191-196.
27. 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. 2008, 4:e1000242.
28. Kumaran R.I., Spector D.L. A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J. Cell Biol. 2008, 180:51-65.
29. Liang J., Wan M., Zhang Y., Gu P., Xin H., Jung S.Y., Qin J., Wong J., Cooney A.J., Liu D., Songyang Z. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat. Cell Biol. 2008, 10:731-739.
30. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
31. Muramatsu D., Singh P.B., Kimura H., Tachibana M., Shinkai Y. Pericentric heterochromatin generated by HP1 protein interaction-defective histone methyltransferase Suv39h1. J. Biol. Chem. 2013, 288:25285-25296.
32. Németh A., Conesa A., Santoyo-Lopez J., Medina I., Montaner D., Péterfia B., Solovei I., Cremer T., Dopazo J., Längst G. Initial genomics of the human nucleolus. PLoS Genet. 2010, 6:e1000889.
33. Noordermeer D., de Wit E., Klous P., van de Werken H., Simonis M., Lopez-Jones M., Eussen B., de Klein A., Singer R.H., de Laat W. Variegated gene expression caused by cell-specific long-range DNA interactions. Nat. Cell Biol. 2011, 13:944-951.
34. Nora E.P., Lajoie B.R., Schulz E.G., Giorgetti L., Okamoto I., Servant N., Piolot T., van Berkum N.L., Meisig J., Sedat J., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
35. Palstra R.J., Simonis M., Klous P., Brasset E., Eijkelkamp B., de Laat W. Maintenance of long-range DNA interactions after inhibition of ongoing RNA polymerase II transcription. PLoS One 2008, 3:e1661.
36. Peric-Hupkes D., Meuleman W., Pagie L., Bruggeman S.W., Solovei I., Brugman W., Gräf S., Flicek P., Kerkhoven R.M., van Lohuizen M., et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 2010, 38:603-613.
37. Phillips-Cremins J.E., Sauria M.E., Sanyal A., Gerasimova T.I., Lajoie B.R., Bell J.S., Ong C.T., Hookway T.A., Guo C., Sun Y., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 2013, 153:1281-1295.
38. Rao S.S., Huntley M.H., Durand N.C., Stamenova E.K., Bochkov I.D., Robinson J.T., Sanborn A.L., Machol I., Omer A.D., Lander E.S., Aiden E.L. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 2014, 159:1665-1680.
39. Shen Y., Yue F., McCleary D.F., Ye Z., Edsall L., Kuan S., Wagner U., Dixon J., Lee L., Lobanenkov V.V., Ren B. A map of the cis-regulatory sequences in the mouse genome. Nature 2012, 488:116-120.
40. Simon J.A., Kingston R.E. Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 2009, 10:697-708.
41. Simonis M., Klous P., Splinter E., Moshkin Y., Willemsen R., de Wit E., van Steensel B., de Laat W. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet. 2006, 38:1348-1354.
42. Splinter E., de Wit E., Nora E.P., Klous P., van de Werken H.J., Zhu Y., Kaaij L.J., van Ijcken W., Gribnau J., Heard E., de Laat W. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev. 2011, 25:1371-1383.
43. Splinter E., de Wit E., van de Werken H.J., Klous P., de Laat W. Determining long-range chromatin interactions for selected genomic sites using 4C-seq technology: from fixation to computation. Methods 2012, 58:221-230.
44. Tanay A., Cavalli G. Chromosomal domains: epigenetic contexts and functional implications of genomic compartmentalization. Curr. Opin. Genet. Dev. 2013, 23:197-203.
45. Therizols P., Illingworth R.S., Courilleau C., Boyle S., Wood A.J., Bickmore W.A. Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells. Science 2014, 346:1238-1242.
46. 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.
47. van Koningsbruggen S., Gierlinski M., Schofield P., Martin D., Barton G.J., Ariyurek Y., den Dunnen J.T., Lamond A.I. High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol. Biol. Cell 2010, 21:3735-3748.
48. Vieux-Rochas M., Fabre P.J., Leleu M., Duboule D., Noordermeer D. Clustering of mammalian Hox genes with other H3K27me3 targets within an active nuclear domain. Proc. Natl. Acad. Sci. USA 2015, 112:4672-4677.
49. Wijchers P.J., Geeven G., Eyres M., Bergsma A.J., Janssen M., Verstegen M., Zhu Y., Schell Y., Vermeulen C., de Wit E., de Laat W. Characterization and dynamics of pericentromere-associated domains in mice. Genome Res. 2015, 25:958-969.
50. Williams R.R., Azuara V., Perry P., Sauer S., Dvorkina M., Jørgensen H., Roix J., McQueen P., Misteli T., Merkenschlager M., Fisher A.G. Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J. Cell Sci. 2006, 119:132-140.