Formation of Chromosomal Domains by Loop Extrusion

Cell Reports

Volumn 15, Issue 9, 2016, Pages 2038-2049

  Fudenberg, Geoffrey ^a,b   Imakaev, Maxim ^c   Lu, Carolyn ^c   Goloborodko, Anton ^c   Abdennur, Nezar ^c   Mirny, Leonid A ^a,b,c  

^a HARVARD UNIVERSITY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; CONDENSIN; TRANSCRIPTION FACTOR CTCF; CELL CYCLE PROTEIN; NONHISTONE PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL DENSITY; CHROMATIN CONDENSATION; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; GENETIC DISTANCE; HUMAN; HUMAN CELL; INTERPHASE; PRIORITY JOURNAL; PROPHASE; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN LOCALIZATION; CHEMISTRY; CHROMOSOME; CONFORMATION; GENE DELETION; GENETICS; INSULATOR ELEMENT; METABOLISM; MOLECULAR MODEL;

CCCTC-BINDING FACTOR; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; INSULATOR ELEMENTS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; SEQUENCE DELETION;

EID: 84971324235     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.04.085     Document Type: Article

References (72)

1. Alipour E., Marko J.F. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res. 2012, 40:11202-11212.
2. Alt F.W., Zhang Y., Meng F.-L., Guo C., Schwer B. Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 2013, 152:417-429.
3. Andrey G., Montavon T., Mascrez B., Gonzalez F., Noordermeer D., Leleu M., Trono D., Spitz F., Duboule D. A switch between topological domains underlies HoxD genes collinearity in mouse limbs. Science 2013, 340:1234167.
4. Barbieri M., Chotalia M., Fraser J., Lavitas L.-M., Dostie J., Pombo A., Nicodemi M. Complexity of chromatin folding is captured by the strings and binders switch model. Proc. Natl. Acad. Sci. USA 2012, 109:16173-16178.
5. Baù D., Sanyal A., Lajoie B.R., Capriotti E., Byron M., Lawrence J.B., Dekker J., Marti-Renom M.A. The three-dimensional folding of the α-globin gene domain reveals formation of chromatin globules. Nat. Struct. Mol. Biol. 2011, 18:107-114.
6. Benedetti F., Dorier J., Burnier Y., Stasiak A. Models that include supercoiling of topological domains reproduce several known features of interphase chromosomes. Nucleic Acids Res. 2014, 42:2848-2855.
7. Boettiger A.N., Bintu B., Moffitt J.R., Wang S., Beliveau B.J., Fudenberg G., Imakaev M., Mirny L.A., Wu C., Zhuang X. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 2016, 529:418-422.
8. Bohn M., Heermann D.W. Diffusion-driven looping provides a consistent framework for chromatin organization. PLoS ONE 2010, 5:e12218.
9. Brackley C.A., Johnson J., Kelly S., Cook P.R., Marenduzzo D. Binding of bivalent transcription factors to active and inactive regions folds human chromosomes into loops, rosettes and domains. arXiv 2015, arXiv: 1511.01848. http://arxiv.org/abs/1511.01848.
10. de Wit E., Vos E.S.M., Holwerda S.J.B., Valdes-Quezada C., Verstegen M.J.A.M., Teunissen H., Splinter E., Wijchers P.J., Krijger P.H.L., de Laat W. CTCF binding polarity determines chromatin looping. Mol. Cell 2015, 60:676-684.
11. Degner S.C., Verma-Gaur J., Wong T.P., Bossen C., Iverson G.M., Torkamani A., Vettermann C., Lin Y.C., Ju Z., Schulz D., et al. CCCTC-binding factor (CTCF) and cohesin influence the genomic architecture of the Igh locus and antisense transcription in pro-B cells. Proc. Natl. Acad. Sci. USA 2011, 108:9566-9571.
12. 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.
13. Dong J., Panchakshari R.A., Zhang T., Zhang Y., Hu J., Volpi S.A., Meyers R.M., Ho Y.-J., Du Z., Robbiani D.F., et al. Orientation-specific joining of AID-initiated DNA breaks promotes antibody class switching. Nature 2015, 525:134-139.
14. Doyle B., Fudenberg G., Imakaev M., Mirny L.A. Chromatin loops as allosteric modulators of enhancer-promoter interactions. PLoS Comput. Biol. 2014, 10:e1003867.
15. Eastman P., Pande V. OpenMM: a hardware-independent framework for molecular simulations. Comput. Sci. Eng. 2010, 12:34-39.
16. Eastman P., Friedrichs M.S., Chodera J.D., Radmer R.J., Bruns C.M., Ku J.P., Beauchamp K.A., Lane T.J., Wang L.P., Shukla D., et al. OpenMM 4: a reusable, extensible, hardware independent library for high performance molecular simulation. J. Chem. Theory Comput. 2013, 9:461-469.
17. Gerlich D., Koch B., Dupeux F., Peters J.-M., Ellenberg J. Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Curr. Biol. 2006, 16:1571-1578.
18. Gibcus J.H., Dekker J. The hierarchy of the 3D genome. Mol. Cell 2013, 49:773-782.
19. Giorgetti L., Galupa R., Nora E.P., Piolot T., Lam F., Dekker J., Tiana G., Heard E. Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell 2014, 157:950-963.
20. Goloborodko A., Marko J.F., Mirny L. Chromosome compaction via active loop extrusion. Biophys J. 2015, 110:2162-2168.
21. Goloborodko A.A., Imakaev M., Marko J., Mirny L. Compaction and segregation of sister chromatids via active loop extrusion. eLife 2016, 10.7554/eLife.14864.
22. Gorkin D.U., Leung D., Ren B. The 3D genome in transcriptional regulation and pluripotency. Cell Stem Cell 2014, 14:762-775.
23. Gruber S. Multilayer chromosome organization through DNA bending, bridging and extrusion. Curr. Opin. Microbiol. 2014, 22:102-110.
24. Guacci V., Yamamoto A., Strunnikov A., Kingsbury J., Hogan E., Meluh P., Koshland D. Structure and function of chromosomes in mitosis of budding yeast. Cold Spring Harb. Symp. Quant. Biol. 1993, 58:677-685.
25. Guo Y., Xu Q., Canzio D., Shou J., Li J., Gorkin D.U., Jung I., Wu H., Zhai Y., Tang Y., et al. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 2015, 162:900-910.
26. Hara K., Zheng G., Qu Q., Liu H., Ouyang Z., Chen Z., Tomchick D.R., Yu H. Structure of cohesin subcomplex pinpoints direct shugoshin-Wapl antagonism in centromeric cohesion. Nat. Struct. Mol. Biol. 2014, 21:864-870.
27. Hofmann A., Heermann D.W. The role of loops on the order of eukaryotes and prokaryotes. FEBS Lett. 2015, 589(20 Pt A):2958-2965.
28. Hou C., Zhao H., Tanimoto K., Dean A. CTCF-dependent enhancer-blocking by alternative chromatin loop formation. Proc. Natl. Acad. Sci. USA 2008, 105:20398-20403.
29. Imakaev M., Fudenberg G., McCord R.P., Naumova N., Goloborodko A., Lajoie B.R., Dekker J., Mirny L.A. Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat. Methods 2012, 9:999-1003.
30. Imakaev M.V., Fudenberg G., Mirny L.A. Modeling chromosomes: Beyond pretty pictures. FEBS Lett. 2015, 589(20 Pt A):3031-3036.
31. Jost D., Carrivain P., Cavalli G., Vaillant C. Modeling epigenome folding: formation and dynamics of topologically associated chromatin domains. Nucleic Acids Res. 2014, 42:9553-9561.
32. Kadauke S., Blobel G.A. Mitotic bookmarking by transcription factors. Epigenetics Chromatin 2013, 6:6.
33. Kagey M.H., Newman J.J., Bilodeau S., Zhan Y., Orlando D.A., van Berkum N.L., Ebmeier C.C., Goossens J., Rahl P.B., Levine S.S., et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 2010, 467:430-435.
34. Kheradpour P., Kellis M. Systematic discovery and characterization of regulatory motifs in ENCODE TF binding experiments. Nucleic Acids Res. 2014, 42:2976-2987.
35. Kind J., Pagie L., de Vries S.S., Nahidiazar L., Dey S.S., Bienko M., Zhan Y., Lajoie B., de Graaf C.A., Amendola M., Fudenberg G., Imakaev M., Mirny L.A., Jalink K., Dekker J., van Oudenaarden A., van Steensel B. Genome-wide maps of nuclear lamina interactions in single human cells. Cell 2015, 163:134-147.
36. Lajoie B.R., Dekker J., Kaplan N. The hitchhiker's guide to Hi-C analysis: practical guidelines. Methods 2015, 72:65-75.
37. Le T.B.K., Imakaev M.V., Mirny L.A., Laub M.T. High-resolution mapping of the spatial organization of a bacterial chromosome. Science 2013, 342:731-734.
38. 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.
39. Lin S.G., Guo C., Su A., Zhang Y., Alt F.W. CTCF-binding elements 1 and 2 in the Igh intergenic control region cooperatively regulate V(D)J recombination. Proc. Natl. Acad. Sci. USA 2015, 112:1815-1820.
40. Lupiáñez D.G., Kraft K., Heinrich V., Krawitz P., Brancati F., Klopocki E., Horn D., Kayserili H., Opitz J.M., Laxova R., et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 2015, 161:1012-1025.
41. Marko J.F., Siggia E.D. Polymer models of meiotic and mitotic chromosomes. Mol. Biol. Cell 1997, 8:2217-2231.
42. Mizuguchi T., Fudenberg G., Mehta S., Belton J.-M., Taneja N., Folco H.D., FitzGerald P., Dekker J., Mirny L., Barrowman J., Grewal S.I. Cohesin-dependent globules and heterochromatin shape 3D genome architecture in S. pombe. Nature 2014, 516:432-435.
43. Nakahashi H., Kwon K.R., Resch W., Vian L., Dose M., Stavreva D., Hakim O., Pruett N., Nelson S., Yamane A., et al. A genome-wide map of CTCF multivalency redefines the CTCF code. Cell Rep. 2013, 3:1678-1689.
44. Narendra V., Rocha P.P., An D., Raviram R., Skok J.A., Mazzoni E.O., Reinberg D. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 2015, 347:1017-1021.
45. Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 2001, 35:673-745.
46. Naughton C., Avlonitis N., Corless S., Prendergast J.G., Mati I.K., Eijk P.P., Cockroft S.L., Bradley M., Ylstra B., Gilbert N. Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures. Nat. Struct. Mol. Biol. 2013, 20:387-395.
47. Naumova N., Imakaev M., Fudenberg G., Zhan Y., Lajoie B.R., Mirny L.A., Dekker J. Organization of the mitotic chromosome. Science 2013, 342:948-953.
48. Nichols M.H., Corces V.G. A CTCF code for 3D genome architecture. Cell 2015, 162:703-705.
49. Nishiyama T., Ladurner R., Schmitz J., Kreidl E., Schleiffer A., Bhaskara V., Bando M., Shirahige K., Hyman A.A., Mechtler K., Peters J.M. Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 2010, 143:737-749.
50. Nolen L.D., Boyle S., Ansari M., Pritchard E., Bickmore W.A. Regional chromatin decompaction in Cornelia de Lange syndrome associated with NIPBL disruption can be uncoupled from cohesin and CTCF. Hum. Mol. Genet. 2013, 22:4180-4193.
51. 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.
52. Parelho V., Hadjur S., Spivakov M., Leleu M., Sauer S., Gregson H.C., Jarmuz A., Canzonetta C., Webster Z., Nesterova T., et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008, 132:422-433.
53. Peterson C.L. The SMC family: novel motor proteins for chromosome condensation?. Cell 1994, 79:389-392.
54. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
55. Rao S.S.P., 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.
56. Rosa A., Everaers R. Structure and dynamics of interphase chromosomes. PLoS Comput. Biol. 2008, 4:e1000153.
57. Rosa A., Becker N.B., Everaers R. Looping probabilities in model interphase chromosomes. Biophys. J. 2010, 98:2410-2419.
58. Sanborn A.L., Rao S.S.P., Huang S.-C., Durand N.C., Huntley M.H., Jewett A.I., Bochkov I.D., Chinnappan D., Cutkosky A., Li J., et al. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc. Natl. Acad. Sci. USA 2015, 112:E6456-E6465.
59. Scolari V.F., Cosentino Lagomarsino M. Combined collapse by bridging and self-adhesion in a prototypical polymer model inspired by the bacterial nucleoid. Soft Matter 2015, 11:1677-1687.
60. 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.
61. Stigler J., Çamdere G.Ö., Koshland D.E., Greene E.C. Single-molecule imaging reveals a collapsed conformational state for DNA-bound cohesin. Cell Rep. 2016, 15:988-998.
62. Sofueva S., Yaffe E., Chan W.-C., Georgopoulou D., Vietri Rudan M., Mira-Bontenbal H., Pollard S.M., Schroth G.P., Tanay A., Hadjur S. Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J. 2013, 32:3119-3129.
63. Symmons O., Uslu V.V., Tsujimura T., Ruf S., Nassari S., Schwarzer W., Ettwiller L., Spitz F. Functional and topological characteristics of mammalian regulatory domains. Genome Res. 2014, 24:390-400.
64. Tedeschi A., Wutz G., Huet S., Jaritz M., Wuensche A., Schirghuber E., Davidson I.F., Tang W., Cisneros D.A., Bhaskara V., et al. Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 2013, 501:564-568.
65. Ulianov S.V., Khrameeva E.E., Gavrilov A.A., Flyamer I.M., Kos P., Mikhaleva E.A., Penin A.A., Logacheva M.D., Imakaev M.V., Chertovich A., et al. Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains. Genome Res. 2016, 26:70-84.
66. Van Bortle K., Nichols M.H., Li L., Ong C.-T., Takenaka N., Qin Z.S., Corces V.G. Insulator function and topological domain border strength scale with architectural protein occupancy. Genome Biol. 2014, 15:R82.
67. Vietri Rudan M., Barrington C., Henderson S., Ernst C., Odom D.T., Tanay A., Hadjur S. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 2015, 10:1297-1309.
68. Wang X., Le T.B.K., Lajoie B.R., Dekker J., Laub M.T., Rudner D.Z. Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis. Genes Dev. 2015, 29:1661-1675.
69. Williamson I., Berlivet S., Eskeland R., Boyle S., Illingworth R.S., Paquette D., Dostie J., Bickmore W.A. Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev. 2014, 28:2778-2791.
70. Xiao T., Wallace J., Felsenfeld G. Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Mol. Cell. Biol. 2011, 31:2174-2183.
71. Yaffe E., Tanay A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet. 2011, 43:1059-1065.
72. Zuin J., Dixon J.R., van der Reijden M.I.J., Ye Z., Kolovos P., Brouwer R.W., van de Corput M.P., van de Werken H.J., Knoch T.A., van IJcken W.F., et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc. Natl. Acad. Sci. USA 2014, 111:996-1001.