Cohesin organizes chromatin loops at DNA replication factories

Genes and Development

Volumn 24, Issue 24, 2010, Pages 2812-2822

  Guillou, Emmanuelle ^a,c   Ibarra, Arkaitz ^a   Coulon, Vincent ^b   Casado Vela, Juan ^a,d   Rico, Daniel ^a   Casal, Ignacio ^a,e   Schwob, Etienne ^b   Losada, Ana ^a   Méndez, Juan ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^c Université Paul Sabatier   (France)

^d CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^e CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Chromatin loop; Cohesin; DNA replication; MCM; Replication origin

Indexed keywords

COHESIN; MINICHROMOSOME MAINTENANCE PROTEIN;

ARTICLE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CHROMATIN LOOP; CHROMATIN STRUCTURE; DNA REPLICATION; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; INTERPHASE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; REPLICON;

CELL CYCLE PROTEINS; CELL LINE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA PACKAGING; DNA REPLICATION; HUMANS; INTERPHASE; REPLICATION ORIGIN; S PHASE;

EID: 78650186593     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.608210     Document Type: Article

References (56)

1. Berezney R, Dubey DD, Huberman JA. 2000. Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108: 471-484.
2. Borlado LR, Mendez J. 2008. CDC6: From DNA replication to cell cycle checkpoints and oncogenesis. Carcinogenesis 29: 237-243.
3. Buongiorno-Nardelli M, Micheli G, Carri MT,Marilley M. 1982. A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature 298: 100-102.
4. Cadoret JC, Meisch F, Hassan-Zadeh V, Luyten I, Guillet C, Duret L, Quesneville H, Prioleau MN. 2008. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci 105: 15837-15842.
5. Casado-Vela J, Martinez-Torrecuadrada JL, Casal JI. 2009. Differential phosphorylation patterns between the Cyclin-A2/ CDK2 complex and their monomers. Protein Expr Purif 66: 15-21.
6. Cayrou C, Coulombe P, Mechali M. 2010. Programming DNA replication origins and chromosome organization. Chromosome Res 18: 137-145.
7. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, Nasmyth K. 2000. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5: 243-254.
8. Courbet S, Gay S, Arnoult N, Wronka G, Anglana M, Brison O, Debatisse M. 2008. Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455: 557-560.
9. Dimitrova DS, Gilbert DM. 1999. The spatial position and replication timing of chromosomal domains are both established in early G1 phase. Mol Cell 4: 983-993.
10. Elcock LS, Bridger JM. 2008. Exploring the effects of a dysfunctional nuclear matrix. Biochem Soc Trans 36: 1378-1383.
11. The ENCODE Project Consortium. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
12. Gause M, Schaaf CA, Dorsett D. 2008. Cohesin and CTCF: Cooperating to control chromosome conformation? Bioessays 30: 715-718.
13. Gillespie PJ, Hirano T. 2004. Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr Biol 14: 1598-1603.
14. Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, Koshland DE, DeRisi JL, Gerton JL. 2004. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol 2: E259. doi: 10.1371/journal.pbio.0020259.
15. Gregson HC, Schmiesing JA, Kim JS, Kobayashi T, Zhou S, Yokomori K. 2001. A potential role for human cohesin in mitotic spindle aster assembly. J Biol Chem 276: 47575-47582.
16. Gruber S, Errington J. 2009. Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137: 685-696.
17. Guacci V, Koshland D, Strunnikov A. 1997. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91: 47-57.
18. Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T, Fraser P, Fisher AG, Merkenschlager M. 2009. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460: 410-413.
19. Hou C, Dale R, Dean A. 2010. Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc Natl Acad Sci 107: 3651-3656.
20. Hozak P, Hassan AB, Jackson DA, Cook PR. 1993. Visualization of replication factories attached to nucleoskeleton. Cell 73: 361-373.
21. Ibarra A, Schwob E, Mendez J. 2008. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci 105: 8956-8961.
22. Jackson DA, Pombo A. 1998. Replicon clusters are stable units of chromosome structure: Evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140: 1285-1295.
23. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, et al. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-405.
24. Karnani N, Taylor C, Malhotra A, Dutta A. 2007. Pan-S replication patterns and chromosomal domains defined by genome-tiling arrays of ENCODE genomic areas. Genome Res 17: 865-876.
25. Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, Kent WJ. 2004. The UCSC Table Browser data retrieval tool. Nucleic Acids Res 32: D493-D496. doi: 10.1093/nar/gkh103.
26. Lemaitre JM, Danis E, Pasero P, Vassetzky Y, Mechali M. 2005. Mitotic remodeling of the replicon and chromosome structure. Cell 123: 787-801.
27. Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F. 2004. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430: 573-578.
28. Losada A, Hirano M, Hirano T. 1998. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev 12: 1986-1997.
29. Losada A, Yokochi T, Kobayashi R, Hirano T. 2000. Identification and characterization of SA/Scc3p subunits in the Xenopus and human cohesin complexes. J Cell Biol 150: 405-416.
30. MacAlpine HK, Gordan R, Powell SK, Hartemink AJ, MacAlpine DM. 2009. Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res 20: 201-211.
31. Mendez J, Stillman B. 2000. Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: Assembly of prereplication complexes in late mitosis. Mol Cell Biol 20: 8602-8612.
32. Mendez J, Stillman B. 2003. Perpetuating the double helix: Molecular machines at eukaryotic DNA replication origins. Bioessays 25: 1158-1167.
33. Michaelis C, Ciosk R, Nasmyth K. 1997. Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell 91: 35-45. (Pubitemid 27431311)
34. Mishiro T, Ishihara K, Hino S, Tsutsumi S, Aburatani H, Shirahige K, Kinoshita Y, Nakao M. 2009. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J 28: 1234-1245.
35. Misteli T. 2007. Beyond the sequence: Cellular organization of genome function. Cell 128: 787-800.
36. Nasmyth K, Haering CH. 2009. Cohesin: Its roles and mechanisms. Annu Rev Genet 43: 525-558.
37. Nativio R, Wendt KS, Ito Y, Huddleston JE, Uribe-Lewis S, Woodfine K, Krueger C, Reik W, Peters JM, Murrell A. 2009. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet 5: e1000739. doi: 10.1371/journal.pgen.1000739.
38. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, et al. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132: 422-433.
39. Peters JM, Tedeschi A, Schmitz J. 2008. The cohesin complex and its roles in chromosome biology. Genes Dev 22: 3089-3114.
40. Phillips JE, Corces VG. 2009. CTCF: Master weaver of the genome. Cell 137: 1194-1211.
41. Ryu MJ, Kim BJ, Lee JW, Lee MW, Choi HK, Kim ST. 2006. Direct interaction between cohesin complex and DNA replication machinery. Biochem Biophys Res Commun 341: 770-775.
42. Sadano H, Sugimoto H, Sakai F, Nomura N, Osumi T. 2000. NXP-1, a human protein related to Rad21/Scc1/Mcd1, is a component of the nuclear matrix. Biochem Biophys Res Commun 267: 418-422.
43. Salic A, Mitchison TJ. 2008. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci 105: 2415-2420.
44. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD, Carroll JS, Flicek P, Odom DT. 2010. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20: 578-588.
45. Schmitz J, Watrin E, Lenart P, Mechtler K, Peters JM. 2007. Sororin is required for stable binding of cohesin to chromatin and for sister chromatid cohesion in interphase. Curr Biol 17: 630-636.
46. Schwob E, de Renty C, Coulon V, Gostan T, Boyer C, Camet-Gabut L, Amato C. 2009. Use of DNA combing for studying DNA replication in vivo in yeast and mammalian cells. Methods Mol Biol 521: 673-687.
47. Sclafani RA, Holzen TM. 2007. Cell cycle regulation of DNA replication. Annu Rev Genet 41: 237-280.
48. Sjögren C, Ström L. 2010. S-phase and DNA damage activated establishment of sister chromatid cohesion: Importance for DNA repair. Exp Cell Res 316: 1445-1453.
49. Smits VA, Warmerdam DO, Martin Y, Freire R. 2010. Mechanisms of ATR-mediated checkpoint signalling. Front Biosci 15: 840-853.
50. Takahashi TS, Yiu P, Chou MF, Gygi S, Walter JC. 2004. Recruitment of Xenopus Scc2 and cohesin to chromatin requires the pre-replication complex. Nat Cell Biol 6: 991-996.
51. Takahashi TS, Wigley DB, Walter JC. 2005. Pumps, paradoxes and ploughshares: Mechanism of the MCM2-7 DNA helicase. Trends Biochem Sci 30: 437-444.
52. Terret ME, Sherwood R, Rahman S, Qin J, Jallepalli PV. 2009. Cohesin acetylation speeds the replication fork. Nature 462: 231-234.
53. Uhlmann F, Nasmyth K. 1998. Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8: 1095-1101.
54. Vogelstein B, Pardoll DM, Coffey DS. 1980. Supercoiled loops and eucaryotic DNA replication. Cell 22: 79-85. (Pubitemid 11226430)
55. Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, Peters JM. 2006. Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr Biol 16: 863-874.
56. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, et al. 2008. Cohesin mediates transcriptional insulation by CCCTCbinding factor. Nature 451: 796-801.