Scc2/Nipbl hops between chromosomal cohesin rings after loading

eLife

Volumn 6, Issue , 2017, Pages

  Rhodes, James ^a   Mazza, Davide ^b,c   Nasmyth, Kim ^a   Uphoff, Stephan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c CEN European Centre for Nanomedicine   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; COHESIN; CELL CYCLE PROTEIN; NIPBL PROTEIN, HUMAN; NONHISTONE PROTEIN; PROTEIN;

ARTICLE; CONFOCAL MICROSCOPY; DNA REPLICATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE TEST; MOTOR ACTIVITY; NONHUMAN; SISTER CHROMATID EXCHANGE; CELL LINE; CHROMATIN; FLUORESCENCE IMAGING; METABOLISM; SINGLE MOLECULE IMAGING;

CELL CYCLE PROTEINS; CELL LINE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; HUMANS; MICROSCOPY, CONFOCAL; OPTICAL IMAGING; PROTEINS; SINGLE MOLECULE IMAGING;

EID: 85032984817     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.30000     Document Type: Article

References (65)

1. Alipour E, Marko JF. 2012. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Research 40:11202-11212. DOI: https://doi.org/10.1093/nar/gks925, PMID: 23074191
2. Arumugam P, Gruber S, Tanaka K, Haering CH, Mechtler K, Nasmyth K. 2003. ATP hydrolysis is required for cohesin’s association with chromosomes. Current Biology 13:1941-1953. DOI: https://doi.org/10.1016/j.cub. 2003.10.036, PMID: 14614819
3. Borck G, Zarhrate M, Cluzeau C, Bal E, Bonnefont JP, Munnich A, Cormier-Daire V, Colleaux L. 2006. Father-to-daughter transmission of Cornelia de Lange syndrome caused by a mutation in the 5’ untranslated region of the NIPBL Gene. Human Mutation 27:731-735. DOI: https://doi.org/10.1002/humu.20380, PMID: 16799922
4. Boyle MI, Jespersgaard C, Nazaryan L, Bisgaard AM, Tümer Z. 2017. A novel RAD21 variant associated with intrafamilial phenotypic variation in Cornelia de Lange syndrome-review of the literature. Clinical Genetics 91: 647-649. DOI: https://doi.org/10.1111/cge.12863, PMID: 27882533
5. Bulger M, Groudine M. 2010. Enhancers: the abundance and function of regulatory sequences beyond promoters. Developmental Biology 339:250-257. DOI: https://doi.org/10.1016/j.ydbio.2009.11.035, PMID: 20025863
6. Busslinger GA, Stocsits RR, van der Lelij P, Axelsson E, Tedeschi A, Galjart N, Peters JM. 2017. Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl. Nature 544:410-507. DOI: https://doi. org/10.1038/nature22063, PMID: 28424523
7. Chan KL, Roig MB, Hu B, Beckouët F, Metson J, Nasmyth K. 2012. Cohesin’s DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell 150:961-974. DOI: https://doi.org/10.1016/j.cell.2012.07. 028, PMID: 22901742
8. Chien R, Zeng W, Kawauchi S, Bender MA, Santos R, Gregson HC, Schmiesing JA, Newkirk DA, Kong X, Ball AR, Calof AL, Lander AD, Groudine MT, Yokomori K. 2011. Cohesin mediates chromatin interactions that regulate mammalian b-globin expression. Journal of Biological Chemistry 286:17870-17878. DOI: https://doi.org/10. 1074/jbc.M110.207365, PMID: 21454523
9. 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. Molecular Cell 5:243-254. DOI: https://doi.org/10.1016/S1097-2765(00)80420-7, PMID: 10882066
10. Davidson IF, Goetz D, Zaczek MP, Molodtsov MI, Huis Int Veld PJ, Weissmann F, Litos G, Cisneros DA, Ocampo-Hafalla M, Ladurner R, Uhlmann F, Vaziri A, Peters JM. 2016. Rapid movement and transcriptional re-localization of human cohesin on DNA. The EMBO Journal 35:2671-2685. DOI: https://doi.org/10.15252/embj. 201695402, PMID: 27799150
11. Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, Minamino M, Saitoh K, Komata M, Katou Y, Clark D, Cole KE, De Baere E, Decroos C, Di Donato N, Ernst S, Francey LJ, Gyftodimou Y, Hirashima K, Hullings M, Ishikawa Y, et al. 2012. HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature 489:313-317. DOI: https://doi.org/10.1038/nature11316, PMID: 22885700
12. Fournier M, Bourriquen G, Lamaze FC, Côté MC, Fournier É, Joly-Beauparlant C, Caron V, Gobeil S, Droit A, Bilodeau S. 2016. FOXA and master transcription factors recruit Mediator and Cohesin to the core transcriptional regulatory circuitry of cancer cells. Scientific Reports 6:34962. DOI: https://doi.org/10.1038/srep34962, PMID: 27739523
13. Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. 2016. Formation of Chromosomal Domains by Loop Extrusion. Cell Reports 15:2038-2049. DOI: https://doi.org/10.1016/j.celrep.2016.04.085, PMID: 27210764
14. Gerlich D, Koch B, Dupeux F, Peters JM, Ellenberg J. 2006. Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Current Biology 16:1571-1578. DOI: https://doi.org/10.1016/j.cub.2006.06.068, PMID: 16890534
15. Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z, Revyakin A, Patel R, Macklin JJ, Normanno D, Singer RH, Lionnet T, Lavis LD. 2015. A general method to improve fluorophores for live-cell and single-molecule microscopy. Nature Methods 12:244-250. DOI: https://doi.org/10.1038/nmeth.3256, PMID: 25599551
16. Gruber S, Haering CH, Nasmyth K. 2003. Chromosomal cohesin forms a ring. Cell 112:765-777. DOI: https://doi. org/10.1016/S0092-8674(03)00162-4, PMID: 12654244
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. DOI: https://doi.org/10. 1016/S0092-8674(01)80008-8, PMID: 9335334
18. Haarhuis JHI, van der Weide RH, Blomen VA, Yáñez-Cuna JO, Amendola M, van Ruiten MS, Krijger PHL, Teunissen H, Medema RH, van Steensel B, Brummelkamp TR, de Wit E, Rowland BD. 2017. The cohesin release factor wapl restricts chromatin loop extension. Cell 169:693-707. DOI: https://doi.org/10.1016/j.cell.2017.04. 013, PMID: 28475897
19. Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K. 2008. The cohesin ring concatenates sister DNA molecules. Nature 454:297-301. DOI: https://doi.org/10.1038/nature07098, PMID: 18596691
20. Haering CH, Löwe J, Hochwagen A, Nasmyth K. 2002. Molecular architecture of SMC proteins and the yeast cohesin complex. Molecular Cell 9:773-788. DOI: https://doi.org/10.1016/S1097-2765(02)00515-4, PMID: 11 983169
21. Hansen AS, Pustova I, Cattoglio C, Tjian R, Darzacq X. 2017. CTCF and cohesin regulate chromatin loop stability with distinct dynamics. eLife 6:2848. DOI: https://doi.org/10.7554/eLife.25776, PMID: 28467304
22. Hu B, Itoh T, Mishra A, Katoh Y, Chan KL, Upcher W, Godlee C, Roig MB, Shirahige K, Nasmyth K. 2011. ATP hydrolysis is required for relocating cohesin from sites occupied by its Scc2/4 loading complex. Current Biology 21:12-24. DOI: https://doi.org/10.1016/j.cub.2010.12.004, PMID: 21185190
23. Hu B, Petela N, Kurze A, Chan KL, Chapard C, Nasmyth K. 2015. Biological chromodynamics: a general method for measuring protein occupancy across the genome by calibrating ChIP-seq. Nucleic Acids Research 43:e132. DOI: https://doi.org/10.1093/nar/gkv670, PMID: 26130708
24. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467:430-435. DOI: https://doi.org/10.1038/nature09380, PMID: 20720539
25. Kanke M, Tahara E, Huis Int Veld PJ, Nishiyama T. 2016. Cohesin acetylation and Wapl-Pds5 oppositely regulate translocation of cohesin along DNA. The EMBO Journal 35:2686-2698. DOI: https://doi.org/10.15252/embj. 201695756, PMID: 27872142
26. Kawauchi S, Calof AL, Santos R, Lopez-Burks ME, Young CM, Hoang MP, Chua A, Lao T, Lechner MS, Daniel JA, Nussenzweig A, Kitzes L, Yokomori K, Hallgrimsson B, Lander AD. 2009. Multiple organ system defects and transcriptional dysregulation in the Nipbl(+/-) mouse, a model of Cornelia de Lange Syndrome. PLoS Genetics 5:e1000650. DOI: https://doi.org/10.1371/journal.pgen.1000650, PMID: 19763162
27. Kikuchi S, Borek DM, Otwinowski Z, Tomchick DR, Yu H. 2016. Crystal structure of the cohesin loader Scc2 and insight into cohesinopathy. PNAS 113:12444-12449. DOI: https://doi.org/10.1073/pnas.1611333113, PMID: 27791135
28. Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, Mechtler K, Peters JM. 2006. Wapl controls the dynamic association of cohesin with chromatin. Cell 127:955-967. DOI: https://doi.org/10.1016/j.cell.2006.09.040, PMID: 17113138
29. Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, Chen Y, DeSalvo G, Epstein C, Fisher-Aylor KI, Euskirchen G, Gerstein M, Gertz J, Hartemink AJ, Hoffman MM, Iyer VR, et al. 2012. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Research 22:1813-1831. DOI: https://doi.org/10.1101/gr.136184.111, PMID: 22955991
30. 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. DOI: https://doi.org/10.1038/nature02742, PMID: 15229615
31. Liu Z, Legant WR, Chen BC, Li L, Grimm JB, Lavis LD, Betzig E, Tjian R. 2014. 3D imaging of Sox2 enhancer clusters in embryonic stem cells. eLife 3:e04236. DOI: https://doi.org/10.7554/eLife.04236, PMID: 25537195
32. Losada A, Hirano M, Hirano T. 1998. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes & Development 12:1986-1997. DOI: https://doi.org/10.1101/gad.12.13.1986, PMID: 9649503
33. Mazza D, Abernathy A, Golob N, Morisaki T, McNally JG. 2012. A benchmark for chromatin binding measurements in live cells. Nucleic Acids Research 40:e119. DOI: https://doi.org/10.1093/nar/gks701, PMID: 22844090
34. Michaelis C, Ciosk R, Nasmyth K. 1997. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91:35-45. DOI: https://doi.org/10.1016/S0092-8674(01)80007-6, PMID: 9335333
35. Misteli T, Gunjan A, Hock R, Bustin M, Brown DT. 2000. Dynamic binding of histone H1 to chromatin in living cells. Nature 408:877-881. DOI: https://doi.org/10.1038/35048610, PMID: 11130729
36. Mueller F, Wach P, McNally JG. 2008. Evidence for a common mode of transcription factor interaction with chromatin as revealed by improved quantitative fluorescence recovery after photobleaching. Biophysical Journal 94:3323-3339. DOI: https://doi.org/10.1529/biophysj.107.123182, PMID: 18199661
37. Murayama Y, Uhlmann F. 2014. Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature 505:367-371. DOI: https://doi.org/10.1038/nature12867, PMID: 24291789
38. Nasmyth K. 2001. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annual Review of Genetics 35:673-745. DOI: https://doi.org/10.1146/annurev.genet.35.102401. 091334, PMID: 11700297
39. Natsume T, Kiyomitsu T, Saga Y, Kanemaki MT. 2016. Rapid protein depletion in human cells by auxin-inducible degron tagging with short homology donors. Cell Reports 15:210-218. DOI: https://doi.org/10.1016/j.celrep. 2016.03.001, PMID: 27052166
40. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, Gribnau J, Barillot E, Blüthgen N, Dekker J, Heard E. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381-385. DOI: https://doi.org/10.1038/nature11049, PMID: 22495304
41. Ouyang Z, Zheng G, Song J, Borek DM, Otwinowski Z, Brautigam CA, Tomchick DR, Rankin S, Yu H. 2013. Structure of the human cohesin inhibitor Wapl. PNAS 110:11355-11360. DOI: https://doi.org/10.1073/pnas. 1304594110, PMID: 23776203
42. Poser I, Sarov M, Hutchins JR, Hériché JK, Toyoda Y, Pozniakovsky A, Weigl D, Nitzsche A, Hegemann B, Bird AW, Pelletier L, Kittler R, Hua S, Naumann R, Augsburg M, Sykora MM, Hofemeister H, Zhang Y, Nasmyth K, White KP, et al. 2008. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nature Methods 5:409-415. DOI: https://doi.org/10.1038/nmeth.1199, PMID: 18391959
43. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nature Protocols 8:2281-2308. DOI: https://doi.org/10.1038/nprot.2013.143, PMID: 24157548
44. Remeseiro S, Cuadrado A, Kawauchi S, Calof AL, Lander AD, Losada A. 2013. Reduction of Nipbl impairs cohesin loading locally and affects transcription but not cohesion-dependent functions in a mouse model of Cornelia de Lange Syndrome. Biochimica Et Biophysica Acta (BBA)-Molecular Basis of Disease 1832:2097-2102. DOI: https://doi.org/10.1016/j.bbadis.2013.07.020
45. Revenkova E, Focarelli ML, Susani L, Paulis M, Bassi MT, Mannini L, Frattini A, Delia D, Krantz I, Vezzoni P, Jessberger R, Musio A. 2009. Cornelia de Lange syndrome mutations in SMC1A or SMC3 affect binding to DNA. Human Molecular Genetics 18:418-427. DOI: https://doi.org/10.1093/hmg/ddn369, PMID: 18996922
46. Rhodes JDP, Haarhuis JHI, Grimm JB, Rowland BD, Lavis LD, Nasmyth KA. 2017. Cohesin Can Remain Associated with Chromosomes during DNA Replication. Cell Reports 20:2749-2755. DOI: https://doi.org/10. 1016/j.celrep.2017.08.092, PMID: 28930671
47. Rohatgi S, Clark D, Kline AD, Jackson LG, Pie J, Siu V, Ramos FJ, Krantz ID, Deardorff MA. 2010. Facial diagnosis of mild and variant CdLS: Insights from a dysmorphologist survey. American Journal of Medical Genetics Part A 152A:1641-1653. DOI: https://doi.org/10.1002/ajmg.a.33441, PMID: 20583156
48. Rollins RA, Morcillo P, Dorsett D. 1999. Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 152:577-593. PMID: 10353901
49. Sanborn AL, Rao SS, Huang SC, Durand NC, Huntley MH, Jewett AI, Bochkov ID, Chinnappan D, Cutkosky A, Li J, Geeting KP, Gnirke A, Melnikov A, McKenna D, Stamenova EK, Lander ES, Aiden EL. 2015. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. PNAS 112:E6456-E6465. DOI: https://doi.org/10.1073/pnas.1518552112, PMID: 26499245
50. Sekiya T, Muthurajan UM, Luger K, Tulin AV, Zaret KS. 2009. Nucleosome-binding affinity as a primary determinant of the nuclear mobility of the pioneer transcription factor FoxA. Genes & Development 23:804-809. DOI: https://doi.org/10.1101/gad.1775509, PMID: 19339686
51. Stewart-Ornstein J, Lahav G. 2016. Dynamics of cdkn1a in single cells defined by an endogenous fluorescent tagging toolkit. Cell Reports 14:1800-1811. DOI: https://doi.org/10.1016/j.celrep.2016.01.045, PMID: 26 876176
52. Stigler J, Çamdere GÖ, Koshland DE, Greene EC. 2016. Single-molecule imaging reveals a collapsed conformational state for dna-bound cohesin. Cell Reports 15:988-998. DOI: https://doi.org/10.1016/j.celrep. 2016.04.003, PMID: 27117417
53. Tedeschi A, Wutz G, Huet S, Jaritz M, Wuensche A, Schirghuber E, Davidson IF, Tang W, Cisneros DA, Bhaskara V, Nishiyama T, Vaziri A, Wutz A, Ellenberg J, Peters JM. 2013. Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 501:564-568. DOI: https://doi.org/10.1038/nature12471, PMID: 23975099
54. Terakawa T, Bisht S, Eeftens JM, Dekker C, Haering CH, Greene EC. 2017. The condensin complex is a mechanochemical motor that translocates along DNA. Science 11:eaan6516. DOI: https://doi.org/10.1126/science.aan6516
55. Teves SS, An L, Hansen AS, Xie L, Darzacq X, Tjian R. 2016. A dynamic mode of mitotic bookmarking by transcription factors. eLife 5:e22280. DOI: https://doi.org/10.7554/eLife.22280, PMID: 27855781
56. Tóth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A, Nasmyth K. 1999. Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes & Development 13:320-333. DOI: https://doi.org/10.1101/gad.13.3.320, PMID: 9990856
57. Uphoff S, Reyes-Lamothe R, Garza de Leon F, Sherratt DJ, Kapanidis AN. 2013. Single-molecule DNA repair in live bacteria. PNAS 110:8063-8068. DOI: https://doi.org/10.1073/pnas.1301804110, PMID: 23630273
58. Uphoff S, Sherratt DJ, Kapanidis AN. 2014. Visualizing protein-DNA interactions in live bacterial cells using photoactivated single-molecule tracking. Journal of Visualized Experiments 85:e51177.
59. van den Berg DL, Azzarelli R, Oishi K, Martynoga B, Urbán N, Dekkers DH, Demmers JA, Guillemot F. 2017. Nipbl interacts with zfp609 and the integrator complex to regulate cortical neuron migration. Neuron 93:348-361. DOI: https://doi.org/10.1016/j.neuron.2016.11.047, PMID: 28041881
60. Wang X, Brandäo HB, Le TB, Laub MT, Rudner DZ. 2017. Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus. Science 355:524-527. DOI: https://doi.org/10.1126/science.aai8982, PMID: 28154080
61. 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. Current Biology 16:863-874. DOI: https://doi.org/10.1016/j.cub.2006.03.049, PMID: 16682347
62. Wegel E, Göhler A, Lagerholm BC, Wainman A, Uphoff S, Kaufmann R, Dobbie IM. 2016. Imaging cellular structures in super-resolution with SIM, STED and Localisation Microscopy: A practical comparison. Scientific Reports 6:27290. DOI: https://doi.org/10.1038/srep27290, PMID: 27264341
63. Wells JN, Gligoris TG, Nasmyth KA, Marsh JA. 2017. Evolution of condensin and cohesin complexes driven by replacement of Kite by Hawk proteins. Current Biology 27:R17-R18. DOI: https://doi.org/10.1016/j.cub.2016. 11.050, PMID: 28073014
64. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796-801. DOI: https://doi.org/10. 1038/nature06634, PMID: 18235444
65. Zuin J, Franke V, van Ijcken WF, van der Sloot A, Krantz ID, van der Reijden MI, Nakato R, Lenhard B, Wendt KS. 2014. A cohesin-independent role for NIPBL at promoters provides insights in CdLS. PLoS Genetics 10: e1004153. DOI: https://doi.org/10.1371/journal.pgen.1004153, PMID: 24550742