1,200
Views
0
CrossRef citations to date
0
Altmetric
Eukaryotic Cells

Transcription-Driven Translocation of Cohesive and Non-Cohesive Cohesin In Vivo

, & ORCID Icon
Pages 254-268 | Received 03 Jan 2023, Accepted 28 Mar 2023, Published online: 13 May 2023

REFERENCES

  • Davidson IF, Peters J-M. Genome folding through loop extrusion by SMC complexes. Nat Rev Mol Cell Biol. 2021;22:445–464. doi:10.1038/s41580-021-00349-7.
  • Remeseiro S, Cuadrado A, Losada A. Cohesin in development and disease. Development. 2013;140:3715–3718. doi:10.1242/dev.090605.
  • Gligoris TG, Scheinost JC, Burmann F, Petela N, Chan KL, Uluocak P, Beckouët F, Gruber S, Nasmyth K, Löwe J. Closing the cohesin ring: structure and function of its Smc3-kleisin interface. Science. 2014;346:963–967. doi:10.1126/science.1256917.
  • Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K. The cohesin ring concatenates sister DNA molecules. Nature. 2008;454:297–301. doi:10.1038/nature07098.
  • Glynn EF, Megee PC, Yu HG, Mistrot C, Ünal E, Koshland DE, DeRisi JL, Gerton JL. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol. 2004;2:e259. doi:10.1371/journal.pbio.0020259.
  • Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature. 2004;430:573–578. doi:10.1038/nature02742.
  • Costantino L, Hsieh TS, Lamothe R, Darzacq X, Koshland D. Cohesin residency determines chromatin loop patterns. eLife. 2020;9:e59889. doi:10.7554/eLife.59889.
  • Dauban L, Montagne R, Thierry A, Lazar-Stefanita L, Bastie N, Gadal O, Cournac A, Koszul R, Beckouet F. Regulation of cohesin-mediated chromosome folding by Eco1 and other partners. Mol Cell. 2020;77:1279–1293.e4. doi:10.1016/j.molcel.2020.01.019.
  • Oomen ME, Hedger AK, Watts JK, Dekker J. Detecting chromatin interactions between and along sister chromatids with SisterC. Nat Methods. 2020;17:1002–1009. doi:10.1038/s41592-020-0930-9.
  • Schalbetter SA, Fudenberg G, Baxter J, Pollard KS, Neale MJ. Principles of meiotic chromosome assembly revealed in S. cerevisiae. Nat Commun. 2019;10:4795. doi:10.1038/s41467-019-12629-0.
  • Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T, Fraser P, Fisher AG, Merkenschlager M. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature. 2009;460:410–413. doi:10.1038/nature08079.
  • Mitter M, Gasser C, Takacs Z, Langer CCH, Tang W, Jessberger G, Beales CT, Neuner E, Ameres SL, Peters J-M, et al. Conformation of sister chromatids in the replicated human genome. Nature. 2020;586:139–144. doi:10.1038/s41586-020-2744-4.
  • Rao SSP, Huang SC, Glenn St Hilaire B, Engreitz JM, Perez EM, Kieffer-Kwon KR, Sanborn AL, Johnstone SE, Bascom GD, Bochkov ID, et al. Cohesin loss eliminates all loop domains. Cell. 2017;171:305–320.e24. doi:10.1016/j.cell.2017.09.026.
  • Uhlmann F. SMC complexes: from DNA to chromosomes. Nat Rev Mol Cell Biol. 2016;17:399–412. doi:10.1038/nrm.2016.30.
  • Lengronne A, McIntyre J, Katou Y, Kanoh Y, Hopfner K-P, Shirahige K, Uhlmann F. Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol Cell. 2006;23:787–799. doi:10.1016/j.molcel.2006.08.018.
  • D'Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, Shirahige K, Uhlmann F. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev. 2008;22:2215–2227. doi:10.1101/gad.1675708.
  • Busslinger GA, Stocsits RR, van der Lelij P, Axelsson E, Tedeschi A, Galjart N, Peters JM. Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl. Nature. 2017;544:503–507. doi:10.1038/nature22063.
  • Ocampo-Hafalla M, Muñoz S, Samora CP, Uhlmann F. Evidence for cohesin sliding along budding yeast chromosomes. Open Biol. 2016;6:e150178. doi:10.1098/rsob.150178.
  • Bausch C, Noone S, Henry JM, Gaudenz K, Sanderson B, Seidel C, Gerton JL. Transcription alters chromosomal locations of cohesin in Saccharomyces cerevisiae. Mol Cell Biol. 2007;27:8522–8532. doi:10.1128/MCB.01007-07.
  • Davidson IF, Goetz D, Zaczek MP, Molodtsov MI, Huis In 't Veld PJ, Weissmann F, Litos G, Cisneros DA, Ocampo-Hafalla M, Ladurner R, et al. Rapid movement and transcriptional re-localization of human cohesin on DNA. Embo J. 2016;35:2671–2685. doi:10.15252/embj.201695402.
  • Kanke M, Tahara E, Huis In’t Veld PJ, Nishiyama T. Cohesin acetylation and Wapl-Pds5 oppositely regulate translocation of cohesin along DNA. Embo J. 2016;35:2686–2698. doi:10.15252/embj.201695756.
  • Stigler J, Çamdere GO, Koshland DE, Greene EC. Single-molecule imaging reveals a collapsed conformational state for DNA-bound cohesin. Cell Rep. 2016;15:988–998. doi:10.1016/j.celrep.2016.04.003.
  • Davidson IF, Bauer B, Goetz D, Tang W, Wutz G, Peters JM. DNA loop extrusion by human cohesin. Science. 2019;366:1338–1345. doi:10.1126/science.aaz3418.
  • Kim Y, Shi Z, Zhang H, Finkelstein IJ, Yu H. Human cohesin compacts DNA by loop extrusion. Science. 2019;366:1345–1349. doi:10.1126/science.aaz4475.
  • Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. Formation of chromosomal domains by loop extrusion. Cell Rep. 2016;15:2038–2049. doi:10.1016/j.celrep.2016.04.085.
  • Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet. 2001;35:673–745. doi:10.1146/annurev.genet.35.102401.091334.
  • Sanborn AL, Rao SS, Huang SC, Durand NC, Huntley MH, Jewett AI, Bochkov ID, 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 U S A. 2015;112:e6456.
  • Gassler J, Brandao HB, Imakaev M, Flyamer IM, Ladstatter S, Bickmore WA, Peters J-M, Mirny LA, Tachibana K. A mechanism of cohesin-dependent loop extrusion organizes zygotic genome architecture. Embo J. 2017;36:3600–3618. doi:10.15252/embj.201798083.
  • Haarhuis JHI, van der Weide RH, Blomen VA, Yanez-Cuna JO, Amendola M, van Ruiten MS, Krijger PHL, Teunissen H, Medema RH, van Steensel B, et al. The cohesin release factor WAPL restricts chromatin loop extension. Cell. 2017;169:693–707.e14. doi:10.1016/j.cell.2017.04.013.
  • Wutz G, Varnai C, Nagasaka K, Cisneros DA, Stocsits RR, Tang W, Schoenfelder S, Jessberger G, Muhar M, Hossain MJ, et al. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. Embo J. 2017;36:3573–3599. doi:10.15252/embj.201798004.
  • Bastié N, Chapard C, Dauban L, Gadal O, Beckouët F, Koszul R. Smc3 acetylation, Pds5 and Scc2 control the translocase activity that establishes cohesin-dependent chromatin loops. Nat Struct Mol Biol. 2022;29:575–585. 10.1038/s41594-022-00780-0.
  • Dequeker BJH, Scherr MJ, Brandao HB, Gassler J, Powell S, Gaspar I, Flyamer IM, Lalic A, Tang W, Stocsits R, et al. MCM complexes are barriers that restrict cohesin-mediated loop extrusion. Nature. 2022;606:197–203. doi:10.1038/s41586-022-04730-0.
  • Banigan EJ, Tang W, Van Den Berg AA, Stocsits RR, Wutz G, Brandão HB, Busslinger GA, Peters J-M, Mirny LA. Transcription shapes 3D chromatin organization by interacting with loop extrusion. Proc Natl Acad Sci U S A. 2023;120:e2210480120. doi:10.1073/pnas.2210480120.
  • Borrie MS, Campor JS, Joshi H, Gartenberg MR. Binding, sliding, and function of cohesin during transcriptional activation. Proc Natl Acad Sci U S A. 2017;114:e1062.
  • Gartenberg MR, Neumann FN, Laroche T, Blaszczyk M, Gasser SM. Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell. 2004;119:955–967. doi:10.1016/j.cell.2004.11.008.
  • Brickner JH, Walter P. Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2004;2:e342. eng. doi:10.1371/journal.pbio.0020342.
  • Karaboja X, Ren Z, Brandao HB, Paul P, Rudner DZ, Wang X. XerD unloads bacterial SMC complexes at the replication terminus. Mol Cell. 2021;81:756–766.e8. doi:10.1016/j.molcel.2020.12.027.
  • Huang L, Pike D, Sleat DE, Nanda V, Lobel P. Potential pitfalls and solutions for use of fluorescent fusion proteins to study the lysosome. PLoS One. 2014;9:e88893. doi:10.1371/journal.pone.0088893.
  • Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol. 2004;22:1567–1572. doi:10.1038/nbt1037.
  • Verma R, Annan RS, Huddleston MJ, Carr SA, Reynard G, Deshaies RJ. Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science. 1997;278:455–460. doi:10.1126/science.278.5337.455.
  • Chan KL, Roig MB, Hu B, Beckouët F, Metson J, Nasmyth K. Cohesin’s DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell. 2012;150:961–974. doi:10.1016/j.cell.2012.07.028.
  • Haering CH, Schoffnegger D, Nishino T, Helmhart W, Nasmyth K, Löwe J. Structure and stability of cohesin’s Smc1-kleisin interaction. Mol Cell. 2004;15:951–964. doi:10.1016/j.molcel.2004.08.030.
  • Ström L, Lindroos HB, Shirahige K, Sjögren C. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell. 2004;16:1003–1015. doi:10.1016/j.molcel.2004.11.026.
  • Uhlmann F, Nasmyth K. Cohesion between sister chromatids must be established during DNA replication. Curr Biol. 1998;8:1095–1101. doi:10.1016/s0960-9822(98)70463-4.
  • Michaelis C, Ciosk R, Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell. 1997;91:35–45. English. doi:10.1016/s0092-8674(01)80007-6.
  • Guacci V, Stricklin J, Bloom MS, Guō X, Bhatter M, Koshland D. A novel mechanism for the establishment of sister chromatid cohesion by the ECO1 acetyltransferase. Mol Biol Cell. 2015;26:117–133. doi:10.1091/mbc.E14-08-1268.
  • Rowland BD, Roig MB, Nishino T, Kurze A, Uluocak P, Mishra A, Beckouët F, Underwood P, Metson J, Imre R, et al. Building sister chromatid cohesion: Smc3 acetylation counteracts an antiestablishment activity. Mol Cell. 2009;33:763–774. eng. doi:10.1016/j.molcel.2009.02.028.
  • Sutani T, Kawaguchi T, Kanno R, Itoh T, Shirahige K. Budding yeast Wpl1(Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr Biol. 2009;19:492–497. doi:10.1016/j.cub.2009.01.062.
  • Li Y, Haarhuis JHI, Sedeno Cacciatore A, Oldenkamp R, van Ruiten MS, Willems L, Teunissen H, Muir KW, de Wit E, Rowland BD, et al. The structural basis for cohesin-CTCF-anchored loops. Nature. 2020;578:472–476. doi:10.1038/s41586-019-1910-z.
  • Zhang Y, Zhang X, Ba Z, Liang Z, Dring EW, Hu H, Lou J, Kyritsis N, Zurita J, Shamim MS, et al. The fundamental role of chromatin loop extrusion in physiological V(D)J recombination. Nature. 2019;573:600–604. doi:10.1038/s41586-019-1547-y.
  • Gutierrez-Escribano P, Newton MD, Llauró A, Huber J, Tanasie L, Davy J, Aly I, Aramayo R, Montoya A, Kramer H, et al. A conserved ATP- and Scc2/4-dependent activity for cohesin in tethering DNA molecules. Sci Adv. 2019;5:eaay6804. doi:10.1126/sciadv.aay6804.
  • Murayama Y, Samora CP, Kurokawa Y, Iwasaki H, Uhlmann F. Establishment of DNA-DNA interactions by the cohesin ring. Cell. 2018;172:465–477.e15. doi:10.1016/j.cell.2017.12.021.
  • Chapard C, Jones R, van Oepen T, Scheinost JC, Nasmyth K. Sister DNA entrapment between juxtaposed Smc heads and kleisin of the cohesin complex. Mol Cell. 2019;75:224–237.e5. doi:10.1016/j.molcel.2019.05.023.
  • Collier JE, Lee BG, Roig MB, Yatskevich S, Petela NJ, Metson J, Voulgaris M, Gonzalez Llamazares A, Lowe J, Nasmyth KA. Transport of DNA within cohesin involves clamping on top of engaged heads by Scc2 and entrapment within the ring by Scc3. eLife. 2020;9:e59560. doi:10.7554/eLife.59560.
  • Xiang S, Koshland D. Cohesin architecture and clustering in vivo. Elife. 2021;10:e62243. doi:10.7554/eLife.62243.
  • Srinivasan M, Scheinost JC, Petela NJ, Gligoris TG, Wissler M, Ogushi S, Collier JE, Voulgaris M, Kurze A, Chan KL, et al. The cohesin ring uses its hinge to organize DNA using non-topological as well as topological mechanisms. Cell. 2018;173:1508–1519.e18. doi:10.1016/j.cell.2018.04.015.
  • Pradhan B, Barth R, Kim E, Davidson IF, Bauer B, van Laar T, Yang W, Ryu JK, van der Torre J, Peters JM, et al. SMC complexes can traverse physical roadblocks bigger than their ring size. Cell Rep. 2022;41:111491. doi:10.1016/j.celrep.2022.111491.
  • Barton RE, Massari LF, Robertson D, Marston AL. Eco1-dependent cohesin acetylation anchors chromatin loops and cohesion to define functional meiotic chromosome domains. eLife. 2022;11:e74447. doi:10.7554/eLife.74447.
  • Wutz G, Ladurner R, St Hilaire BG, Stocsits RR, Nagasaka K, Pignard B, Sanborn A, Tang W, Varnai C, Ivanov MP, et al. ESCO1 and CTCF enable formation of long chromatin loops by protecting cohesin(STAG1) from WAPL. eLife. 2020;9:e52091. doi:10.7554/eLife.52091.
  • Chatzidaki EE, Powell S, Dequeker BJH, Gassler J, Silva MCC, Tachibana K. Ovulation suppression protects against chromosomal abnormalities in mouse eggs at advanced maternal age. Curr Biol. 2021;31:4038–4051.e7. doi:10.1016/j.cub.2021.06.076.
  • Chou CC, Patel MT, Gartenberg MR. A series of conditional shuttle vectors for targeted genomic integration in budding yeast. FEMS Yeast Res. 2015;15:fov010.
  • Morawska M, Ulrich HD. An expanded tool kit for the auxin-inducible degron system in budding yeast. Yeast. 2013;30:341–351. doi:10.1002/yea.2967.
  • Bloom MS, Koshland D, Guacci V. Cohesin function in cohesion, condensation, and DNA repair is regulated by Wpl1p via a common mechanism in Saccharomyces cerevisiae. Genetics. 2018;208:111–124. doi:10.1534/genetics.117.300537.