1932

Abstract

SMC (structural maintenance of chromosomes) protein complexes are an evolutionarily conserved family of motor proteins that hold sister chromatids together and fold genomes throughout the cell cycle by DNA loop extrusion. These complexes play a key role in a variety of functions in the packaging and regulation of chromosomes, and they have been intensely studied in recent years. Despite their importance, the detailed molecular mechanism for DNA loop extrusion by SMC complexes remains unresolved. Here, we describe the roles of SMCs in chromosome biology and particularly review in vitro single-molecule studies that have recently advanced our understanding of SMC proteins. We describe the mechanistic biophysical aspects of loop extrusion that govern genome organization and its consequences.

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2023-06-20
2024-10-07
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Literature Cited

  1. 1.
    Pellicer J, Fay MF, Leitch IJ. 2010. The largest eukaryotic genome of them all?. Botanical J. Linnean Soc. 164:110–15
    [Google Scholar]
  2. 2.
    Bennett GM, Moran NA. 2013. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol. Evol. 5:91675–88
    [Google Scholar]
  3. 3.
    Petrushenko ZM, She W, Rybenkov V. 2011. A new family of bacterial condensins. Mol. Microbiol. 81:4881–96
    [Google Scholar]
  4. 4.
    Flemming Z 1882. Zellsubstanz, Kern und Zellteilung Leipzig, Ger: F.C.W. Vogel
    [Google Scholar]
  5. 5.
    Kossel A. 1879. Ueber die chemische Zusammensetzung der Peptone. Biol. Chem. 3:1–258–62
    [Google Scholar]
  6. 6.
    Paulson JR, Laemmli UK. 1977. The structure of histone-depleted metaphase chromosomes. Cell 12:3817–28
    [Google Scholar]
  7. 7.
    Leidescher S, Ribisel J, Ullrich S, Feodorova Y, Hildebrand E et al. 2022. Spatial organization of transcribed eukaryotic genes. Nat. Cell Biol. 24:3327–39
    [Google Scholar]
  8. 8.
    MacGregor H 2013. Lampbrush chromosomes. Brenner's Encyclopedia of Genetics S Maloy, K Hughes 190–94. Berlin, Heidelberg: Springer Berlin Heidelberg. , 2nd ed..
    [Google Scholar]
  9. 9.
    Englesberg E, Squires C, Meronk F. 1969. The L-arabinose operon in Escherichia coli B/r: a genetic demonstration of two functional states of the product of a regulator gene. PNAS 62:41100–7
    [Google Scholar]
  10. 10.
    Müller HP, Sogo JM, Schaffner W. 1989. An enhancer stimulates transcription in trans when attached to the promoter via a protein bridge. Cell 58:4767–77
    [Google Scholar]
  11. 11.
    Wood C, Tonegawa S. 1983. Diversity and joining segments of mouse immunoglobulin heavy chain genes are closely linked and in the same orientation: implications for the joining mechanism. PNAS 80:103030–34
    [Google Scholar]
  12. 12.
    Matthews KS. 1992. DNA looping. Microbiol. Rev. 56:1123–36
    [Google Scholar]
  13. 13.
    Mirny LA. 2011. The fractal globule as a model of chromatin architecture in the cell. Chromosome Res 19:137–51
    [Google Scholar]
  14. 14.
    Studier FW, Bandyopadhyay PK. 1988. Model for how type I restriction enzymes select cleavage sites in DNA. PNAS 85:134677–81
    [Google Scholar]
  15. 15.
    Riggs AD. 1990. DNA methylation and late replication probably aid cell memory, and type I DNA reeling could aid chromosome folding and enhancer function. Philos. Trans. R. Soc. B 326:1235285–97
    [Google Scholar]
  16. 16.
    Seidel R, van Noort J, van der Scheer C, Bloom JGP, Dekker NH et al. 2004. Real-time observation of DNA translocation by the type I restriction modification enzyme EcoR124I. Nat. Struct. Mol. Biol. 11:9838–43
    [Google Scholar]
  17. 17.
    Larionov VL, Karpova TS, Kouprina NY, Jouravleva GA. 1985. A mutant of Saccharomyces cerevisiae with impaired maintenance of centromeric plasmids. Curr. Genet. 10:115–20
    [Google Scholar]
  18. 18.
    Strunnikov AV, Larionov VL, Koshland D. 1993. SMC1: An essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. J. Cell Biol. 123:61635–48
    [Google Scholar]
  19. 19.
    Wang X, Le TBK, Lajoie BR, Dekker J, Laub MT, Rudner DZ. 2015. Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis. Genes Dev 29:151661–75
    [Google Scholar]
  20. 20.
    Sanborn AL, Rao SSP, Huang SC, Durand NC, Huntley MH et al. 2015. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. PNAS 112:47E6456–65
    [Google Scholar]
  21. 21.
    Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A et al. 2018. Real-time imaging of DNA loop extrusion by condensin. Science 360:6384102–5
    [Google Scholar]
  22. 22.
    Rattner JB, Lin CC. 1985. Radial loops and helical coils coexist in metaphase chromosomes. Cell 42:1291–96
    [Google Scholar]
  23. 23.
    Saitoh N, Goldberg IG, Wood ER, Earnshaw WC. 1994. ScII: An abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure. J. Cell Biol. 127:2303–18
    [Google Scholar]
  24. 24.
    Alipour E, Marko JF. 2012. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res 40:2211202–12
    [Google Scholar]
  25. 25.
    Goloborodko A, Imakaev MV, Marko JF, Mirny L 2016. Compaction and segregation of sister chromatids via active loop extrusion. eLife 5:e14864
    [Google Scholar]
  26. 26.
    Hirota T, Gerlich D, Koch B, Ellenberg J, Peters JM. 2004. Distinct functions of condensin I and II in mitotic chromosome assembly. J. Cell Sci. 117:266435–45
    [Google Scholar]
  27. 27.
    Ono T, Losada A, Hirano M, Myers MP, Neuwald AF, Hirano T. 2003. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115:1109–21
    [Google Scholar]
  28. 28.
    Gibcus JH, Samejima K, Goloborodko A, Samejima I, Naumova N et al. 2018. A pathway for mitotic chromosome formation. Science 359:6376eaao6135
    [Google Scholar]
  29. 29.
    Walther N, Hossain MJ, Politi AZ, Koch B, Kueblbeck M et al. 2018. A quantitative map of human condensins provides new insights into mitotic chromosome architecture. J. Cell Biol. 217:72309–28
    [Google Scholar]
  30. 30.
    Nasmyth K. 2001. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35:673–745
    [Google Scholar]
  31. 31.
    Gruber S, Errington J. 2009. Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137:4685–96
    [Google Scholar]
  32. 32.
    Wang X, Brandão HB, Le TBK, Laub MT, Rudner DZ. 2017. Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus. Science 355:6324524–27
    [Google Scholar]
  33. 33.
    Wang X, Hughes AC, Brandão HB, Walker B, Lierz C et al. 2018. In vivo evidence for ATPase-dependent DNA translocation by the Bacillus subtilis SMC condensin complex. Mol. Cell. 71:5841–47.e5
    [Google Scholar]
  34. 34.
    Jun S, Mulder B. 2006. Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. PNAS 103:3312388–93
    [Google Scholar]
  35. 35.
    Gogou C, Japaridze A, Dekker C. 2021. Mechanisms for chromosome segregation in bacteria. Front. Microbiol. 12:685687
    [Google Scholar]
  36. 36.
    Nolivos S, Upton AL, Badrinarayanan A, Müller J, Zawadzka K et al. 2016. MatP regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation. Nat. Commun. 7:110466
    [Google Scholar]
  37. 37.
    Japaridze A, van Wee R, Gogou C, Kerssemakers JWJ, Dekker C. 2022. MukBEF-dependent chromosomal organization in widened Escherichia coli. bioRxiv 2022.07.13.499882. https://doi.org/10.1101/2022.07.13.499882
    [Crossref]
  38. 38.
    Mäkelä J, Sherratt DJ. 2020. Organization of the Escherichia coli chromosome by a MukBEF axial core. Mol. Cell. 78:2250–60.e5
    [Google Scholar]
  39. 39.
    Srinivasan M, Fumasoni M, Petela NJ, Murray A, Nasmyth KA 2020. Cohesion is established during DNA replication utilising chromosome associated cohesin rings as well as those loaded de novo onto nascent DNAs. eLife 9:e56611
    [Google Scholar]
  40. 40.
    Zheng G, Kanchwala M, Xing C, Yu H 2018. MCM2–7-dependent cohesin loading during S phase promotes sister-chromatid cohesion. eLife 7:e33920
    [Google Scholar]
  41. 41.
    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. 6:10991–96
    [Google Scholar]
  42. 42.
    Takahashi TS, Basu A, Bermudez V, Hurwitz J, Walter JC. 2008. Cdc7–Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts. Genes Dev 22:141894–905
    [Google Scholar]
  43. 43.
    Gruber S, Haering CH, Nasmyth K. 2003. Chromosomal cohesin forms a ring. Cell 112:6765–77
    [Google Scholar]
  44. 44.
    Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K. 2008. The cohesin ring concatenates sister DNA molecules. Nature 454:7202297–301
    [Google Scholar]
  45. 45.
    Peters J-M, Nishiyama T. 2012. Sister chromatid cohesion. Cold Spring Harbor Perspect. Biol 4:11a011130
    [Google Scholar]
  46. 46.
    Onn I, Heidinger-Pauli JM, Guacci V, Ünal E, Koshland DE. 2008. Sister chromatid cohesion: a simple concept with a complex reality. Annu. Rev. Cell Dev. Biol. 24:105–29
    [Google Scholar]
  47. 47.
    Murayama Y, Samora CP, Kurokawa Y, Iwasaki H, Uhlmann F. 2018. Establishment of DNA-DNA interactions by the cohesin ring. Cell 172:3465–77.e15
    [Google Scholar]
  48. 48.
    Gutierrez-Escribano P, Newton MD, Llauró A, Huber J, Tanasie L et al. 2019. A conserved ATP- and Scc2/4-dependent activity for cohesin in tethering DNA molecules. Sci. Adv. 5:11eaay6804
    [Google Scholar]
  49. 49.
    Nagasaka K, Davidson IF, Stocsits RR, Tang W, Wutz G et al. 2022. Cohesin mediates DNA loop extrusion and sister chromatid cohesion by distinct mechanisms. bioRxiv 2022.09.23.509019. https://doi.org/10.1101/2022.09.23.509019
    [Crossref]
  50. 50.
    Liu Y, Dekker J. 2022. CTCF–CTCF loops and intra-TAD interactions show differential dependence on cohesin ring integrity. Nat. Cell Biol. 24:1516–27
    [Google Scholar]
  51. 51.
    Li Y, Haarhuis JHI, Sedeño Cacciatore Á, Oldenkamp R, van Ruiten MS et al. 2020. The structural basis for cohesin–CTCF-anchored loops. Nature 578:7795472–76
    [Google Scholar]
  52. 52.
    Cameron G, Gruszka D, Xie S, Nasmyth KA, Srinivasan M, Yardimci H. 2022. Sister chromatid cohesion establishment during DNA replication termination. bioRxiv 2022.09.15.508094. https://doi.org/10.1101/2022.09.15.508094
    [Crossref]
  53. 53.
    Ladurner R, Kreidl E, Ivanov MP, Ekker H, Idarraga-Amado MH et al. 2016. Sororin actively maintains sister chromatid cohesion. EMBO J 35:6635–53
    [Google Scholar]
  54. 54.
    Nishiyama T, Ladurner R, Schmitz J, Kreidl E, Schleiffer A et al. 2010. Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143:5737–49
    [Google Scholar]
  55. 55.
    Higashi TL, Ikeda M, Tanaka H, Nakagawa T, Bando M et al. 2012. The prereplication complex recruits XEco2 to chromatin to promote cohesin acetylation in Xenopus egg extracts. Curr. Biol. 22:11977–88
    [Google Scholar]
  56. 56.
    Zhang J, Shi X, Li Y, Kim BJ, Jia J et al. 2008. Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol. Cell. 31:1143–51
    [Google Scholar]
  57. 57.
    Ben-Shahar TR, Heeger S, Lehane C, East P, Flynn H et al. 2008. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321:5888563–66
    [Google Scholar]
  58. 58.
    Ünal E, Heidinger-Pauli JM, Kim W, Guacci V, Onn I et al. 2008. A molecular determinant for the establishment of sister chromatid cohesion. Science 321:5888566–69
    [Google Scholar]
  59. 59.
    Song J, Lafont A, Chen J, Wu FM, Shirahige K, Rankin S. 2012. Cohesin acetylation promotes sister chromatid cohesion only in association with the replication machinery. J. Biol. Chem. 287:4134325–36
    [Google Scholar]
  60. 60.
    Kinoshita K, Tsubota Y, Tane S, Aizawa Y, Sakata R et al. 2022. A loop extrusion-independent mechanism contributes to condensin I-mediated chromosome shaping. J. Cell Biol. 221:3e202109016
    [Google Scholar]
  61. 61.
    Ryu JK, Bouchoux C, Liu HW, Kim E, Minamino M et al. 2021. Bridging-induced phase separation induced by cohesin SMC protein complexes. Sci. Adv. 7:7eabe5905
    [Google Scholar]
  62. 62.
    Cattoglio C, Pustova I, Walther N, Ho JJ, Hantsche-Grininger M et al. 2019. Determining cellular CTCF and cohesin abundances to constrain 3D genome models. eLife 8:e40164
    [Google Scholar]
  63. 63.
    Eng T, Guacci V, Koshland D. 2015. Interallelic complementation provides functional evidence for cohesin–cohesin interactions on DNA. Mol. Biol. Cell. 26:234224–35
    [Google Scholar]
  64. 64.
    Srinivasan M, Scheinost JC, Petela NJ, Gligoris TG, Wissler M et al. 2018. The cohesin ring uses its hinge to organize DNA using non-topological as well as topological mechanisms. Cell 173:61508–19.e18
    [Google Scholar]
  65. 65.
    Xiang S, Koshland D 2021. Cohesin architecture and clustering in vivo. eLife 10:e62243
    [Google Scholar]
  66. 66.
    Dixon JR, Selvaraj S, Yue F, Kim A, Li Y et al. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:7398376–80
    [Google Scholar]
  67. 67.
    Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID et al. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:71665–80
    [Google Scholar]
  68. 68.
    Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T et al. 2009. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460:7253410–13
    [Google Scholar]
  69. 69.
    Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I et al. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:7398381–85
    [Google Scholar]
  70. 70.
    Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S et al. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:3422–33
    [Google Scholar]
  71. 71.
    Wendt KS, Yoshida K, Itoh T, Bando M, Koch B et al. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:7180796–801
    [Google Scholar]
  72. 72.
    Rao SSP, Huang SC, Glenn St Hilaire B, Engreitz JM, Perez EM et al. 2017. Cohesin loss eliminates all loop domains. Cell 171:2305–20.e24
    [Google Scholar]
  73. 73.
    Nora EP, Goloborodko A, Valton AL, Gibcus JH, Uebersohn A et al. 2017. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169:5930–44.e22
    [Google Scholar]
  74. 74.
    Gassler J, Brandão HB, Imakaev M, Flyamer IM, Ladstätter S et al. 2017. A mechanism of cohesin-dependent loop extrusion organizes zygotic genome architecture. EMBO J 36:243600–18
    [Google Scholar]
  75. 75.
    Schwarzer W, Abdennur N, Goloborodko A, Pekowska A, Fudenberg G et al. 2017. Two independent modes of chromatin organization revealed by cohesin removal. Nature 551:767851–56
    [Google Scholar]
  76. 76.
    Wutz G, Várnai C, Nagasaka K, Cisneros DA, Stocsits RR et al. 2017. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. EMBO J 36:243573–99
    [Google Scholar]
  77. 77.
    de Wit E, Vos ESM, Holwerda SJB, Valdes-Quezada C, Verstegen MJAM et al. 2015. CTCF binding polarity determines chromatin looping. Mol. Cell. 60:4676–84
    [Google Scholar]
  78. 78.
    Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. 2016. Formation of chromosomal domains by loop extrusion. Cell Rep 15:92038–49
    [Google Scholar]
  79. 79.
    Nichols MH, Corces VG. 2015. A CTCF code for 3D genome architecture. Cell 162:4703–5
    [Google Scholar]
  80. 80.
    Tedeschi A, Wutz G, Huet S, Jaritz M, Wuensche A et al. 2013. Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 501:7468564–68
    [Google Scholar]
  81. 81.
    Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom DT et al. 2015. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep 10:81297–309
    [Google Scholar]
  82. 82.
    Flyamer IM, Gassler J, Imakaev M, Brandão HB, Ulianov SV et al. 2017. Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature 544:7648110–14
    [Google Scholar]
  83. 83.
    Gabriele M, Brandão HB, Grosse-Holz S, Jha A, Dailey GM et al. 2022. Dynamics of CTCF- and cohesin-mediated chromatin looping revealed by live-cell imaging. Science 376:6592476–501
    [Google Scholar]
  84. 84.
    Beckwith K, Ødegård-Fougner Ø, Morero N, Barton C, Schueder F et al. 2021. Visualization of loop extrusion by DNA nanoscale tracing in single human cells. bioRxiv 2021.04.12.439407 https://www.biorxiv.org/content/10.1101/2021.04.12.439407v2
  85. 85.
    Smith EM, Lajoie BR, Jain G, Dekker J. 2016. Invariant TAD boundaries constrain cell-type-specific looping interactions between promoters and distal elements around the CFTR locus. Am. J. Hum. Genet. 98:1185–201
    [Google Scholar]
  86. 86.
    Spielmann M, Lupiáñez DG, Mundlos S. 2018. Structural variation in the 3D genome. Nat. Rev. Genet. 19:7453–67
    [Google Scholar]
  87. 87.
    Zuin J, Roth G, Zhan Y, Cramard J, Redolfi J et al. 2022. Nonlinear control of transcription through enhancer–promoter interactions. Nature 604:7906571–77
    [Google Scholar]
  88. 88.
    Doyle B, Fudenberg G, Imakaev M, Mirny LA. 2014. Chromatin loops as allosteric modulators of enhancer-promoter interactions. PLOS Comput. Biol. 10:10e1003867
    [Google Scholar]
  89. 89.
    Symmons O, Pan L, Remeseiro S, Aktas T, Klein F et al. 2016. The Shh topological domain facilitates the action of remote enhancers by reducing the effects of genomic distances. Dev. Cell. 39:5529–43
    [Google Scholar]
  90. 90.
    Krefting J, Andrade-Navarro MA, Ibn-Salem J. 2018. Evolutionary stability of topologically associating domains is associated with conserved gene regulation. BMC Biol 16:187
    [Google Scholar]
  91. 91.
    Ghavi-Helm Y, Jankowski A, Meiers S, Viales RR, Korbel JO, Furlong EEM. 2019. Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression. Nat. Genet. 51:81272–82
    [Google Scholar]
  92. 92.
    Williamson I, Kane L, Devenney PS, Flyamer IM, Anderson E et al. 2019. Developmentally regulated Shh expression is robust to TAD perturbations. Development 146:19dev179523
    [Google Scholar]
  93. 93.
    Alexander JM, Guan J, Li B, Maliskova L, Song M et al. 2019. Live-cell imaging reveals enhancer-dependent Sox2 transcription in the absence of enhancer proximity. eLife 8:e41769
    [Google Scholar]
  94. 94.
    Benabdallah NS, Williamson I, Illingworth RS, Kane L, Boyle S et al. 2019. Decreased enhancer-promoter proximity accompanying enhancer activation. Mol. Cell. 76:3473–84.e7
    [Google Scholar]
  95. 95.
    Davidson IF, Bauer B, Goetz D, Tang W, Wutz G, Peters JM. 2019. DNA loop extrusion by human cohesin. Science 366:64711338–45
    [Google Scholar]
  96. 96.
    Lee R, Kang M-K, Kim Y-J, Yang B, Shim H et al. 2022. CTCF-mediated chromatin looping provides a topological framework for the formation of phase-separated transcriptional condensates. Nucleic Acids Res 50:1207–26
    [Google Scholar]
  97. 97.
    Conte M, Irani E, Chiariello AM, Abraham A, Bianco S et al. 2021. Loop-extrusion and polymer phase-separation can co-exist at the single-molecule level to shape chromatin folding. Nat. Commun. 13:4070
    [Google Scholar]
  98. 98.
    Goel VY, Huseyin MK, Hansen AS. 2022. Region Capture Micro-C reveals coalescence of enhancers and promoters into nested microcompartments. bioRxiv 2022.07.12.499637. https://doi.org/10.1101/2022.07.12.499637
    [Crossref]
  99. 99.
    Chakraborty S, Kopitchinski N, Eraso A, Awasthi P, Chari R et al. 2022. High affinity enhancer-promoter interactions can bypass CTCF/cohesin-mediated insulation and contribute to phenotypic robustness. bioRxiv 2021.12.30.474562. https://doi.org/10.1101/2021.12.30.474562
  100. 100.
    Rinzema NJ, Sofiadis K, Tjalsma SJD, Verstegen MJAM, Oz Y et al. 2021. Building regulatory landscapes: enhancer recruits cohesin to create contact domains, engage CTCF sites and activate distant genes. bioRxiv 2021.10.05.463209. https://doi.org/10.1101/2021.10.05.463209
  101. 101.
    Horsfield JA. 2022. Full circle: a brief history of cohesin and the regulation of gene expression. FEBS J https://doi.org/10.1111/febs.16362
    [Google Scholar]
  102. 102.
    Ryba T, Hiratani I, Lu J, Itoh M, Kulik M et al. 2010. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res 20:6761–70
    [Google Scholar]
  103. 103.
    Pope BD, Ryba T, Dileep V, Yue F, Wu W et al. 2014. Topologically associating domains are stable units of replication-timing regulation. Nature 515:7527402–5
    [Google Scholar]
  104. 104.
    Li Y, Xue B, Zhang M, Zhang L, Hou Y et al. 2021. Transcription-coupled structural dynamics of topologically associating domains regulate replication origin efficiency. Genome Biol 22:1206
    [Google Scholar]
  105. 105.
    Emerson DJ, Zhao PA, Cook AL, Barnett RJ, Klein KN et al. 2022. Cohesin-mediated loop anchors confine the locations of human replication origins. Nature 606:812–19
    [Google Scholar]
  106. 106.
    Dequeker BJH, Scherr MJ, Brandão HB, Gassler J, Powell S et al. 2022. MCM complexes are barriers that restrict cohesin-mediated loop extrusion. Nature 606:7912197–203
    [Google Scholar]
  107. 107.
    Jeppsson K, Sakata T, Nakato R, Milanova S, Shirahige K, Björkegren C. 2022. Cohesin-dependent chromosome loop extrusion is limited by transcription and stalled replication forks. Sci. Adv. 8:23eabn7063
    [Google Scholar]
  108. 108.
    Sjögren C, Nasmyth K. 2001. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol. 11:12991–95
    [Google Scholar]
  109. 109.
    De Piccoli G, Cortes-Ledesma F, Ira G, Torres-Rosell J, Uhle S et al. 2006. Smc5–Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat. Cell Biol. 8:91032–34
    [Google Scholar]
  110. 110.
    Potts PR, Porteus MH, Yu H. 2006. Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J 25:143377–88
    [Google Scholar]
  111. 111.
    Ström L, Karlsson C, Lindroos HB, Wedahl S, Katou Y et al. 2007. Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317:5835242–45
    [Google Scholar]
  112. 112.
    Arnould C, Rocher V, Finoux AL, Clouaire T, Li K et al. 2021. Loop extrusion as a mechanism for formation of DNA damage repair foci. Nature 590:7847660–65
    [Google Scholar]
  113. 113.
    Ünal E, Heidinger-Pauli JM, Koshland D. 2007. DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317:5835245–48
    [Google Scholar]
  114. 114.
    Shi Z, Gao H, Bai XC, Yu H. 2020. Cryo-EM structure of the human cohesin-NIPBL-DNA complex. Science 368:64981454–59
    [Google Scholar]
  115. 115.
    Alt A, Dang HQ, Wells OS, Polo LM, Smith MA et al. 2017. Specialized interfaces of Smc5/6 control hinge stability and DNA association. Nat. Commun. 8:114011
    [Google Scholar]
  116. 116.
    Shroff R, Arbel-Eden A, Pilch D, Ira G, Bonner WM et al. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14:191703–11
    [Google Scholar]
  117. 117.
    Piazza A, Bordelet H, Dumont A, Thierry A, Savocco J et al. 2021. Cohesin regulates homology search during recombinational DNA repair. Nat. Cell Biol. 23:111176–86
    [Google Scholar]
  118. 118.
    Pradhan B, Kanno T, Igarashi MU, Loke MS, Baaske MDet al 2023. The Smc5/6 complex is a DNA loop-extruding motor. Nature 616843–48
    [Google Scholar]
  119. 119.
    Peters J-M. 2021. How DNA loop extrusion mediated by cohesin enables V(D)J recombination. Curr. Opin. Cell Biol. 70:75–83
    [Google Scholar]
  120. 120.
    Kimura K, Hirano T. 1997. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell 90:4625–34
    [Google Scholar]
  121. 121.
    Kimura K, Rybenkov VV, Crisona NJ, Hirano T, Cozzarelli NR. 1999. 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 98:2239–48
    [Google Scholar]
  122. 122.
    Kim E, Gonzalez AM, Pradhan B, van der Torre J, Dekker C. 2022. Condensin-driven loop extrusion on supercoiled DNA. Nat. Struct. Mol. Biol. 29:719–27
    [Google Scholar]
  123. 123.
    Strick TR, Kawaguchi T, Hirano T. 2004. Real-time detection of single-molecule DNA compaction by condensin I. Curr. Biol. 14:10874–80
    [Google Scholar]
  124. 124.
    Eeftens JM, Bisht S, Kerssemakers J, Kschonsak M, Haering CH, Dekker C. 2017. Real-time detection of condensin-driven DNA compaction reveals a multistep binding mechanism. EMBO J 36:233448–57
    [Google Scholar]
  125. 125.
    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 358:6363672–76
    [Google Scholar]
  126. 126.
    Davidson IF, Goetz D, Zaczek MP, Molodtsov MI, Huis in ’t Veld PJ et al. 2016. Rapid movement and transcriptional re-localization of human cohesin on DNA. EMBO J 35:242671–85
    [Google Scholar]
  127. 127.
    Stigler J, Çamdere G, Koshland DE, Greene EC. 2016. Single-molecule imaging reveals a collapsed conformational state for DNA-bound cohesin. Cell Rep 15:5988–98
    [Google Scholar]
  128. 128.
    Kim Y, Shi Z, Zhang H, Finkelstein IJ, Yu H. 2019. Human cohesin compacts DNA by loop extrusion. Science 366:64711345–49
    [Google Scholar]
  129. 129.
    Gutierrez-Escribano P, Hormeño S, Madariaga-Marcos J, Solé-Soler R, O'Reilly FJ et al. 2020. Purified Smc5/6 complex exhibits DNA substrate recognition and compaction. Mol. Cell. 80:61039–54.e6
    [Google Scholar]
  130. 130.
    Golfier S, Quail T, Kimura H, Brugués J 2020. Cohesin and condensin extrude DNA loops in a cell-cycle dependent manner. eLife 9:e53885
    [Google Scholar]
  131. 131.
    Kong M, Cutts EE, Pan D, Beuron F, Kaliyappan T et al. 2020. Human condensin I and II drive extensive ATP-dependent compaction of nucleosome-bound DNA. Mol. Cell. 79:199–114.e9
    [Google Scholar]
  132. 132.
    Ryu J-K, Rah S-H, Janissen R, Kerssemakers JWJ, Bonato A et al. 2022. Condensin extrudes DNA loops in steps up to hundreds of base pairs that are generated by ATP binding events. Nucleic Acids Res 50:2820–32
    [Google Scholar]
  133. 133.
    Tran NT, Laub MT, Le TBK. 2017. SMC progressively aligns chromosomal arms in caulobacter crescentus but is antagonized by convergent transcription. Cell Rep 20:92057–71
    [Google Scholar]
  134. 134.
    Banigan EJ, Mirny LA. 2020. Loop extrusion: theory meets single-molecule experiments. Curr. Opin. Cell Biol. 64:124–38
    [Google Scholar]
  135. 135.
    Kato Y, Miyakawa T, Tanokura M. 2018. Overview of the mechanism of cytoskeletal motors based on structure. Biophys. Rev. 10:571–81
    [Google Scholar]
  136. 136.
    Kschonsak M, Merkel F, Bisht S, Metz J, Rybin V et al. 2017. Structural basis for a safety-belt mechanism that anchors condensin to chromosomes. Cell 171:588–600
    [Google Scholar]
  137. 137.
    Shaltiel IA, Datta S, Lecomte L, Hassler M, Kschonsak M et al. 2022. A hold-and-feed mechanism drives directional DNA loop extrusion by condensin. Science 376:65971087–94
    [Google Scholar]
  138. 138.
    Murayama Y, Uhlmann F. 2014. Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature 505:7483367–71
    [Google Scholar]
  139. 139.
    Collier JE, Nasmyth KA. 2022. DNA passes through cohesin's hinge as well as its Smc3-kleisin interface. bioRxiv 2022.05.30.494034. https://doi.org/10.1101/2022.05.30.494034
  140. 140.
    Nasmyth K. 2011. Cohesin: a catenase with separate entry and exit gates?. Nat. Cell Biol. 13:101170–77
    [Google Scholar]
  141. 141.
    Pradhan B, Barth R, Kim E, Davidson IF, Bauer B et al. 2021. SMC complexes can traverse physical roadblocks bigger than their ring size. Cell Rep 41:3111491
    [Google Scholar]
  142. 142.
    Oldenkamp R, Rowland BD. 2022. A walk through the SMC cycle: from catching DNAs to shaping the genome. Mol. Cell. 82:91616–30
    [Google Scholar]
  143. 143.
    Ryu J, Katan AJ, van der Sluis EO, Wisse T, de Groot R et al. 2020. The condensin holocomplex cycles dynamically between open and collapsed states. Nat. Struct. Mol. Biol. 27:1134–41
    [Google Scholar]
  144. 144.
    Eeftens JM, Katan AJ, Kschonsak M, Hassler M, de Wilde L et al. 2016. Condensin Smc2-Smc4 dimers are flexible and dynamic. Cell Rep 14:81813–18
    [Google Scholar]
  145. 145.
    Bauer BW, Davidson IF, Canena D, Wutz G, Tang W et al. 2021. Cohesin mediates DNA loop extrusion by a “swing and clamp” mechanism. Cell 184:215448–64
    [Google Scholar]
  146. 146.
    Higashi TL, Pobegalov G, Tang M, Molodtsov MI, Uhlmann F 2021. A Brownian ratchet model for DNA loop extrusion by the cohesin complex. eLife 10:e67530
    [Google Scholar]
  147. 147.
    Higashi TL, Eickhoff P, Sousa JS, Locke J, Nans A et al. 2020. A structure-based mechanism for DNA entry into the cohesin ring. Mol. Cell. 79:6917–33.e9
    [Google Scholar]
  148. 148.
    Marko JF, De Los Rios P, Barducci A, Gruber S. 2019. DNA-segment-capture model for loop extrusion by structural maintenance of chromosome (SMC) protein complexes. Nucleic Acids Res 47:136956–72
    [Google Scholar]
  149. 149.
    Nomidis SK, Carlon E, Gruber S, Marko JF. 2022. DNA tension-modulated translocation and loop extrusion by SMC complexes revealed by molecular dynamics simulations. Nucleic Acids Res 50:94974–87
    [Google Scholar]
  150. 150.
    Lee H, Avila LBR, Gruber S, Lee H, Avila LBR et al. 2017. Structure of full-length SMC and rearrangements required for chromosome organization. Mol. Cell 67:2334–47
    [Google Scholar]
  151. 151.
    Lee BG, Merkel F, Allegretti M, Hassler M, Cawood C et al. 2020. Cryo-EM structures of holo condensin reveal a subunit flip-flop mechanism. Nat. Struct. Mol. Biol. 27:8743–51
    [Google Scholar]
  152. 152.
    Pradhan B, Barth R, Kim E, Davidson IF, van der Torre J et al. 2022. Can pseudotopological models for SMC-driven DNA loop extrusion explain the traversal of physical roadblocks bigger than the SMC ring size?. bioRxiv 2022.08.02.502451. https://doi.org/10.1101/2022.08.02.502451
  153. 153.
    Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN et al. 2008. CTCF physically links cohesin to chromatin. PNAS 105:248309–14
    [Google Scholar]
  154. 154.
    Tang Z, Luo OJ, Li X, Zheng M, Zhu JJ et al. 2015. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163:71611–27
    [Google Scholar]
  155. 155.
    Pugacheva EM, Kubo N, Loukinov D, Tajmul M, Kang S et al. 2020. CTCF mediates chromatin looping via N-terminal domain-dependent cohesin retention. PNAS 117:42020–31
    [Google Scholar]
  156. 156.
    Nora EP, Caccianini L, Fudenberg G, So K, Kameswaran V et al. 2020. Molecular basis of CTCF binding polarity in genome folding. Nat. Commun. 11:15612
    [Google Scholar]
  157. 157.
    Luppino JM, Park DS, Nguyen SC, Lan Y, Xu Z et al. 2020. Cohesin promotes stochastic domain intermingling to ensure proper regulation of boundary-proximal genes. Nat. Genet. 52:8840–48
    [Google Scholar]
  158. 158.
    Davidson IF, Barth R, Zaczek M, van der Torre J, Tang W et al. 2023. CTCF is a DNA-tension-dependent barrier to cohesin-mediated loop extrusion. Nature 616:822–27
    [Google Scholar]
  159. 159.
    Karaboja X, Ren Z, Brandão HB, Paul P, Rudner DZ, Wang X. 2021. XerD unloads bacterial SMC complexes at the replication terminus. Mol. Cell. 81:4756–66.e8
    [Google Scholar]
  160. 160.
    Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA et al. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467:7314430–35
    [Google Scholar]
  161. 161.
    Ramasamy S, Aljahani A, Karpinska MA, Cao TBN, Cruz JN, Oudelaar AM. 2022. The Mediator complex regulates enhancer-promoter interactions. bioRxiv 2022.06.15.496245. https://doi.org/10.1101/2022.06.15.496245
    [Crossref]
  162. 162.
    Mattingly M, Seidel C, Muñoz S, Hao Y, Zhang Y et al. 2022. Mediator recruits the cohesin loader Scc2 to RNA Pol II-transcribed genes and promotes sister chromatid cohesion. Curr. Biol. 32:132884–96.e6
    [Google Scholar]
  163. 163.
    Weintraub AS, Li CH, Zamudio AV, Sigova AA, Hannett NM et al. 2017. YY1 is a structural regulator of enhancer–promoter loops. Cell 171:71573–88.e28
    [Google Scholar]
  164. 164.
    Beagan JA, Duong MT, Titus KR, Zhou L, Cao Z et al. 2017. YY1 and CTCF orchestrate a 3D chromatin looping switch during early neural lineage commitment. Genome Res 27:71139–52
    [Google Scholar]
  165. 165.
    Pan X, Papasani M, Hao Y, Calamito M, Wei F et al. 2013. YY1 controls Igκ repertoire and B-cell development, and localizes with condensin on the Igκ locus. EMBO J 32:81168–82
    [Google Scholar]
  166. 166.
    Busslinger GA, Stocsits RR, van der Lelij P, Axelsson E, Tedeschi A et al. 2017. Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl.. Nature 544:7651503–7
    [Google Scholar]
  167. 167.
    Heinz S, Texari L, Hayes MGB, Urbanowski M, Chang MW et al. 2018. Transcription elongation can affect genome 3D structure. Cell 174:61522–36.e22
    [Google Scholar]
  168. 168.
    Banigan EJ, Tang W, van den Berg AA, Stocsits RR, Wutz G et al. 2022. Transcription shapes 3D chromatin organization by interacting with loop-extruding cohesin complexes. bioRxiv 2022.01.07.475367. https://www.biorxiv.org/content/10.1101/2022.01.07.475367v1
  169. 169.
    Brandão HB, Paul P, van den Berg AA, Rudner DZ, Wang X, Mirny LA 2019. RNA polymerases as moving barriers to condensin loop extrusion. PNAS 116:4120489–99
    [Google Scholar]
  170. 170.
    Lee K, Hsiung CCS, Huang P, Raj A, Blobel GA 2015. Dynamic enhancer–gene body contacts during transcription elongation. Genes Dev 29:191992–97
    [Google Scholar]
  171. 171.
    Schaaf CA, Kwak H, Koenig A, Misulovin Z, Gohara DW et al. 2013. Genome-wide control of RNA polymerase II activity by cohesin. PLOS Genetics 9:3e1003382
    [Google Scholar]
  172. 172.
    Pan H, Jin M, Ghadiyaram A, Kaur P, Miller HE et al. 2021. Cohesin SA1 and SA2 are RNA binding proteins that localize to RNA containing regions on DNA. Nucleic Acids Res 48:105639–55
    [Google Scholar]
  173. 173.
    Brandão HB, Ren Z, Karaboja X, Mirny LA, Wang X. 2021. DNA-loop-extruding SMC complexes can traverse one another in vivo. Nat. Struct. Mol. Biol. 28:8642–51
    [Google Scholar]
  174. 174.
    Anchimiuk A, Lioy VS, Bock FP, Minnen A, Boccard F, Gruber S 2021. A low Smc flux avoids collisions and facilitates chromosome organization in Bacillus subtilis. eLife 10:e65467
    [Google Scholar]
  175. 175.
    Kim E, Kerssemakers J, Shaltiel IA, Haering CH, Dekker C. 2020. DNA-loop extruding condensin complexes can traverse one another. Nature 579:7799438–42
    [Google Scholar]
  176. 176.
    Banigan EJ, van den Berg AA, Brandão HB, Marko JF, Mirny LA 2020. Chromosome organization by one-sided and two-sided loop extrusion. eLife 9:e53558
    [Google Scholar]
  177. 177.
    Muñoz S, Minamino M, Casas-Delucchi CS, Patel H, Uhlmann F 2019. A role for chromatin remodeling in cohesin loading onto chromosomes. Mol. Cell. 74:4664–73.e5
    [Google Scholar]
  178. 178.
    Otterstrom J, Castells-Garcia A, Vicario C, Gomez-Garcia PA, Cosma MP, Lakadamyali M. 2019. Super-resolution microscopy reveals how histone tail acetylation affects DNA compaction within nucleosomes in vivo. Nucleic Acids Res 47:168470–84
    [Google Scholar]
  179. 179.
    Portillo-Ledesma S, Tsao LH, Wagley M, Lakadamyali M, Cosma MP, Schlick T. 2021. Nucleosome clutches are regulated by chromatin internal parameters. J. Mol. Biol. 433:6166701
    [Google Scholar]
  180. 180.
    Guérin TM, Béneut C, Barinova N, López V, Lazar-Stefanita L et al. 2019. Condensin-mediated chromosome folding and internal telomeres drive dicentric severing by cytokinesis. Mol. Cell. 75:1131–44.e3
    [Google Scholar]
  181. 181.
    Le Bihan Y-V, Matot B, Pietrement O, Giraud-Panis M-J, Gasparini S et al. 2013. Effect of Rap1 binding on DNA distortion and potassium permanganate hypersensitivity. Acta Crystallogr D69:3409–19
    [Google Scholar]
  182. 182.
    Cummings CT, Rowley MJ. 2022. Implications of dosage deficiencies in CTCF and cohesin on genome organization, gene expression, and human neurodevelopment. Genes 13:4583
    [Google Scholar]
  183. 183.
    Oscar H 1890. Lehrbuch der Entwicklungsgeschichte des Menschen und der Wirbeltiere Jena, Ger: Gustav Fischer
    [Google Scholar]
  184. 184.
    Wells JN, Gligoris TG, Nasmyth KA, Marsh JA. 2017. Evolution of condensin and cohesin complexes driven by replacement of Kite by Hawk proteins. Curr. Biol. 27:1R17–18
    [Google Scholar]
  185. 185.
    Kikuchi S, Borek DM, Otwinowski Z, Tomchick DR, Yu H. 2016. Crystal structure of the cohesin loader Scc2 and insight into cohesinopathy. PNAS 113:4412444–49
    [Google Scholar]
  186. 186.
    Haarhuis JHI, van der Weide RH, Blomen VA, Yáñez-Cuna JO, Amendola M et al. 2017. The cohesin release factor WAPL restricts chromatin loop extension. Cell 169:4693–707.e14
    [Google Scholar]
  187. 187.
    Yu Y, Li S, Ser Z, Kuang H, Than T et al. 2022. Cryo-EM structure of DNA-bound Smc5/6 reveals DNA clamping enabled by multi-subunit conformational changes. PNAS 119:23e2202799119
    [Google Scholar]
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