CoChat
Sign Up
Cited by 96Genomics and Chromatin DynamicsDNA Repair MechanismsMicrotubule and mitosis dynamics

Looping the Genome with SMC Complexes

Open access
Kim, Eugene, Barth, Roman, Dekker, Cees·2023·Annual Review of Biochemistry
DOI 10.1146/annurev-biochem-032620-110506
Open this paper in CoChat — free accountOpen PDF

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1146/annurev-biochem-032620-110506

Cites

29 of 29 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • SMC complexes form and extrude loops of DNA, causing structural changes on the size of hundreds to thousands of base pairs per loop.

    “SMC complexes form and extrude loops of DNA, causing structural changes on the size of hundreds to thousands of base pairs per loop.32”

    From Bringing the genetically minimal cell to life on a computer in 4D (2026) · cites this paper as [32]

    The Introduction says SMC complexes fold genomes into loops, and the Abstract identifies DNA loop extrusion as the mechanism. But the Introduction describes the large-scale loops as 0.1–1 million base pairs, not hundreds to thousands of base pairs per loop; §3.1.1 gives a figure of up to 200 base pairs per extrusion step, which is not a loop size. (LLM, conf=0.90)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 122

  1. Pellicer J, Fay MF, Leitch IJ. 2010. The largest eukaryotic genome of them all? Botanical J. Linnean Soc. 164(1):10-15
  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(9):1675-88
  3. Petrushenko ZM, She W, Rybenkov V. 2011. A new family of bacterial condensins. Mol. Microbiol. 81(4):881-96
  4. Flemming Z. 1882. Zellsubstanz, Kern und Zellteilung. Leipzig, Ger.: F.C.W. Vogel 5. Kossel A. 1879. Ueber die chemische Zusammensetzung der Peptone. Biol. Chem. 3(1-2):58-62
  5. Paulson JR, Laemmli UK. 1977. The structure of histone-depleted metaphase chromosomes. Cell 12(3):817-28
  6. Leidescher S, Ribisel J, Ullrich S, Feodorova Y, Hildebrand E, et al. 2022. Spatial organization of transcribed eukaryotic genes. Nat. Cell Biol. 24(3):327-39
  7. MacGregor H. 2013. Lampbrush chromosomes. In Brenner's Encyclopedia of Genetics, ed. S Maloy, K Hughes, pp. 190-94. Berlin, Heidelberg: Springer Berlin Heidelberg. 2nd ed.
  8. 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(4):1100-7
  9. Müller HP, Sogo JM, Schaffner W. 1989. An enhancer stimulates transcription in trans when attached to the promoter via a protein bridge. Cell 58(4):767-77
  10. 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(10):3030-34
  11. Matthews KS. 1992. DNA looping. Microbiol. Rev. 56(1):123-36
  12. Mirny LA. 2011. The fractal globule as a model of chromatin architecture in the cell. Chromosome Res. 19(1):37-51
  13. Studier FW, Bandyopadhyay PK. 1988. Model for how type I restriction enzymes select cleavage sites in DNA. PNAS 85(13):4677-81
  14. 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(9):838-43
  15. Larionov VL, Karpova TS, Kouprina NY, Jouravleva GA. 1985. A mutant of Saccharomyces cerevisiae with impaired maintenance of centromeric plasmids. Curr. Genet. 10(1):15-20
  16. 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(6):1635-48
  17. 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(15):1661-75
  18. Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A, et al. 2018. Real-time imaging of DNA loop extrusion by condensin. Science 360(6384):102-5
  19. Rattner JB, Lin CC. 1985. Radial loops and helical coils coexist in metaphase chromosomes. Cell 42(1):291-96
  20. Saitoh N, Goldberg IG, Wood ER, Earnshaw WC. 1994. ScII: An abundant chromosome scaffold pro- tein is a member of a family of putative ATPases with an unusual predicted tertiary structure. J. Cell Biol. 127(2):303-18
  21. 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(26):6435-45
  22. 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(1):109-21
  23. 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(7):2309-28
  24. Gruber S, Errington J. 2009. Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137(4):685-96
  25. 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(5):841-47.e5
  26. Jun S, Mulder B. 2006. Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. PNAS 103(33):12388-93
  27. 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(1):10466
  28. Japaridze A, van Wee R, Gogou C, Kerssemakers JWJ, Dekker C. 2022. MukBEF-dependent chromo- somal organization in widened Escherichia coli. bioRxiv 2022.07.13.499882. https://doi.org/10.1101/ 2022.07.13.499882 · DOI
  29. Mäkelä J, Sherratt DJ. 2020. Organization of the Escherichia coli chromosome by a MukBEF axial core. Mol. Cell. 78(2):250-60.e5
  30. Zheng G, Kanchwala M, Xing C, Yu H. 2018. MCM2-7-dependent cohesin loading during S phase promotes sister-chromatid cohesion. eLife 7:e33920 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(10):991-96
  31. 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(14):1894-905
  32. Gruber S, Haering CH, Nasmyth K. 2003. Chromosomal cohesin forms a ring. Cell 112(6):765-77
  33. Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K. 2008. The cohesin ring concatenates sister DNA molecules. Nature 454(7202):297-301
  34. Peters J-M, Nishiyama T. 2012. Sister chromatid cohesion. Cold Spring Harbor Perspect. Biol. 4(11):a011130
  35. Murayama Y, Samora CP, Kurokawa Y, Iwasaki H, Uhlmann F. 2018. Establishment of DNA-DNA interactions by the cohesin ring. Cell 172(3):465-77.e15
  36. 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 · DOI
  37. 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 · DOI
  38. Ladurner R, Kreidl E, Ivanov MP, Ekker H, Idarraga-Amado MH, et al. 2016. Sororin actively maintains sister chromatid cohesion. EMBO J. 35(6):635-53
  39. Nishiyama T, Ladurner R, Schmitz J, Kreidl E, Schleiffer A, et al. 2010. Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143(5):737-49
  40. 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(11):977-88
  41. 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(1):143-51
  42. 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(5888):563-66
  43. 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(5888):566-69
  44. 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(41):34325-36
  45. 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(3):e202109016
  46. 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 63. Eng T, Guacci V, Koshland D. 2015. Interallelic complementation provides functional evidence for cohesin-cohesin interactions on DNA. Mol. Biol. Cell. 26(23):4224-35
  47. 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(6):1508- 19.e18
  48. 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(7398):376-80 36 Kim • Barth • Dekker 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(7):1665-80
  49. 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(7253):410-13
  50. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, et al. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132(3):422-33
  51. 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(24):3600-18
  52. Nichols MH, Corces VG. 2015. A CTCF code for 3D genome architecture. Cell. 162(4):703-5
  53. 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(7468):564-68
  54. 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(7648):110-14
  55. 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(6592):476-501
  56. 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 · DOI
  57. 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(1):185-201
  58. Spielmann M, Lupiáñez DG, Mundlos S. 2018. Structural variation in the 3D genome. Nat. Rev. Genet. 19(7):453-67
  59. Zuin J, Roth G, Zhan Y, Cramard J, Redolfi J, et al. 2022. Nonlinear control of transcription through enhancer-promoter interactions. Nature 604(7906):571-77
  60. 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(5):529-43
  61. Krefting J, Andrade-Navarro MA, Ibn-Salem J. 2018. Evolutionary stability of topologically associating domains is associated with conserved gene regulation. BMC Biol. 16(1):87
  62. 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 94. Benabdallah NS, Williamson I, Illingworth RS, Kane L, Boyle S, et al. 2019. Decreased enhancer- promoter proximity accompanying enhancer activation. Mol. Cell. 76(3):473-84.e7
  63. 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(1):207-26
  64. 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 · DOI
  65. 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. · DOI
  66. Rinzema NJ, Sofiadis K, Tjalsma SJD, Verstegen MJAM, Oz Y, et al. 2021. Building regulatory land- scapes: 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. 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 102. · DOI
  67. 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(6):761-70 103.
  68. 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(7527):402-5 104.
  69. 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(1):206 105.
  70. 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(7912):197-203 107.
  71. Sjögren C, Nasmyth K. 2001. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol. 11(12):991-95 109.
  72. 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(9):1032-34 110.
  73. Potts PR, Porteus MH, Yu H. 2006. Human SMC5/6 complex promotes sister chromatid homolo- gous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J. 25(14):3377-88 111.
  74. 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(5835):242-45 112.
  75. Ünal E, Heidinger-Pauli JM, Koshland D. 2007. DNA double-strand breaks trigger genome-wide sister- chromatid cohesion through Eco1 (Ctf7). Science 317(5835):245-48 114.
  76. Shi Z, Gao H, Bai XC, Yu H. 2020. Cryo-EM structure of the human cohesin-NIPBL-DNA complex. Science 368(6498):1454-59 115.
  77. 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(1):14011 116.
  78. 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(19):1703-11 117.
  79. 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(11):1176-86 118.
  80. Kimura K, Hirano T. 1997. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell 90(4):625-34 121.
  81. Kimura K, Rybenkov VV, Crisona NJ, Hirano T, Cozzarelli NR. 1999. 13S condensin actively recon- figures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 98(2):239-48 122.
  82. Strick TR, Kawaguchi T, Hirano T. 2004. Real-time detection of single-molecule DNA compaction by condensin I. Curr. Biol. 14(10):874-80 124.
  83. 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(23):3448-57 125.
  84. 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(6363):672-76 126.
  85. 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(6):1039-54.e6 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 131.
  86. 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(1):99-114.e9 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(2):820-32 133.
  87. Tran NT, Laub MT, Le TBK. 2017. SMC progressively aligns chromosomal arms in caulobacter crescentus but is antagonized by convergent transcription. Cell Rep. 20(9):2057-71 134.
  88. 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(6597):1087-94 138.
  89. Murayama Y, Uhlmann F. 2014. Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature 505(7483):367-71 139.
  90. 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. · DOI
  91. Nasmyth K. 2011. Cohesin: a catenase with separate entry and exit gates? Nat. Cell Biol. 13(10):1170-77 141.
  92. 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(3):111491 142.
  93. Oldenkamp R, Rowland BD. 2022. A walk through the SMC cycle: from catching DNAs to shaping the genome. Mol. Cell. 82(9):1616-30 143.
  94. 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(8):1813-18 145.
  95. 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(21):5448-64 146.
  96. 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(6):917-33.e9 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(13):6956-72 149.
  97. 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(9):4974- 87 150.
  98. 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(2):334-47 151.
  99. 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(8):743-51 152.
  100. 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. · DOI
  101. 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(7):1611-27 155.
  102. 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(4):2020-31 156.
  103. 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(1):5612 157.
  104. 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(8):840-48 158.
  105. Ramasamy S, Aljahani A, Karpinska MA, Cao TBN, Cruz JN, Oudelaar AM. 2022. The Mediator com- plex regulates enhancer-promoter interactions. bioRxiv 2022.06.15.496245. https://doi.org/10.1101/ 2022.06.15.496245 162. · DOI
  106. 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(13):2884-96.e6 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(7):1573-88.e28 164.
  107. 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(8):1168-82 166.
  108. Heinz S, Texari L, Hayes MGB, Urbanowski M, Chang MW, et al. 2018. Transcription elongation can affect genome 3D structure. Cell 174(6):1522-36.e22 168.
  109. Banigan EJ, Tang W, van den Berg AA, Stocsits RR, Wutz G, et al. 2022. Transcription shapes 3D chro- matin 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. · DOI
  110. 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(41):20489-99 170.
  111. Lee K, Hsiung CCS, Huang P, Raj A, Blobel GA. 2015. Dynamic enhancer-gene body contacts during transcription elongation. Genes Dev. 29(19):1992-97 171.
  112. 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(3):e1003382 172.
  113. 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(10):5639-55 173.
  114. 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(8):642-51 174.
  115. Kim E, Kerssemakers J, Shaltiel IA, Haering CH, Dekker C. 2020. DNA-loop extruding condensin complexes can traverse one another. Nature 579(7799):438-42 176.
  116. 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(4):664-73.e5 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(16):8470-84 179.
  117. 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(6):166701 180.
  118. 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(1):131-44.e3 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(3):409-19 182.
  119. Cummings CT, Rowley MJ. 2022. Implications of dosage deficiencies in CTCF and cohesin on genome organization, gene expression, and human neurodevelopment. Genes 13(4):583 183.
  120. 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(1):R17-18 185.
  121. Kikuchi S, Borek DM, Otwinowski Z, Tomchick DR, Yu H. 2016. Crystal structure of the cohesin loader Scc2 and insight into cohesinopathy. PNAS 113(44):12444-49 186.
  122. 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(23):e2202799119 Thiolase: A Versatile Biocatalyst Employing Coenzyme A-Thioester Chemistry for Making and Breaking C-C Bonds Rajesh K. Harijan, Subhadra Dalwani, Tiila-Riikka Kiema, Rajaram Venkatesan, and Rik K. Wierenga p p p p p p p p p p p p p p p

Cited by

Sorted by citations

Authors
Kim, E., Barth, R., & Dekker, C.
Affiliations
  • Max Planck Institute of Biophysics (DE)
  • Delft University of Technology (NL)
Corresponding author
Dekker, Cees
ORCID
Venue
Annual Review of Biochemistry
Publisher
Annual Reviews
Published
2023-06-20
Volume
92
Issue
1
Pages
15-41
ISSN
  • 0066-4154 (ISSN-L)
  • 1545-4509
DOI
10.1146/annurev-biochem-032620-110506
OpenAlex
W4367836142
Cited by
96
References
29
Citations by year
2026: 25 · 2025: 37 · 2024: 26 · 2023: 7 · 2020: 1
FWCI
2.51
Type
journal article
Language
en
Open access
Licence
Locations
  • Annual Review of Biochemistry (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research Repository (Delft University of Technology) (submittedVersion, cc-by)
Funders
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (OCENW.GROOT.2019.012)
  • Max-Planck-Gesellschaft
  • National Institute of General Medical Sciences (R35GM138317)
  • H2020 European Research Council (883684)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
Keywords
SMC complex, structural maintenance of chromosomes, DNA loop extrusion, sister chromatid cohesion, genome folding, chromosome organization, motor proteins, single-molecule biophysics, cell cycle
MeSH terms
Chromosomal Proteins, Non-Histone, Chromosomes, DNA, Cell Cycle Proteins, Multiprotein Complexes

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review