Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Cohesin: a catenase with separate entry and exit gates?

Nature Cell Biology volume 13, pages 1170–1177 (2011)Cite this article

Subjects

Abstract

Cohesin confers both intrachromatid and interchromatid cohesion through formation of a tripartite ring within which DNA is thought to be entrapped. Here, I discuss what is known about the four stages of the cohesin ring cycle using the ring model as an intellectual framework. I postulate that cohesin loading onto chromosomes, catalysed by a separate complex called kollerin, is mediated by the entry of DNA into cohesin rings, whereas dissociation, catalysed by Wapl and several other cohesin subunits (an activity that will be called releasin here), is mediated by the subsequent exit of DNA. I suggest that the ring's entry and exit gates may be separate, with the former and latter taking place at Smc1–Smc3 and Smc3–kleisin interfaces, respectively. Establishment of cohesion during S phase involves neutralization of releasin through acetylation of Smc3 at a site close to the putative exit gate of DNA, which locks rings shut until opened irreversibly by kleisin cleavage through the action of separase, an event that triggers the metaphase to anaphase transition.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structure of the cohesin ring.
Figure 2: Three types of ring model.
Figure 3: (a) Cohesin's association and dissociation from chromatin.

Similar content being viewed by others

References

  1. Onn, I., Heidinger-Pauli, J. M., Guacci, V., Unal, E. & Koshland, D. E. Sister chromatid cohesion: a simple concept with a complex reality. Annu. Rev. Cell Dev. Biol. 24, 105–129 (2008).

    Article  PubMed  CAS  Google Scholar 

  2. Nasmyth, K. & Haering, C. H. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 43, 525–528 (2009).

    Article  PubMed  CAS  Google Scholar 

  3. Haering, C. H., Löwe, J., Hochwagen, A. & Nasmyth, K. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9, 773–788 (2002).

    Article  PubMed  CAS  Google Scholar 

  4. Shintomi, K. & Hirano, T. Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl–Pds5 and Sgo1. Genes Dev. 23, 2224–2236 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Kueng, S. et al. Wapl controls the dynamic association of cohesin with chromatin. Cell 127, 955–967 (2006).

    Article  PubMed  CAS  Google Scholar 

  6. Michaelis, C., Ciosk, R. & Nasmyth, K. Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35–45 (1997).

    Article  PubMed  CAS  Google Scholar 

  7. Guacci, V., Koshland, D. & Strunnikov, A. A direct link between sister chromatid cohesion and chromosome condensation revealed through analysis of MCD1 in S. cerevisiae. Cell 91, 47–57 (1997).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Oliveira, R. A., Hamilton, R. S., Pauli, A., Davis, I. & Nasmyth, K. Cohesin cleavage and Cdk inhibition trigger formation of daughter nuclei. Nat. Cell Biol. 12, 185–192 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Tachibana-Konwalski, K. et al. Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev. 24, 2505–2516 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Uhlmann, F., Wernic, D., Poupart, M. A., Koonin, E. & Nasmyth, K. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103, 375–386 (2000).

    Article  PubMed  CAS  Google Scholar 

  11. Thomas, S. E. et al. Identification of two proteins required for conjunction and regular segregation of achiasmate homologs in Drosophila male meiosis. Cell 123, 555–568 (2005).

    Article  PubMed  CAS  Google Scholar 

  12. Sjögren, C. & Nasmyth, K. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol. 11, 991–995 (2001).

    Article  PubMed  Google Scholar 

  13. Klein, F. et al. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98, 91–103 (1999).

    Article  PubMed  CAS  Google Scholar 

  14. Kim, K. P. et al. Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143, 924–937 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Guillou, E. et al. Cohesin organizes chromatin loops at DNA replication factories. Genes Dev. 24, 2812–2822 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Sakuno, T., Tada, K. & Watanabe, Y. Kinetochore geometry defined by cohesion within the centromere. Nature 458, 852–858 (2009).

    Article  PubMed  CAS  Google Scholar 

  17. Lin, W., Jin, H., Liu, X., Hampton, K. & Yu, H. G. Scc2 regulates gene expression by recruiting cohesin to the chromosome as a transcriptional activator during yeast meiosis. Mol. Biol. Cell 22, 1985–1996 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Landeira, D., Bart, J. M., Van Tyne, D. & Navarro, M. Cohesin regulates VSG monoallelic expression in trypanosomes. J. Cell Biol. 186, 243–254 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Schuldiner, O. et al. piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev. Cell 14, 227–238 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Pauli, A. et al. Cell-type-specific TEV protease cleavage reveals cohesion functions in Drosophila neurons. Dev. Cell 14, 239–251 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Pauli, A. et al. A direct role for cohesin in gene regulation and ecdysone response in Drosophila salivary glands. Curr. Biol. 20, 1787–1798 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Misulovin, Z. et al. Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome. Chromosoma 117, 89–102 (2008).

    Article  PubMed  CAS  Google Scholar 

  23. Horsfield, J. A. et al. Cohesin-dependent regulation of Runx genes. Development 134, 2639–2649 (2007).

    Article  PubMed  CAS  Google Scholar 

  24. Wendt, K. S. et al. Cohesin mediates transcriptional insulation by CCCTCbinding factor. Nature 451, 796–801 (2008).

    Article  CAS  PubMed  Google Scholar 

  25. Parelho, V. et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132, 422–433 (2008).

    Article  CAS  PubMed  Google Scholar 

  26. Seitan, V. et al. A role for cohesin in T cell receptor rearrangement and thymocyte differentiation. Nature 476, 467–471 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Schmidt, D. et al. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res. 20, 578–588 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Schöckel L, Möckel M, Mayer B, Boos D & Stemmann O. Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat. Cell Biol. 13, 966–972 (2011).

    Article  PubMed  CAS  Google Scholar 

  29. Gruber, S., Haering, C. H. & Nasmyth, K. Chromosomal cohesin forms a ring. Cell 112, 765–777 (2003).

    Article  PubMed  CAS  Google Scholar 

  30. Haering, C. H., Farcas, A., Arumugam, P., Metson, J. & Nasmyth, K. The cohesin ring concatenates sister DNAs. Nature 454, 297–301 (2008).

    Article  PubMed  CAS  Google Scholar 

  31. Sun, Y. et al. Separase is recruited to mitotic chromosomes to dissolve sister chromatid cohesion in a DNA-dependent manner. Cell 137, 123–132 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Arumugam, P. et al. ATP hydrolysis is required for cohesin's association with chromosomes. Curr. Biol. 13, 1941–1953 (2003).

    Article  PubMed  CAS  Google Scholar 

  33. Hu, B. et al. ATP hydrolysis is required for relocating cohesin from sites occupied by its Scc2/4 loading complex. Curr. Biol. 21, 12–24 (2011).

    Article  PubMed  CAS  Google Scholar 

  34. Ciosk, R. et al. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol. Cell 5, 243–254 (2000).

    Article  PubMed  CAS  Google Scholar 

  35. Furuya, K., Takahashi, K. & Yanagida, M. Faithful anaphase is ensured by Mis4, a sister chromatid cohesin molecule required in S phase and not destroyed in G1 phase. Genes Dev. 12, 3408–3418 (1998).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Gandhi, R., Gillespie, P. J. & Hirano, T. Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Curr. Biol. 16, 2406–2417 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Weber, S. A. et al. The kinetochore is an enhancer of pericentric cohesion binding. PLoS Biol. 2, E260 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Lengronne, A. et al. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430, 573–578 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Fernius, J. & Marston, A. L. Establishment of cohesion at the pericentromere by the Ctf19 kinetochore subcomplex and the replication fork-associated factor, Csm3. PLoS Genet. 5, e1000629 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Takahashi, T. S., Basu, A., Bermudez, V., Hurwitz, J. & Walter, J. C. Cdc7–Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts. Genes Dev. 22, 1894–1905 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Gruber, S. et al. Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 127, 523–537 (2006).

    Article  PubMed  CAS  Google Scholar 

  42. Carter, A. P., Cho, C., Jin, L. & Vale, R. D. Crystal structure of the dynein motor domain. Science 331, 1159–1165 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Ström, L. & Sjögren, C. DNA damage-induced cohesion. Cell Cycle 4, 536–539 (2005).

    Article  PubMed  Google Scholar 

  44. Ström, L. et al. Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317, 242–245 (2007).

    Article  PubMed  CAS  Google Scholar 

  45. Unal, E., Heidinger-Pauli, J. M. & Koshland, D. DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317, 245–248 (2007).

    Article  PubMed  CAS  Google Scholar 

  46. Gorman, J., Plys, A. J., Visnapuu, M. L., Alani, E. & Greene, E. C. Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat. Struct. Mol. Biol. 17, 932–938 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Zhang, J. et al. Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol. Cell 31, 143–151 (2008).

    Article  PubMed  CAS  Google Scholar 

  48. Unal, E. et al. A molecular determinant for the establishment of sister chromatid cohesion. Science 321, 566–569 (2008).

    Article  PubMed  CAS  Google Scholar 

  49. Ben-Shahar, T. R. et al. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321, 563–566 (2008).

    Article  CAS  Google Scholar 

  50. Ivanov, D. et al. Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr. Biol. 12, 1–20 (2002).

    Article  Google Scholar 

  51. Rowland, B. D. et al. Building sister chromatid cohesion: smc3 acetylation counteracts an antiestablishment activity. Mol. Cell 33, 763–774 (2009).

    Article  PubMed  CAS  Google Scholar 

  52. Feytout, A., Vaur, S., Genier, S., Vazquez, S. & Javerzat, J. P. Psm3 acetylation on conserved lysine residues is dispensable for viability in fission yeast but contributes to Eso1-mediated sister chromatid cohesion by antagonizing Wpl1. Mol. Cell Biol. 31, 1771–1786 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Heidinger-Pauli, J. M., Unal, E. & Koshland, D. Distinct targets of the Eco1 acetyltransferase modulate cohesion in S phase and in response to DNA damage. Mol. Cell 34, 311–321 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Moldovan, G. L., Pfander, B. & Jentsch, S. PCNA controls establishment of sister chromatid cohesion during S phase. Mol. Cell 23, 723–732 (2006).

    Article  PubMed  CAS  Google Scholar 

  55. Lengronne, A. et al. Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol. Cell 23, 787–799 (2006).

    Article  PubMed  CAS  Google Scholar 

  56. Kurze, A. et al. A positively charged channel within the Smc1/Smc3 hinge required for sister chromatid cohesion. EMBO J. 30, 364–378 (2011).

    Article  PubMed  CAS  Google Scholar 

  57. Nishiyama, T. et al. Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143, 737–749 (2010).

    Article  PubMed  CAS  Google Scholar 

  58. Rankin, S., Ayad, N. G. & Kirschner, M. W. Sororin, a substrate of the anaphase-promoting complex, is required for sister chromatid cohesion in vertebrates. Mol. Cell 18, 185–200 (2005).

    Article  PubMed  CAS  Google Scholar 

  59. Lafont, A. L., Song, J. & Rankin, S. Sororin cooperates with the acetyltransferase Eco2 to ensure DNA replication-dependent sister chromatid cohesion. Proc. Natl Acad. Sci. USA 107, 20364–20369 (2010).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  60. Beckouet, F. et al. An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Mol. Cell 39, 689–699 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Borges, V. et al. Hos1 deacetylates Smc3 to close the cohesin acetylation cycle. Mol. Cell 39, 677–688 (2010).

    Article  PubMed  CAS  Google Scholar 

  62. Xiong, B., Lu, S. & Gerton, J. L. Hos1 is a lysine deacetylase for the Smc3 subunit of cohesin. Curr. Biol. 20, 1660–1665 (2010).

    Article  PubMed  CAS  Google Scholar 

  63. Tanaka, K., Hao, Z., Kai, M. & Okayama, H. Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J. 20, 5779–5790 (2001).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Sutani, T., Kawaguchi, T., Kanno, R., Itoh, T. & Shirahige, K. Budding yeast Wpl1(Rad61)–Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr. Biol. 19, 492–497 (2009).

    Article  PubMed  CAS  Google Scholar 

  65. Lyons, N. A. & Morgan, D. O. Cdk1-dependent destruction of eco1 prevents cohesion establishment after s phase. Mol. Cell 42, 378–389 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Haering, C. H. et al. Structure and stability of cohesin's Smc1-kleisin interaction. Mol. Cell 15, 951–964 (2004).

    Article  PubMed  CAS  Google Scholar 

  67. Heidinger-Pauli, J. M., Unal, E., Guacci, V. & Koshland, D. The kleisin subunit of cohesin dictates damage-induced cohesion. Mol. Cell 31, 47–56 (2008).

    Article  PubMed  CAS  Google Scholar 

  68. Gerlich, D., Koch, B., Dupeux, F., Peters, J. M. & Ellenberg, J. Live-cell imaging reveals a stable cohesin–chromatin interaction after but not before DNA replication. Curr. Biol. 16, 1571–1578 (2006).

    Article  PubMed  CAS  Google Scholar 

  69. Mishra, A. et al. Both interaction surfaces within cohesin's hinge domain are essential for its stable association with chromatin. Curr. Biol. 20, 279–289 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Yeh, E. et al. Pericentric chromatin is organized into an intramolecular loop in mitosis. Curr. Biol. 18, 81–90 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Revenkova, E., Herrmann, K., Adelfalk, C. & Jessberger, R. Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr. Biol. 20, 1529–1533 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Lister, L. M. et al. Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr. Biol. 20, 1511–1521 (2010).

    Article  PubMed  CAS  Google Scholar 

  73. Chiang, T., Duncan, F. E., Schindler, K., Schultz, R. M. & Lampson, M. A. Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr. Biol. 20, 1522–1528 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Hassold, T. & Hunt, P. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280–291 (2001).

    Article  CAS  PubMed  Google Scholar 

  75. Mc Intyre, J. et al. In vivo analysis of cohesin architecture using FRET in the budding yeast Saccharomyces cerevisiae. EMBO J. 26, 3783–3793 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Losada, A., Hirano, M. & Hirano, T. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev. 12, 1986–1997 (1998).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Waizenegger, I., Hauf, S., Meinke, A. & Peters, J. M. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103, 399–410 (2000).

    Article  PubMed  CAS  Google Scholar 

  78. Sumara, I. et al. The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol. Cell 9, 515–525 (2002).

    Article  PubMed  CAS  Google Scholar 

  79. Peters, J. M., Tedeschi, A. & Schmitz, J. The cohesin complex and its roles in chromosome biology. Genes Dev. 22, 3089–3114 (2008).

    Article  PubMed  CAS  Google Scholar 

  80. Hauf, S. et al. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol. 3, e69 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Salic, A., Waters, J. C. & Mitchison, T. J. Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis. Cell 118, 567–578 (2004).

    Article  PubMed  CAS  Google Scholar 

  82. McGuinness, B. E., Hirota, T., Kudo, N. R., Peters, J. M. & Nasmyth, K. Shugoshin prevents dissociation of cohesin from centromeres during mitosis in vertebrate cells. PLoS Biol. 3, 433–449 (2005).

    Article  CAS  Google Scholar 

  83. Riedel, C. G. et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441, 53–61 (2006).

    Article  PubMed  CAS  Google Scholar 

  84. Xu, Z. et al. Structure and function of the PP2A–shugoshin interaction. Mol. Cell 35, 426–441 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Uhlmann, F., Lottspeich, F. & Nasmyth, K. Sister chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1p. Nature 400, 37–42 (1999).

    Article  PubMed  CAS  Google Scholar 

  86. Hauf, S., Waizenegger, I. & Peters, J. M. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293, 1320–1323 (2001).

    Article  PubMed  CAS  Google Scholar 

  87. Hirano, T., Kobayashi, R. & Hirano, M. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E, and a Xenopus homolog of the Drosophila Barren protein. Cell 89, 511–521 (1997).

    Article  PubMed  CAS  Google Scholar 

  88. Rawlings, J. S., Gatzka, M., Thomas, P. G. & Ihle, J. N. Chromatin condensation via the condensin II complex is required for peripheral T-cell quiescence. EMBO J. 30, 263–276 (2011).

    Article  PubMed  CAS  Google Scholar 

  89. Renshaw, M. J. et al. Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev. Cell 19, 232–244 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Swedlow, J. R. & Hirano, T. The making of the mitotic chromosome: modern insights into classical questions. Mol. Cell 11, 557–569 (2003).

    Article  PubMed  CAS  Google Scholar 

  91. Kimura, K., Hirano, T. ATP-dependent positive supercoiling of DNA by 13S condensin: A biochemical implication for chromosome condensation. Cell 90, 625–634 (1997).

    Article  PubMed  CAS  Google Scholar 

  92. Kimura, K., Rybenkov, V. V., Crisona, N. J., Hirano, T. & Cozzarelli, N. R. 13S condensin actively reconfigures DNA by introducing global positive writhe: Implications for chromosome condensation. Cell 98, 239–248 (1999).

    Article  PubMed  CAS  Google Scholar 

  93. Baxter, J. et al. Positive supercoiling of mitotic DNA drives decatenation by topoisomerase II in eukaryotes. Science 331, 1328–1332 (2011).

    Article  PubMed  CAS  Google Scholar 

  94. Cuylen, S., Metz, J. & Haering, C. H. Condensin structures chromosomal DNA through topological links. Nat. Stuct. Mol. Biol. 18, 894–901 (2011).

    Article  CAS  Google Scholar 

  95. Ivanov, D. & Nasmyth, K. A topological interaction between cohesin rings and a circular minichromosome. Cell 122, 849–860 (2005).

    Article  PubMed  CAS  Google Scholar 

  96. Ivanov, D. & Nasmyth, K. A physical assay for sister chromatid cohesion in vitro. Mol. Cell 27, 300–310 (2007).

    Article  PubMed  CAS  Google Scholar 

  97. Wang, L. H., Mayer, B., Stemmann, O. & Nigg, E. A. Centromere DNA decatenation depends on cohesin removal and is required for mammalian cell division. J. Cell Sci. 123, 806–813 (2010).

    Article  PubMed  CAS  Google Scholar 

  98. Farcas, A., Uluocak, P., Helmhart, W. & Nasmyth, K. Cohesin's concatenation of sister DNAs maintains their intertwining. Mol. Cell http://dx.doi.org/10.1016/j.molcel.2011.07.034 (2011).

  99. Li, Y. et al. Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. Proc. Natl Acad. Sci. USA 107, 18832–18837 (2010).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  100. Chiu, A., Revenkova, E. & Jessberger, R. DNA interaction and dimerization of eukaryotic SMC hinge domains. J. Biol. Chem. 279, 26233–26242 (2004).

    Article  PubMed  CAS  Google Scholar 

  101. Woo, J. S. et al. Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell 136, 85–96 (2009).

    Article  PubMed  CAS  Google Scholar 

  102. Arumugam, P., Nishino, T., Haering, C. H., Gruber, S. & Nasmyth, K. Cohesin's ATPase activity is stimulated by the C-terminal Winged-Helix domain of its kleisin subunit. Curr. Biol. 16, 1998–2008 (2006).

    Article  PubMed  CAS  Google Scholar 

  103. Lim, H. S., Kim, J. S., Park, Y. B., Gwon, G. H. & Cho, Y. Crystal structure of the Mre11–Rad50–ATPγS complex: understanding the interplay between Mre11 and Rad50. Genes Dev. 25, 1091–1104 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Panizza, S., Tanaka, T., Hohchwagen, A., Eisenhaber, F. & Nasmyth, K. Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr. Biol. 10, 1557–1564 (2000).

    Article  PubMed  CAS  Google Scholar 

  105. Neuwald, A. F. & Hirano, T. HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions. Genome Res. 10, 1445–1452 (2000).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Huang, C. E., Milutinovich, M. & Koshland, D. Rings, bracelet or snaps: fashionable alternatives for Smc complexes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 537–542 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Zhang, N. et al. A handcuff model for the cohesin complex. J. Cell Biol. 183, 1019–1031 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

I am grateful to R. Oliveira and D. Sherratt for comments on the manuscript and to M. Tarsounas for suggesting kollerin as a name for cohesin's loading complex.

Author information

Authors and Affiliations

  1. Department of Biochemistry, Kim Nasmyth is at University of Oxford, South Parks Road, Oxford, OX1 3QU, UK,

    Kim Nasmyth

Authors
  1. Kim Nasmyth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kim Nasmyth.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nasmyth, K. Cohesin: a catenase with separate entry and exit gates?. Nat Cell Biol 13, 1170–1177 (2011). https://doi.org/10.1038/ncb2349

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ncb2349

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing