Cohesin: A catenase with separate entry and exit gates?

Nature Cell Biology

Volumn 13, Issue 10, 2011, Pages 1170-1177

  Nasmyth, Kim ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; COHESIN; CYCLIN DEPENDENT KINASE 1; KLEISIN; MEMBRANE PROTEIN; NUCLEOTIDE BINDING PROTEIN; PROTEIN SMC1; PROTEIN SMC3; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ACETYLATION; CATALYSIS; CELL CYCLE S PHASE; CENTRIOLE; CHROMOSOME SEGREGATION; CRYSTAL STRUCTURE; DIMERIZATION; DISSOCIATION; DISSOCIATION CONSTANT; DNA REPLICATION; HYDROLYSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; DNA; HUMANS; MITOSIS; MODELS, GENETIC; SIGNAL TRANSDUCTION;

EID: 80053495083     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2349     Document Type: Review

References (107)

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).
2. Nasmyth, K. & Haering, C. H. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 43, 525-528 (2009).
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). (Pubitemid 34460575)
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).
5. Kueng, S. et al. Wapl controls the dynamic association of cohesin with chromatin. Cell 127, 955-967 (2006). (Pubitemid 44792249)
6. Michaelis, C., Ciosk, R. & Nasmyth, K. Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45 (1997). (Pubitemid 27431311)
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). (Pubitemid 27431312)
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).
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).
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).
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). (Pubitemid 41608460)
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). (Pubitemid 32589193)
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). (Pubitemid 29331199)
14. Kim, K. P. et al. Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143, 924-937 (2010).
15. Guillou, E. et al. Cohesin organizes chromatin loops at DNA replication factories. Genes Dev. 24, 2812-2822 (2010).
16. Sakuno, T., Tada, K. & Watanabe, Y. Kinetochore geometry defined by cohesion within the centromere. Nature 458, 852-858 (2009).
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).
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).
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). (Pubitemid 351189171)
20. Pauli, A. et al. Cell-type-specific TEV protease cleavage reveals cohesion functions in Drosophila neurons. Dev. Cell 14, 239-251 (2008). (Pubitemid 351189182)
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).
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).
23. Horsfield, J. A. et al. Cohesin-dependent regulation of Runx genes. Development 134, 2639-2649 (2007). (Pubitemid 47225960)
24. Wendt, K. S. et al. Cohesin mediates transcriptional insulation by CCCTCbinding factor. Nature 451, 796-801 (2008). (Pubitemid 351253176)
25. Parelho, V. et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132, 422-433 (2008).
26. Seitan, V. et al. A role for cohesin in T cell receptor rearrangement and thymocyte differentiation. Nature 476, 467-471 (2011).
27. Schmidt, D. et al. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res. 20, 578-588 (2010).
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).
29. Gruber, S., Haering, C. H. & Nasmyth, K. Chromosomal cohesin forms a ring. Cell 112, 765-777 (2003). (Pubitemid 36378881)
30. Haering, C. H., Farcas, A., Arumugam, P., Metson, J. & Nasmyth, K. The cohesin ring concatenates sister DNAs. Nature 454, 297-301 (2008).
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).
32. Arumugam, P. et al. ATP hydrolysis is required for cohesin's association with chromosomes. Curr. Biol. 13, 1941-1953 (2003). (Pubitemid 37425203)
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).
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). (Pubitemid 30628083)
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). (Pubitemid 28520988)
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). (Pubitemid 44894912)
37. Weber, S. A. et al. The kinetochore is an enhancer of pericentric cohesion binding. PLoS Biol. 2, E260 (2004).
38. Lengronne, A. et al. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430, 573-578 (2004). (Pubitemid 38998632)
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).
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). (Pubitemid 352008638)
41. Gruber, S. et al. Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 127, 523-537 (2006). (Pubitemid 44647422)
42. Carter, A. P., Cho, C., Jin, L. & Vale, R. D. Crystal structure of the dynein motor domain. Science 331, 1159-1165 (2011).
43. Ström, L. & Sjögren, C. DNA damage-induced cohesion. Cell Cycle 4, 536-539 (2005). (Pubitemid 41359774)
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). (Pubitemid 47076199)
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). (Pubitemid 47076200)
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).
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). (Pubitemid 351905926)
48. Unal, E. et al. A molecular determinant for the establishment of sister chromatid cohesion. Science 321, 566-569 (2008).
49. Ben-Shahar, T. R. et al. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321, 563-566 (2008).
50. Ivanov, D. et al. Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr. Biol. 12, 1-20 (2002).
51. Rowland, B. D. et al. Building sister chromatid cohesion: smc3 acetylation counteracts an antiestablishment activity. Mol. Cell 33, 763-774 (2009).
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).
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).
54. Moldovan, G. L., Pfander, B. & Jentsch, S. PCNA controls establishment of sister chromatid cohesion during S phase. Mol. Cell 23, 723-732 (2006). (Pubitemid 44292556)
55. Lengronne, A. et al. Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol. Cell 23, 787-799 (2006). (Pubitemid 44344523)
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).
57. Nishiyama, T. et al. Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143, 737-749 (2010).
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).
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).
60. Beckouet, F. et al. An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Mol. Cell 39, 689-699 (2010).
61. Borges, V. et al. Hos1 deacetylates Smc3 to close the cohesin acetylation cycle. Mol. Cell 39, 677-688 (2010).
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).
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). (Pubitemid 33010053)
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).
65. Lyons, N. A. & Morgan, D. O. Cdk1-dependent destruction of eco1 prevents cohesion establishment after s phase. Mol. Cell 42, 378-389 (2011).
66. Haering, C. H. et al. Structure and stability of cohesin's Smc1-kleisin interaction. Mol. Cell 15, 951-964 (2004). (Pubitemid 39277991)
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). (Pubitemid 351905925)
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). (Pubitemid 44142999)
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).
70. Yeh, E. et al. Pericentric chromatin is organized into an intramolecular loop in mitosis. Curr. Biol. 18, 81-90 (2008).
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).
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).
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).
74. Hassold, T. & Hunt, P. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280-291 (2001). (Pubitemid 33674776)
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). (Pubitemid 47295869)
76. Losada, A., Hirano, M. & Hirano, T. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev. 12, 1986-1997 (1998). (Pubitemid 28323873)
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).
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). (Pubitemid 34273783)
79. Peters, J. M., Tedeschi, A. & Schmitz, J. The cohesin complex and its roles in chromosome biology. Genes Dev. 22, 3089-3114 (2008).
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).
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). (Pubitemid 39179710)
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).
83. Riedel, C. G. et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441, 53-61 (2006).
84. Xu, Z. et al. Structure and function of the PP2A-shugoshin interaction. Mol. Cell 35, 426-441 (2009).
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). (Pubitemid 29315102)
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). (Pubitemid 32777422)
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). (Pubitemid 27511762)
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).
89. Renshaw, M. J. et al. Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev. Cell 19, 232-244 (2010).
90. Swedlow, J. R. & Hirano, T. The making of the mitotic chromosome: modern insights into classical questions. Mol. Cell 11, 557-569 (2003). (Pubitemid 36385113)
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). (Pubitemid 27357955)
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). (Pubitemid 29355127)
93. Baxter, J. et al. Positive supercoiling of mitotic DNA drives decatenation by topoisomerase II in eukaryotes. Science 331, 1328-1332 (2011).
94. Cuylen, S., Metz, J. & Haering, C. H. Condensin structures chromosomal DNA through topological links. Nat. Stuct. Mol. Biol. 18, 894-901 (2011).
95. Ivanov, D. & Nasmyth, K. A topological interaction between cohesin rings and a circular minichromosome. Cell 122, 849-860 (2005). (Pubitemid 41345203)
96. Ivanov, D. & Nasmyth, K. A physical assay for sister chromatid cohesion in vitro. Mol. Cell 27, 300-310 (2007). (Pubitemid 47058310)
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).
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).
100. Chiu, A., Revenkova, E. & Jessberger, R. DNA interaction and dimerization of eukaryotic SMC hinge domains. J. Biol. Chem. 279, 26233-26242 (2004). (Pubitemid 38798771)
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).
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). (Pubitemid 44573822)
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).
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). (Pubitemid 32062656)
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).
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). (Pubitemid 41529651)
107. Zhang, N. et al. A handcuff model for the cohesin complex. J. Cell Biol. 183, 1019-1031 (2008).