Chromosoma

, Volume 116, Issue 4, pp 321–329 | Cite as

Cohesin regulation: fashionable ways to wear a ring

Review

Abstract

Cohesin is a multiprotein complex, conserved from yeast to humans, that mediates sister chromatid cohesion. Its ring-shaped structure first suggested that it may perform its task by embracing the sister chromatids. The interaction of cohesin with chromatin is tightly regulated throughout the cell cycle, and several proteins contribute to cohesin loading and mobilization along DNA, establishment of cohesin-mediated cohesion, and removal of cohesin during mitosis. Recent studies suggest that distinct cohesin populations exist in different chromosomal regions and have particular requirements in their dynamic interaction with chromatin. In this review, I briefly summarize these studies and discuss their implications for current and future models of cohesin behavior.

References

  1. Anderson DE, Losada A, Erickson HP, Hirano T (2002) Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol 156:419–424PubMedCrossRefGoogle Scholar
  2. Antoniacci LM, Skibbens RV (2006) Sister-chromatid telomere cohesion is nonredundant and resists both spindle forces and telomere motility. Curr Biol 16:902–906PubMedCrossRefGoogle Scholar
  3. Baetz KK, Krogan NJ, Emili A, Greenblatt J, Hieter P (2004) The ctf13-30/CTF13 genomic haploinsufficiency modifier screen identifies the yeast chromatin remodeling complex RSC, which is required for the establishment of sister chromatid cohesion. Mol Cell Biol 24:1232–1244PubMedCrossRefGoogle Scholar
  4. Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542PubMedCrossRefGoogle Scholar
  5. Blat Y, Kleckner N (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98:249–259PubMedCrossRefGoogle Scholar
  6. Blower MD, Karpen GH (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat Cell Biol 3:730–739PubMedCrossRefGoogle Scholar
  7. Chang CR, Wu CS, Hom Y, Gartenberg MR (2005a) Targeting of cohesin by transcriptionally silent chromatin. Genes Dev 19:3031–3042PubMedCrossRefGoogle Scholar
  8. Chang P, Coughlin M, Mitchison TJ (2005b) Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 7:1133–1139PubMedCrossRefGoogle Scholar
  9. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, Nasmyth K (2000) Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5:243–254PubMedCrossRefGoogle Scholar
  10. Cleveland DW, Mao Y, Sullivan KF (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112:407–421PubMedCrossRefGoogle Scholar
  11. D’Amours D, Stegmeier F, Amon A (2004) Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell 117:455–469PubMedCrossRefGoogle Scholar
  12. Donze D, Adams CR, Rine J, Kamakaka RT (1999) The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev 13:698–708PubMedGoogle Scholar
  13. Dorsett D (2006) Roles of the sister chromatid cohesion apparatus in gene expression, development, and human syndromes. Chromosoma 116:1–13PubMedCrossRefGoogle Scholar
  14. Dorsett D, Eissenberg JC, Misulovin Z, Martens A, Redding B, McKim K (2005) Effects of sister chromatid cohesion proteins on cut gene expression during wing development in Drosophila. Development 132:4743–4753PubMedCrossRefGoogle Scholar
  15. Dynek JN, Smith S (2004) Resolution of sister telomere association is required for progression through mitosis. Science 304:97–100PubMedCrossRefGoogle Scholar
  16. Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, Takami Y, Nakayama T, Oshimura M (2004) Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 6:784–791PubMedCrossRefGoogle Scholar
  17. Gandhi R, Gillespie PJ, Hirano T (2006) Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Curr Biol 16:2406–2417PubMedCrossRefGoogle Scholar
  18. Gerlich D, Koch B, Dupeux F, Peters JM, Ellenberg J (2006) Live-cell imaging reveals a stable cohesin–chromatin interaction after but not before DNA replication. Curr Biol 16:1571–1578PubMedCrossRefGoogle Scholar
  19. Gillespie PJ, Hirano T (2004) Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr Biol 14:1598–1603PubMedCrossRefGoogle Scholar
  20. Gimenez-Abian JF, Sumara I, Hirota T, Hauf S, Gerlich D, de la Torre C, Ellenberg J, Peters JM (2004) Regulation of sister chromatid cohesion between chromosome arms. Curr Biol 14:1187–1193PubMedCrossRefGoogle Scholar
  21. Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, Koshland DE, DeRisi JL, Gerton JL (2004) Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol 2:E259PubMedCrossRefGoogle Scholar
  22. Gonzalez C, Casal Jimenez J, Ripoll P, Sunkel CE (1991) The spindle is required for the process of sister chromatid separation in Drosophila neuroblasts. Exp Cell Res 192:10–15PubMedCrossRefGoogle Scholar
  23. Goshima G, Yanagida M (2001) Time course analysis of precocious separation of sister centromeres in budding yeast: continuously separated or frequently reassociated? Genes Cells 6:765–773PubMedCrossRefGoogle Scholar
  24. Gruber S, Haering CH, Nasmyth K (2003) Chromosomal cohesin forms a ring. Cell 112:765–777PubMedCrossRefGoogle Scholar
  25. Guenatri M, Bailly D, Maison C, Almouzni G (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166:493–505PubMedCrossRefGoogle Scholar
  26. Haering CH, Lowe J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9:773–788PubMedCrossRefGoogle Scholar
  27. Hakimi MA, Bochar DA, Schmiesing JA, Dong Y, Barak OG, Speicher DW, Yokomori K, Shiekhattar R (2002) A chromatin remodelling complex that loads cohesin onto human chromosomes. Nature 418:994–998PubMedCrossRefGoogle Scholar
  28. Hall IM, Noma K, Grewal SI (2003) RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc Natl Acad Sci U S A 100:193–198PubMedCrossRefGoogle Scholar
  29. Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters JM (2005) Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol 3:e69PubMedCrossRefGoogle Scholar
  30. He X, Asthana S, Sorger PK (2000) Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 101:763–775PubMedCrossRefGoogle Scholar
  31. 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 117:6435–6445PubMedCrossRefGoogle Scholar
  32. Hoque MT, Ishikawa F (2001) Human chromatid cohesin component hRad21 is phosphorylated in M phase and associated with metaphase centromeres. J Biol Chem 276:5059–5067PubMedCrossRefGoogle Scholar
  33. Huang J, Hsu JM, Laurent BC (2004) The RSC nucleosome-remodeling complex is required for Cohesin’s association with chromosome arms. Mol Cell 13:739–750PubMedCrossRefGoogle Scholar
  34. Huang CE, Milutinovich M, Koshland D (2005) Rings, bracelet or snaps: fashionable alternatives for Smc complexes. Philos Trans R Soc Lond B Biol Sci 360:537–542PubMedCrossRefGoogle Scholar
  35. Huang J, Brito IL, Villen J, Gygi SP, Amon A, Moazed D (2006) Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Genes Dev 20:2887–2901PubMedCrossRefGoogle Scholar
  36. Ivanov D, Nasmyth K (2005) A topological interaction between cohesin rings and a circular minichromosome. Cell 122:849–860PubMedCrossRefGoogle Scholar
  37. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19:489–501PubMedCrossRefGoogle Scholar
  38. Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, Watanabe Y (2006) Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441:46–52PubMedCrossRefGoogle Scholar
  39. Kobayashi T, Ganley AR (2005) Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309:1581–1584PubMedCrossRefGoogle Scholar
  40. Kobayashi T, Horiuchi T, Tongaonkar P, Vu L, Nomura M (2004) SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell 117:441–453PubMedCrossRefGoogle Scholar
  41. Kueng S, Hegemann B, Peters BH, Lipp JS, Schleiffer A, Mechtler K, Peters JM (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127:955–967PubMedCrossRefGoogle Scholar
  42. Laloraya S, Guacci V, Koshland D (2000) Chromosomal addresses of the cohesin component Mcd1p. J Cell Biol 151:1047–1056PubMedCrossRefGoogle Scholar
  43. Lam WW, Peterson EA, Yeung M, Lavoie BD (2006) Condensin is required for chromosome arm cohesion during mitosis. Genes Dev 20:2973–2984PubMedCrossRefGoogle Scholar
  44. Lau A, Blitzblau H, Bell SP (2002) Cell-cycle control of the establishment of mating-type silencing in S. cerevisiae. Genes Dev 16:2935–2945PubMedCrossRefGoogle Scholar
  45. Lechner MS, Schultz DC, Negorev D, Maul GG, Rauscher FJ, 3rd (2005) The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem Biophys Res Commun 331:929–937PubMedCrossRefGoogle Scholar
  46. Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F (2004) Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430:573–578PubMedCrossRefGoogle Scholar
  47. Lengronne A, McIntyre J, Katou Y, Kanoh Y, Hopfner KP, Shirahige K, Uhlmann F (2006) Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol Cell 23:787–799PubMedCrossRefGoogle Scholar
  48. Lopez JM, Karpen GH, Orr-Weaver TL (2000) Sister-chromatid cohesion via MEI-S332 and kinetochore assembly are separable functions of the Drosophila centromere. Curr Biol 10:997–1000PubMedCrossRefGoogle Scholar
  49. Losada A, Hirano T (2005) Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev 19:1269–1287PubMedCrossRefGoogle Scholar
  50. Losada A, Yokochi T, Kobayashi R, Hirano T (2000) Identification and characterization of SA/Scc3p subunits in the Xenopus and human cohesin complexes. J Cell Biol 150:405–416PubMedCrossRefGoogle Scholar
  51. Losada A, Hirano M, Hirano T (2002) Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev 16:3004–3016PubMedCrossRefGoogle Scholar
  52. Losada A, Yokochi T, Hirano T (2005) Functional contribution of Pds5 to cohesin-mediated cohesion in human cells and Xenopus egg extracts. J Cell Sci 118:2133–2141PubMedCrossRefGoogle Scholar
  53. MacCallum DE, Losada A, Kobayashi R, Hirano T (2002) ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B. Mol Biol Cell 13:25–39PubMedCrossRefGoogle Scholar
  54. Machin F, Torres-Rosell J, Jarmuz A, Aragon L (2005) Spindle-independent condensation-mediated segregation of yeast ribosomal DNA in late anaphase. J Cell Biol 168:209–219PubMedCrossRefGoogle Scholar
  55. Martienssen RA, Zaratiegui M, Goto DB (2005) RNA interference and heterochromatin in the fission yeast Schizosaccharomyces pombe. Trends Genet 21:450–456PubMedCrossRefGoogle Scholar
  56. Megee PC, Mistrot C, Guacci V, Koshland D (1999) The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences. Mol Cell 4:445–450PubMedCrossRefGoogle Scholar
  57. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ (2005) Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci U S A 102:12135–12140PubMedCrossRefGoogle Scholar
  58. Nasmyth K, Haering CH (2005) The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74:595–648PubMedCrossRefGoogle Scholar
  59. Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, Grewal SI, Watanabe Y (2002) Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 4:89–93PubMedCrossRefGoogle Scholar
  60. Obuse C, Yang H, Nozaki N, Goto S, Okazaki T, Yoda K (2004) Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNA binding protein 1 (DDB-1) is a component of the CEN-complex, while BMI-1 is transiently co-localized with the centromeric region in interphase. Genes Cells 9:105–120PubMedCrossRefGoogle Scholar
  61. Pal-Bhadra M, Leibovitch BA, Gandhi SG, Rao M, Bhadra U, Birchler JA, Elgin SC (2004) Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303:669–672PubMedCrossRefGoogle Scholar
  62. Rabitsch KP, Petronczki M, Javerzat JP, Genier S, Chwalla B, Schleiffer A, Tanaka TU, Nasmyth K (2003) Kinetochore recruitment of two nucleolar proteins is required for homolog segregation in meiosis I. Dev Cell 4:535–548PubMedCrossRefGoogle Scholar
  63. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, Mudrak I, Ogris E, Mechtler K, Pelletier L, Buchholz F, Shirahige K, Nasmyth K (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441:53–61PubMedCrossRefGoogle Scholar
  64. Rollins RA, Morcillo P, Dorsett D (1999) Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 152:577–593PubMedGoogle Scholar
  65. Rollins RA, Korom M, Aulner N, Martens A, Dorsett D (2004) Drosophila nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Mol Cell Biol 24:3100–3111PubMedCrossRefGoogle Scholar
  66. Skibbens RV (2005) Unzipped and loaded: the role of DNA helicases and RFC clamp-loading complexes in sister chromatid cohesion. J Cell Biol 169:841–846PubMedCrossRefGoogle Scholar
  67. Sullivan M, Higuchi T, Katis VL, Uhlmann F (2004) Cdc14 phosphatase induces rDNA condensation and resolves cohesin-independent cohesion during budding yeast anaphase. Cell 117:471–482PubMedCrossRefGoogle Scholar
  68. Sumara I, Vorlaufer E, Stukenberg PT, Kelm O, Redemann N, Nigg EA, Peters JM (2002) The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell 9:515–525PubMedCrossRefGoogle Scholar
  69. Suter B, Tong A, Chang M, Yu L, Brown GW, Boone C, Rine J (2004) The origin recognition complex links replication, sister chromatid cohesion and transcriptional silencing in Saccharomyces cerevisiae. Genetics 167:579–591PubMedCrossRefGoogle Scholar
  70. 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 6:991–996PubMedCrossRefGoogle Scholar
  71. Tanaka T, Cosma MP, Wirth K, Nasmyth K (1999) Identification of cohesin association sites at centromeres and along chromosome arms. Cell 98:847–858PubMedCrossRefGoogle Scholar
  72. Tanaka T, Fuchs J, Loidl J, Nasmyth K (2000) Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nat Cell Biol 2:492–499PubMedCrossRefGoogle Scholar
  73. Tang Z, Shu H, Qi W, Mahmood NA, Mumby MC, Yu H (2006) PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev Cell 10:575–585PubMedCrossRefGoogle Scholar
  74. Tomonaga T, Nagao K, Kawasaki Y, Furuya K, Murakami A, Morishita J, Yuasa T, Sutani T, Kearsey SE, Uhlmann F, Nasmyth K, Yanagida M (2000) Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. Genes Dev 14:2757–2770PubMedCrossRefGoogle Scholar
  75. Tonkin ET, Wang TJ, Lisgo S, Bamshad MJ, Strachan T (2004) NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat Genet 36:636–641PubMedCrossRefGoogle Scholar
  76. Topp CN, Dawe RK (2006) Reinterpreting pericentromeric heterochromatin. Curr Opin Plant Biol 9:647–653PubMedCrossRefGoogle Scholar
  77. Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8:1095–1101PubMedCrossRefGoogle Scholar
  78. Uhlmann F, Lottspeich F, Nasmyth K (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400:37–42PubMedCrossRefGoogle Scholar
  79. Vig BK (1987) Sequence of centromere separation: a possible role for repetitive DNA. Mutagenesis 2:155–159PubMedCrossRefGoogle Scholar
  80. Waizenegger IC, Hauf S, Meinke A, Peters JM (2000) Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103:399–410PubMedCrossRefGoogle Scholar
  81. Warren WD, Steffensen S, Lin E, Coelho P, Loupart M, Cobbe N, Lee JY, McKay MJ, Orr-Weaver T, Heck MM, Sunkel CE (2000) The Drosophila RAD21 cohesin persists at the centromere region in mitosis. Curr Biol 10:1463–1466PubMedCrossRefGoogle Scholar
  82. Watanabe Y (2005) Shugoshin: guardian spirit at the centromere. Curr Opin Cell Biol 17:590–595PubMedCrossRefGoogle Scholar
  83. Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, Peters JM (2006) Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr Biol 16:863–874PubMedCrossRefGoogle Scholar
  84. Weber SA, Gerton JL, Polancic JE, DeRisi JL, Koshland D, Megee PC (2004) The kinetochore is an enhancer of pericentric cohesin binding. PLoS Biol 2:E260PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Spanish National Cancer Research CenterMadridSpain

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