Skip to main content

Advertisement

SpringerLink
Log in

Cohesins: chromatin architects in chromosome segregation, control of gene expression and much more

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Cells have evolved to develop molecules and control mechanisms that guarantee correct chromosome segregation and ensure the proper distribution of genetic material to daughter cells. In this sense, the establishment, maintenance, and removal of sister chromatid cohesion is one of the most fascinating and dangerous processes in the life of a cell because errors in the control of these processes frequently lead to cell death or aneuploidy. The main protagonist in this mechanism is a four-protein complex denominated the cohesin complex. In the last 10 years, we have improved our understanding of the key players in the regulation of sister chromatid cohesion during cell division in mitosis and meiosis. The last 2 years have seen an increase in evidence showing that cohesins have important functions in non-dividing cells, revealing new, unexplored roles for these proteins in the control of gene expression, development, and other essential cell functions in mammals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  4. Carramolino L, Lee BC, Zaballos A, Peled A, Barthelemy I, Shav-Tal Y, Prieto I, Carmi P, Gothelf Y, Gonzalez de Buitrago G, Aracil M, Marquez G, Barbero JL, Zipori D (1997) SA-1, a nuclear protein encoded by one member of a novel gene family: molecular cloning and detection in hemopoietic organs. Gene 195:151–159

    Article  PubMed  CAS  Google Scholar 

  5. Losada A, Yokochi T, Kobayashi R, Hirano T (2000) Identification and characterization of SA/Scc3 subunits in the Xenopus and human cohesin complexes. J Cell Biol 150:405–416

    Article  PubMed  CAS  Google Scholar 

  6. Sumara I, Vorlaufer E, Gieffers C, Peters BH, Peters JM (2000) Characterization of vertebrate cohesin complexes and their regulation in prophase. J Cell Biol 151:749–762

    Article  PubMed  CAS  Google Scholar 

  7. Gruber S, Haering CH, Nasmyth K (2003) Chromosomal cohesin forms a ring. Cell 112:765–777

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  9. Nasmyth K (2001) Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet 35:673–745

    Article  PubMed  CAS  Google Scholar 

  10. 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 5:243–254

    Article  PubMed  CAS  Google Scholar 

  11. 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 16:863–874

    Article  PubMed  CAS  Google Scholar 

  12. Skibbens RV, Corson LB, Koshland D, Hieter P (1999) Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev 13:307–319

    Article  PubMed  CAS  Google Scholar 

  13. Toth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A, Nasmyth K (1999) Yeast cohesin complex requires a conserved protein, Eco1p(Cft7), to establish cohesion between sister chromatids during DNA replication. Genes Dev 13:320–323

    Article  PubMed  CAS  Google Scholar 

  14. Tanaka K, Yonekawa T, Kawasaki Y, Kai M, Furuya K, Iwasaki M, Murakami H, Yanagida M, Okayama H (2000) Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase. Mol Cell Biol 20:3459–3469

    Article  PubMed  CAS  Google Scholar 

  15. Ivanov D, Schleiffer A, Eisenhaber F, Mechtler K, Haering CH, Nasmyth K (2002) Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr Biol 12:323–328

    Article  PubMed  CAS  Google Scholar 

  16. Hanna JS, Kroll ES, Lundblad V, Spencer FA (2001) Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol Cell Biol 21:3144–3158

    Article  PubMed  CAS  Google Scholar 

  17. Mayer ML, Pot I, Chang M, Xu H, Aneliunas V, Kwok T, Newitt R, Aebersold R, Boone C, Brown GW, Hieter P (2004) Identification of protein complexes required for efficient sister chromatid cohesion. Mol Cell Biol 15:1736–1745

    Article  CAS  Google Scholar 

  18. Wang F, Yoder J, Antoshechkin I, Han M (2003) Caenorhabditis elegans EVL-14/PDS-5 and SCC-3 are essential for sister chromatid cohesion in meiosis and mitosis. Mol Cell Biol 23:7698–7707

    Article  PubMed  CAS  Google Scholar 

  19. Zhang Z, Ren Q, Yang H, Conrad MN, Guacci V, Kateneva A, Dresser ME (2005) Budding yeast PDS5 plays an important role in meiosis and is required for sister chromatid cohesion. Mol Microbiol 56:670–680

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  21. Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, Mechtler K, Peters JM (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127:955–967

    Article  PubMed  CAS  Google Scholar 

  22. Rankin S, Ayad NG, Kirschner MW (2005) Sororin, a substrate of the anaphase-promoting complex, is required for sister chromatid cohesion in vertebrates. Mol Cell 18:185–200

    Article  PubMed  CAS  Google Scholar 

  23. Dai J, Sullivan BA, Higgins JM (2006) Regulation of mitotic chromosome cohesion by Haspin and Aurora B. Dev Cell 11:741–750

    Article  PubMed  CAS  Google Scholar 

  24. Uhlmann F, Lottspeich F, Nasmyth K (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400:37–42

    Article  PubMed  CAS  Google Scholar 

  25. Cohen-Fix O, Peters JM, Kirschner MW, Koshland D (1996) Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev 10:3081–3093

    Article  PubMed  CAS  Google Scholar 

  26. Funabiki H, Yamano H, Kumada K, Nagao K, Hunt T, Yanagida M (1996) Cut2 proteolysis required for sister-chromatid separation in fission yeast. Nature 381:438–441

    Article  PubMed  CAS  Google Scholar 

  27. Ciosk R, Zacharie W, Michaelis C, Shevchenco A, Mann M, Nasmyth K (1998) An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93:1067–1076

    Article  PubMed  CAS  Google Scholar 

  28. Zou H, McGarry TJ, Bernal T, Kirschner MW (1999) Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science 285:418–422

    Article  PubMed  CAS  Google Scholar 

  29. 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 103:399–410

    Article  PubMed  CAS  Google Scholar 

  30. Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters JM (2005) Dissociation of cohesions from chromosome arms and loss of arm cohesion during early mitosis depends on phsophorylation of SA2. PLoS Biol 3:419–432

    Article  CAS  Google Scholar 

  31. Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K (2000) Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103:375–386

    Article  PubMed  CAS  Google Scholar 

  32. Nakajima M, Kumada K, Hatakeyama K, Noda T, Peters JM, Hirota T (2007) The complete removal of cohesin from chromosome arms depends on separase. J Cell Biol 120:4188–4196

    CAS  Google Scholar 

  33. Vernì F, Gandhi R, Goldberg ML, Gatti M (2000) Genetic and molecular analysis of wings apart-like (wapl), a gene controlling heterochromatin organization in Drosophila melanogaster. Genetics 154:1693–1710

    PubMed  Google Scholar 

  34. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300:1152–1155

    Article  PubMed  CAS  Google Scholar 

  35. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 21:6984–6998

    Article  PubMed  CAS  Google Scholar 

  36. Parisi S, McKay MJ, Molnar M, Thompson MA, van der Spek PJ, van Drunen-Schoenmaker E, Kanaar R, Lehmann E, Hoeijmakers JH, Kohli J (1999) Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 19:3515–3528

    PubMed  CAS  Google Scholar 

  37. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464

    Article  PubMed  CAS  Google Scholar 

  38. Prieto I, Suja JA, Pezzi N, Kremer L, Martínez-A C, Rufas JS, Barbero JL (2001) Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat Cell Biol 3:761–766

    Article  PubMed  CAS  Google Scholar 

  39. Suja JA, Barbero JL (2009) Cohesin complexes and sister chromatid cohesion in mammalian meiosis In: Benavente R, Volff JN (eds). Genome dynamics, vol 5. Karger, Basel, pp 94-116

  40. Alexandru G, Uhlmann F, Mechtler K, Poupart MA, Nasmyth K (2001) Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell 105:459–472

    Article  PubMed  CAS  Google Scholar 

  41. Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R (2002) The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 157:219–229

    Article  PubMed  CAS  Google Scholar 

  42. Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427:510–517

    Article  PubMed  CAS  Google Scholar 

  43. Llano E, Gómez R, Gutiérrez-Caballero C, Herrán Y, Sánchez-Martín M, Vázquez-Quiñones L, Hernández T, de Alava E, Cuadrado A, Barbero JL, Suja JA, Pendás AM (2008) Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes Dev 22:2400–2413

    Article  PubMed  CAS  Google Scholar 

  44. 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 441:46–52

    Article  PubMed  CAS  Google Scholar 

  45. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Gálová 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 441:53–61

    Article  PubMed  CAS  Google Scholar 

  46. Salic A, Waters JC, Mitchison TJ (2004) Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis. Cell 118:567–578

    Article  PubMed  CAS  Google Scholar 

  47. Gómez R, Valdeolmillos A, Parra MT, Viera A, Carreiro C, Roncal F, Rufas JS, Barbero JL, Suja JA (2007) Mammalian SGO2 appears at the inner centromere domain and redistributes depending on tension across centromeres during meiosis II and mitosis. EMBO Rep 8:173–180

    Article  PubMed  Google Scholar 

  48. Huang H, Feng J, Famulski J, Rattner JB, Liu ST, Kao GD, Muschel R, Chan GK, Yen TJ (2007) Tripin/hSgo2 recruits MCAK to the inner centromere to correct defective kinetochore attachments. J Cell Biol 177:24–413

    Article  Google Scholar 

  49. Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, Miyake M, Watanabe Y (2008) Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 10:42–52

    Article  PubMed  CAS  Google Scholar 

  50. Rankin S (2005) Sororin, the cell cycle and sister chromatid cohesion. Cell Cycle 4:1039–1042

    PubMed  CAS  Google Scholar 

  51. Díaz-Martínez LA, Giménez-Abián JF, Clarke DJ (2007) Regulation of centromeric cohesion by sororin independently of the APC/C. Cell Cycle 6:714–724

    PubMed  Google Scholar 

  52. Schmitz J, Watrin E, Lénárt P, Mechtler K, Peters JM (2007) Sororin is required for stable binding of cohesin to chromatin and for sister chromatid cohesion in interphase. Curr Biol 17:630–636

    Article  PubMed  CAS  Google Scholar 

  53. 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 2:1325–1339

    Article  CAS  Google Scholar 

  54. Antoniacci LM, Skibbens RV (2006) Sister-chromatid telomere cohesion is non-redundant and resists both spindle forces and telomere motility. Curr Biol 16:902–906

    Article  PubMed  CAS  Google Scholar 

  55. Dynek JN, Smith S (2004) Resolution of sister telomere association is required for progression through mitosis. Science 304:97–100

    Article  PubMed  CAS  Google Scholar 

  56. Chang P, Coughlin M, Mitchison TJ (2005) Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 7:1133–1139

    Article  PubMed  CAS  Google Scholar 

  57. Canudas S, Houghtaling BR, Kim JY, Dynek JN, Chang WG, Smith S (2007) Protein requirements for sister telomere association in human cells. EMBO J 26:4867–4878

    Article  PubMed  CAS  Google Scholar 

  58. Trelles-Sticken E, Adelfalk C, Loidl J, Scherthan H (2005) Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 170:213–223

    Article  PubMed  CAS  Google Scholar 

  59. Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, Liebe B, Scherthan H, Jessberger R (2004) Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6:555–562

    Article  PubMed  CAS  Google Scholar 

  60. Scherthan H (2007) Telomere attachment and clustering during meiosis. Cell Mol Life Sci 64:117–124

    Article  PubMed  CAS  Google Scholar 

  61. Watrin E, Peters JM (2006) Cohesin and DNA damage repair. Exp Cell Res 312:2687–2693

    Article  PubMed  CAS  Google Scholar 

  62. Gullerova M, Proudfoot NJ (2008) Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell 132:983–995

    Article  PubMed  CAS  Google Scholar 

  63. Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, Yaeger D, Jukofsky L, Wasserman N, Bottani A, Morris CA, Nowaczyk MJ, Toriello H, Bamshad MJ, Carey JC, Rappaport E, Kawauchi S, Lander AD, Calof AL, Li HH, Devoto M, Jackson LG (2004) Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster nipped-B. Nat Genet 36:631–635

    Article  PubMed  CAS  Google Scholar 

  64. 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 36:636–641

    Article  PubMed  CAS  Google Scholar 

  65. Musio A, Selicorni A, Focarelli ML, Gervasini C, Milani D, Russo S, Vezzoni P, Larizza L (2006) X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Genet 38:528–530

    Article  PubMed  CAS  Google Scholar 

  66. Deardorff MA, Kaur M, Yaeger D, Rampuria A, Korolev S, Pie J, Gil-Rodríguez C, Arnedo M, Loeys B, Kline AD, Wilson M, Lillquist K, Siu V, Ramos FJ, Musio A, Jackson LS, Dorsett D, Krantz ID (2007) Mutations in cohesin complex members SMC3 and SMC1A cause a mild variant of Cornelia de Lange syndrome with predominant mental retardation. Am J Hum Genet 80:485–494

    Article  PubMed  CAS  Google Scholar 

  67. Van Den Berg DJ, Francke U (1993) Roberts syndrome: a review of 100 cases and a new rating system for severity. Am J Med Genet 47:1104–1123

    Article  Google Scholar 

  68. Vega H, Waisfisz Q, Gordillo M, Sakai N, Yanagihara I, Yamada M, van Gosliga D, Kayserili H, Xu C, Ozono K, Jabs EW, Inui K, Joenje H (2005) Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat Genet 37:468–470

    Article  PubMed  CAS  Google Scholar 

  69. Gordillo M, Vega H, Trainer AH, Hou F, Sakai N, Luque R, Kayserili H, Basaran S, Skovby F, Hennekam RC, Uzielli ML, Schnur RE, Manouvrier S, Chang S, Blair E, Hurst JA, Forzano F, Meins M, Simola KO, Raas-Rothschild A, Schultz RA, McDaniel LD, Ozono K, Inui K, Zou H, Jabs EW (2008) The molecular mechanism underlying Roberts syndrome involves loss of ESCO2 acetyltransferase activity. Hum Mol Genet 17:2172–2180

    Article  PubMed  CAS  Google Scholar 

  70. Zhang B, Jain S, Song H, Fu M, Heuckeroth RO, Erlich JM, Jay PY, Milbrandt J (2007) Mice lacking sister chromatid cohesion protein PDS5B exhibit developmental abnormalities reminiscent of Cornelia de Lange syndrome. Development 134:3191–3201

    Article  PubMed  CAS  Google Scholar 

  71. 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 118:2133–2141

    Article  PubMed  CAS  Google Scholar 

  72. McNairn AJ, Gerton JL (2008) Cohesinopathies: one ring, many obligations. Mutat Res 647:103–111

    PubMed  CAS  Google Scholar 

  73. Liu J, Krantz ID (2008) Cohesin and human disease. Annu Rev Genomics Hum Genet 9:303–320

    Article  PubMed  CAS  Google Scholar 

  74. Donze D, Adams CR, Rine J, Kamakaka RT (1999) The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev 13:698–708

    Article  PubMed  CAS  Google Scholar 

  75. Hagstrom KA, Meyer BJ (2003) Condensin and cohesin: more than chromosome compactor and glue. Nat Rev Genet 4:520–534

    Article  PubMed  CAS  Google Scholar 

  76. 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 24:3100–3111

    Article  PubMed  CAS  Google Scholar 

  77. Lara-Pezzi E, Pezzi N, Prieto I, Barthelemy I, Carreiro C, Martínez A, Maldonado-Rodríguez A, López-Cabrera M, Barbero JL (2004) Evidence of a transcriptional co-activator function of cohesin STAG/SA/Scc3. J Biol Chem 279:6553–6559

    Article  PubMed  CAS  Google Scholar 

  78. Stedman W, Kang H, Lin S, Kissil JL, Bartolomei MS, Lieberman PM (2008) Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J 27:654–666

    Article  PubMed  CAS  Google Scholar 

  79. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796–801

    Article  PubMed  CAS  Google Scholar 

  80. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, Cobb BS, Yokomori K, Dillon N, Aragon L, Fisher AG, Merkenschlager M (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422–433

    Article  PubMed  CAS  Google Scholar 

  81. Rubio E-D, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN, Baliga NS, Aebersold R, Ranish JA, Krumm A (2008) CTCF physically links cohesin to chromatin. Proc Natl Acad Sci USA 105:8309–8314

    Article  PubMed  CAS  Google Scholar 

  82. Unal E, Heidinger-Pauli JM, Kim W, Guacci V, Onn I, Gygi SP, Koshland DE (2008) A molecular determinant for the establishment of sister chromatid cohesion. Science 321:566–569

    Article  PubMed  Google Scholar 

  83. Ben-Shahar TR, Heeger S, Lehane C, East P, Flynn H, Skehel M, Uhlmann F (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321:563–566

    Article  PubMed  CAS  Google Scholar 

  84. Zhang J, Shi X, Li Y, Kim BJ, Jia J, Huang Z, Yang T, Fu X, Jung SY, Wang Y, Zhang P, Kim ST, Pan X, Qin J (2008) Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol Cell 31:143–151

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  86. Schuldiner O, Berdnik D, Levy JM, Wu JS, Luginbuhl D, Gontang AC, Luo L (2008) piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev Cell 14:227–238

    Article  PubMed  CAS  Google Scholar 

  87. Takagi S, Benard C, Pak J, Livingstone D, Hekimi S (1997) Cellular and axonal migrations are misguided along both body axes in the maternal-effect mau-2 mutants of Caenorhabditis elegans. Development 124:5115–5126

    PubMed  CAS  Google Scholar 

  88. Seitan VC, Banks P, Laval S, Majid NA, Dorsett D, Rana A, Smith J, Bateman A, Krpic S, Hostert A, Rollins RA, Erdjument-Bromage H, Tempst P, Benard CY, Hekimi S, Newbury SF, Strachan T (2006) Metazoan Scc4 homologs link sister chromatid cohesion to cell and axon migration guidance. PLoS Biol 4:1411–1425

    Article  CAS  Google Scholar 

  89. Pauli A, Althoff F, Oliveira RA, Heidmann S, Schuldiner O, Lehner CF, Dickson BJ, Nasmyth K (2008) Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons. Dev Cell 14:239–251

    Article  PubMed  CAS  Google Scholar 

  90. Horsfield JA, Anagnostou SH, Hu JK, Cho KHY, Geister R, Lieschke G, Crosier KE, Crosier PS (2007) Cohesin dependent regulation of Runx genes. Development 134:2639–2649

    Article  PubMed  CAS  Google Scholar 

  91. Revenkova E, Focarelli ML, Susani L, Paulis M, Bassi MT, Mannini L, Frattini A, Delia D, Krantz I, Vezzoni P, Jessberger R, Musio A (2008) Cornelia de Lange syndrome mutations in SMC1A or SMC3 affect binding to DNA. Hum Mol Genet 18:418–427

    Google Scholar 

  92. Gregson CH, Schmiesing JA, Kim JS, Kobayashi SZ, Yokomori K (2001) Potential role for human cohesin in mitotic spindle aster assembly. J Biol Chem 276:47575–47582

    Article  PubMed  CAS  Google Scholar 

  93. Wong W, Blobel G (2008) Cohesin subunit SMC1 associates with mitotic microtubules at the spindle pole. Proc Natl Acad Sci USA 105:15441–15445

    Article  PubMed  CAS  Google Scholar 

  94. Yazdi PT, Wang Y, Zhao S, Patel N, Lee EY-HP, In Y (2002) SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev 16: 571-582

  95. Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB (2004) Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev 18:1423–1438

    Article  PubMed  CAS  Google Scholar 

  96. Kim ST, Xu B, Kastan MB (2002) Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev 16:560–570

    Article  PubMed  CAS  Google Scholar 

  97. Luo H, Li Y, Mu JJ, Zhang J, Tonaka T, Hamamori Y, Jung SY, Wang Y, Qin J (2008) Regulation of intra-S phase checkpoint by ionizing radiation (IR)-dependent and IR-independent phosphorylation of SMC3. J Biol Chem 283:19176–19182

    Google Scholar 

  98. Shimizu K, Shirataki H, Honda T, Minami S, Takai Y (1998) Complex formation of SMAP/KAP3, a KIF3A/B ATPase motor-associated protein, with a human chromosome-associated polypeptide. J Biol Chem 273:6591–6594

    Article  PubMed  CAS  Google Scholar 

  99. Guan J, Etwurtzel E, Kvist U, Yuan L (2008) Cohesin protein SMC1 is a centrosomal protein. Biochem Biophys Res Commun 372:761–764

    Article  PubMed  CAS  Google Scholar 

  100. Wang X, Yang Y, Dai W (2006) Different subcellular localizations of two human Sgo1 isoforms. Cell Cycle 5:635–640

    PubMed  CAS  Google Scholar 

  101. Wang X, Yang Y, Duan Q, Jiang N, Huang Y, Darzynkiewicz Z, Dai W (2008) sSgo1, a major splice variant of Sgo1, functions in centriole cohesion where it is regulated by Plk1. Dev Cell 14:331–341

    Article  PubMed  CAS  Google Scholar 

  102. Skibbens RV (2008) Mechanisms of sister chromatid pairing. Int Rev Cell Mol Biol 269:283–339

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I apologize to all colleagues whose contributions have not been referenced due to space restrictions. We thank C. Mark for editorial assistance. This work was supported by the Spanish Ministerio de Educación y Ciencia (grants BFU2006-04406/BMC) and the Comunidad de Madrid (P-BIO-0189-2006).

Author information

Authors and Affiliations

  1. Departamento de Biología Celular y del Desarrollo, Centro de Investigaciones Biológicas (CSIC), C/Ramiro de Maeztu 9, 28040, Madrid, Spain

    José L. Barbero

Authors
  1. José L. Barbero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José L. Barbero.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barbero, J.L. Cohesins: chromatin architects in chromosome segregation, control of gene expression and much more. Cell. Mol. Life Sci. 66, 2025–2035 (2009). https://doi.org/10.1007/s00018-009-0004-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-009-0004-8

Keywords

Search

Navigation