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Centromeric Cohesin: Molecular Glue and Much More

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Centromeres and Kinetochores

Part of the book series: Progress in Molecular and Subcellular Biology ((PMSB,volume 56))

Abstract

Sister chromatid cohesion, mediated by the cohesin complex, is a prerequisite for faithful chromosome segregation during mitosis. Premature release of sister chromatid cohesion leads to random segregation of the genetic material and consequent aneuploidy. Multiple regulatory mechanisms ensure proper timing for cohesion establishment, concomitant with DNA replication, and cohesion release during the subsequent mitosis. Here we summarize the most important phases of the cohesin cycle and the coordination of cohesion release with the progression through mitosis. We further discuss recent evidence that has revealed additional functions for centromeric localization of cohesin in the fidelity of mitosis in metazoans. Beyond its well-established role as “molecular glue”, centromeric cohesin complexes are now emerging as a scaffold for multiple fundamental processes during mitosis, including the formation of correct chromosome and kinetochore architecture, force balance with the mitotic spindle, and the association with key molecules that regulate mitotic fidelity, particularly at the chromosomal inner centromere. Centromeric chromatin may be thus seen as a dynamic place where cohesin ensures mitotic fidelity by multiple means.

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References

  • Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, Arellano-Santoyo H, Gonen T, Ranish JA, Asbury CL, Biggins S (2010) Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468:576–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Arumugam P, Gruber S, Tanaka K, Haering CH, Mechtler K, Nasmyth K (2003) ATP hydrolysis is required for cohesin’s association with chromosomes. Curr Biol 13:1941–1953

    Article  CAS  PubMed  Google Scholar 

  • Bachant J, Alcasabas A, Blat Y, Kleckner N, Elledge SJ (2002) The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol Cell 9:1169–1182

    Article  CAS  PubMed  Google Scholar 

  • Baumann C, Korner R, Hofmann K, Nigg EA (2007) PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 128:101–114

    Article  CAS  PubMed  Google Scholar 

  • Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542

    Article  CAS  PubMed  Google Scholar 

  • Biggins S (2015) Under tension: kinetochores and basic research. Genetics 200:681–682

    Article  PubMed  PubMed Central  Google Scholar 

  • Biggins S, Murray AW (2001) The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev 15:3118–3129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blat Y, Kleckner N (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98:249–259

    Article  CAS  PubMed  Google Scholar 

  • Buheitel J, Stemmann O (2013) Prophase pathway-dependent removal of cohesin from human chromosomes requires opening of the Smc3-Scc1 gate. EMBO J 32:666–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burkhardt S, Borsos M, Szydlowska A, Godwin J, Williams SA, Cohen PE, Hirota T, Saitou M, Tachibana-Konwalski K (2016) Chromosome cohesion established by Rec8-cohesin in fetal oocytes is maintained without detectable turnover in oocytes arrested for months in mice. Curr Biol 26:678–685

    Google Scholar 

  • Carmena M, Wheelock M, Funabiki H, Earnshaw WC (2012) The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat Rev Mol Cell Biol 13:789–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carretero M, Ruiz-Torres M, Rodriguez-Corsino M, Barthelemy I, Losada A (2013) Pds5B is required for cohesion establishment and Aurora B accumulation at centromeres. EMBO J 32:2938–2949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A et al (2000) Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5:243–254

    Article  CAS  PubMed  Google Scholar 

  • Ciosk R, Zachariae W, Michaelis C, Shevchenko 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  CAS  PubMed  Google Scholar 

  • Dawlaty MM, Malureanu L, Jeganathan KB, Kao E, Sustmann C, Tahk S, Shuai K, Grosschedl R, van Deursen JM (2008) Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha. Cell 133:103–115

    Google Scholar 

  • De Koninck M, Losada A (2016) Cohesin mutations in cancer. Cold Spring Harb Perspect Med 6:a026476

    Google Scholar 

  • Diaz-Martinez LA, Gimenez-Abian JF, Clarke DJ (2008) Chromosome cohesion—rings, knots, orcs and fellowship. J Cell Sci 121:2107–2114

    Article  CAS  PubMed  Google Scholar 

  • Dorsett D (2007) Roles of the sister chromatid cohesion apparatus in gene expression, development, and human syndromes. Chromosoma 116:1–13

    Article  PubMed  Google Scholar 

  • Dreier MR, Bekier ME 2nd, Taylor WR (2011) Regulation of sororin by Cdk1-mediated phosphorylation. J Cell Sci 124:2976–2987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drpic D, Pereira AJ, Barisic M, Maresca TJ, Maiato H (2015) Polar ejection forces promote the conversion from lateral to end-on kinetochore-microtubule attachments on mono-oriented chromosomes. Cell Rep 13:460–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eckert CA, Gravdahl DJ, Megee PC (2007) The enhancement of pericentromeric cohesin association by conserved kinetochore components promotes high-fidelity chromosome segregation and is sensitive to microtubule-based tension. Genes Dev 21:278–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eichinger CS, Kurze A, Oliveira RA, Nasmyth K (2013) Disengaging the Smc3/kleisin interface releases cohesin from Drosophila chromosomes during interphase and mitosis. EMBO J 32:656–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farcas AM, Uluocak P, Helmhart W, Nasmyth K (2011) Cohesin’s concatenation of sister DNAs maintains their intertwining. Mol Cell 44:97–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Funabiki H, Kumada K, Yanagida M (1996) Fission yeast Cut1 and Cut2 are essential for sister chromatid separation, concentrate along the metaphase spindle and form large complexes. EMBO J 15:6617–6628

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 16:1571–1578

    Article  CAS  PubMed  Google Scholar 

  • 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:E259

    Google Scholar 

  • Gorr IH, Boos D, Stemmann O (2005) Mutual inhibition of separase and Cdk1 by two-step complex formation. Mol Cell 19:135–141

    Article  CAS  PubMed  Google Scholar 

  • Gruber S, Arumugam P, Katou Y, Kuglitsch D, Helmhart W, Shirahige K, Nasmyth K (2006) Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 127:523–537

    Google Scholar 

  • Guacci V (2007) Sister chromatid cohesion: the cohesin cleavage model does not ring true. Genes Cells 12:693–708

    CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Haarhuis JH, Elbatsh AM, van den Broek B, Camps D, Erkan H, Jalink K, Medema RH, Rowland BD (2013) WAPL-mediated removal of cohesin protects against segregation errors and aneuploidy. Curr Biol 23:2071–2077

    Google Scholar 

  • Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K (2008) The cohesin ring concatenates sister DNA molecules. Nature 454:297–301

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hahn M, Dambacher S, Dulev S, Kuznetsova AY, Eck S, Worz S, Sadic D, Schulte M, Mallm JP, Maiser A et al (2013) Suv4-20h2 mediates chromatin compaction and is important for cohesin recruitment to heterochromatin. Genes Dev 27, 859–872

    Google Scholar 

  • Hara K, Zheng G, Qu Q, Liu H, Ouyang Z, Chen Z, Tomchick DR, Yu H (2014). Structure of cohesin subcomplex pinpoints direct shugoshin-Wapl antagonism in centromeric cohesion. Nat Struct Mol Biol 21:864–870

    Google Scholar 

  • 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:e69

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • He E, Kapuy O, Oliveira RA, Uhlmann F, Tyson JJ, Novak B (2011) System-level feedbacks make the anaphase switch irreversible. Proc Natl Acad Sci U S A 108:10016–10021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellmuth S, Pohlmann C, Brown A, Bottger F, Sprinzl M, Stemmann O (2015) Positive and negative regulation of vertebrate separase by Cdk1-cyclin B1 may explain why securin is dispensable. J Biol Chem 290:8002–8010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirano T, Funahashi S, Uemura T, Yanagida M (1986) Isolation and characterization of Schizosaccharomyces pombe cutmutants that block nuclear division but not cytokinesis. EMBO J 5:2973–2979

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holland AJ, Cleveland DW (2009) Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat Rev Mol Cell Biol 10:478–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hornig NC, Knowles PP, McDonald NQ, Uhlmann F (2002) The dual mechanism of separase regulation by securin. Curr Biol 12:973–982

    Article  CAS  PubMed  Google Scholar 

  • Hornig NC, Uhlmann F (2004) Preferential cleavage of chromatin-bound cohesin after targeted phosphorylation by Polo-like kinase. EMBO J 23:3144–3153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Itoh T, Mishra A, Katoh Y, Chan KL, Upcher W, Godlee C, Roig MB, Shirahige K, Nasmyth K (2011) ATP hydrolysis is required for relocating cohesin from sites occupied by its Scc2/4 loading complex. Curr Biol 21:12–24

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jallepalli PV, Waizenegger IC, Bunz F, Langer S, Speicher MR, Peters JM, Kinzler KW, Vogelstein B, Lengauer C (2001) Securin is required for chromosomal stability in human cells. Cell 105:445–457

    Article  CAS  PubMed  Google Scholar 

  • Kamenz J, Hauf S (2016) Time to split up: Dynamics of chromosome separation. Trends Cell Biol 27:42

    Google Scholar 

  • Karamysheva Z, Diaz-Martinez LA, Crow SE, Li B, Yu H (2009) Multiple anaphase-promoting complex/cyclosome degrons mediate the degradation of human Sgo1. J Biol Chem 284:1772–1780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenney RD, Heald R (2006) Essential roles for cohesin in kinetochore and spindle function in Xenopus egg extracts. J Cell Sci 119:5057–5066

    Article  CAS  PubMed  Google Scholar 

  • Kerrebrock AW, Miyazaki WY, Birnby D, Orr-Weaver TL (1992) The Drosophila mei-S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation. Genetics 130:827–841

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Koch B, Kueng S, Ruckenbauer C, Wendt KS, Peters JM (2008) The Suv39 h-HP1 histone methylation pathway is dispensable for enrichment and protection of cohesin at centromeres in mammalian cells. Chromosoma 117:199–210

    Article  PubMed  CAS  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Lenart P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N, Peters JM (2007) The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr Biol 17:304–315

    Article  CAS  PubMed  Google Scholar 

  • 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 430:573–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin Z, Luo X, Yu H (2016) Structural basis of cohesin cleavage by separase. Nature 532:131–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu D, Vader G, Vromans MJ, Lampson MA, Lens SM (2009a) Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323:1350–1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Jia L, Yu H (2013a) Phospho-H2A and cohesin specify distinct tension-regulated Sgo1 pools at kinetochores and inner centromeres. Curr Biol 23:1927–1933

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Rankin S, Yu H (2013b) Phosphorylation-enabled binding of SGO1-PP2A to cohesin protects sororin and centromeric cohesion during mitosis. Nat Cell Biol 15:40–49

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Deibler RW, Chan HS, Zechiedrich L (2009b) The why and how of DNA unlinking. Nucleic Acids Res 37:661–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Losada A (2014) Cohesin in cancer: chromosome segregation and beyond. Nat Rev Cancer 14:389–393

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maresca TJ, Salmon ED (2010) Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal. J Cell Sci 123:825–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marston AL (2015) Shugoshins: tension-sensitive pericentromeric adaptors safeguarding chromosome segregation. Mol Cell Biol 35:634–648

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McGuinness BE, Hirota T, Kudo NR, Peters JM, Nasmyth K (2005) Shugoshin prevents dissociation of cohesin from centromeres during mitosis in vertebrate cells. PLoS Biol 3:e86

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Megee PC, Koshland D (1999) A functional assay for centromere-associated sister chromatid cohesion. Science 285:254–257

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mirchenko L, Uhlmann F (2010) Sli15(INCENP) dephosphorylation prevents mitotic checkpoint reengagement due to loss of tension at anaphase onset. Curr Biol 20:1396–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirkovic M, Hutter LH, Novak B, Oliveira RA (2015) Premature sister chromatid separation is poorly detected by the spindle assembly checkpoint as a result of system-level feedback. Cell Rep 13:470–478

    Article  PubMed  CAS  Google Scholar 

  • Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8:379–393

    Article  CAS  PubMed  Google Scholar 

  • Nagasaka K, Hossain MJ, Roberti MJ, Ellenberg J, Hirota T (2016) Sister chromatid resolution is an intrinsic part of chromosome organization in prophase. Nat Cell Biol 18:692–699

    Article  CAS  PubMed  Google Scholar 

  • Nannas NJ, Murray AW (2014) Tethering sister centromeres to each other suggests the spindle checkpoint detects stretch within the kinetochore. PLoS Genet 10:e1004492

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nasmyth K, Haering CH (2009) Cohesin: Its roles and mechanisms. Annu Rev Genet 43:525–558

    Article  CAS  PubMed  Google Scholar 

  • Ng TM, Waples WG, Lavoie BD, Biggins S (2009) Pericentromeric sister chromatid cohesion promotes kinetochore biorientation. Mol Biol Cell 20:3818–3827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicklas RB, Ward SC, Gorbsky GJ (1995) Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J Cell Biol 130:929–939

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama T, Ladurner R, Schmitz J, Kreidl E, Schleiffer A, Bhaskara V, Bando M, Shirahige K, Hyman AA, Mechtler K et al (2010) Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143:737–749

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama T, Sykora MM, Huis in ‘t Veld PJ, Mechtler K, Peters JM (2013) Aurora B and Cdk1 mediate Wapl activation and release of acetylated cohesin from chromosomes by phosphorylating Sororin. Proc Natl Acad Sci U S A 110:13404–13409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:89–93

    Article  CAS  PubMed  Google Scholar 

  • Ocampo-Hafalla M, Munoz S, Samora CP, Uhlmann F (2016) Evidence for cohesin sliding along budding yeast chromosomes. Open Biol 6:150178

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ocampo-Hafalla MT, Katou Y, Shirahige K, Uhlmann F (2007) Displacement and re-accumulation of centromeric cohesin during transient pre-anaphase centromere splitting. Chromosoma 116:531–544

    Article  PubMed  PubMed Central  Google Scholar 

  • Ocampo-Hafalla MT, Uhlmann F (2011) Cohesin loading and sliding. J Cell Sci 124:685–691

    Article  CAS  PubMed  Google Scholar 

  • Oliveira RA, Hamilton RS, Pauli A, Davis I, Nasmyth K (2010) Cohesin cleavage and Cdk inhibition trigger formation of daughter nuclei. Nat Cell Biol 12:185–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira RA, Kotadia S, Tavares A, Mirkovic M, Bowlin K, Eichinger CS et al (2014) Centromere-independent accumulation of cohesin at ectopic heterochromatin sites induces chromosome stretching during anaphase. PLoS Biol 12:e1001962

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oliveira RA, Nasmyth K (2010) Getting through anaphase: splitting the sisters and beyond. Biochem Soc Trans 38:1639–1644

    Article  CAS  PubMed  Google Scholar 

  • Parry DH, Hickson GR, O’Farrell PH (2003) Cyclin B destruction triggers changes in kinetochore behavior essential for successful anaphase. Curr Biol 13:647–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel J, Tan SL, Hartshorne GM, McAinsh AD (2015) Unique geometry of sister kinetochores in human oocytes during meiosis I may explain maternal age-associated increases in chromosomal abnormalities. Biol Open 5:178–184

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Primorac I, Musacchio A (2013) Panta rhei: the APC/C at steady state. J Cell Biol 201:177–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Remeseiro S, Cuadrado A, Losada A (2013) Cohesin in development and disease. Development 140:3715–3718

    Article  CAS  PubMed  Google Scholar 

  • Renshaw MJ, Ward JJ, Kanemaki M, Natsume K, Nedelec FJ, Tanaka TU (2010) Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev Cell 19:232–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rudra S, Skibbens RV (2013) Cohesin codes—interpreting chromatin architecture and the many facets of cohesin function. J Cell Sci 126:31–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu H, Furuta M, Kirkpatrick D, Gygi SP, Azuma Y (2010) PIASy-dependent SUMOylation regulates DNA topoisomerase IIalpha activity. J Cell Biol 191:783–794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sen N, Leonard J, Torres R, Garcia-Luis J, Palou-Marin G, Aragon L (2016) Physical proximity of sister chromatids promotes top2-dependent intertwining. Mol Cell 64:134–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shindo N, Kumada K, Hirota T (2012) Separase sensor reveals dual roles for separase coordinating cohesin cleavage and cdk1 inhibition. Dev Cell 23:112–123

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Sonoda E, Matsusaka T, Morrison C, Vagnarelli P, Hoshi O, Ushiki T, Nojima K, Fukagawa T, Waizenegger IC, Peters JM et al (2001) Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells. Dev Cell 1:759–770

    Article  CAS  PubMed  Google Scholar 

  • Stemmann O, Zou H, Gerber SA, Gygi SP, Kirschner MW (2001) Dual inhibition of sister chromatid separation at metaphase. Cell 107:715–726

    Article  CAS  PubMed  Google Scholar 

  • Stephens AD, Quammen CW, Chang B, Haase J, Taylor RM 2nd, Bloom K (2013) The spatial segregation of pericentric cohesin and condensin in the mitotic spindle. Mol Biol Cell 24:3909–3919

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stigler J, Camdere GO, Koshland DE, Greene EC (2016) Single-molecule imaging reveals a collapsed conformational state for dna-bound cohesin. Cell Rep 15:988–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stratmann R, Lehner CF (1996) Separation of sister chromatids in mitosis requires the Drosophila pimples product, a protein degraded after the metaphase/anaphase transition. Cell 84:25–35

    Article  CAS  PubMed  Google Scholar 

  • Sullivan M, Morgan DO (2007) Finishing mitosis, one step at a time. Nat Rev Mol Cell Biol 8:894–903

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:515–525

    Article  CAS  PubMed  Google Scholar 

  • Tachibana-Konwalski K, Godwin J, Borsos M, Rattani A, Adams DJ, Nasmyth K (2013) Spindle assembly checkpoint of oocytes depends on a kinetochore structure determined by cohesin in meiosis I. Curr Biol 23:2534–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka T, Cosma MP, Wirth K, Nasmyth K (1999) Identification of cohesin association sites at centromeres and along chromosome arms. Cell 98:847–858

    Article  CAS  PubMed  Google Scholar 

  • 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 2:492–499

    Article  CAS  PubMed  Google Scholar 

  • Tanno Y, Kitajima TS, Honda T, Ando Y, Ishiguro K, Watanabe Y (2010) Phosphorylation of mammalian Sgo2 by Aurora B recruits PP2A and MCAK to centromeres. Genes Dev 24:2169–2179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanno Y, Susumu H, Kawamura M, Sugimura H, Honda T, Watanabe Y (2015) The inner centromere-shugoshin network prevents chromosomal instability. Science 349:1237–1240

    Article  CAS  PubMed  Google Scholar 

  • Tedeschi A, Wutz G, Huet S, Jaritz M, Wuensche A, Schirghuber E, Davidson IF, Tang W, Cisneros DA, Bhaskara V et al (2013) Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 501:564–568

    Article  CAS  PubMed  Google Scholar 

  • Tomkins D, Hunter A, Roberts M (1979) Cytogenetic findings in Roberts-SC phocomelia syndrome(s). Am J Med Genet 4:17–26

    Article  CAS  PubMed  Google Scholar 

  • Toth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A, Nasmyth K (1999) Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev 13:320–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toyoda Y, Yanagida M (2006) Coordinated requirements of human topo II and cohesin for metaphase centromere alignment under Mad2-dependent spindle checkpoint surveillance. Mol Biol Cell 17:2287–2302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8:1095–1101

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Uzunova K, Dye BT, Schutz H, Ladurner R, Petzold G, Toyoda Y, Jarvis MA, Brown NG, Poser I, Novatchkova M et al (2012) APC15 mediates CDC20 autoubiquitylation by APC/C(MCC) and disassembly of the mitotic checkpoint complex. Nat Struct Mol Biol 19:1116–1123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vagnarelli P, Morrison C, Dodson H, Sonoda E, Takeda S, Earnshaw WC (2004) Analysis of Scc1-deficient cells defines a key metaphase role of vertebrate cohesin in linking sister kinetochores. EMBO Rep 5:167–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Lelij P, Chrzanowska KH, Godthelp BC, Rooimans MA, Oostra AB, Stumm M, Zdzienicka MZ, Joenje H, de Winter JP (2010) Warsaw breakage syndrome, a cohesinopathy associated with mutations in the XPD helicase family member DDX11/ChlR1. Am J Hum Genet 86:262–266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vass S, Cotterill S, Valdeolmillos AM, Barbero JL, Lin E, Warren WD, Heck MM (2003) Depletion of Drad21/Scc1 in Drosophila cells leads to instability of the cohesin complex and disruption of mitotic progression. Curr Biol 13:208–218

    Article  CAS  PubMed  Google Scholar 

  • Vazquez-Novelle MD, Petronczki M (2010) Relocation of the chromosomal passenger complex prevents mitotic checkpoint engagement at anaphase. Curr Biol 20:1402–1407

    Article  CAS  PubMed  Google Scholar 

  • Vazquez-Novelle MD, Sansregret L, Dick AE, Smith CA, McAinsh AD, Gerlich DW, Petronczki M (2014) Cdk1 inactivation terminates mitotic checkpoint surveillance and stabilizes kinetochore attachments in anaphase. Curr Biol 24:638–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verni 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waizenegger I, Gimenez-Abian JF, Wernic D, Peters JM (2002) Regulation of human separase by securin binding and autocleavage. Curr Biol 12:1368–1378

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Warren WD, Steffensen S, Lin E, Coelho P, Loupart M, Cobbe N, Lee JY, McKay MJ, Orr-Weaver T, Heck MM et al (2000) The Drosophila RAD21 cohesin persists at the centromere region in mitosis. Curr Biol 10:1463–1466

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • 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:E260

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Webster A, Schuh M (2016) Mechanisms of aneuploidy in human eggs. Trends Cell Biol 21:55

    Google Scholar 

  • Weitzer S, Lehane C, Uhlmann F (2003) A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr Biol 13:1930–1940

    Article  CAS  PubMed  Google Scholar 

  • Woodman J, Fara T, Dzieciatkowska M, Trejo M, Luong N, Hansen KC, Megee PC (2014) Cell cycle-specific cleavage of Scc2 regulates its cohesin deposition activity. Proc Natl Acad Sci U S A 111:7060–7065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yaakov G, Thorn K, Morgan DO (2012) Separase biosensor reveals that cohesin cleavage timing depends on phosphatase PP2A(Cdc55) regulation. Dev Cell 23:124–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamagishi Y, Honda T, Tanno Y, Watanabe Y (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330:239–243

    Article  CAS  PubMed  Google Scholar 

  • Ye AA, Cane S, Maresca TJ (2016) Chromosome biorientation produces hundreds of piconewtons at a metazoan kinetochore. Nat Commun 7:13221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zielinska AP, Holubcova Z, Blayney M, Elder K, Schuh M (2015) Sister kinetochore splitting and precocious disintegration of bivalents could explain the maternal age effect. Elife 4:e11389

    Article  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

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  1. Instituto Gulbenkian de Ciência, Rua da Quinta Grande, 2780-156, Oeiras, Portugal

    Mihailo Mirkovic & Raquel A. Oliveira

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  1. Mihailo Mirkovic
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  2. Raquel A. Oliveira
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Correspondence to Raquel A. Oliveira .

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  1. Department of Biochemistry and Biophysics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Ben E. Black

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Mirkovic, M., Oliveira, R.A. (2017). Centromeric Cohesin: Molecular Glue and Much More. In: Black, B. (eds) Centromeres and Kinetochores. Progress in Molecular and Subcellular Biology, vol 56. Springer, Cham. https://doi.org/10.1007/978-3-319-58592-5_20

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