Current Genetics

, Volume 64, Issue 5, pp 1005–1013 | Cite as

Cohesin dynamic association to chromatin and interfacing with replication forks in genome integrity maintenance

  • Sara Villa-Hernández
  • Rodrigo BermejoEmail author


Proliferating cells need to accurately duplicate and pass their genetic material on to daughter cells. Problems during replication and partition challenge the structural and numerical integrity of chromosomes. Diverse mechanisms, as the DNA replication checkpoint, survey the correct progression of replication and couple it with other cell cycle events to preserve genome integrity. The structural maintenance of chromosomes (SMC) cohesin complex primarily contributes to chromosome duplication by mediating the tethering of newly replicated sister chromatids, thus assisting their equal segregation in mitosis. In addition, cohesin exerts important functions in genome organization, gene expression and DNA repair. These are determined by cohesin’s ability to bring together different DNA segments and, hence, by the fashion and dynamics of its interaction with chromatin. It recently emerged that cohesin contributes to the protection of stalled replication forks through a mechanism requiring its timely mobilization from unreplicated DNA and relocation to nascent strands. This mechanism relies on DNA replication checkpoint-dependent cohesin ubiquitylation and promotes nascent sister chromatid entrapment, likely contributing to preserve stalled replisome-fork architectural integrity. Here we review how cohesin dynamic association to chromatin is controlled through post-translational modifications to dictate its functions during chromosome duplication. We also discuss recent insights on the mechanism that mediates interfacing of replisome components with chromatin-bound cohesin and its contribution to the establishment of sister chromatid cohesion and the protection of stalled replication forks.


Cohesin DNA replication Sister chromatid cohesion Replication forks DNA replication checkpoint Cell cycle Genome integrity 



We apologise for all the relevant findings and studies that could not be included in this review. This work was supported by the Ministry of Economy, Industry and Competitiveness—MINECO (BFU2014-52529-R and BFU2017-87013-R to R.B) and the Spanish Formación del Personal Investigador (FPI) program (to S.V-H.).


  1. Alabert C, Bukowski-Wills J-C, Lee S-B et al (2014) Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat Cell Biol 16:281–293. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alexandru G, Uhlmann F, Mechtler K et al (2001) Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell 105:459–472CrossRefPubMedCentralGoogle Scholar
  3. Alzu A, Bermejo R, Begnis M et al (2012) Senataxin associates with replication forks to protect fork integrity across RNA-polymerase-II-transcribed genes. Cell 151:835–846. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Azvolinsky A, Dunaway S, Torres JZ et al (2006) The S. cerevisiae Rrm3p DNA helicase moves with the replication forkand affects replication of allyeast chromosomes. Genes Dev 20:3104–3116. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Ball HL, Myers JS, Cortez D (2005) ATRIP binding to replication protein A-single-stranded DNA promotes ATR—ATRIP localization but is dispensable for Chk1 phosphorylation. Mol Biol Cell 16:2372–2381. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bando M, Katou Y, Komata M et al (2009) Csm3, Tof1, and Mrc1 form a heterotrimeric mediator complex that associates with DNA replication forks. J Biol Chem 284:34355–34365. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bartek J, Lukas J (2007) DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19:238–245. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bartkova J, Horejsí Z, Koed K et al (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434:864–870. CrossRefGoogle Scholar
  9. Bauerschmidt C, Woodcock M, Stevens DL et al (2011) Cohesin phosphorylation and mobility of SMC1 at ionizing radiation-induced DNA double-strand breaks in human cells. Exp Cell Res 317:330–337. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Beckouet F, Hu B, Roig MB et al (2010) An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Mol Cell 39:689–699. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bell SP, Labib K (2016) Chromosome duplication in Saccharomyces cerevisiae. Genetics 203:1027–1067. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bellaoui M, Chang M, Ou J et al (2003) Elg1 forms an alternative RFC complex important for DNA replication and genome integrity. EMBO J 22:4304–4313. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bermejo R, Doksani Y, Capra T et al (2007) Top1- and Top2-mediated topological transitions at replication forks ensure fork progression and stability and prevent DNA damage checkpoint activation. Genes Dev 21:1921–1936. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bermejo R, Capra T, Jossen R et al (2011) The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 146:233–246. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Branzei D, Foiani M (2010) Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 11:208–219. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Byun TS, Pacek M, Yee MC et al (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 19:1040–1052. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Calzada A, Hodgson B, Kanemaki M et al (2005) Molecular anatomy and regulation of a stable replisome eukaryotic DNA at a paused replication fork. Genes Dev 19:1905–1919. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Carretero M, Remeseiro S, Losada A (2010) Cohesin ties up the genome. Curr Opin Cell Biol 22:781–787. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chan K-L, Roig MB, Hu B et al (2012) Cohesin’s DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell 150:961–974. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Chan K-L, Gligoris T, Upcher W et al (2013) Pds5 promotes and protects cohesin acetylation. Proc Natl Acad Sci 110:13020–13025. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Chao WCH, Murayama Y, Muñoz S et al (2017) Structure of the cohesin loader Scc2. Nat Commun 8:13952. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Colosio A, Frattini C, Pellicanò G et al (2016) Nucleolytic processing of aberrant replication intermediates by an Exo1-Dna2-Sae2 axis counteracts fork collapse-driven chromosome instability. Nucleic Acids Res 12:gkw858. CrossRefGoogle Scholar
  23. Cotta-ramusino C, Fachinetti D, Lucca C et al (2005) Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol Cell 17:153–159. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Dantuma NP, Hoppe T (2012) Growing sphere of influence: Cdc48/p97 orchestrates ubiquitin-dependent extraction from chromatin. Trends Cell Biol 22:483–491. CrossRefPubMedPubMedCentralGoogle Scholar
  25. De Piccoli G, Katou Y, Itoh T et al (2012) Replisome stability at defective DNA replication forks is independent of S phase checkpoint kinases. Mol Cell 45:696–704. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ding DQ, Haraguchi T, Hiraoka Y (2016) A cohesin-based structural platform supporting homologous chromosome pairing in meiosis. Curr Genet 62:499–502. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Dorsett D (2011) Cohesin: genomic insights into controlling gene transcription and development. Curr Opin Genet Dev 21:199–206. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Doublié S, Zahn KE (2014) Structural insights into eukaryotic DNA replication. Front Microbiol 5:444. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Fragkos M, Naim V (2017) Rescue from replication stress during mitosis. Cell Cycle 16:613–633. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Frattini C, Villa-Hernández S, Pellicanò G et al (2017) Cohesin ubiquitylation and mobilization facilitate stalled replication fork dynamics. Mol Cell 68:758–772.e4. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Fujita M, Sasanuma H, Yamamoto KN et al (2013) Interference in DNA replication can cause mitotic chromosomal breakage unassociated with double-strand breaks. PLoS One. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Fumasoni M, Zwicky K, Vanoli F et al (2015) Error-free DNA damage tolerance and sister chromatid proximity during DNA replication rely on the Pol a/Primase/Ctf4 complex. Mol Cell 57:812–823. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gaillard H, García-Muse T, Aguilera A (2015) Replication stress and cancer. Nat Rev Cancer 15:276–289. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gan H, Yu C, Devbhandari S et al (2017) Checkpoint kinase Rad53 couples leading- and lagging-strand DNA synthesis under replication stress. Mol Cell 68:446–455.e3. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gelot C, Guirouilh-Barbat J, Le Guen T et al (2016) The cohesin complex prevents the end joining of distant DNA double-strand ends. Mol Cell. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Gligoris T, Löwe J (2016) Structural insights into ring formation of cohesin and related smc complexes. Trends Cell Biol 26:680–693. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Haarhuis JHI, van der Weide RH, Blomen VA et al (2017) The cohesin release factor WAPL restricts chromatin loop extension. Cell 169:693–707.e14. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Haering CH, Lo J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9:773–788CrossRefPubMedCentralGoogle Scholar
  39. Harreman M, Taschner M, Sigurdsson S et al (2009) Distinct ubiquitin ligases act sequentially for RNA polymerase II polyubiquitylation. Proc Natl Acad Sci USA 106:20705–20710. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hauf S, Roitinger E, Koch B et al (2005) Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol 3:0419–0432. CrossRefGoogle Scholar
  41. Heidinger-Pauli JM, Unal E, Koshland D (2009) Distinct targets of the Eco1 acetyltransferase modulate cohesion in S phase and in response to DNA damage. Mol Cell 34:311–321. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hill VK, Kim J-S, Waldman T (2016) Cohesin mutations in human cancer. Biochim Biophys Acta Rev Cancer 1866:1–11. CrossRefGoogle Scholar
  43. Hirano T (2015) Chromosome dynamics during mitosis. Cold Spring Harb Perspect Biol 7:1–14. CrossRefGoogle Scholar
  44. Jossen R, Bermejo R (2013) The DNA damage checkpoint response to replication stress: a game of forks. Front Genet 4:26. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kagey MH, Newman JJ, Bilodeau S et al (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467:430–435. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Katou Y, Kanoh Y, Bando M et al (2003) S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424:1078–1083. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Koninck M, De Losada A (2016) Cohesin mutations in human cancer. Cold Spring Harb Perspect Med. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kueng S, Hegemann B, Peters BH et al (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127:955–967. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kurat CF, Yeeles JTP, Patel H et al (2017) Chromatin controls DNA replication origin selection, lagging-strand synthesis, and replication fork rates. Mol Cell 65:117–130. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kurze A, Michie K, Dixon SE et al (2011) A positively charged channel within the Smc1/Smc3 hinge required for sister chromatid cohesion. EMBO J 30:364–378. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lai MS, Seki M, Tada S, Enomoto T (2012) Rmi1 functions in S phase-mediated cohesion establishment via a pathway involving the Ctf18-RFC complex and Mrc1. Biochem Biophys Res Commun 427:682–686. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Lecona E, Fernández-Capetillo O (2014) Replication stress and cancer: it takes two to tango. Exp Cell Res 329:26–34. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Li S, Yue Z, Tanaka TU (2017) Smc3 deacetylation by Hos1 facilitates efficient dissolution of sister chromatid cohesion during early anaphase. Mol Cell 68:605–614.e4. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lin SJ, O’Connell MJ (2017) DNA Topoisomerase II modulates acetyl-regulation of cohesin-mediated chromosome dynamics. Curr Genet 63:923–930. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Liu H, Rankin S, Yu H (2013) Phosphorylation-enabled binding of SGO1-PP2A to cohesin protects sororin and centromeric cohesion during mitosis. Nat Cell Biol 15:40–49. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Lopez-Serra L, Lengronne A, Borges V et al (2013) Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Curr Biol 23:64–69. CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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 16:3004–3016. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Lujan SA, Williams JS, Kunkel TA (2016) DNA polymerases divide the labor of genome replication. Trends Cell Biol 26:640–654. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Maradeo ME, Skibbens RV (2010) Replication factor C complexes play unique pro- and anti-establishment roles in sister chromatid cohesion. PLoS One 5:1–9. CrossRefGoogle Scholar
  60. Maric M, Maculins T, De Piccoli G, Labib K (2014) Cdc48 and a ubiquitin ligase drive disassembly of the CMG helicase at the end of DNA replication. Science 346:1253596–1253596. CrossRefPubMedPubMedCentralGoogle Scholar
  61. McAleenan A, Clemente-Blanco A, Cordon-Preciado V et al (2013) Post-replicative repair involves separase-dependent removal of the kleisin subunit of cohesin. Nature 493:250–254. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Mehta GD, Rizvi SMA, Ghosh SK (2012) Cohesin: a guardian of genome integrity. Biochim Biophys Acta Mol Cell Res 1823:1324–1342. CrossRefGoogle Scholar
  63. Michaelis C, Ciosk R, Nasmyth K (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91:35–45. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Morales C, Losada A (2018) Establishing and dissolving cohesion during the vertebrate cell cycle. Curr Opin Cell Biol. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Murayama Y, Uhlmann F (2015) DNA entry into and exit out of the cohesin ring by an interlocking gate mechanism. Cell 163:1628–1640. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Murayama Y, Samora CP, Kurokawa Y et al (2018) Establishment of DNA–DNA interactions by the cohesin ring. Cell. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Nasmyth K (2011) Cohesin: a catenase with separate entry and exit gates? Nat Cell Biol 13:1170–1177. CrossRefGoogle Scholar
  68. Pasero P, Vindigni A (2017) Nucleases acting at stalled forks: how to reboot the replication program with a few shortcuts. Annu Rev Genet 51:477–499. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Poli J, Tsaponina O, Crabbé L et al (2012) dNTP pools determine fork progression and origin usage under replication stress. EMBO J 31:883–894. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Remeseiro S, Cuadrado A, Carretero M et al (2012) Cohesin-SA1 deficiency drives aneuploidy and tumourigenesis in mice due to impaired replication of telomeres. EMBO J 31:2076–2089. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Rhodes JDP, Haarhuis JHI, Grimm JB et al (2017) Cohesin can remain associated with chromosomes during DNA replication. Cell Rep 20:2749–2755. CrossRefPubMedPubMedCentralGoogle Scholar
  72. Ribeyre C, Zellweger R, Chauvin M et al (2016) Nascent DNA proteomics reveals a chromatin remodeler required for Topoisomerase I loading at replication forks. Cell Rep. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Robellet X, Vanoosthuyse V, Bernard P (2017) The loading of condensin in the context of chromatin. Curr Genet 63:577–589. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Rossi SE, Ajazi A, Carotenuto W et al (2015) Rad53-mediated regulation of Rrm3 and Pif1 DNA helicases contributes to prevention of aberrant fork transitions under replication stress. Cell Rep 13:80–92. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rudra S, Skibbens RV (2012) Sister chromatid cohesion establishment occurs in concert with lagging strand synthesis. Cell Cycle 11:2114–2121. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Samora CP, Saksouk J, Goswami P et al (2016) Ctf4 links DNA replication with sister chromatid cohesion establishment by recruiting the Chl1 helicase to the replisome. Mol Cell. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Seeber A, Hegnauer AM, Hustedt N et al (2016) RPA mediates recruitment of MRX to forks and double-strand breaks to hold sister chromatids together. Mol Cell. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Siddiqui K, On KF, Diffley JFX (2013) Regulating DNA replication in eukarya. Cold Spring Harb Perspect Biol 5:1–17. CrossRefGoogle Scholar
  79. Skibbens RV (2016) Of rings and rods: regulating cohesin entrapment of DNA to generate intra- and intermolecular tethers. PLOS Genet 12:e1006337. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Sogo JM, Lopes M, Foiani M (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297:599–602. CrossRefPubMedPubMedCentralGoogle Scholar
  81. Solomon DA, Kim J-SS, Waldman T (2014) Cohesin gene mutations in tumorigenesis: from discovery to clinical significance. BMB Rep 47:299–310. CrossRefPubMedPubMedCentralGoogle Scholar
  82. Stolz A, Hilt W, Buchberger A, Wolf DH (2011) Cdc48: a power machine in protein degradation. Trends Biochem Sci 36:515–523. CrossRefPubMedPubMedCentralGoogle Scholar
  83. Ström L, Lindroos HB, Shirahige K, Sjögren C (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16:1003–1015. CrossRefPubMedPubMedCentralGoogle Scholar
  84. Sutani T, Kawaguchi T, Kanno R et al (2009) Budding yeast Wpl1(Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr Biol 19:492–497. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Tercero JA, Diffley JF (2001) Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412:553–557. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Thattikota Y, Tollis S, Palou R et al (2018) Cdc48/VCP promotes chromosome morphogenesis by releasing condensin from self-entrapment in chromatin. Mol Cell 69:664–676.e5. CrossRefPubMedPubMedCentralGoogle Scholar
  87. Tittel-Elmer M, Alabert C, Pasero P, Cobb J (2009) The MRX complex stabilizes the replisome independently of the S phase checkpoint during replication stress. EMBO J 28:1142–1156. CrossRefPubMedPubMedCentralGoogle Scholar
  88. Tittel-Elmer M, Lengronne A, Davidson MB et al (2012) Cohesin association to replication sites depends on Rad50 and promotes fork restart. Mol Cell. CrossRefPubMedPubMedCentralGoogle Scholar
  89. Tourrière H, Versini G, Cordón-Preciado V et al (2005) Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol Cell 19:699–706. CrossRefPubMedPubMedCentralGoogle Scholar
  90. Uhlmann F (2016) SMC complexes: from DNA to chromosomes. Nat Rev Mol Cell Biol. CrossRefPubMedPubMedCentralGoogle Scholar
  91. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  92. van den Boom J, Wolf M, Weimann L et al (2016) VCP/p97 extracts sterically trapped Ku70/80 rings from DNA in double-strand break repair. Mol Cell 64:189–198. CrossRefPubMedPubMedCentralGoogle Scholar
  93. Verma R, Oania R, Fang R et al (2011) Cdc48/p97 mediates UV-dependent turnover of RNA Pol II. Mol Cell 41:82–92. CrossRefPubMedPubMedCentralGoogle Scholar
  94. Villa F, Simon AC, Ortiz Bazan MA et al (2016) Ctf4 is a Hub in the eukaryotic replisome that links multiple CIP-box proteins to the CMG helicase. Mol Cell. CrossRefPubMedPubMedCentralGoogle Scholar
  95. Wenzel ES, Singh ATK (2018) Cell-cycle checkpoints and aneuploidy on the path to cancer. In Vivo (Brooklyn) 32:1–5. CrossRefGoogle Scholar
  96. Xiong B, Lu S, Gerton JL (2010) Hos1 is a lysine deacetylase for the Smc3 subunit of cohesin. Curr Biol 20:1660–1665. CrossRefPubMedPubMedCentralGoogle Scholar
  97. Xu H, Boone C, Brown GW (2007) Genetic dissection of parallel sister-chromatid cohesion pathways. Genetics 176:1417–1429. CrossRefPubMedPubMedCentralGoogle Scholar
  98. Yazdi PT, Wang Y, Zhao S et al (2002) SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev 16:571–582. CrossRefPubMedPubMedCentralGoogle Scholar
  99. Yeeles JTP, Janska A, Early A, Diffley JFX (2017) How the Eukaryotic Replisome Achieves Rapid And Efficient DNA replication. Mol Cell 65:105–116. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Zakari M, Yuen K, Gerton JL (2015) Etiology and pathogenesis of the cohesinopathies. Wiley Interdiscip Rev Dev Biol. CrossRefPubMedPubMedCentralGoogle Scholar
  101. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542–1548. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centro de Investigaciones Biológicas (CIB-CSIC)MadridSpain
  2. 2.Wolfson Centre for Age-Related DiseasesKing’s College LondonLondonUK

Personalised recommendations