Skip to main content
SpringerLink
Log in

Linking Chromosome Duplication and Segregation via Sister Chromatid Cohesion

  • Protocol
  • First Online:
Cell Cycle Control

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1170))

Abstract

DNA replication during S phase generates two identical copies of each chromosome. Each chromosome is destined for a daughter cell, but each daughter must receive one and only one copy of each chromosome. To ensure accurate chromosome segregation, eukaryotic cells are equipped with a mechanism to pair the chromosomes during chromosome duplication and hold the pairs until a bi-oriented mitotic spindle is formed and the pairs are pulled apart. This mechanism is known as sister chromatid cohesion, and its actions span the entire cell cycle. During G1, before DNA is copied during S phase, proteins termed cohesins are loaded onto DNA. Paired chromosomes are held together through G2 phase, and finally the cohesins are dismantled during mitosis. The processes governing sister chromatid cohesion ensure that newly replicated sisters are held together from the moment they are generated to the metaphase–anaphase transition, when sisters separate.

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

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Hirano T (2002) The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev 16(4): 399–414

    CAS  PubMed  Google Scholar 

  2. Haering CH, Lowe J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9(4):773–788

    CAS  PubMed  Google Scholar 

  3. Hirano T, Mitchison TJ (1994) A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79(3): 449–458

    CAS  PubMed  Google Scholar 

  4. Hirano T, Kobayashi R, Hirano M (1997) Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 89(4):511–521

    CAS  PubMed  Google Scholar 

  5. Fousteri MI, Lehmann AR (2000) A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J 19(7):1691–1702

    CAS  PubMed Central  PubMed  Google Scholar 

  6. Taylor EM, Moghraby JS, Lees JH, Smit B, Moens PB, Lehmann AR (2001) Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex. Mol Biol Cell 12(6): 1583–1594

    CAS  PubMed Central  PubMed  Google Scholar 

  7. Verkade HM, Bugg SJ, Lindsay HD, Carr AM, O’Connell MJ (1999) Rad18 is required for DNA repair and checkpoint responses in fission yeast. Mol Biol Cell 10(9):2905–2918

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Usui T, Ohta T, Oshiumi H, Tomizawa J, Ogawa H, Ogawa T (1998) Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95(5): 705–716

    CAS  PubMed  Google Scholar 

  9. Cobbe N, Heck MM (2000) Review: SMCs in the world of chromosome biology—from prokaryotes to higher eukaryotes. J Struct Biol 129(2–3):123–143

    CAS  PubMed  Google Scholar 

  10. Hirano M, Hirano T (2006) Opening closed arms: long-distance activation of SMC ATPase by hinge-DNA interactions. Mol Cell 21(2): 175–186

    CAS  PubMed  Google Scholar 

  11. Melby TE, Ciampaglio CN, Briscoe G, Erickson HP (1998) The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 142(6):1595–1604

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Furuya K, Takahashi K, Yanagida M (1998) Faithful anaphase is ensured by Mis4, a sister chromatid cohesion molecule required in S phase and not destroyed in G1 phase. Genes Dev 12(21):3408–3418

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Haering CH, Schoffnegger D, Nishino T, Helmhart W, Nasmyth K, Lowe J (2004) Structure and stability of cohesin’s Smc1-kleisin interaction. Mol Cell 15(6):951–964

    CAS  PubMed  Google Scholar 

  14. Schleiffer A, Kaitna S, Maurer-Stroh S, Glotzer M, Nasmyth K, Eisenhaber F (2003) Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol Cell 11(3):571–575

    CAS  PubMed  Google Scholar 

  15. 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(3):422–433

    CAS  PubMed  Google Scholar 

  16. 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(7180):796–801

    CAS  PubMed  Google Scholar 

  17. Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98(1):91–103

    CAS  PubMed  Google Scholar 

  18. 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(3):320–333

    Google Scholar 

  19. 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(3):405–416

    CAS  PubMed Central  PubMed  Google Scholar 

  20. Kurlandzka A, Rytka J, Gromadka R, Murawski M (1995) A new essential gene located on Saccharomyces cerevisiae chromosome IX. Yeast 11(9):885–890

    CAS  PubMed  Google Scholar 

  21. Zhang N, Jiang Y, Mao Q, Demeler B, Tao YJ, Pati D (2013) Characterization of the interaction between the cohesin subunits Rad21 and SA1/2. PLoS One 8(7):e69458

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Gruber S, Haering CH, Nasmyth K (2003) Chromosomal cohesin forms a ring. Cell 112(6):765–777

    CAS  PubMed  Google Scholar 

  23. Nasmyth K (2011) Cohesin: a catenase with separate entry and exit gates? Nat Cell Biol 13(10):1170–1177

    CAS  PubMed  Google Scholar 

  24. 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(1455):537–542

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Zhang N, Kuznetsov SG, Sharan SK, Li K, Rao PH, Pati D (2008) A handcuff model for the cohesin complex. J Cell Biol 183(6): 1019–1031

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Zhang N, Pati D (2009) Handcuff for sisters: a new model for sister chromatid cohesion. Cell Cycle 8(3):399–402

    PubMed Central  PubMed  Google Scholar 

  27. Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K (2008) The cohesin ring concatenates sister DNA molecules. Nature 454(7202):297–301

    CAS  PubMed  Google Scholar 

  28. 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(2):243–254

    CAS  PubMed  Google Scholar 

  29. 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(22):1941–1953

    CAS  PubMed  Google Scholar 

  30. Weitzer S, Lehane C, Uhlmann F (2003) A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr Biol 13(22): 1930–1940

    CAS  PubMed  Google Scholar 

  31. 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(1): 12–24

    CAS  PubMed  Google Scholar 

  32. 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(3):523–537

    CAS  PubMed  Google Scholar 

  33. Anderson DE, Trujillo KM, Sung P, Erickson HP (2001) Structure of the Rad50 × Mre11 DNA repair complex from Saccharomyces cerevisiae by electron microscopy. J Biol Chem 276(40):37027–37033

    CAS  PubMed  Google Scholar 

  34. Williams GJ, Lees-Miller SP, Tainer JA (2010) Mre11-Rad50-Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair (Amst) 9(12):1299–1306

    CAS  Google Scholar 

  35. Hopfner KP, Karcher A, Shin DS, Craig L, Arthur LM, Carney JP, Tainer JA (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101(7):789–800

    CAS  PubMed  Google Scholar 

  36. Mishra A, Hu B, Kurze A, Beckouet F, Farcas AM, Dixon SE, Katou Y, Khalid S, Shirahige K, Nasmyth K (2010) Both interaction surfaces within cohesin’s hinge domain are essential for its stable chromosomal association. Curr Biol 20(4):279–289

    CAS  PubMed Central  PubMed  Google Scholar 

  37. 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(6999): 573–578

    CAS  PubMed Central  PubMed  Google Scholar 

  38. Gillespie PJ, Hirano T (2004) Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr Biol 14(17):1598–1603

    CAS  PubMed  Google Scholar 

  39. 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(10): 991–996

    CAS  PubMed  Google Scholar 

  40. Fernius J, Marston AL (2009) Establishment of cohesion at the pericentromere by the Ctf19 kinetochore subcomplex and the replication fork-associated factor, Csm3. PLoS Genet 5(9):e1000629

    PubMed Central  PubMed  Google Scholar 

  41. Takahashi TS, Basu A, Bermudez V, Hurwitz J, Walter JC (2008) Cdc7-Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts. Genes Dev 22(14):1894–1905

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Schmidt CK, Brookes N, Uhlmann F (2009) Conserved features of cohesin binding along fission yeast chromosomes. Genome Biol 10(5):R52

    PubMed Central  PubMed  Google Scholar 

  43. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467(7314):430–435

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD, Carroll JS, Flicek P, Odom DT (2010) A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20(5):578–588

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Misulovin Z, Schwartz YB, Li XY, Kahn TG, Gause M, MacArthur S, Fay JC, Eisen MB, Pirrotta V, Biggin MD, Dorsett D (2008) Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome. Chromosoma 117(1): 89–102

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Lee BK, Iyer VR (2012) Genome-wide studies of CCCTC-binding factor (CTCF) and cohesin provide insight into chromatin structure and regulation. J Biol Chem 287(37):30906–30913

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Xiao T, Wallace J, Felsenfeld G (2011) Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Mol Cell Biol 31(11):2174–2183

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8(20): 1095–1101

    CAS  PubMed  Google Scholar 

  49. 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(6):787–799

    CAS  PubMed  Google Scholar 

  50. 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(15): 1571–1578

    CAS  PubMed  Google Scholar 

  51. 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(3):307–319

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Hou F, Zou H (2005) Two human orthologues of Eco1/Ctf7 acetyltransferases are both required for proper sister-chromatid cohesion. Mol Biol Cell 16(8):3908–3918

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Williams BC, Garrett-Engele CM, Li Z, Williams EV, Rosenman ED, Goldberg ML (2003) Two putative acetyltransferases, san and deco, are required for establishing sister chromatid cohesion in Drosophila. Curr Biol 13(23):2025–2036

    CAS  PubMed  Google Scholar 

  54. Bellows AM, Kenna MA, Cassimeris L, Skibbens RV (2003) Human EFO1p exhibits acetyltransferase activity and is a unique combination of linker histone and Ctf7p/Eco1p chromatid cohesion establishment domains. Nucleic Acids Res 31(21):6334–6343

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Ben-Shahar T, 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(5888):563–566

    CAS  Google Scholar 

  56. 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 (5888): 566–569

    PubMed  Google Scholar 

  57. 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(1):143–151

    CAS  PubMed  Google Scholar 

  58. Heidinger-Pauli JM, Onn I, Koshland D (2010) Genetic evidence that the acetylation of the Smc3p subunit of cohesin modulates its ATP-bound state to promote cohesion establishment in Saccharomyces cerevisiae. Genetics 185(4):1249–1256

    CAS  PubMed Central  PubMed  Google Scholar 

  59. 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(5): 955–967

    CAS  PubMed  Google Scholar 

  60. 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(24):2406–2417

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Rowland BD, Roig MB, Nishino T, Kurze A, Uluocak P, Mishra A, Beckouet F, Underwood P, Metson J, Imre R, Mechtler K, Katis VL, Nasmyth K (2009) Building sister chromatid cohesion: smc3 acetylation counteracts an antiestablishment activity. Mol Cell 33(6): 763–774

    CAS  PubMed  Google Scholar 

  62. Sutani T, Kawaguchi T, Kanno R, Itoh T, Shirahige K (2009) Budding yeast Wpl1 (Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr Biol 19(6):492–497

    Google Scholar 

  63. 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(2):185–200

    CAS  PubMed  Google Scholar 

  64. Schmitz J, Watrin E, Lenart 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(7):630–636

    CAS  PubMed  Google Scholar 

  65. Nishiyama T, Ladurner R, Schmitz J, Kreidl E, Schleiffer A, Bhaskara V, Bando M, Shirahige K, Hyman AA, Mechtler K, Peters JM (2010) Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143(5): 737–749

    CAS  PubMed  Google Scholar 

  66. Terret ME, Sherwood R, Rahman S, Qin J, Jallepalli PV (2009) Cohesin acetylation speeds the replication fork. Nature 462(7270): 231–234

    CAS  PubMed Central  PubMed  Google Scholar 

  67. 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(4):323–328

    CAS  PubMed  Google Scholar 

  68. Moldovan GL, Pfander B, Jentsch S (2006) PCNA controls establishment of sister chromatid cohesion during S phase. Mol Cell 23(5):723–732

    CAS  PubMed  Google Scholar 

  69. Moldovan GL, Pfander B, Jentsch S (2007) PCNA, the maestro of the replication fork. Cell 129(4):665–679

    CAS  PubMed  Google Scholar 

  70. Majka J, Burgers PM (2004) The PCNA-RFC families of DNA clamps and clamp loaders. Prog Nucleic Acid Res Mol Biol 78: 227–260

    CAS  PubMed  Google Scholar 

  71. Formosa T, Nittis T (1999) Dna2 mutants reveal interactions with Dna polymerase alpha and Ctf4, a Pol alpha accessory factor, and show that full Dna2 helicase activity is not essential for growth. Genetics 151(4): 1459–1470

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Hanna JS, Kroll ES, Lundblad V, Spencer FA (2001) Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol Cell Biol 21(9):3144–3158

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Mayer ML, Gygi SP, Aebersold R, Hieter P (2001) Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol Cell 7(5):959–970

    CAS  PubMed  Google Scholar 

  74. Naiki T, Kondo T, Nakada D, Matsumoto K, Sugimoto K (2001) Chl12 (Ctf18) forms a novel replication factor C-related complex and functions redundantly with Rad24 in the DNA replication checkpoint pathway. Mol Cell Biol 21(17):5838–5845

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Bermudez VP, Maniwa Y, Tappin I, Ozato K, Yokomori K, Hurwitz J (2003) The alternative Ctf18-Dcc1-Ctf8-replication factor C complex required for sister chromatid cohesion loads proliferating cell nuclear antigen onto DNA. Proc Natl Acad Sci U S A 100 (18):10237–10242

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Xu H, Boone C, Klein HL (2004) Mrc1 is required for sister chromatid cohesion to aid in recombination repair of spontaneous damage. Mol Cell Biol 24(16):7082–7090

    CAS  PubMed Central  PubMed  Google Scholar 

  77. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, Ashikari T, Sugimoto K, Shirahige K (2003) S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424(6952):1078–1083

    CAS  PubMed  Google Scholar 

  78. Lou H, Komata M, Katou Y, Guan Z, Reis CC, Budd M, Shirahige K, Campbell JL (2008) Mrc1 and DNA polymerase epsilon function together in linking DNA replication and the S phase checkpoint. Mol Cell 32(1): 106–117

    CAS  PubMed Central  PubMed  Google Scholar 

  79. Gambus A, van Deursen F, Polychronopoulos D, Foltman M, Jones RC, Edmondson RD, Calzada A, Labib K (2009) A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase alpha within the eukaryotic replisome. EMBO J 28(19):2992–3004

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Zhu W, Ukomadu C, Jha S, Senga T, Dhar SK, Wohlschlegel JA, Nutt LK, Kornbluth S, Dutta A (2007) Mcm10 and And-1/CTF4 recruit DNA polymerase alpha to chromatin for initiation of DNA replication. Genes Dev 21(18): 2288–2299

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Tanaka H, Katou Y, Yagura M, Saitoh K, Itoh T, Araki H, Bando M, Shirahige K (2009) Ctf4 coordinates the progression of helicase and DNA polymerase alpha. Genes Cells 14(7): 807–820

    CAS  PubMed  Google Scholar 

  82. Bermudez VP, Farina A, Tappin I, Hurwitz J (2010) Influence of the human cohesion establishment factor Ctf4/AND-1 on DNA replication. J Biol Chem 285(13):9493–9505

    CAS  PubMed Central  PubMed  Google Scholar 

  83. Leman AR, Noguchi E (2012) Local and global functions of Timeless and Tipin in replication fork protection. Cell Cycle 11(21):3945–3955

    CAS  PubMed Central  PubMed  Google Scholar 

  84. 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 Biol Cell 15(4): 1736–1745

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Warren CD, Eckley DM, Lee MS, Hanna JS, Hughes A, Peyser B, Jie C, Irizarry R, Spencer FA (2004) S-phase checkpoint genes safeguard high-fidelity sister chromatid cohesion. Mol Biol Cell 15(4):1724–1735

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Ansbach AB, Noguchi C, Klansek IW, Heidlebaugh M, Nakamura TM, Noguchi E (2008) RFCCtf18 and the Swi1-Swi3 complex function in separate and redundant pathways required for the stabilization of replication forks to facilitate sister chromatid cohesion in Schizosaccharomyces pombe. Mol Biol Cell 19(2):595–607

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Errico A, Cosentino C, Rivera T, Losada A, Schwob E, Hunt T, Costanzo V (2009) Tipin/Tim1/And1 protein complex promotes Pol alpha chromatin binding and sister chromatid cohesion. EMBO J 28(23):3681–3692

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Tanaka H, Kubota Y, Tsujimura T, Kumano M, Masai H, Takisawa H (2009) Replisome progression complex links DNA replication to sister chromatid cohesion in Xenopus egg extracts. Genes Cells 14(8):949–963

    CAS  PubMed  Google Scholar 

  89. Leman AR, Noguchi C, Lee CY, Noguchi E (2010) Human Timeless and Tipin stabilize replication forks and facilitate sister-chromatid cohesion. J Cell Sci 123(Pt 5):660–670

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Dheekollu J, Wiedmer A, Hayden J, Speicher D, Gotter AL, Yen T, Lieberman PM (2011) Timeless links replication termination to mitotic kinase activation. PLoS One 6(5): e19596

    CAS  PubMed Central  PubMed  Google Scholar 

  91. Smith-Roe SL, Patel SS, Simpson DA, Zhou YC, Rao S, Ibrahim JG, Kaiser-Rogers KA, Cordeiro-Stone M, Kaufmann WK (2011) Timeless functions independently of the Tim-Tipin complex to promote sister chromatid cohesion in normal human fibroblasts. Cell Cycle 10(10):1618–1624

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Sommariva E, Pellny TK, Karahan N, Kumar S, Huberman JA, Dalgaard JZ (2005) Schizosaccharomyces pombe Swi1, Swi3, and Hsk1 are components of a novel S-phase response pathway to alkylation damage. Mol Cell Biol 25(7):2770–2784

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Noguchi E, Noguchi C, McDonald WH, Yates JR 3rd, Russell P (2004) Swi1 and Swi3 are components of a replication fork protection complex in fission yeast. Mol Cell Biol 24(19):8342–8355

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Liu Y, Kao HI, Bambara RA (2004) Flap endonuclease 1: a central component of DNA metabolism. Annu Rev Biochem 73: 589–615

    CAS  PubMed  Google Scholar 

  95. Rudra S, Skibbens RV (2012) Sister chromatid cohesion establishment occurs in concert with lagging strand synthesis. Cell Cycle 11(11):2114–2121

    CAS  PubMed Central  PubMed  Google Scholar 

  96. Farina A, Shin JH, Kim DH, Bermudez VP, Kelman Z, Seo YS, Hurwitz J (2008) Studies with the human cohesin establishment factor, ChlR1. Association of ChlR1 with Ctf18-RFC and Fen1. J Biol Chem 283(30): 20925–20936

    CAS  PubMed Central  PubMed  Google Scholar 

  97. Wu Y, Suhasini AN, Brosh RM Jr (2009) Welcome the family of FANCJ-like helicases to the block of genome stability maintenance proteins. Cell Mol Life Sci 66(7):1209–1222

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Holloway SL, Poruthu J, Scata K (1999) Chromosome segregation and cancer. Exp Cell Res 253(2):308–314

    CAS  PubMed  Google Scholar 

  99. Petronczki M, Chwalla B, Siomos MF, Yokobayashi S, Helmhart W, Deutschbauer AM, Davis RW, Watanabe Y, Nasmyth K (2004) Sister-chromatid cohesion mediated by the alternative RF-CCtf18/Dcc1/Ctf8, the helicase Chl1 and the polymerase-alpha-associated protein Ctf4 is essential for chromatid disjunction during meiosis II. J Cell Sci 117(Pt 16):3547–3559

    CAS  PubMed  Google Scholar 

  100. Skibbens RV (2004) Chl1p, a DNA helicase-like protein in budding yeast, functions in sister-chromatid cohesion. Genetics 166(1):33–42

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Parish JL, Rosa J, Wang X, Lahti JM, Doxsey SJ, Androphy EJ (2006) The DNA helicase ChlR1 is required for sister chromatid cohesion in mammalian cells. J Cell Sci 119(Pt 23): 4857–4865

    CAS  PubMed  Google Scholar 

  102. Shah N, Inoue A, Woo Lee S, Beishline K, Lahti JM, Noguchi E (2013) Roles of ChlR1 DNA helicase in replication recovery from DNA damage. Exp Cell Res 319(14): 2244–2253

    CAS  PubMed  Google Scholar 

  103. Sherwood R, Takahashi TS, Jallepalli PV (2010) Sister acts: coordinating DNA replication and cohesion establishment. Genes Dev 24(24):2723–2731

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Onn I, Heidinger-Pauli JM, Guacci V, Unal E, Koshland DE (2008) Sister chromatid cohesion: a simple concept with a complex reality. Annu Rev Cell Dev Biol 24:105–129

    CAS  PubMed  Google Scholar 

  105. Lyons NA, Morgan DO (2011) Cdk1-dependent destruction of Eco1 prevents cohesion establishment after S phase. Mol Cell 42(3):378–389

    CAS  PubMed Central  PubMed  Google Scholar 

  106. Lyons NA, Fonslow BR, Diedrich JK, Yates JR 3rd, Morgan DO (2013) Sequential primed kinases create a damage-responsive phosphodegron on Eco1. Nat Struct Mol Biol 20(2):194–201

    CAS  PubMed Central  PubMed  Google Scholar 

  107. Unal E, Heidinger-Pauli JM, Koshland D (2007) DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317(5835): 245–248

    PubMed  Google Scholar 

  108. Strom L, Karlsson C, Lindroos HB, Wedahl S, Katou Y, Shirahige K, Sjogren C (2007) Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317(5835):242–245

    PubMed  Google Scholar 

  109. Strom L, Lindroos HB, Shirahige K, Sjogren C (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16(6):1003–1015

    PubMed  Google Scholar 

  110. Kurze A, Michie KA, Dixon SE, Mishra A, Itoh T, Khalid S, Strmecki L, Shirahige K, Haering CH, Lowe J, Nasmyth K (2011) A positively charged channel within the Smc1/Smc3 hinge required for sister chromatid cohesion. EMBO J 30(2):364–378

    CAS  PubMed Central  PubMed  Google Scholar 

  111. Panizza S, Tanaka T, Hochwagen A, Eisenhaber F, Nasmyth K (2000) Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr Biol 10(24): 1557–1564

    CAS  PubMed  Google Scholar 

  112. Chan KL, Roig MB, Hu B, Beckouet F, Metson J, Nasmyth K (2012) Cohesin’s DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell 150(5): 961–974

    CAS  PubMed Central  PubMed  Google Scholar 

  113. Lopez-Serra L, Lengronne A, Borges V, Kelly G, Uhlmann F (2013) Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Curr Biol 23(1):64–69

    CAS  PubMed  Google Scholar 

  114. Chan KL, Gligoris T, Upcher W, Kato Y, Shirahige K, Nasmyth K, Beckouet F (2013) Pds5 promotes and protects cohesin acetylation. Proc Natl Acad Sci U S A 110: 13020–13025

    CAS  PubMed Central  PubMed  Google Scholar 

  115. Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H (2008) A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 7(7):1389–1396

    CAS  PubMed Central  PubMed  Google Scholar 

  116. Hegemann B, Hutchins JR, Hudecz O, Novatchkova M, Rameseder J, Sykora MM, Liu S, Mazanek M, Lenart P, Heriche JK, Poser I, Kraut N, Hyman AA, Yaffe MB, Mechtler K, Peters JM (2011) Systematic phosphorylation analysis of human mitotic protein complexes. Sci Signal 4(198):rs12

    PubMed  Google Scholar 

  117. 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(3):e69

    PubMed Central  PubMed  Google Scholar 

  118. 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(3):515–525

    CAS  PubMed  Google Scholar 

  119. 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

    CAS  PubMed Central  PubMed  Google Scholar 

  120. Salic A, Waters JC, Mitchison TJ (2004) Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis. Cell 118(5):567–578

    CAS  PubMed  Google Scholar 

  121. 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(3):e86

    PubMed Central  PubMed  Google Scholar 

  122. 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(1):40–49

    CAS  PubMed Central  PubMed  Google Scholar 

  123. 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(7089):46–52

    CAS  PubMed  Google Scholar 

  124. Hauf S, Waizenegger IC, Peters JM (2001) Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293(5533):1320–1323

    CAS  PubMed  Google Scholar 

  125. Uhlmann F, Lottspeich F, Nasmyth K (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400(6739):37–42

    CAS  PubMed  Google Scholar 

  126. Waizenegger I, Gimenez-Abian JF, Wernic D, Peters JM (2002) Regulation of human separase by securin binding and autocleavage. Curr Biol 12(16):1368–1378

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  128. 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(24): 3081–3093

    CAS  PubMed  Google Scholar 

  129. Yamamoto A, Guacci V, Koshland D (1996) Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s). J Cell Biol 133(1): 99–110

    CAS  PubMed  Google Scholar 

  130. Thornton BR, Toczyski DP (2003) Securin and B-cyclin/CDK are the only essential targets of the APC. Nat Cell Biol 5(12): 1090–1094

    CAS  PubMed  Google Scholar 

  131. Hunt P, Hassold T (2010) Female meiosis: coming unglued with age. Curr Biol 20(17): R699–R702

    CAS  PubMed  Google Scholar 

  132. Hassold T, Abruzzo M, Adkins K, Griffin D, Merrill M, Millie E, Saker D, Shen J, Zaragoza M (1996) Human aneuploidy: incidence, origin, and etiology. Environ Mol Mutagen 28(3):167–175

    CAS  PubMed  Google Scholar 

  133. Nagaoka SI, Hassold TJ, Hunt PA (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13(7):493–504

    CAS  PubMed Central  PubMed  Google Scholar 

  134. Liu J, Zhang Z, Bando M, Itoh T, Deardorff MA, Clark D, Kaur M, Tandy S, Kondoh T, Rappaport E, Spinner NB, Vega H, Jackson LG, Shirahige K, Krantz ID (2009) Transcriptional dysregulation in NIPBL and cohesin mutant human cells. PLoS Biol 7(5): e1000119

    PubMed Central  PubMed  Google Scholar 

  135. 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(5):528–530

    CAS  PubMed  Google Scholar 

  136. 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(6):636–641

    CAS  PubMed  Google Scholar 

  137. 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(6):631–635

    CAS  PubMed  Google Scholar 

  138. Deardorff MA, Kaur M, Yaeger D, Rampuria A, Korolev S, Pie J, Gil-Rodriguez 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(3):485–494

    CAS  PubMed Central  PubMed  Google Scholar 

  139. Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, Minamino M, Saitoh K, Komata M, Katou Y, Clark D, Cole KE, de Baere E, Decroos C, di Donato N, Ernst S, Francey LJ, Gyftodimou Y, Hirashima K, Hullings M, Ishikawa Y, Jaulin C, Kaur M, Kiyono T, Lombardi PM, Magnaghi-Jaulin L, Mortier GR, Nozaki N, Petersen MB, Seimiya H, Siu VM, Suzuki Y, Takagaki K, Wilde JJ, Willems PJ, Prigent C, Gillessen-Kaesbach G, Christianson DW, Kaiser FJ, Jackson LG, Hirota T, Krantz ID, Shirahige K (2012) HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature 489(7415):313–317

    CAS  PubMed Central  PubMed  Google Scholar 

  140. Vrouwe MG, Elghalbzouri-Maghrani E, Meijers M, Schouten P, Godthelp BC, Bhuiyan ZA, Redeker EJ, Mannens MM, Mullenders LH, Pastink A, Darroudi F (2007) Increased DNA damage sensitivity of Cornelia de Lange syndrome cells: evidence for impaired recombinational repair. Hum Mol Genet 16(12):1478–1487

    CAS  PubMed  Google Scholar 

  141. 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(5):468–470

    CAS  PubMed  Google Scholar 

  142. Suhasini AN, Brosh RM Jr (2013) Disease-causing missense mutations in human DNA helicase disorders. Mutat Res 752(2): 138–152

    CAS  PubMed Central  PubMed  Google Scholar 

  143. 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(2):262–266

    PubMed Central  PubMed  Google Scholar 

  144. Capo-Chichi JM, Bharti SK, Sommers JA, Yammine T, Chouery E, Patry L, Rouleau GA, Samuels ME, Hamdan FF, Michaud JL, Brosh RM Jr, Megarbane A, Kibar Z (2013) Identification and biochemical characterization of a novel mutation in DDX11 causing Warsaw breakage syndrome. Hum Mutat 34(1):103–107

    CAS  PubMed  Google Scholar 

  145. Deans AJ, West SC (2011) DNA interstrand crosslink repair and cancer. Nat Rev Cancer 11(7):467–480

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by NIH grants (AG035480 to A.R.L. and GM0776043 to E.N.).

Author information

Authors and Affiliations

  1. Department of Biology, Duke University, Durham, NC, USA

    Adam R. Leman

  2. Duke Center for Systems Biology, Duke University, Durham, NC, USA

    Adam R. Leman

  3. Department of Biochemistry and Molecular Biology, Drexel University College of Medicine, 245 15th Street, MS 497, Philadelphia, PA, 19102, USA

    Eishi Noguchi

Authors
  1. Adam R. Leman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eishi Noguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eishi Noguchi .

Editor information

Editors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Drexel University College of Medicine, Philadelphia, Pennsylvania, USA

    Eishi Noguchi

  2. Dept of Biochemistry & Molecular Biology, Drexel University College of Medicine, Philadelphia, USA

    Mariana C. Gadaleta

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this protocol

Cite this protocol

Leman, A.R., Noguchi, E. (2014). Linking Chromosome Duplication and Segregation via Sister Chromatid Cohesion. In: Noguchi, E., Gadaleta, M. (eds) Cell Cycle Control. Methods in Molecular Biology, vol 1170. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-0888-2_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-0888-2_5

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-0887-5

  • Online ISBN: 978-1-4939-0888-2

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation