Skip to main content
SpringerLink
Log in

The Roles of Cohesins in Mitosis, Meiosis, and Human Health and Disease

  • Protocol
  • First Online:
Cell Cycle Control

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

Abstract

Mitosis and meiosis are essential processes that occur during development. Throughout these processes, cohesion is required to keep the sister chromatids together until their separation at anaphase. Cohesion is created by multiprotein subunit complexes called cohesins. Although the subunits differ slightly in mitosis and meiosis, the canonical cohesin complex is composed of four subunits that are quite diverse. The cohesin complexes are also important for DNA repair, gene expression, development, and genome integrity. Here we provide an overview of the roles of cohesins during these different events as well as their roles in human health and disease, including the cohesinopathies. Although the exact roles and mechanisms of these proteins are still being elucidated, this review serves as a guide for the current knowledge of cohesins.

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. 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

    CAS  PubMed  Google Scholar 

  2. 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

    CAS  PubMed  Google Scholar 

  3. Guacci V, Koshland D, Strunnikov AV (1997) A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91(1):47–57

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  5. 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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  7. Carramolino L, Lee BC, Zaballos A, Peled A, Barthelemy I, Shav-Tal Y, Prieto I, Carmi P, Gothelf Y, Gonzalez de Buitrago G, Aracil M, Marquez G, Barbero JL, Zipori D (1997) SA-1, a nuclear protein encoded by one member of a novel gene family: molecular cloning and detection in hemopoietic organs. Gene 195(2):151–159

    CAS  PubMed  Google Scholar 

  8. 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 

  9. Sumara I, Vorlaufer E, Gieffers C, Peters BH, Peters J-M (2000) Characterization of vertebrate cohesin complexes and their regulation in prophase. J Cell Biol 151(4):749–761

    CAS  PubMed Central  PubMed  Google Scholar 

  10. 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 

  11. Anderson DE, Losada A, Erickson HP, Hirano T (2002) Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol 156(3):419–424

    CAS  PubMed Central  PubMed  Google Scholar 

  12. 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 

  13. 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(23):3118–3129

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E, Stark MJR, Nasmyth K (2002) Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108:317–329

    CAS  PubMed  Google Scholar 

  15. He X, Rines DR, Espelin CW, Sorger PK (2001) Molecular analysis of kinetochore-microtubule attachment in budding yeast. Cell 106(2):195–206

    CAS  PubMed  Google Scholar 

  16. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW (1999) The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev 13(5):532–544

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Strunnikov AV, Larionov VL, Koshland D (1993) SMC1: an essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. J Cell Biol 123(6):1635–1648

    CAS  PubMed  Google Scholar 

  18. Strunnikov AV, Hogan E, Koshland D (1995) SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes Dev 9:587–599

    CAS  PubMed  Google Scholar 

  19. Hoque MT, Ishikawa F (2002) Cohesin defects lead to premature sister chromatid separation, kinetochore dysfunction, and spindle-assembly checkpoint activation. J Biol Chem 277(44):42306–42314

    CAS  PubMed  Google Scholar 

  20. Britton RA, Lin DC, Grossman AD (1998) Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12(9):1254–1259

    CAS  PubMed Central  PubMed  Google Scholar 

  21. Sonoda E, Matsusaka T, Morrison C, Vagnarelli P, Hoshi O, Ushiki T, Nojima K, Fukagawa T, Waizenegger IC, Peters J-M, Earnshaw WC, Takeda S (2001) Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells. Dev Cell 1:759–770

    CAS  PubMed  Google Scholar 

  22. Vass S, Cotterill S, Valdeolmillos AM, Barbero JL, Lin E, Warren WD, Heck MMS (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

    CAS  PubMed  Google Scholar 

  23. Diaz-Martinez LA, Gimenez-Abian JF, Clarke DJ (2007) Cohesin is dispensable for centromere cohesion in human cells. PLoS One 2(3):e318

    PubMed Central  PubMed  Google Scholar 

  24. Chang C-R, Wu C-S, Hom Y, Gartenberg MR (2005) Targeting of cohesin by transcriptionally silent chromatin. Genes Dev 19(24):3031–3042

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Losada A, Hirano T (2001) Intermolecular DNA interactions stimulated by the cohesin complex in vitro: Implications for sister chromatid cohesion. Curr Biol 11(4):268–272

    CAS  PubMed  Google Scholar 

  26. 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 

  27. 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 

  28. Sjogren C, Nasmyth K (2001) Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr Biol 11:991–995

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  31. 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(6):1067–1076

    CAS  PubMed  Google Scholar 

  32. Tomonaga T, Nagao K, Kawasaki Y, Furuya K, Murakami A, Morishita J, Yuasa T, Sutani T, Kearsey SE, Uhlmann F, Nasmyth K, Yanagida M (2000) Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. Genes Dev 14:2757–2770

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Losada A, Hirano M, Hirano T (1998) Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev 12(13):1986–1997

    CAS  PubMed Central  PubMed  Google Scholar 

  34. Waizenegger IC, Hauf S, Meinke A, Peters J-M (2000) Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103:399–410

    CAS  PubMed  Google Scholar 

  35. Sumara I, Vorlaufer E, Stukenberg PT, Kelm O, Redemann N, Nigg EA, Peters J-M (2002) The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell 9:515–525

    CAS  PubMed  Google Scholar 

  36. Alexandru G, Uhlmann F, Mechtler K, Poupart M-A, Nasmyth K (2001) Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell 105(4):459–472

    CAS  PubMed  Google Scholar 

  37. Hoque MT, Ishikawa F (2001) Human chromatid cohesin component hRad21 is phosphorylated in M phase and associated with metaphase centromeres. J Biol Chem 276(7):5059–5067

    CAS  PubMed  Google Scholar 

  38. Gimenez-Abian JF, Sumara I, Hirota T, Hauf S, Gerlich D, de la Torre C, Ellenberg J, Peters J-M (2004) Regulation of sister chromatid cohesion between chromosome arms. Curr Biol 14(13):1187–1193

    CAS  PubMed  Google Scholar 

  39. Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters J-M (2005) Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol 3(3):0419–0432

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  42. 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  44. Funabiki H, Yamano H, Kumada K, Nagao K, Hunt T, Yanagida M (1996) Cut2 proteolysis required for sister-chromatid separation in fission yeast. Nature 381(6581):438–441

    CAS  PubMed  Google Scholar 

  45. 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 

  46. Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, Peters J-M (2006) Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr Biol 16:863–874

    CAS  PubMed  Google Scholar 

  47. Lechner MS, Schultz DC, Negorev D, Maul GG, Rauscher FJ III (2005) The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem Biophys Res Commun 331(4):929–937

    CAS  PubMed  Google Scholar 

  48. Seitan VC, Banks P, Laval S, Majid NA, Dorsett D, Rana A, Smith J, Bateman A, Krpic S, Hostert A, Rollins RA, Erdjument-Bromage H, Tempst P, Benard CY, Hekimi S, Newbury SF, Strachan T (2006) Metazoan Scc4 homologs link sister chromatid cohesion to cell and axon migration guidance. PLoS Biol 4(8):e242

    Google Scholar 

  49. Hartman T, Stead K, Koshland D, Guacci V (2000) Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae. J Cell Biol 151(3):613–626

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  51. 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 

  52. 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

    CAS  PubMed  Google Scholar 

  53. Dai J, Sullivan BA, Higgins JMG (2006) Regulation of mitotic chromosome cohesion by Haspin and Aurora B. Dev Cell 11(5):741–750

    CAS  PubMed  Google Scholar 

  54. Wang F, Yoder J, Antoshechkin I, Han M (2003) Caenorhabditis elegans EVL-14/PDS5 and SCC-3 are essential for sister chromatid cohesion in meiosis and mitosis. Mol Cell Biol 23(21):7698–7707

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Losada A, Yokochi T, Hirano T (2005) Functional contribution of Pds5 to cohesin-mediated cohesion in human cells and Xenopus egg extracts. J Cell Sci 118(Pt 10):2133–2141

    CAS  PubMed  Google Scholar 

  56. Zhang B, Chang J, Fu M, Huang J, Kashyap R, Salavaggione E, Jain S, Shashikant K, Deardorff MA, Giovannucci Uzielli ML, Dorsett D, Beebe DC, Jay PY, Heuckeroth RO, Krantz ID, Millbrandt J (2009) Dosage effects of cohesin regulatory factor PDS5 on mammalian development: implications for cohesinopathies. PLoS One 4(5):1–17

    Google Scholar 

  57. Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, Mechtler K, Peters J-M (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127(5):955–967

    CAS  PubMed  Google Scholar 

  58. Kuroda M, Oikawa K, Ohbayashi T, Yoshida K, Yamada K, Mimura J, Matsuda Y, Fujii-Kuriyama Y, Mukai K (2005) A dioxin sensitive gene, mammalian WAPL, is implicated in spermatogenesis. FEBS J 579(1):167–172

    CAS  Google Scholar 

  59. Zhang J, Hakansson H, Kuroda M, Yuan L (2008) Wapl localization on the synaptonemal complex, a meiosis-specific proteinaceous structure that binds homologous chromosomes, in the female mouse. Reprod Domest Anim 43(1):124–126

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  61. 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

    CAS  PubMed Central  PubMed  Google Scholar 

  62. 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 

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

    PubMed  Google Scholar 

  64. 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. PNAS 100(18):10237–10242

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Bylund GO, Burgers PM (2005) Replication protein A-directed unloading of PCNA by the Ctf18 cohesion establishment complex. Mol Cell Biol 25(13):5445–5455

    CAS  PubMed Central  PubMed  Google Scholar 

  66. 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 

  67. 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 7:959–970

    CAS  PubMed  Google Scholar 

  68. Lengronne A, McIntyre J, Katou Y, Kanoh Y, Hopfner K-P, 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 

  69. 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 

  70. Noguchi E, Noguchi C, McDonald WH, Yates JRI, 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 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  72. 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(4857–4865)

    Google Scholar 

  73. 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 

  74. Berkowitz KM, Sowash AR, Koenig LR, Urcuyo D, Khan F, Yang F, Wang PJ, Jongens TA, Kaestner KH (2012) Disruption of CHTF18 causes defective meiotic recombination in male mice. PLoS Genet 8(11):e1002996

    CAS  PubMed Central  PubMed  Google Scholar 

  75. 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 

  76. Kim S-T, Xu B, Kastan MB (2002) Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev 16(5):560–570

    CAS  PubMed Central  PubMed  Google Scholar 

  77. Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, Koshland D (2004) DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 16:991–1002

    PubMed  Google Scholar 

  78. Covo S, Westmoreland JW, Gordenin DA, Resnick MA (2010) Cohesin is limiting for the suppression of DNA damage-induced recombination between homologous chromosomes. PLoS Genet 6(7):1–16

    Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB (2004) Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev 18(12):1423–1438

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Luo H, Li Y, Mu J-J, Zhang J, Tonaka T, Hamamori Y, Jung SY, Wang Y, Qin J (2008) Regulation of intra-S phase checkpoint by ionizing radiation (IR)-dependent and IR-independent phosphorylation of SMC3. J Biol Chem 283(28):19176–19183

    CAS  PubMed Central  PubMed  Google Scholar 

  82. Klein F, Mahr P, Galova M, Buonomo SBC, 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 

  83. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400(6743):461–464

    CAS  PubMed  Google Scholar 

  84. Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88(3):375–384

    CAS  PubMed  Google Scholar 

  85. Alani E, Padmore R, Kleckner N (1990) Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61:419–436

    CAS  PubMed  Google Scholar 

  86. Nairz K, Klein F (1997) mre11S - a yeast mutation that blocks double-strand break processing and permits nonhomologous synapsis in meiosis. Genes Dev 11:2272–2290

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Prinz S, Amon A, Klein F (1997) Isolation of COM1, a new gene required to complete meiotic double-strand break induced recombination in Saccharomyces cerevisiae. Genetics 146:781–795

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Hunter N, Kleckner N (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106(1):59–70

    CAS  PubMed  Google Scholar 

  89. Yokobayashi S, Yamamoto M, Watanabe Y (2003) Cohesins determine the attachment manner of kinetochores to spindle microtubules at meiosis I in fission yeast. Mol Cell Biol 23(11):3965–3973

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Kateneva AV, Konovchenko AA, Guacci V, Dresser ME (2005) Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae. J Cell Biol 171(2):241–253

    CAS  PubMed Central  PubMed  Google Scholar 

  91. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300(5622):1152–1155

    CAS  PubMed  Google Scholar 

  92. Lee J, Iwai T, Yokota T, Yamashita M (2003) Temporally and spatially selective loss of Rec8 protein from meiotic chromosomes during mammalian meiosis. J Cell Sci 116(Pt 13):2781–2790

    CAS  PubMed  Google Scholar 

  93. Parisi S, McKay MJ, Molnar M, Thompson MA, van der Spek PJ, van Drunen-Schoenmaker E, Kanaar R, Lehmann E, Hoeijmakers JHJ, Kohli J (1999) Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 19(5):3515–3528

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Pezzi N, Prieto I, Kremer L, Jurado LAP, Valero C, del Mazo J, Martinez-A C, Barbero JL (2000) STAG3, a novel gene encoding a protein involved in meiotic chromosome pairing and location of STAG3-related genes flanking the Williams-Beuren syndrome deletion. FASEB J 14(3):581–595

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  96. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 21(20):6984–6998

    CAS  PubMed Central  PubMed  Google Scholar 

  97. Prieto I, Pezzi N, Buesa JM, Kremer L, Barthelemy I, Carreiro C, Roncal F, Martinez A, Gomez L, Fernandez R, Martinez AC, Barbero JL (2002) STAG2 and Rad21 mammalian mitotic cohesins are implicated in meiosis. EMBO Rep 3(6):543–550

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Gutierrez-Caballero C, Herran Y, Sanchez-Martin M, Suja JA, Barbero JL, Llano E, Pendas AM (2011) Identification and molecular characterization of the mammalian alpha-kleisin RAD21L. Cell Cycle 10(9):1477–1487

    CAS  PubMed  Google Scholar 

  99. Herran Y, Gutierrez-Caballero C, Sanchez-Martin M, Hernandez T, Viera A, Barbero JL, De Alava E, de Rooij DG, Suja JA, Llano E, Pendas AM (2011) The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility. EMBO J 30(15):3091–3105

    CAS  PubMed Central  PubMed  Google Scholar 

  100. Ishiguro K, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y (2011) A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep 12(3):267–275

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Lee J, Hirano T (2011) RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol 192(2):263–276

    CAS  PubMed Central  PubMed  Google Scholar 

  102. 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-a-associated protein Ctf4 is essential for chromatid disjunction during meiosis II. J Cell Sci 117(16):3547–3559

    CAS  PubMed  Google Scholar 

  103. Lightfoot J, Testori S, Barroso C, Martinez-Perez E (2011) Loading of meiotic cohesin by SCC-2 is required for early processing of DSBs and for the DNA damage checkpoint. Curr Biol 21(17):1421–1430

    CAS  PubMed  Google Scholar 

  104. Sym M, Engebrecht J, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378

    CAS  PubMed  Google Scholar 

  105. Meuwissen RLJ, Offenberg HH, Dietrch AJJ, Riesewijk A, van Iersel M, Heyting C (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 11(13):5091–5100

    CAS  PubMed Central  PubMed  Google Scholar 

  106. Schmekel K, Meuwissen RLJ, Dietrch AJJ, Vink ACG, van Marle J, van Veen H, Heyting C (1996) Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp Cell Res 226:20–30

    CAS  PubMed  Google Scholar 

  107. Schalk JAC, Dietrch AJJ, Vink ACG, Offenberg HH, van Aalderen M, Heyting C (1998) Localization of SCP2 and SCP3 protein molecules within synaptonemal complexes of the rat. Chromosoma 107:540–548

    CAS  PubMed  Google Scholar 

  108. Parra MT, Viera A, Gomez R, Page J, Benavente R, Santos JL, Rufas JS, Suja JA (2004) Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 117:1221–1234

    CAS  PubMed  Google Scholar 

  109. Xu H, Beasley M, Verschoor S, Inselman A, Handel MA, McKay MJ (2004) A new role for the mitotic RAD21/SCC1 cohesin in meiotic chromosome cohesion and segregation in the mouse. EMBO Rep 5:378–384

    CAS  PubMed Central  PubMed  Google Scholar 

  110. Eijpe M, Heyting C, Gross B, Jessberger R (2000) Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes. J Cell Sci 113:673–682

    CAS  PubMed  Google Scholar 

  111. Suja JA, Antonio C, Debec A, Rufas JS (1999) Phosphorylated proteins are involved in sister-chromatid arm cohesion during meiosis I. J Cell Sci 112:2957–2969

    CAS  PubMed  Google Scholar 

  112. Eijpe M, Offenberg HH, Jessberger R, Revenkova E, Heyting C (2003) Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1b and SMC3. J Cell Biol 160(5):657–670

    CAS  PubMed Central  PubMed  Google Scholar 

  113. Suja JA, Barbero JL (2009) Cohesin complexes and sister chromatid cohesion in mammalian meiosis. Genome Dyn 5:94–116

    CAS  PubMed  Google Scholar 

  114. Kouznetsova A, Novak I, Jessberger R, Hoog C (2005) SYCP2 and SYCP3 are required for cohesin core integrity at diplotene but not for centromere cohesion at the first meiotic division. J Cell Sci 118:2271–2278

    CAS  PubMed  Google Scholar 

  115. Gomez R, Valdeolmillos AM, Parra MT, Viera A, Carreiro C, Roncal F, Rufas JS, Barbero JL, Suja JA (2007) Mammalian SGO2 appears at the inner centromere domain and redistributes depending on tension across centromeres during meiosis II and mitosis. EMBO Rep 8(2):173–180

    CAS  PubMed Central  PubMed  Google Scholar 

  116. Prieto I, Tease C, Pezzi N, Buesa JM, Ortega S, Kremer L, Martinez A, Martinez-A C, Hulten MA, Barbero JL (2004) Cohesin component dynamics during meiotic prophase I in mammalian oocytes. Chromosome Res 12:197–213

    CAS  PubMed  Google Scholar 

  117. Garcia-Cruz R, Brieno MA, Roig I, Grossmann M, Velilla E, Pujol A, Cabero L, Pessarrodona A, Barbero JL, Garcia Caldes M (2010) Dynamics of cohesin proteins REC8, STAG3, SMC1b and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes. Hum Reprod 25(9):2316–2327

    CAS  PubMed  Google Scholar 

  118. Crackower MA, Kolas NK, Noguchi J, Sarao R, Kikuchi K, Kaneko H, Kobayashi E, Kawai Y, Kozieradzki I, Landers R, Mo R, Hui C-C, Nieves E, Cohen PE, Osborne LR, Wada T, Kunieda T, Moens PB, Penninger JM (2003) Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science 300(5623):1291–1295

    CAS  PubMed Central  PubMed  Google Scholar 

  119. Holloway K, Roberson EC, Corbett KL, Kolas NK, Nieves E, Cohen PE (2011) NEK1 facilitates cohesin removal during mammalian spermatogenesis. Genes 2(1):260–279

    CAS  PubMed Central  PubMed  Google Scholar 

  120. Buonomo SB, Clyne RK, Fuchs J, Loidl J, Uhlmann F, Nasmyth K (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 103(3):387–398

    CAS  PubMed  Google Scholar 

  121. Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15:1349–1360

    CAS  PubMed Central  PubMed  Google Scholar 

  122. Siomos MF, Badrinath A, Pasierbek P, Livingstone D, White J, Glotzer M, Nasmyth K (2001) Separase is required for chromosome segregation during meiosis I in Caenorhabditis elegans. Curr Biol 11:1825–1835

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  124. Kaitna S, Pasierbek P, Jantsch M, Loidl J, Glotzer M (2002) The aurora B kinase AIR-2 regulated kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr Biol 12:798–812

    CAS  PubMed  Google Scholar 

  125. Kitajima T, Miyazaki Y, Yamamoto M, Watanabe Y (2003) Rec8 cleavage by separase is required for meiotic nuclear division in fission yeast. EMBO J 22(20):5643–5653

    CAS  PubMed Central  PubMed  Google Scholar 

  126. Herbert M, Levasseur M, Homer H, Yallop K, Murdoch A, McDougall A (2003) Homologue disjunction in mouse oocytes requires proteolysis of securin and cyclin B1. Nat Cell Biol 5(11):1023–1025

    CAS  PubMed  Google Scholar 

  127. Terret ME, Wassmann K, Waizenegger IC, Maro B, Peters J-M, Verlhac M-H (2003) The meiosis I-to-meiosis II transition in mouse oocytes requires separase activity. Curr Biol 13:1797–1802

    CAS  PubMed  Google Scholar 

  128. Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427(6974):510–517

    CAS  PubMed  Google Scholar 

  129. Rabitsch KP, Gregan J, Schleiffer A, Javerzat J-P, Eisenhaber F, Nasmyth K (2004) Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Curr Biol 14:287–301

    CAS  PubMed  Google Scholar 

  130. Marston AL, Tham W-H, Shah H, Amon A (2004) A genome-wide screen identifies genes required for centromeric cohesion. Science 303:1367–1370

    CAS  PubMed  Google Scholar 

  131. Katis VL, Galova M, Rabitsch KP, Gregan J, Nasmyth K (2004) Maintenance of cohesin at centromeres after meiosis I in budding yeast requires a kinetochore-associated protein related to MEI-S332. Curr Biol 14(7):560–572

    CAS  PubMed  Google Scholar 

  132. 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 

  133. Ridel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, Mudrak I, Ogris E, Mechtler K, Pelletier L, Buchholz F, Shirahige K, Nasmyth K (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441(7089):53–61

    Google Scholar 

  134. Llano E, Gomez R, Gutierrez-Caballero C, Herran Y, Sanchez-Martin M, Vazquez-Quinones L, Hernandez T, de Alava E, Cuadrado A, Barbero JL, Suja JA, Pendas AM (2008) Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes Dev 22:2400–2413

    CAS  PubMed Central  PubMed  Google Scholar 

  135. Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, Miyake M, Watanabe Y (2008) Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 10(1):42–52

    CAS  PubMed  Google Scholar 

  136. Yin S, Ai J-S, Shi L-H, Wei L, Yuan J, Ouyang Y-C, Hou Y, Chen D-Y, Schatten H, Sun Q-Y (2008) Shugoshin 1 may play important roles in separation of homologous chromosomes and sister chromatids during mouse oocyte meiosis. PLoS One 3(10):1–7

    Google Scholar 

  137. Brar GA, Kiburz BM, Zhang Y, Kim JE, White F, Amon A (2006) Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441(7092):532–536

    CAS  PubMed  Google Scholar 

  138. Katis VL, Lipp JJ, Imre R, Bogdanova A, Okaz E, Habermann B, Mechtler K, Nasmyth K, Zachariae W (2010) Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev Cell 18(3):397–409

    CAS  PubMed Central  PubMed  Google Scholar 

  139. Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, Liebe B, Scherthan H, Jessberger R (2004) Cohesin SMC1b is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6(6):555–562

    CAS  PubMed  Google Scholar 

  140. Xu H, Beasley MD, Warren WD, van der Horst GTJ, McKay MJ (2005) Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 8:949–961

    CAS  PubMed  Google Scholar 

  141. Yuan L, Liu J-G, Zhao J, Brundell E, Daneholt B, Hoog C (2000) The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell 5:73–83

    CAS  PubMed  Google Scholar 

  142. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, Wang PJ (2006) Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J Cell Biol 173(4):497–507

    CAS  PubMed Central  PubMed  Google Scholar 

  143. de Vries FAT, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, Liu J-G, van Zeeland AA, Heyting C, Pastink A (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19(11):1376–1389

    PubMed Central  PubMed  Google Scholar 

  144. Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, Yaeger D, Jukofsky L, Wasserman N, Bottani A, Morris CA, Nowaczyk MJM, Toriello H, Bamshad MJ, Carey JC, Rappaport E, Kawauchi S, Lander AD, Calof AL, Li H, 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 

  145. Tonkin ET, Wang T-J, 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 

  146. 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 

  147. 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 LG, 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 

  148. Gillis LA, McCallum J, Kaur M, DeScipio C, Yaeger D, Mariani A, Kline AD, Li H, Devoto M, Jackson LG, Krantz ID (2004) NIPBL mutational analysis in 120 individuals with Cornelia de Lange syndrome and evaluation of genotype-phenotype correlations. Am J Hum Genet 75(4):610–623

    CAS  PubMed Central  PubMed  Google Scholar 

  149. Kaur M, DeScipio C, McCallum J, Yaeger D, Devoto M, Jackson LG, Spinner NB, Krantz ID (2005) Precocious sister chromatid separation (PSCS) in Cornelia de Lange syndrome. Am J Med Genet 138A(1):27–31

    Google Scholar 

  150. Vrouwe MG, Elghalbzouri-Maghrani E, Meijers M, Schouten P, Godthelp BC, Bhuiyan ZA, Redeker EJ, Mannens MM, Mullenders LHF, 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 

  151. Revenkova E, Focarelli ML, Susani L, Paulis M, Bassi MT, Mannini L, Frattini A, Delia D, Krantz ID, Vezzoni P, Jessberger R, Musio A (2009) Cornelia de Lange syndrome mutations in SMC1A or SMC3 affect binding to DNA. Hum Mol Genet 18(3):418–427

    CAS  PubMed Central  PubMed  Google Scholar 

  152. Kawauchi S, Calof AL, Santos R, Lopez-Burks ME, Young CM, Hoang MP, Chua A, Lao T, Lechner MS, Daniel JA, Nussenzweig A, Kitzes L, Yokomori K, Hallgrimsson B, Lander AD (2009) Multiple organ system defects and transcriptional dysregulation in the Nipbl +/- mouse, a model of Cornelia de Lange syndrome. PLoS Genet 5(9):1–17

    Google Scholar 

  153. 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 

  154. Schule B, Oviedo A, Johnston K, Pai S, Francke U (2005) Inactivating mutations in ESCO2 cause SC phocomelia and Roberts syndrome: no phenotype-genotype correlation. Am J Hum Genet 77(6):1117–1128

    CAS  PubMed Central  PubMed  Google Scholar 

  155. Vega H, Trainer AH, Gordillo M, Crosier M, Kayserili H, Skovby F, Giovannucci Uzielli ML, Schnur RE, Manouvrier S, Blair E, Hurst JA, Forzano F, Meins M, Simola KOJ, Raas-Rothschild A, Hennekam RCM, Jabs EW (2010) Phenotypic variability in 49 cases of ESCO2 mutations, including novel missense and codon deletion in the acetyltransferase domain, correlates with ESCO2 expression and establishes the clinical criteria for Roberts syndrome. J Med Genet 47(1):30–37

    CAS  PubMed  Google Scholar 

  156. 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 

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

    CAS  PubMed  Google Scholar 

  158. Monnich M, Banks S, Eccles M, Dickinson E, Horsfield J (2009) Expression of cohesin and condensin genes during zebrafish development supports a non-proliferative role for cohesin. Gene Expr Patterns 9:586–594

    CAS  PubMed  Google Scholar 

  159. Ritchie K, Seah C, Moulin J, Isaac C, Dick F, Berube NG (2008) Loss of ATRX leads to chromosome cohesion and congression defects. J Cell Biol 180(2):315–324

    CAS  PubMed Central  PubMed  Google Scholar 

  160. Kernohan KD, Jiang Y, Tremblay DC, Bonvissuto AC, Eubanks JH, Mann MRW, Berube NG (2010) ATRX partners with cohesin and MeCP2 and contributes to developmental silencing of imprinted genes in the brain. Dev Cell 18(2):191–202

    CAS  PubMed  Google Scholar 

  161. 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

    PubMed Central  PubMed  Google Scholar 

  162. Hassold TJ, Jacobs PA (1984) Trisomy in man. Annu Rev Genet 18:69–97

    CAS  PubMed  Google Scholar 

  163. Hunt PA, Hassold TJ (2010) Female meiosis: coming unglued with age. Curr Biol 20(17):R699–R702

    CAS  PubMed  Google Scholar 

  164. Revenkova E, Hermann K, Adelfalk C, Jessberger R (2010) Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol 20:1529–1533

    CAS  PubMed Central  PubMed  Google Scholar 

  165. Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA (2005) SMC1b-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37(12):1351–1355

    CAS  PubMed  Google Scholar 

  166. Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20(17):1522–1528

    CAS  PubMed Central  PubMed  Google Scholar 

  167. Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y, Jessberger R, Kirkwood TB, Hoog C, Herbert M (2010) Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20(17):1511–1521

    CAS  PubMed  Google Scholar 

  168. Chiang T, Schultz RM, Lampson MA (2012) Meiotic origins of maternal age-related aneuploidy. Biol Reprod 86(1):1–7

    PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported in part by the NIH (1R01GM106262 to KMB). We thank Dr. Soumya Rudra for critical reading of the manuscript. We apologize to any authors/researchers whose contributions we may have overlooked.

Author information

Authors and Affiliations

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

    Amanda S. Brooker & Karen M. Berkowitz

  2. Department of Obstetrics and Gynecology, Drexel University College of Medicine, Philadelphia, PA, USA

    Karen M. Berkowitz

Authors
  1. Amanda S. Brooker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karen M. Berkowitz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karen M. Berkowitz .

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

Brooker, A.S., Berkowitz, K.M. (2014). The Roles of Cohesins in Mitosis, Meiosis, and Human Health and Disease. 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_11

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-0888-2_11

  • 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