The roles of cohesins in mitosis, meiosis, and human health and disease

Methods in Molecular Biology

Volumn 1170, Issue , 2014, Pages 229-266

  Brooker, Amanda S ^a   Berkowitz, Karen M ^a  

^a NONE

Author keywords

Aneuploidy; Cell cycle; Chromosome segregation; Cohesin; Cohesinopathies; Human health; Maternal age effect; Meiosis; Mitosis; Sister chromatid cohesion

Indexed keywords

COHESIN; CELL CYCLE PROTEIN; NONHISTONE PROTEIN;

AGING; ANAPHASE; ARTICLE; CELL ADHESION; CHROMOSOME SEGREGATION; DE LANGE SYNDROME; DISSOCIATION; GENERAL ASPECTS OF DISEASE; GENOME; HEALTH STATUS; HUMAN; MEIOSIS; MENTAL DEFICIENCY; METAPHASE; MITOSIS; MUTANT; NONHUMAN; PACHYTENE; PHOCOMELIA; PRIORITY JOURNAL; PROTEIN FUNCTION; ROBERTS SYNDROME; SISTER CHROMATID; X CHROMOSOME LINKED DISORDER; ALPHA THALASSEMIA; ANIMAL; CHROMATID; CRANIOFACIAL MALFORMATION; GENETICS; HYPERTELORISM; METABOLISM; PATHOLOGY; X LINKED MENTAL RETARDATION;

ALPHA-THALASSEMIA; ANIMALS; CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; CRANIOFACIAL ABNORMALITIES; DE LANGE SYNDROME; ECTROMELIA; HUMANS; HYPERTELORISM; MEIOSIS; MENTAL RETARDATION, X-LINKED; MITOSIS;

EID: 84922480384     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4939-0888-2_11     Document Type: Article

References (168)

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.
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.
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.
4. Michaelis C, Ciosk R, Nasmyth K (1997) Cohesins: chromosomal proteins that prevents premature separation of sister chromatids. Cell 91:35–45.
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.
6. Gruber S, Haering CH, Nasmyth K (2003) Chromosomal cohesin forms a ring. Cell 112(6):765–777.
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.
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.
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.
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.
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.
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.
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.
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 kinetochorespindle pole connections. Cell 108:317–329.
15. He X, Rines DR, Espelin CW, Sorger PK (2001) Molecular analysis of kinetochoremicrotubule attachment in budding yeast. Cell 106(2):195–206.
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.
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.
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.
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.
20. Britton RA, Lin DC, Grossman AD (1998) Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12(9):1254–1259.
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.
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.
23. Diaz-Martinez LA, Gimenez-Abian JF, Clarke DJ (2007) Cohesin is dispensable for centromere cohesion in human cells. PLoS One 2(3):e318.
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.
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.
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.
27. Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8(20): 1095–1101.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
52. Rankin S, Ayad NG, Kirschner MW (2005) Sororin, a substrate of the anaphasepromoting complex, is required for sister chromatid cohesion in vertebrates. Mol Cell 18:185–200.
53. Dai J, Sullivan BA, Higgins JMG (2006) Regulation of mitotic chromosome cohesion by Haspin and Aurora B. Dev Cell 11(5): 741–750.
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.
55. Losada A, Yokochi T, Hirano T (2005) Functional contribution of Pds5 to cohesinmediated cohesion in human cells and Xenopus egg extracts. J Cell Sci 118(Pt 10):2133–2141.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
69. Ansbach AB, Noguchi C, Klansek IW, Heidlebaugh M, Nakamura TM, Noguchi E (2008) RFC Ctf18 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.
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.
71. Skibbens RV (2004) Chl1p, a DNA helicaselike protein in budding yeast, functions in sister- chromatid cohesion. Genetics 166:33–42.
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).
73. Terret ME, Sherwood R, Rahman S, Qin J, Jallepalli PV (2009) Cohesin acetylation speeds the replication fork. Nature 462(7270): 231–234.
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.
75. Rudra S, Skibbens RV (2012) Sister chromatid cohesion establishment occurs in concert with lagging strand synthesis. Cell Cycle 11(11):2114–2121.
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.
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.
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.
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.
80. Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB (2004) Phosphorylation of SMC1 is a critical downstream event in the ATMNBS1- BRCA1 pathway. Genes Dev 18(12): 1423–1438.
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.
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.
83. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400(6743): 461–464.
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.
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.
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.
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.
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.
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.
90. Kateneva AV, Konovchenko AA, Guacci V, Dresser ME (2005) Recombination protein Tid1p controls resolution of cohesindependent linkages in meiosis in Saccharomyces cerevisiae. J Cell Biol 171(2):241–253.
91. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300(5622):1152–1155.
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.
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.
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.
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.
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.
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.
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.
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.
100. Ishiguro K, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y (2011) A new meiosisspecific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep 12(3):267–275.
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.
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-C Ctf18/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.
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.
104. Sym M, Engebrecht J, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378.
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.
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.
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.
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.
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.
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.
111. Suja JA, Antonio C, Debec A, Rufas JS (1999) Phosphorylated proteins are involved in sisterchromatid arm cohesion during meiosis I. J Cell Sci 112:2957–2969.
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.
113. Suja JA, Barbero JL (2009) Cohesin complexes and sister chromatid cohesion in mammalian meiosis. Genome Dyn 5:94–116.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
128. Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427(6974):510–517.
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.
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.
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.
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.
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.
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.
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.
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.
137. Brar GA, Kiburz BM, Zhang Y, Kim JE, White F, Amon A (2006) Rec8 phosphorylation and recombination promote the stepwise loss of cohesins in meiosis. Nature 441(7092):532–536.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
152. +/- mouse, a model of Cornelia de Lange syndrome. PLoS Genet 5(9):1–17.
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.
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.
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.
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.
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.
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.
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.
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.
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.
162. Hassold TJ, Jacobs PA (1984) Trisomy in man. Annu Rev Genet 18:69–97.
163. Hunt PA, Hassold TJ (2010) Female meiosis: coming unglued with age. Curr Biol 20(17): R699–R702.
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.
165. Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA (2005) SMC1bdeficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37(12):1351–1355.
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.
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.
168. Chiang T, Schultz RM, Lampson MA (2012) Meiotic origins of maternal age-related aneuploidy. Biol Reprod 86(1):1–7.