Arabidopsis thaliana WAPL Is Essential for the Prophase Removal of Cohesin during Meiosis

PLoS Genetics

Volumn 10, Issue 7, 2014, Pages

  De, Kuntal ^a   Sterle, Lauren ^a   Krueger, Laura ^a   Yang, Xiaohui ^a   Makaroff, Christopher A ^a  

^a MIAMI UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; ADENOSINE TRIPHOSPHATASE; COHESIN; DNA; ARABIDOPSIS PROTEIN; CELL CYCLE PROTEIN; CTF7 PROTEIN, ARABIDOPSIS; NONHISTONE PROTEIN; WAPL PROTEIN, ARABIDOPSIS;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; CHROMOSOME ANALYSIS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA REPLICATION; EMBRYO DEVELOPMENT; FEMALE; FEMALE FERTILITY; GAMETOPHYTE; GENE; GENE FUNCTION; GENE INSERTION; IMMUNOLOCALIZATION; MALE; MALE FERTILITY; MEIOSIS; MITOSIS; NONHUMAN; PLANT DEVELOPMENT; PLANT GROWTH; PROPHASE; SISTER CHROMATID; SOMATIC CELL; WAPL GENE; ARABIDOPSIS; CELL CYCLE; CHROMOSOME; GENETICS; HUMAN; METABOLISM; SISTER CHROMATID EXCHANGE;

ACETYLTRANSFERASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; DNA REPLICATION; HUMANS; MEIOSIS; MITOSIS; PROPHASE; SISTER CHROMATID EXCHANGE;

EID: 84905474696     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004497     Document Type: Article

References (68)

1. Xiong B, Gerton JL, (2010) Regulators of the cohesin network. Annu Rev Biochem 79: 131-153.
2. Merkenschlager M, (2010) Cohesin: a global player in chromosome biology with local ties to gene regulation. Cur Opin Gen & Dev 20: 555-561.
3. Nasmyth K, Haering CH, (2009) Cohesin: Its Roles and Mechanisms. Ann Rev Genet 43: 525-558.
4. Remeseiro S, Losada A, (2013) Cohesin, a chromatin engagement ring. Cur Opin Cell Biol 25: 63-71.
5. Dorsett D, Merkenschlager M, (2013) Cohesin at active genes: a unifying theme for cohesin and gene expression from model organisms to humans. Cur Opin Cell Biol 25: 11-17.
6. Seitan VC, Merkenschlager M, (2012) Cohesin and chromatin organisation. Cur Opin Gen Dev 22: 93-100.
7. Yuan L, Yang X, Makaroff CA, (2011) Plant cohesins, common themes and unique roles. Cur Protein and Peptide Sci 12: 93-104.
8. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, et al. (2000) Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5: 243-254.
9. Takahashi TS, Yiu PY, Chou MF, Gygi S, Walter JC, (2004) Recruitment of Xenopus SCC2 and cohesin to chromatin requires the pre-replication complex. Nat Cell Biol 6: 991-1001.
10. Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, et al. (2006) Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Cur Biol 16: 863-874.
11. Bernard P, Schmidt CK, Vaur S, Dheur S, Drogat J, et al. (2008) Cell-cycle regulation of cohesin stability along fission yeast chromosomes. EMBO J 27: 111-121.
12. Chan KL, Roig MB, Hu B, Beckouet F, Metson J, et al. (2012) Cohesin's DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell 150: 961-974.
13. Sutani T, Kawaguchi T, Kanno R, Itoh T, Shirahige K, (2009) Budding yeast Wpl1 (Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Cur Biol 19: 492-497.
14. Panizza S, Tanaka TU, Hochwagen A, Eisenhaber F, Nasmyth K, (2000) Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Cur Biol 10: 1557-1564.
15. Lafont AL, Song JH, Rankin S, (2011) Sororin cooperates with the acetyltransferase Eco2 to ensure DNA replication-dependent sister chromatid cohesion. Proc Natl Acad Sci USA 107: 20364-20369.
16. Gandhi R, Gillespie PJ, Hirano T, (2006) Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Cur Biol 16: 2406-2417.
17. Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, et al. (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127: 955-967.
18. Nishiyama T, Ladurner R, Schmitz J, Kreidl E, Schleiffer A, et al. (2011) Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143: 737-749.
19. 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. Cur Biol 17: 630-636.
20. Unal E, Heidinger-Pauli JM, Kim W, Guacci V, Onn I, et al. (2008) A molecular determinant for the establishment of sister chromatid cohesion. Science 321: 566-569.
21. Zhang JL, Shi XM, Li YH, Kim BJ, Jia JL, et al. (2008) Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol Cell 31: 143-151.
22. Beckouet F, Hu B, Roig MB, Sutani T, Komata M, et al. An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Mol Cell 39: 689-699.
23. Ben-Shahar TR, Heeger S, Lehane C, East P, Flynn H, et al. (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321: 563-566.
24. Rowland BD, Roig MB, Nishino T, Kurze A, Uluocak P, et al. (2009) Building sister chromatid cohesion: Smc3 acetylation counteracts an antiestablishment activity. Mol Cell 33: 763-774.
25. Waizenegger IC, Hauf S, Meinke A, Peters JM, (2000) Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103: 399-410.
26. Buheitel J, Stemmann O, (2013) Prophase pathway-dependent removal of cohesin from human chromosomes requires opening of the Smc3-Scc1 gate. EMBO J 32: 666-676.
27. Eichinger CS, Kurze A, Oliveira RA, Nasmyth K, (2013) Disengaging the Smc3/kleisin interface releases cohesin from Drosophila chromosomes during interphase and mitosis. EMBO J 32: 656-665.
28. Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, et al. (2005) Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. Plos Biol 3: 419-432.
29. Zhang NG, Panigrahi AK, Mao QL, Pati D, (2011) Interaction of sororin protein with Polo-like Kinase 1 mediates resolution of chromosomal arm cohesion. J Biol Chem 286: 41826-41837.
30. Xu Z, Cetin B, Anger M, Cho US, Helmhart W, et al. (2009) Structure and function of the PP2A-Shugoshin interaction. Mol Cell 35: 426-441.
31. Tang ZY, Shu HJ, Qi W, Mahmood NA, Mumby MC, et al. (2006) PP2A is required for centromeric localization of Sgol and proper chromosome segregation. Dev Cell 10: 575-585.
32. Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, et al. (2006) Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441: 46-52.
33. 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.
34. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, et al. (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441: 53-61.
35. Buonomo SBC, Clyne RK, Fuchs J, Loidl J, Uhlmann F, et al. (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by Separin. Cell 103: 387-398.
36. Siomos MF, Badrinath A, Pasierbek P, Livingstone D, White J, et al. (2001) Separase is required for chromosome segregation during meiosis I in Caenorhabditis elegans. Cur Biol 23: 1825-1835.
37. Verni F, Gandhi R, Goldberg ML, Gatti M, (2000) Genetic and molecular analysis of wings apart-like (wapl), a gene controlling heterochromatin organization in Drosophila melanogaster. Genetics 154: 1693-1710.
38. Ouyang ZQ, Zheng G, Song JH, Borek DM, Otwinowski Z, et al. (2013) Structure of the human cohesin inhibitor Wapl. Proceed Natl Acad Sci USA 110: 11355-11360.
39. Chatterjee A, Zakian S, Hu XW, Singleton MR, (2013) Structural insights into the regulation of cohesion establishment by Wpl1. EMBO J 32: 677-687.
40. Cunningham MD, Gause M, Cheng YZ, Noyes A, Dorsett D, et al. (2012) Wapl antagonizes cohesin binding and promotes Polycomb-group silencing in Drosophila. Development 139: 4172-4179.
41. Shintomi K, Hirano T, (2009) Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes & Dev 23: 2224-2236.
42. Armstrong S, Franklin F, Jones G, (2001) Nucleolus-associated telomere clustering and pairing preceed meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114: 4207-04217.
43. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH, (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes & Dev 19: 2488-2500.
44. Cai X, Dong FG, Edelmann RE, Makaroff CA, (2003) The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci 116: 2999-3007.
45. Jiang L, Yuan L, Xia M, Makaroff CA, (2010) Proper levels of the Arabidopsis cohesion establishment factor CTF7 are essential for embryo and megagametophyte, but not endosperm, development. Plant Physiol 154: 820-832.
46. Bolanos-Villegas P, Yang XH, Wang HJ, Juan CT, Chuang MH, et al. (2013) Arabidopsis CHROMOSOME TRANSMISSION FIDELITY 7 (AtCTF7/ECO1) is required for DNA repair, mitosis and meiosis. Plant J 75: 927-940.
47. Tedeschi A, Wutz G, Huet S, Jaritz M, Wuensche A, et al. (2013) Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 501: 564-570.
48. Bennett CB, Lewis LK, Karthikeyan G, Lobachev KS, Jin YH, et al. (2001) Genes required for ionizing radiation resistance in yeast. Nature Genet 29: 426-434.
49. Lopez-Serra L, Lengronne A, Borges V, Kelly G, Uhlmann F, (2013) Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Cur Biol 23: 64-69.
50. Tanaka K, Hao ZL, Kai M, Okayama H, (2001) Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J 20: 5779-5790.
51. Lengronne A, McIntyre J, Katou Y, Kanoh Y, Hopfner KP, et al. (2006) Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol Cell 23: 787-799.
52. Heidinger-Pauli JM, Unal E, Koshland D, (2009) Distinct targets of the Eco1 acetyltransferase modulate cohesion in S phase and in response to DNA damage. Mol Cell 34: 311-321.
53. Sumara I, Vorlaufer E, Stukenberg P, Kelm O, Redemann N, et al. (2002) The dissociation of cohesin from chromosomes in prophase is regulated by polo-like kinase. Mol Cell 9: 515-525.
54. Gimenez-Abian JF, Sumara I, Hirota T, Hauf S, Gerlich D, et al. (2004) Regulation of sister chromatid cohesion between chromosome arms. Cur Biol 14: 1187-1193.
55. Nishiyama T, Sykora MM, t Velda P, 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 USA 110: 13404-13409.
56. Chan KL, Gligoris T, Upcher W, Kato Y, Shirahige K, et al. (2013) Pds5 promotes and protects cohesin acetylation. Proc Natl Acad Sci USA 110: 13020-13025.
57. Liu Z, Makaroff CA, (2006) Arabidopsis separase AESP is essential for embryo development and the release of cohesin during meiosis. Plant Cell 18: 1213-1225.
58. Ross KJ, Fransz P, Jones GH, (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4: 507-516.
59. Yang X, Boateng KA, Yuan L, Wu S, Baskin TI, et al. (2011) The radially swollen 4 separase mutation of Arabidopsis thaliana blocks chromosome disjunction and disrupts the radial microtubule system in meiocytes. Plos ONE 6: e19459.
60. Lam WS, Yang XH, Makaroff CA, (2005) Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that ASMC3 may function beyond chromosome cohesion. J Cell Sci 118: 3037-3048.
61. Armstrong S, Caryl A, Jones G, Franklin F, (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: 3645-3655.
62. Fransz P, Alonso-Blanco C, Liharska TB, Peeters AJM, Zabel P, et al. (1996) High resolution physcial mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibers. Plant J 9: 421-430.
63. Caryl AP, Armstrong SJ, Jones GH, Franklin FCH, (2000) A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109: 62-71.
64. Martinez-Zapater JM, Estelle MA, Somerville CR, (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet 204: 417-423.
65. Vielle-Calzada JP, Baskar R, Grossniklaus U, (2000) Delayed activation of the paternal genome during seed development. Nature 404: 91-94.
66. Herr JM, (1971) New clearing-squash technique for study of ovule development in angiosperms. Amer J Bot 58: 785-791.
67. Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V, (2000) The dyad gene is required for progression through female meiosis in Arabidopsis. Development 127: 197-207.
68. Alexander MP, (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44: 117-122.