WAPL Is Essential for the Prophase Removal of Cohesin during Meiosis

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Wapl has been shown to play an integral role in the removal of cohesin from chromosomes during mitotic prophase. While Wapl's role appears to be conserved between yeast, fly and animal cells, structural and possible mechanistic differences have also been identified. As part of a study to better understand the protein and its role(s) we have characterized Wapl in plants. We show that Arabidopsis contains two copies of WAPL that share overlapping functions. Inactivation of the individual genes has no effect. Plants containing mutations in both genes growth normally but exhibit reduced fertility due to alterations in meiosis. Cohesin removal from chromosomes during meiotic prophase is blocked in wapl mutant plants resulting in unresolved bivalents and uneven chromosome segregation. In contrast, cohesin appears to be removed normally in mitotic cells. These results demonstrate that WAPL plays a critical role in removing cohesin from meiotic chromosomes. They also suggest that the mechanism involved in prophase removal of cohesin may vary between mitosis and meiosis in plants. Finally, wapl mutations suppress ctf7-associated lethality and restore normal growth and partial fertility to ctf7 mutant plants, suggesting that sister chromatid cohesion is not essential for plant growth and development.

Vyšlo v časopise: WAPL Is Essential for the Prophase Removal of Cohesin during Meiosis. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004497
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004497

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Zdroje

1. XiongB, GertonJL (2010) Regulators of the cohesin network. Annu Rev Biochem 79: 131–153.

2. MerkenschlagerM (2010) Cohesin: a global player in chromosome biology with local ties to gene regulation. Cur Opin Gen & Dev 20: 555–561.

3. NasmythK, HaeringCH (2009) Cohesin: Its Roles and Mechanisms. Ann Rev Genet 43: 525–558.

4. RemeseiroS, LosadaA (2013) Cohesin, a chromatin engagement ring. Cur Opin Cell Biol 25: 63–71.

5. DorsettD, MerkenschlagerM (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. SeitanVC, MerkenschlagerM (2012) Cohesin and chromatin organisation. Cur Opin Gen Dev 22: 93–100.

7. YuanL, YangX, MakaroffCA (2011) Plant cohesins, common themes and unique roles. Cur Protein and Peptide Sci 12: 93–104.

8. CioskR, ShirayamaM, ShevchenkoA, TanakaT, TothA, 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. TakahashiTS, YiuPY, ChouMF, GygiS, WalterJC (2004) Recruitment of Xenopus SCC2 and cohesin to chromatin requires the pre-replication complex. Nat Cell Biol 6: 991–1001.

10. WatrinE, SchleifferA, TanakaK, EisenhaberF, NasmythK, et al. (2006) Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Cur Biol 16: 863–874.

11. BernardP, SchmidtCK, VaurS, DheurS, DrogatJ, et al. (2008) Cell-cycle regulation of cohesin stability along fission yeast chromosomes. EMBO J 27: 111–121.

12. ChanKL, RoigMB, HuB, BeckouetF, MetsonJ, et al. (2012) Cohesin's DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell 150: 961–974.

13. SutaniT, KawaguchiT, KannoR, ItohT, ShirahigeK (2009) Budding yeast Wpl1 (Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Cur Biol 19: 492–497.

14. PanizzaS, TanakaTU, HochwagenA, EisenhaberF, NasmythK (2000) Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Cur Biol 10: 1557–1564.

15. LafontAL, SongJH, RankinS (2011) Sororin cooperates with the acetyltransferase Eco2 to ensure DNA replication-dependent sister chromatid cohesion. Proc Natl Acad Sci USA 107: 20364–20369.

16. GandhiR, GillespiePJ, HiranoT (2006) Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Cur Biol 16: 2406–2417.

17. KuengS, HegemannB, PetersBH, LippJJ, SchleifferA, et al. (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127: 955–967.

18. NishiyamaT, LadurnerR, SchmitzJ, KreidlE, SchleifferA, et al. (2011) Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143: 737–749.

19. SchmitzJ, WatrinE, LenartP, MechtlerK, PetersJM (2007) Sororin is required for stable binding of cohesin to chromatin and for sister chromatid cohesion in interphase. Cur Biol 17: 630–636.

20. UnalE, Heidinger-PauliJM, KimW, GuacciV, OnnI, et al. (2008) A molecular determinant for the establishment of sister chromatid cohesion. Science 321: 566–569.

21. ZhangJL, ShiXM, LiYH, KimBJ, JiaJL, 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. BeckouetF, HuB, RoigMB, SutaniT, KomataM, et al. An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Mol Cell 39: 689–699.

23. Ben-ShaharTR, HeegerS, LehaneC, EastP, FlynnH, et al. (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321: 563–566.

24. RowlandBD, RoigMB, NishinoT, KurzeA, UluocakP, et al. (2009) Building sister chromatid cohesion: Smc3 acetylation counteracts an antiestablishment activity. Mol Cell 33: 763–774.

25. WaizeneggerIC, HaufS, MeinkeA, PetersJM (2000) Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103: 399–410.

26. BuheitelJ, StemmannO (2013) Prophase pathway-dependent removal of cohesin from human chromosomes requires opening of the Smc3-Scc1 gate. EMBO J 32: 666–676.

27. EichingerCS, KurzeA, OliveiraRA, NasmythK (2013) Disengaging the Smc3/kleisin interface releases cohesin from Drosophila chromosomes during interphase and mitosis. EMBO J 32: 656–665.

28. HaufS, RoitingerE, KochB, DittrichCM, MechtlerK, 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. ZhangNG, PanigrahiAK, MaoQL, PatiD (2011) Interaction of sororin protein with Polo-like Kinase 1 mediates resolution of chromosomal arm cohesion. J Biol Chem 286: 41826–41837.

30. XuZ, CetinB, AngerM, ChoUS, HelmhartW, et al. (2009) Structure and function of the PP2A-Shugoshin interaction. Mol Cell 35: 426–441.

31. TangZY, ShuHJ, QiW, MahmoodNA, MumbyMC, et al. (2006) PP2A is required for centromeric localization of Sgol and proper chromosome segregation. Dev Cell 10: 575–585.

32. KitajimaTS, SakunoT, IshiguroK, IemuraS, NatsumeT, et al. (2006) Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441: 46–52.

33. UhlmannF, LottspeichF, NasmythK (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400: 37–42.

34. RiedelCG, KatisVL, KatouY, MoriS, ItohT, et al. (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441: 53–61.

35. BuonomoSBC, ClyneRK, FuchsJ, LoidlJ, UhlmannF, 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. SiomosMF, BadrinathA, PasierbekP, LivingstoneD, WhiteJ, et al. (2001) Separase is required for chromosome segregation during meiosis I in Caenorhabditis elegans. Cur Biol 23: 1825–1835.

37. VerniF, GandhiR, GoldbergML, GattiM (2000) Genetic and molecular analysis of wings apart-like (wapl), a gene controlling heterochromatin organization in Drosophila melanogaster. Genetics 154: 1693–1710.

38. OuyangZQ, ZhengG, SongJH, BorekDM, OtwinowskiZ, et al. (2013) Structure of the human cohesin inhibitor Wapl. Proceed Natl Acad Sci USA 110: 11355–11360.

39. ChatterjeeA, ZakianS, HuXW, SingletonMR (2013) Structural insights into the regulation of cohesion establishment by Wpl1. EMBO J 32: 677–687.

40. CunninghamMD, GauseM, ChengYZ, NoyesA, DorsettD, et al. (2012) Wapl antagonizes cohesin binding and promotes Polycomb-group silencing in Drosophila. Development 139: 4172–4179.

41. ShintomiK, HiranoT (2009) Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes & Dev 23: 2224–2236.

42. ArmstrongS, FranklinF, JonesG (2001) Nucleolus-associated telomere clustering and pairing preceed meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114: 4207–04217.

43. HigginsJD, Sanchez-MoranE, ArmstrongSJ, JonesGH, FranklinFCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes & Dev 19: 2488–2500.

44. CaiX, DongFG, EdelmannRE, MakaroffCA (2003) The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci 116: 2999–3007.

45. JiangL, YuanL, XiaM, MakaroffCA (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-VillegasP, YangXH, WangHJ, JuanCT, ChuangMH, et al. (2013) Arabidopsis CHROMOSOME TRANSMISSION FIDELITY 7 (AtCTF7/ECO1) is required for DNA repair, mitosis and meiosis. Plant J 75: 927–940.

47. TedeschiA, WutzG, HuetS, JaritzM, WuenscheA, et al. (2013) Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 501: 564–570.

48. BennettCB, LewisLK, KarthikeyanG, LobachevKS, JinYH, et al. (2001) Genes required for ionizing radiation resistance in yeast. Nature Genet 29: 426–434.

49. Lopez-SerraL, LengronneA, BorgesV, KellyG, UhlmannF (2013) Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Cur Biol 23: 64–69.

50. TanakaK, HaoZL, KaiM, OkayamaH (2001) Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J 20: 5779–5790.

51. LengronneA, McIntyreJ, KatouY, KanohY, HopfnerKP, et al. (2006) Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol Cell 23: 787–799.

52. Heidinger-PauliJM, UnalE, KoshlandD (2009) Distinct targets of the Eco1 acetyltransferase modulate cohesion in S phase and in response to DNA damage. Mol Cell 34: 311–321.

53. SumaraI, VorlauferE, StukenbergP, KelmO, RedemannN, et al. (2002) The dissociation of cohesin from chromosomes in prophase is regulated by polo-like kinase. Mol Cell 9: 515–525.

54. Gimenez-AbianJF, SumaraI, HirotaT, HaufS, GerlichD, et al. (2004) Regulation of sister chromatid cohesion between chromosome arms. Cur Biol 14: 1187–1193.

55. NishiyamaT, SykoraMM, t VeldaP, MechtlerK, PetersJM (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. ChanKL, GligorisT, UpcherW, KatoY, ShirahigeK, et al. (2013) Pds5 promotes and protects cohesin acetylation. Proc Natl Acad Sci USA 110: 13020–13025.

57. LiuZ, MakaroffCA (2006) Arabidopsis separase AESP is essential for embryo development and the release of cohesin during meiosis. Plant Cell 18: 1213–1225.

58. RossKJ, FranszP, JonesGH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4: 507–516.

59. YangX, BoatengKA, YuanL, WuS, BaskinTI, 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. LamWS, YangXH, MakaroffCA (2005) Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that ASMC3 may function beyond chromosome cohesion. J Cell Sci 118: 3037–3048.

61. ArmstrongS, CarylA, JonesG, FranklinF (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. FranszP, Alonso-BlancoC, LiharskaTB, PeetersAJM, ZabelP, 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. CarylAP, ArmstrongSJ, JonesGH, FranklinFCH (2000) A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109: 62–71.

64. Martinez-ZapaterJM, EstelleMA, SomervilleCR (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet 204: 417–423.

65. Vielle-CalzadaJP, BaskarR, GrossniklausU (2000) Delayed activation of the paternal genome during seed development. Nature 404: 91–94.

66. HerrJM (1971) New clearing-squash technique for study of ovule development in angiosperms. Amer J Bot 58: 785–791.

67. SiddiqiI, GaneshG, GrossniklausU, SubbiahV (2000) The dyad gene is required for progression through female meiosis in Arabidopsis. Development 127: 197–207.

68. AlexanderMP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44: 117–122.