Monopolin Subunit Csm1 Associates with MIND Complex to Establish Monopolar Attachment of Sister Kinetochores at Meiosis I

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Sexually reproducing organisms halve their cellular ploidy during gametogenesis by undergoing a specialized form of cell division known as meiosis. During meiosis, a single round of DNA replication is followed by two rounds of nuclear divisions (referred to as meiosis I and II). While sister kinetochores bind to microtubules emanating from opposite spindle poles during mitosis, they bind to microtubules originating from the same spindle pole during meiosis I. This phenomenon is referred to as mono-orientation and is essential for setting up the reductional mode of chromosome segregation during meiosis I. In budding yeast, mono-orientation depends on a four component protein complex referred to as monopolin which consists of two nucleolar proteins Csm1 and Lrs4, meiosis-specific protein Mam1 of unknown function and casein kinase Hrr25. Monopolin complex binds to kinetochores during meiosis I and prevents bipolar attachments. Although monopolin associates with kinetochores during meiosis I, its binding site(s) on the kinetochore is not known and its mechanism of action has not been established. By carrying out an imaging-based screen we have found that the MIND complex, a component of the central kinetochore, is required for monopolin association with kinetochores during meiosis. Furthermore, we demonstrate that interaction of monopolin subunit Csm1 with the N-terminal domain of MIND complex subunit Dsn1, is essential for both the association of monopolin with kinetochores and for monopolar attachment of sister kinetochores during meiosis I. As such this provides the first functional evidence for a monopolin-binding site at the kinetochore.

Vyšlo v časopise: Monopolin Subunit Csm1 Associates with MIND Complex to Establish Monopolar Attachment of Sister Kinetochores at Meiosis I. PLoS Genet 9(7): e32767. doi:10.1371/journal.pgen.1003610
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003610

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1. KerrGW, SarkarS, ArumugamP (2012) How to halve ploidy: lessons from budding yeast meiosis. Cell Mol Life Sci 69 : 3037–51.

2. PetronczkiM, SiomosMF, NasmythK (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112 : 423–440.

3. TothA, RabitschKP, GalovaM, SchleifferA, BuonomoSB, et al. (2000) Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I. Cell 103 : 1155–1168.

4. RabitschKP, PetronczkiM, JaverzatJP, GenierS, ChwallaB, et al. (2003) Kinetochore recruitment of two nucleolar proteins is required for homolog segregation in meiosis I. Dev Cell 4 : 535–548.

5. PetronczkiM, MatosJ, MoriS, GreganJ, BogdanovaA, et al. (2006) Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 126 : 1049–1064.

6. HuangJ, BritoIL, VillenJ, GygiSP, AmonA, et al. (2006) Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Genes Dev 20 : 2887–2901.

7. ClyneRK, KatisVL, JessopL, BenjaminKR, HerskowitzI, et al. (2003) Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 5 : 480–485.

8. MatosJ, LippJJ, BogdanovaA, GuillotS, OkazE, et al. (2008) Dbf4-dependent CDC7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell 135 : 662–678.

9. CorbettKD, YipCK, EeLS, WalzT, AmonA, et al. (2010) The monopolin complex crosslinks kinetochore components to regulate chromosome-microtubule attachments. Cell 142 : 556–567.

10. CorbettKD, HarrisonSC (2012) Molecular architecture of the yeast monopolin complex. Cell Rep 1 : 583–589.

11. GreganJ, RiedelCG, PidouxAL, KatouY, RumpfC, et al. (2007) The kinetochore proteins Pcs1 and Mde4 and heterochromatin are required to prevent merotelic orientation. Curr Biol 17 : 1190–1200.

12. RumpfC, CipakL, SchleifferA, PidouxA, MechtlerK, et al. (2010) Laser microsurgery provides evidence for merotelic kinetochore attachments in fission yeast cells lacking Pcs1 or Clr4. Cell Cycle 9 : 3997–4004.

13. TadaK, SusumuH, SakunoT, WatanabeY (2011) Condensin association with histone H2A shapes mitotic chromosomes. Nature 474 : 477–483.

14. WestermannS, DrubinDG, BarnesG (2007) Structures and functions of yeast kinetochore complexes. Annu Rev Biochem 76 : 563–591.

15. SantaguidaS, MusacchioA (2009) The life and miracles of kinetochores. EMBO J 28 : 2511–2531.

16. WongJ, NakajimaY, WestermannS, ShangC, KangJS, et al. (2007) A protein interaction map of the mitotic spindle. Mol Biol Cell 18 : 3800–3809.

17. GrandinN, ReedSI (1993) Differential function and expression of Saccharomyces cerevisiae B-type cyclins in mitosis and meiosis. Mol Cell Biol 13 : 2113–2125.

18. FerniusJ, MarstonAL (2009) Establishment of cohesion at the pericentromere by the Ctf19 kinetochore subcomplex and the replication fork-associated factor, Csm3. PLoS Genet 5: e1000629.

19. PrzewlokaMR, VenkeiZ, Bolanos-GarciaVM, DebskiJ, DadlezM, et al. (2011) CENP-C is a structural platform for kinetochore assembly. Curr Biol 21 : 399–405.

20. ScrepantiE, De AntoniA, AlushinGM, PetrovicA, MelisT, et al. (2011) Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr Biol 21 : 391–398.

21. MarstonAL, LeeBH, AmonA (2003) The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation. Dev Cell 4 : 711–726.

22. BuonomoSB, RabitschKP, FuchsJ, GruberS, SullivanM, et al. (2003) Division of the nucleolus and its release of CDC14 during anaphase of meiosis I depends on separase, SPO12, and SLK19. Dev Cell 4 : 727–739.

23. KeeneyS, GirouxCN, KlecknerN (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88 : 375–384.

24. HornungP, MaierM, AlushinGM, LanderGC, NogalesE, et al. (2011) Molecular architecture and connectivity of the budding yeast Mtw1 kinetochore complex. J Mol Biol 405 : 548–559.

25. MichaelisC, CioskR, NasmythK (1997) Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell 91 : 35–45.

26. BritoIL, Monje-CasasF, AmonA (2010) The Lrs4-Csm1 monopolin complex associates with kinetochores during anaphase and is required for accurate chromosome segregation. Cell Cycle 9 : 3611–3618.

27. JoglekarAP, BouckDC, MolkJN, BloomKS, SalmonED (2006) Molecular architecture of a kinetochore-microtubule attachment site. Nat Cell Biol 8 : 581–585.

28. TanakaK, ChangHL, KagamiA, WatanabeY (2009) CENP-C functions as a scaffold for effectors with essential kinetochore functions in mitosis and meiosis. Dev Cell 17 : 334–343.

29. PetrovicA, PasqualatoS, DubeP, KrennV, SantaguidaS, et al. (2010) The MIS12 complex is a protein interaction hub for outer kinetochore assembly. J Cell Biol 190 : 835–852.

30. JohzukaK, HoriuchiT (2009) The cis element and factors required for condensin recruitment to chromosomes. Mol Cell 34 : 26–35.

31. LiX, DaweRK (2009) Fused sister kinetochores initiate the reductional division in meiosis I. Nat Cell Biol 11 : 1103–1108.

32. KerrGW, SarkarS, TibblesKL, PetronczkiM, MillarJB, et al. (2011) Meiotic nuclear divisions in budding yeast require PP2A(Cdc55)-mediated antagonism of Net1 phosphorylation by Cdk. J Cell Biol 193 : 1157–1166.

33. HieterP, MannC, SnyderM, DavisRW (1985) Mitotic stability of yeast chromosomes: a colony color assay that measures nondisjunction and chromosome loss. Cell 40 : 381–392.