Geometry and Force Behind Kinetochore Orientation: Lessons from Meiosis

Overview

Journal Nat Rev Mol Cell Biol

Specialties Cell Biology
Molecular Biology

Date 2012 May 17

PMID 22588367

Citations 101

Authors

Yoshinori Watanabe

Affiliations

Soon will be listed here.

Abstract

During mitosis, replicated chromosomes (sister chromatids) become attached at the kinetochore by spindle microtubules emanating from opposite poles and segregate equationally. In the first division of meiosis, however, sister chromatids become attached from the same pole and co-segregate, whereas homologous chromosomes connected by chiasmata segregate to opposite poles. Disorder in this specialized chromosome attachment in meiosis is the leading cause of miscarriage in humans. Recent studies have elucidated the molecular mechanisms determining chromosome orientation, and consequently segregation, in meiosis. Comparative studies of meiosis and mitosis have led to the general principle that kinetochore geometry and tension exerted by microtubules synergistically generate chromosome orientation.

Citing Articles

Meiosis-specific distal cohesion site decoupled from the kinetochore.

Pan B, Bruno M, Macfarlan T, Akera T Nat Commun. 2025; 16(1):2116.

PMID: 40032846 PMC: 11876576. DOI: 10.1038/s41467-025-57438-w.

Hybrid female sterility due to cohesin protection errors in oocytes.

El Yakoubi W, Pan B, Akera T bioRxiv. 2025; .

PMID: 40027736 PMC: 11870456. DOI: 10.1101/2025.02.16.638358.

Distinct and interdependent functions of three RING proteins regulate recombination during mammalian meiosis.

Ito M, Yun Y, Kulkarni D, Lee S, Sandhu S, Nunez B Proc Natl Acad Sci U S A. 2025; 122(2):e2412961121.

PMID: 39761402 PMC: 11745341. DOI: 10.1073/pnas.2412961121.

Meiosis-specific decoupling of the pericentromere from the kinetochore.

Pan B, Bruno M, Macfarlan T, Akera T bioRxiv. 2024; .

PMID: 39091844 PMC: 11291024. DOI: 10.1101/2024.07.21.604490.

Meiosis-specific functions of kinetochore protein SPC105R required for chromosome segregation in oocytes.

Joshi J, Changela N, Mahal L, Jang J, Defosse T, Wang L Mol Biol Cell. 2024; 35(8):ar105.

PMID: 38865189 PMC: 11321039. DOI: 10.1091/mbc.E24-02-0067.

References

Ellermeier C, Smith G . Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 2005; 102(31):10952-7. PMC: 1182449. DOI: 10.1073/pnas.0504805102. View

Tanaka T, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E . Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell. 2002; 108(3):317-29. DOI: 10.1016/s0092-8674(02)00633-5. View

Solomon D, Kim T, Diaz-Martinez L, Fair J, Elkahloun A, Harris B . Mutational inactivation of STAG2 causes aneuploidy in human cancer. Science. 2011; 333(6045):1039-43. PMC: 3374335. DOI: 10.1126/science.1203619. View

Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K . AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci. 2005; 118(Pt 20):4621-32. DOI: 10.1242/jcs.02583. View

Kitajima T, Miyazaki Y, Yamamoto M, Watanabe Y . Rec8 cleavage by separase is required for meiotic nuclear divisions in fission yeast. EMBO J. 2003; 22(20):5643-53. PMC: 213781. DOI: 10.1093/emboj/cdg527. View

Hodges C, Hunt P . Simultaneous analysis of chromosomes and chromosome-associated proteins in mammalian oocytes and embryos. Chromosoma. 2002; 111(3):165-9. DOI: 10.1007/s00412-002-0195-3. View

Welburn J, Vleugel M, Liu D, Yates 3rd J, Lampson M, Fukagawa T . Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol Cell. 2010; 38(3):383-92. PMC: 2873218. DOI: 10.1016/j.molcel.2010.02.034. View

Kiburz B, Amon A, Marston A . Shugoshin promotes sister kinetochore biorientation in Saccharomyces cerevisiae. Mol Biol Cell. 2007; 19(3):1199-209. PMC: 2262988. DOI: 10.1091/mbc.e07-06-0584. View

Neale M, Keeney S . Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature. 2006; 442(7099):153-8. PMC: 5607947. DOI: 10.1038/nature04885. View

10.

Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo N, Adams D . Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev. 2010; 24(22):2505-16. PMC: 2975927. DOI: 10.1101/gad.605910. View

11.

Miyazaki W . Sister-chromatid cohesion in mitosis and meiosis. Annu Rev Genet. 1994; 28:167-87. DOI: 10.1146/annurev.ge.28.120194.001123. View

12.

Vanoosthuyse V, Prykhozhij S, Hardwick K . Shugoshin 2 regulates localization of the chromosomal passenger proteins in fission yeast mitosis. Mol Biol Cell. 2007; 18(5):1657-69. PMC: 1855032. DOI: 10.1091/mbc.e06-10-0890. View

13.

Huang H, Feng J, Famulski J, Rattner J, Liu S, Kao G . Tripin/hSgo2 recruits MCAK to the inner centromere to correct defective kinetochore attachments. J Cell Biol. 2007; 177(3):413-24. PMC: 2064832. DOI: 10.1083/jcb.200701122. View

14.

Lister L, Kouznetsova A, Hyslop L, Kalleas D, Pace S, Barel J . Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol. 2010; 20(17):1511-21. DOI: 10.1016/j.cub.2010.08.023. View

15.

Revenkova E, Herrmann K, Adelfalk C, Jessberger R . Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol. 2010; 20(17):1529-33. PMC: 2945217. DOI: 10.1016/j.cub.2010.08.024. View

16.

Monje-Casas F, Prabhu V, Lee B, Boselli M, Amon A . Kinetochore orientation during meiosis is controlled by Aurora B and the monopolin complex. Cell. 2007; 128(3):477-90. PMC: 1808280. DOI: 10.1016/j.cell.2006.12.040. View

17.

Lee J, Hirano T . RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol. 2011; 192(2):263-76. PMC: 3172173. DOI: 10.1083/jcb.201008005. View

18.

Hamant O, Golubovskaya I, Meeley R, Fiume E, Timofejeva L, Schleiffer A . A REC8-dependent plant Shugoshin is required for maintenance of centromeric cohesion during meiosis and has no mitotic functions. Curr Biol. 2005; 15(10):948-54. DOI: 10.1016/j.cub.2005.04.049. View

19.

Pidoux A, Allshire R . Kinetochore and heterochromatin domains of the fission yeast centromere. Chromosome Res. 2004; 12(6):521-34. DOI: 10.1023/B:CHRO.0000036586.81775.8b. View

20.

Xu H, Beasley M, Warren W, van der Horst G, McKay M . Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell. 2005; 8(6):949-61. DOI: 10.1016/j.devcel.2005.03.018. View