Shugoshins Function As a Guardian for Chromosomal Stability in Nuclear Division

Overview

Journal Cell Cycle

Specialty Cell Biology

Date 2012 Jun 27

PMID 22732496

Citations 13

Authors

Yixin Yao

Wei Dai

Affiliations

Soon will be listed here.

Abstract

Accurate chromosome segregation during mitosis and meiosis is regulated and secured by several distinctly different yet intricately connected regulatory mechanisms. As chromosomal instability is a hallmark of a majority of tumors as well as a cause of infertility for germ cells, extensive research in the past has focused on the identification and characterization of molecular components that are crucial for faithful chromosome segregation during cell division. Shugoshins, including Sgo1 and Sgo2, are evolutionarily conserved proteins that function to protect sister chromatid cohesion, thus ensuring chromosomal stability during mitosis and meiosis in eukaryotes. Recent studies reveal that Shugoshins in higher animals play an essential role not only in protecting centromeric cohesion of sister chromatids and assisting bi-orientation attachment at the kinetochores, but also in safeguarding centriole cohesion/engagement during early mitosis. Many molecular components have been identified that play essential roles in modulating/mediating Sgo functions. This review primarily summarizes recent advances on the mechanisms of action of Shugoshins in suppressing chromosomal instability during nuclear division in eukaryotic organisms.

Citing Articles

A tale of two serines: the effects of histone H2A mutations S122A and S129A on chromosome nondisjunction in Saccharomyces cerevisiae.

Kozmin S, Dominska M, Kokoska R, Petes T Genetics. 2024; 229(1):1-31.

PMID: 39558477 PMC: 11708911. DOI: 10.1093/genetics/iyae194.

Exploring Plant Meiosis: Insights from the Kinetochore Perspective.

Zhou K, Zhang C, Niu F, Bai H, Wu D, Deng J Curr Issues Mol Biol. 2023; 45(10):7974-7995.

PMID: 37886947 PMC: 10605258. DOI: 10.3390/cimb45100504.

High SGO2 predicted poor prognosis and high therapeutic value of lung adenocarcinoma and promoted cell proliferation, migration, invasion, and epithelial-to-mesenchymal transformation.

Wu Z, Zhuo T, Li Z, Zhu Y, Wu J, Liang G J Cancer. 2023; 14(12):2301-2314.

PMID: 37576392 PMC: 10414046. DOI: 10.7150/jca.86285.

Sustained Shugoshin 1 downregulation reduces tumor growth and metastasis in a mouse xenograft tumor model of triple-negative breast cancer.

Jusino S, Rivera-Rivera Y, Chardon-Colon C, Rodriguez-Rodriguez P, Roman-Gonzalez J, Julia-Hernandez V Cell Div. 2023; 18(1):6.

PMID: 37122033 PMC: 10150544. DOI: 10.1186/s13008-023-00088-5.

Parallel pathways for recruiting effector proteins determine centromere drive and suppression.

Kumon T, Ma J, Akins R, Stefanik D, Nordgren C, Kim J Cell. 2021; 184(19):4904-4918.e11.

PMID: 34433012 PMC: 8448984. DOI: 10.1016/j.cell.2021.07.037.

References

DAVIS B . Genetic analysis of a meiotic mutant resulting in precocious sister-centromere separation in Drosophila melanogaster. Mol Gen Genet. 1971; 113(3):251-72. DOI: 10.1007/BF00339546. View

Fernius J, Hardwick K . Bub1 kinase targets Sgo1 to ensure efficient chromosome biorientation in budding yeast mitosis. PLoS Genet. 2007; 3(11):e213. PMC: 2098806. DOI: 10.1371/journal.pgen.0030213. View

Mazzorana M, Montoya G, Mortuza G . The centrosome: a target for cancer therapy. Curr Cancer Drug Targets. 2011; 11(5):600-12. DOI: 10.2174/156800911795655949. View

Kitajima T, Kawashima S, Watanabe Y . The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature. 2004; 427(6974):510-7. DOI: 10.1038/nature02312. View

Shintomi K, Hirano T . Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes Dev. 2009; 23(18):2224-36. PMC: 2751989. DOI: 10.1101/gad.1844309. View

Wang Z, Christman M . Replication-related activities establish cohesion between sister chromatids. Cell Biochem Biophys. 2002; 35(3):289-301. DOI: 10.1385/CBB:35:3:289. View

Wang X, Yang Y, Dai W . Differential subcellular localizations of two human Sgo1 isoforms: implications in regulation of sister chromatid cohesion and microtubule dynamics. Cell Cycle. 2006; 5(6):635-40. View

Hunt P, Lemaire R, Embury P, Sheean L, Mroz K . Analysis of chromosome behavior in intact mammalian oocytes: monitoring the segregation of a univalent chromosome during female meiosis. Hum Mol Genet. 1995; 4(11):2007-12. DOI: 10.1093/hmg/4.11.2007. View

Waizenegger I, Hauf S, Meinke A, Peters J . Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell. 2000; 103(3):399-410. DOI: 10.1016/s0092-8674(00)00132-x. View

10.

Tsou M, Stearns T . Controlling centrosome number: licenses and blocks. Curr Opin Cell Biol. 2005; 18(1):74-8. DOI: 10.1016/j.ceb.2005.12.008. View

11.

Dai J, Sullivan B, Higgins J . Regulation of mitotic chromosome cohesion by Haspin and Aurora B. Dev Cell. 2006; 11(5):741-50. DOI: 10.1016/j.devcel.2006.09.018. View

12.

Fu G, Ding X, Yuan K, Aikhionbare F, Yao J, Cai X . Phosphorylation of human Sgo1 by NEK2A is essential for chromosome congression in mitosis. Cell Res. 2007; 17(7):608-18. DOI: 10.1038/cr.2007.55. 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.

Clarke A, Tang T, Ooi D, Orr-Weaver T . POLO kinase regulates the Drosophila centromere cohesion protein MEI-S332. Dev Cell. 2004; 8(1):53-64. DOI: 10.1016/j.devcel.2004.12.003. View

15.

Schiebel E . gamma-tubulin complexes: binding to the centrosome, regulation and microtubule nucleation. Curr Opin Cell Biol. 2000; 12(1):113-8. DOI: 10.1016/s0955-0674(99)00064-2. View

16.

Moore D, Page A, Tang T, Kerrebrock A . The cohesion protein MEI-S332 localizes to condensed meiotic and mitotic centromeres until sister chromatids separate. J Cell Biol. 1998; 140(5):1003-12. PMC: 2132693. DOI: 10.1083/jcb.140.5.1003. View

17.

Lee J, Dej K, Lopez J, Orr-Weaver T . Control of centromere localization of the MEI-S332 cohesion protection protein. Curr Biol. 2004; 14(14):1277-83. DOI: 10.1016/j.cub.2004.07.023. View

18.

Cheung C, Coumar M, Chang J, Hsieh H . Aurora kinase inhibitor patents and agents in clinical testing: an update (2009-10). Expert Opin Ther Pat. 2011; 21(6):857-84. DOI: 10.1517/13543776.2011.574614. View

19.

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

20.

Clift D, Marston A . The role of shugoshin in meiotic chromosome segregation. Cytogenet Genome Res. 2011; 133(2-4):234-42. PMC: 3077332. DOI: 10.1159/000323793. View