The Drosophila Meiotic Kleisin C(2)M Functions Before the Meiotic Divisions

Overview

Journal Chromosoma

Specialty Molecular Biology

Date 2004 Sep 18

PMID 15375666

Citations 33

Authors

Doris Heidmann

Susann Horn

Stefan Heidmann

Alexander Schleiffer

Kim Nasmyth

Christian F Lehner

Affiliations

Soon will be listed here.

Abstract

Stepwise and regionally controlled resolution of sister chromatid cohesion is thought to be crucial for faithful chromosome segregation during meiotic divisions. In yeast, the meiosis-specific alpha-kleisin subunit of the cohesin complex, Rec8, is protected from cleavage by separase but only during meiosis I and specifically within the pericentromeric region. While the Drosophila genome does not contain an obvious Rec8 orthologue, as other animal and plant genomes, it includes c(2)M, which encodes a distant alpha-kleisin family member involved in female meiosis. C(2)M associates in vivo with the Smc3 cohesin subunit, as previously shown for yeast Rec8. In contrast to Rec8, however, C(2)M accumulates predominantly after the pre-meiotic S-phase. Moreover, after association with the synaptonemal complex, it disappears again and cannot be detected on meiotic chromosomes by metaphase I. C(2)M cleavage fragments are not observed during completion of the meiotic divisions, and mutations within putative separase cleavage sites do not interfere with meiotic chromosome segregation. Therefore, C(2)M appears to function within the synaptonemal complex during prophase I but possibly not thereafter. This suggests that C(2)M may not confer sister chromatid cohesion needed for meiosis I and II chromosome segregation.

Citing Articles

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References

Arumugam P, Gruber S, Tanaka K, Haering C, Mechtler K, Nasmyth K . ATP hydrolysis is required for cohesin's association with chromosomes. Curr Biol. 2003; 13(22):1941-53. DOI: 10.1016/j.cub.2003.10.036. View

Gruber S, Haering C, Nasmyth K . Chromosomal cohesin forms a ring. Cell. 2003; 112(6):765-77. DOI: 10.1016/s0092-8674(03)00162-4. View

Page S, Hawley R . c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev. 2001; 15(23):3130-43. PMC: 312841. DOI: 10.1101/gad.935001. View

Leismann O, Lehner C . Drosophila securin destruction involves a D-box and a KEN-box and promotes anaphase in parallel with Cyclin A degradation. J Cell Sci. 2003; 116(Pt 12):2453-60. DOI: 10.1242/jcs.00411. View

Cai X, Dong F, Edelmann R, Makaroff C . The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci. 2003; 116(Pt 14):2999-3007. DOI: 10.1242/jcs.00601. View

Jager H, Herzig A, Lehner C, Heidmann S . Drosophila separase is required for sister chromatid separation and binds to PIM and THR. Genes Dev. 2001; 15(19):2572-84. PMC: 312799. DOI: 10.1101/gad.207301. View

Uhlmann F, Wernic D, Poupart M, Koonin E, Nasmyth K . Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell. 2000; 103(3):375-86. DOI: 10.1016/s0092-8674(00)00130-6. View

Jacobs H, Knoblich J, Lehner C . Drosophila Cyclin B3 is required for female fertility and is dispensable for mitosis like Cyclin B. Genes Dev. 1998; 12(23):3741-51. PMC: 317254. DOI: 10.1101/gad.12.23.3741. View

Schleiffer A, Kaitna S, Maurer-Stroh S, Glotzer M, Nasmyth K, Eisenhaber F . Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol Cell. 2003; 11(3):571-5. DOI: 10.1016/s1097-2765(03)00108-4. View

10.

Bickel S, Orr-Weaver T, Balicky E . The sister-chromatid cohesion protein ORD is required for chiasma maintenance in Drosophila oocytes. Curr Biol. 2002; 12(11):925-9. DOI: 10.1016/s0960-9822(02)00846-1. View

11.

Marston A, Tham W, Shah H, Amon A . A genome-wide screen identifies genes required for centromeric cohesion. Science. 2004; 303(5662):1367-70. DOI: 10.1126/science.1094220. View

12.

Sumara I, Vorlaufer E, Stukenberg P, Kelm O, Redemann N, Nigg E . The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell. 2002; 9(3):515-25. DOI: 10.1016/s1097-2765(02)00473-2. View

13.

Funabiki H, Yamano H, Kumada K, Nagao K, Hunt T, Yanagida M . Cut2 proteolysis required for sister-chromatid seperation in fission yeast. Nature. 1996; 381(6581):438-41. DOI: 10.1038/381438a0. View

14.

Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C . Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J Cell Biol. 2003; 160(5):657-70. PMC: 2173354. DOI: 10.1083/jcb.200212080. View

15.

Hong A, Lee-Kong S, Iida T, Sugimura I, Lilly M . The p27cip/kip ortholog dacapo maintains the Drosophila oocyte in prophase of meiosis I. Development. 2003; 130(7):1235-42. DOI: 10.1242/dev.00352. View

16.

Waizenegger I, Gimenez-Abian J, Wernic D, Peters J . Regulation of human separase by securin binding and autocleavage. Curr Biol. 2002; 12(16):1368-78. DOI: 10.1016/s0960-9822(02)01073-4. View

17.

Rabitsch K, Gregan J, Schleiffer A, Javerzat J, Eisenhaber F, Nasmyth K . Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Curr Biol. 2004; 14(4):287-301. DOI: 10.1016/j.cub.2004.01.051. View

18.

Zou H, McGarry T, Bernal T, Kirschner M . Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science. 1999; 285(5426):418-22. DOI: 10.1126/science.285.5426.418. View

19.

Klein F, Mahr P, Galova M, Buonomo S, Michaelis C, Nairz K . A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell. 1999; 98(1):91-103. DOI: 10.1016/S0092-8674(00)80609-1. View

20.

Anderson D, Losada A, Erickson H, Hirano T . Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol. 2002; 156(3):419-24. PMC: 2173330. DOI: 10.1083/jcb.200111002. View