SCF Ubiquitin Ligase Regulates Synaptonemal Complex Formation During Meiosis

Overview

Journal Life Sci Alliance

Specialties Biochemistry
Biology
Cell Biology
Molecular Biology

Date 2020 Dec 9

PMID 33293336

Citations 11

Authors

Zhihui Zhu

Mohammad Bani Ismail

Miki Shinohara

Akira Shinohara

Affiliations

Soon will be listed here.

Abstract

Homologous chromosomes pair with each other during meiosis, culminating in the formation of the synaptonemal complex (SC), which is coupled with meiotic recombination. In this study, we showed that a meiosis-specific depletion mutant of a cullin (Cdc53) in the SCF (Skp-Cullin-F-box) ubiquitin ligase, which plays a critical role in cell cycle regulation during mitosis, is deficient in SC formation. However, the mutant is proficient in forming crossovers, indicating the uncoupling of meiotic recombination with SC formation in the mutant. Furthermore, the deletion of the gene encoding a meiosis-specific AAA+ ATPase suppresses SC-assembly defects induced by depletion. On the other hand, the double mutant is defective in meiotic crossover formation, suggesting the assembly of SC with unrepaired DNA double-strand breaks. A temperature-sensitive mutant of , which encodes an F-box protein of SCF, shows meiotic defects similar to those of the -depletion mutant. These results suggest that SCF, probably SCF-dependent protein ubiquitylation, regulates and collaborates with Pch2 in SC assembly and meiotic recombination.

Citing Articles

Make it or break it: Protein homeostasis in the synaptonemal complex.

Kursel L, Rog O Proc Natl Acad Sci U S A. 2024; 121(41):e2416357121.

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A chromosome-coupled ubiquitin-proteasome pathway is required for meiotic surveillance.

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Skp1 proteins are structural components of the synaptonemal complex in .

Blundon J, Cesar B, Bae J, cavka I, Haversat J, Ries J Sci Adv. 2024; 10(7):eadl4876.

PMID: 38354250 PMC: 10866564. DOI: 10.1126/sciadv.adl4876.

The Msh5 complex shows homeostatic localization in response to DNA double-strand breaks in yeast meiosis.

Shinohara M, Shinohara A Front Cell Dev Biol. 2023; 11:1170689.

PMID: 37274743 PMC: 10232913. DOI: 10.3389/fcell.2023.1170689.

Chromosome architecture and homologous recombination in meiosis.

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References

Pyatnitskaya A, Borde V, De Muyt A . Crossing and zipping: molecular duties of the ZMM proteins in meiosis. Chromosoma. 2019; 128(3):181-198. DOI: 10.1007/s00412-019-00714-8. View

Alani E, Padmore R, Kleckner N . Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 1990; 61(3):419-36. DOI: 10.1016/0092-8674(90)90524-i. View

Storlazzi A, Xu L, Schwacha A, Kleckner N . Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc Natl Acad Sci U S A. 1996; 93(17):9043-8. PMC: 38592. DOI: 10.1073/pnas.93.17.9043. View

Bishop D, Park D, Xu L, Kleckner N . DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992; 69(3):439-56. DOI: 10.1016/0092-8674(92)90446-j. View

Shinohara M, Oh S, Hunter N, Shinohara A . Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet. 2008; 40(3):299-309. DOI: 10.1038/ng.83. View

Lee B, Amon A . Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science. 2003; 300(5618):482-6. DOI: 10.1126/science.1081846. View

Zachariae W, Shevchenko A, Andrews P, Ciosk R, Galova M, Stark M . Mass spectrometric analysis of the anaphase-promoting complex from yeast: identification of a subunit related to cullins. Science. 1998; 279(5354):1216-9. DOI: 10.1126/science.279.5354.1216. View

Roeder G . Pch2 links chromatin silencing to meiotic checkpoint control. Cell. 1999; 97(3):313-24. DOI: 10.1016/s0092-8674(00)80741-2. View

Fung J, Rockmill B, Odell M, Roeder G . Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell. 2004; 116(6):795-802. DOI: 10.1016/s0092-8674(04)00249-1. View

10.

Giroux C, Dresser M, Tiano H . Genetic control of chromosome synapsis in yeast meiosis. Genome. 1989; 31(1):88-94. DOI: 10.1139/g89-017. View

11.

Wach A, Brachat A, Pohlmann R, Philippsen P . New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast. 1994; 10(13):1793-808. DOI: 10.1002/yea.320101310. View

12.

Hooker G, Roeder G . A Role for SUMO in meiotic chromosome synapsis. Curr Biol. 2006; 16(12):1238-43. DOI: 10.1016/j.cub.2006.04.045. View

13.

Willems A, Schwab M, Tyers M . A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta. 2004; 1695(1-3):133-70. DOI: 10.1016/j.bbamcr.2004.09.027. View

14.

Yu H, Peters J, King R, Page A, Hieter P, Kirschner M . Identification of a cullin homology region in a subunit of the anaphase-promoting complex. Science. 1998; 279(5354):1219-22. DOI: 10.1126/science.279.5354.1219. View

15.

Voelkel-Meiman K, Taylor L, Mukherjee P, Humphryes N, Tsubouchi H, MacQueen A . SUMO localizes to the central element of synaptonemal complex and is required for the full synapsis of meiotic chromosomes in budding yeast. PLoS Genet. 2013; 9(10):e1003837. PMC: 3789832. DOI: 10.1371/journal.pgen.1003837. View

16.

Leung W, Humphryes N, Afshar N, Argunhan B, Terentyev Y, Tsubouchi T . The synaptonemal complex is assembled by a polySUMOylation-driven feedback mechanism in yeast. J Cell Biol. 2015; 211(4):785-93. PMC: 4657171. DOI: 10.1083/jcb.201506103. View

17.

Baudat F, Manova K, Yuen J, Jasin M, Keeney S . Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell. 2000; 6(5):989-98. DOI: 10.1016/s1097-2765(00)00098-8. View

18.

Nakatsukasa K, Okumura F, Kamura T . Proteolytic regulation of metabolic enzymes by E3 ubiquitin ligase complexes: lessons from yeast. Crit Rev Biochem Mol Biol. 2015; 50(6):489-502. DOI: 10.3109/10409238.2015.1081869. View

19.

Zickler D, Kleckner N . Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 2000; 33:603-754. DOI: 10.1146/annurev.genet.33.1.603. View

20.

Li X, Li X, Schimenti J . Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet. 2007; 3(8):e130. PMC: 1941754. DOI: 10.1371/journal.pgen.0030130. View