Mapping and Analysis of Swi5 and Sfr1 Phosphorylation Sites
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
P 30516
Austrian Science Fund FWF - Austria
PubMed
34208949
PubMed Central
PMC8305525
DOI
10.3390/genes12071014
PII: genes12071014
Knihovny.cz E-zdroje
- Klíčová slova
- DNA repair, Schizosaccharomyces pombe, Sfr1, Swi5, meiosis, phosphorylation, recombination,
- MeSH
- fosforylace MeSH
- homologní rekombinace * MeSH
- meióza MeSH
- oprava DNA * MeSH
- poškození DNA * MeSH
- Schizosaccharomyces pombe - proteiny genetika metabolismus MeSH
- Schizosaccharomyces genetika metabolismus MeSH
- vazba proteinů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- Schizosaccharomyces pombe - proteiny MeSH
- Sfr1 protein, S pombe MeSH Prohlížeč
- Swi5 protein, S pombe MeSH Prohlížeč
The evolutionarily conserved Swi5-Sfr1 complex plays an important role in homologous recombination, a process crucial for the maintenance of genomic integrity. Here, we purified Schizosaccharomyces pombe Swi5-Sfr1 complex from meiotic cells and analyzed it by mass spectrometry. Our analysis revealed new phosphorylation sites on Swi5 and Sfr1. We found that mutations that prevent phosphorylation of Swi5 and Sfr1 do not impair their function but swi5 and sfr1 mutants encoding phosphomimetic aspartate at the identified phosphorylation sites are only partially functional. We concluded that during meiosis, Swi5 associates with Sfr1 and both Swi5 and Sfr1 proteins are phosphorylated. However, the functional relevance of Swi5 and Sfr1 phosphorylation remains to be determined.
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Jasin M., Rothstein R. Repair of Strand Breaks by Homologous Recombination. Cold Spring Harb. Perspect. Biol. 2013;5:a012740. doi: 10.1101/cshperspect.a012740. PubMed DOI PMC
Ferrari S.R., Grubb J., Bishop D.K. The Mei5-Sae3 Protein Complex Mediates Dmc1 Activity in Saccharomyces cerevisiae. J. Biol. Chem. 2009;284:11766–11770. doi: 10.1074/jbc.C900023200. PubMed DOI PMC
Akamatsu Y., Tsutsui Y., Morishita T., Siddique M.S., Kurokawa Y., Ikeguchi M., Yamao F., Arcangioli B., Iwasaki H. Fission Yeast Swi5/Sfr1 and Rhp55/Rhp57 Differentially Regulate Rhp51-Dependent Recombination Outcomes. EMBO J. 2007;26:1352–1362. doi: 10.1038/sj.emboj.7601582. PubMed DOI PMC
Hyppa R.W., Smith G.R. Crossover Invariance Determined by Partner Choice for Meiotic DNA Break Repair. Cell. 2010;142:243–255. doi: 10.1016/j.cell.2010.05.041. PubMed DOI PMC
Lorenz A., Osman F., Sun W., Nandi S., Steinacher R., Whitby M.C. The Fission Yeast FANCM Ortholog Directs Non-Crossover Recombination During Meiosis. Science. 2012;336:1585–1588. doi: 10.1126/science.1220111. PubMed DOI PMC
Argunhan B., Sakakura M., Afshar N., Kurihara M., Ito K., Maki T., Kanamaru S., Murayama Y., Tsubouchi H., Takahashi M., et al. Cooperative interactions facilitate stimulation of Rad51 by the Swi5-Sfr1 auxiliary factor complex. eLife. 2020;9 doi: 10.7554/eLife.52566. PubMed DOI PMC
Haruta N., Kurokawa Y., Murayama Y., Akamatsu Y., Unzai S., Tsutsui Y., Iwasaki H. The Swi5–Sfr1 complex stimulates Rhp51/Rad51 and Dmc1-mediated DNA strand exchange in vitro. Nat. Struct. Mol. Biol. 2006;13:823–830. doi: 10.1038/nsmb1136. PubMed DOI
Kuwabara N., Murayama Y., Hashimoto H., Kokabu Y., Ikeguchi M., Sato M., Mayanagi K., Tsutsui Y., Iwasaki H., Shimizu T. Mechanistic Insights into the Activation of Rad51-Mediated Strand Exchange from the Structure of a Recombination Activator, the Swi5-Sfr1 Complex. Structure. 2012;20:440–449. doi: 10.1016/j.str.2012.01.005. PubMed DOI
Loidl J. Conservation and Variability of Meiosis across the Eukaryotes. Annu. Rev. Genet. 2016;50:293–316. doi: 10.1146/annurev-genet-120215-035100. PubMed DOI
Nambiar M., Chuang Y.-C., Smith G.R. Distributing meiotic crossovers for optimal fertility and evolution. DNA Repair. 2019;81:102648. doi: 10.1016/j.dnarep.2019.102648. PubMed DOI PMC
Akamatsu Y., Jasin M. Role for the Mammalian Swi5-Sfr1 Complex in DNA Strand Break Repair through Homologous Recombination. PLoS Genet. 2010;6:e1001160. doi: 10.1371/journal.pgen.1001160. PubMed DOI PMC
Khasanov F.K., Salakhova A.F., Khasanova O.S., Grishchuk A.L., Chepurnaja O.V., Korolev V.G., Kohli J., Bashkirov V.I. Genetic analysis reveals different roles of Schizosaccharomyces pombe sfr1/dds20 in meiotic and mitotic DNA recombination and repair. Curr. Genet. 2008;54:197–211. doi: 10.1007/s00294-008-0212-z. PubMed DOI
Ellermeier C., Schmidt H., Smith G.R. Swi5 Acts in Meiotic DNA Joint Molecule Formation in Schizosaccharomyces pombe. Genetics. 2004;168:1891–1898. doi: 10.1534/genetics.104.034280. PubMed DOI PMC
Akamatsu Y., Dziadkowiec D., Ikeguchi M., Shinagawa H., Iwasaki H. Two different Swi5-containing protein complexes are involved in mating-type switching and recombination repair in fission yeast. Proc. Natl. Acad. Sci. USA. 2003;100:15770–15775. doi: 10.1073/pnas.2632890100. PubMed DOI PMC
Yuan J., Chen J. The Role of the Human SWI5-MEI5 Complex in Homologous Recombination Repair. J. Biol. Chem. 2011;286:9888–9893. doi: 10.1074/jbc.M110.207290. PubMed DOI PMC
Krejci L., Altmannova V., Spirek M., Zhao X. Homologous recombination and its regulation. Nucleic Acids Res. 2012;40:5795–5818. doi: 10.1093/nar/gks270. PubMed DOI PMC
Phadnis N., Cipak L., Polakova S.B., Hyppa R.W., Cipakova I., Anrather D., Karvaiova L., Mechtler K., Smith G.R., Gregan J. Casein Kinase 1 and Phosphorylation of Cohesin Subunit Rec11 (SA3) Promote Meiotic Recombination through Linear Element Formation. PLoS Genet. 2015;11:e1005225. doi: 10.1371/journal.pgen.1005225. PubMed DOI PMC
Moreno S., Klar A., Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991;194:795–823. doi: 10.1016/0076-6879(91)94059-l. PubMed DOI
Forsburg S.L., Rhind N. Basic methods for fission yeast. Yeast. 2006;23:173–183. doi: 10.1002/yea.1347. PubMed DOI PMC
Gregan J., Rabitsch P.K., Rumpf C., Novatchkova M., Schleiffer A., Nasmyth K. High-throughput knockout screen in fission yeast. Nat. Protoc. 2006;1:2457–2464. doi: 10.1038/nprot.2006.385. PubMed DOI PMC
Cipak L., Gupta S., Rajovic I., Jin Q.-W., Anrather D., Ammerer G., McCollum D., Gregan J. Crosstalk between casein kinase II and Ste20-related kinase Nak1. Cell Cycle. 2013;12:884–888. doi: 10.4161/cc.24095. PubMed DOI PMC
Rabitsch K.P., Gregan J., Schleiffer A., Javerzat J.-P., 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;14:287–301. doi: 10.1016/j.cub.2004.01.051. PubMed DOI
Cipak L., Hyppa R.W., Smith G.R., Gregan J. ATP analog-sensitive Pat1 protein kinase for synchronous fission yeast meiosis at physiological temperature. Cell Cycle. 2012;11:1626–1633. doi: 10.4161/cc.20052. PubMed DOI PMC
Cipak L., Spirek M., Novatchkova M., Chen Z., Rumpf C., Lugmayr W., Mechtler K., Ammerer G., Csaszar E., Gregan J. An Improved Strategy for Tandem Affinity Purification-Tagging of Schizosaccharomyces pombe Genes. Proteomics. 2009;9:4825–4828. doi: 10.1002/pmic.200800948. PubMed DOI PMC
Carpy A., Krug K., Graf S., Koch A., Popic S., Hauf S., Macek B. Absolute Proteome and Phosphoproteome Dynamics during the Cell Cycle of Schizosaccharomyces pombe (Fission Yeast) Mol. Cell. Proteom. 2014;13:1925–1936. doi: 10.1074/mcp.M113.035824. PubMed DOI PMC
Sivakova B., Jurcik J., Lukacova V., Selicky T., Cipakova I., Barath P., Cipak L. Label-Free Quantitative Phosphoproteomics of the Fission Yeast Schizosaccharomyces pombe Using Strong Anion Exchange- and Porous Graphitic Carbon-Based Fractionation Strategies. Int. J. Mol. Sci. 2021;22:1747. doi: 10.3390/ijms22041747. PubMed DOI PMC
Koch A., Krug K., Pengelley S., Macek B., Hauf S. Mitotic Substrates of the Kinase Aurora with Roles in Chromatin Regulation Identified Through Quantitative Phosphoproteomics of Fission Yeast. Sci. Signal. 2011;4:rs6. doi: 10.1126/scisignal.2001588. PubMed DOI
Swaffer M.P., Jones A.W., Flynn H.R., Snijders B., Nurse P. Quantitative Phosphoproteomics Reveals the Signaling Dynamics of Cell-Cycle Kinases in the Fission Yeast Schizosaccharomyces pombe. Cell Rep. 2018;24:503–514. doi: 10.1016/j.celrep.2018.06.036. PubMed DOI PMC
Kettenbach A.N., Deng L., Wu Y., Baldissard S., Adamo M.E., Gerber S., Moseley J.B. Quantitative Phosphoproteomics Reveals Pathways for Coordination of Cell Growth and Division by the Conserved Fission Yeast Kinase Pom1*. Mol. Cell. Proteom. 2015;14:1275–1287. doi: 10.1074/mcp.M114.045245. PubMed DOI PMC
Wyatt M.D., Pittman D.L. Methylating Agents and DNA Repair Responses: Methylated Bases and Sources of Strand Breaks. Chem. Res. Toxicol. 2006;19:1580–1594. doi: 10.1021/tx060164e. PubMed DOI PMC
Martín-Castellanos C., Blanco M., Rozalén A.E., Pérez-Hidalgo L., García A.I., Conde F.M., Mata J., Ellermeier C., Davis L., San-Segundo P., et al. A Large-Scale Screen in S. pombe Identifies Seven Novel Genes Required for Critical Meiotic Events. Curr. Biol. 2005;15:2056–2062. doi: 10.1016/j.cub.2005.10.038. PubMed DOI PMC
Nabeshima K., Nakagawa T., Straight A.F., Murray A., Chikashige Y., Yamashita Y.M., Hiraoka Y., Yanagida M. Dynamics of Centromeres during Metaphase–Anaphase Transition in Fission Yeast: Dis1 Is Implicated in Force Balance in Metaphase Bipolar Spindle. Mol. Biol. Cell. 1998;9:3211–3225. doi: 10.1091/mbc.9.11.3211. PubMed DOI PMC
Yamamoto A., Hiraoka Y. Monopolar spindle attachment of sister chromatids is ensured by two distinct mechanisms at the first meiotic division in fission yeast. EMBO J. 2003;22:2284–2296. doi: 10.1093/emboj/cdg222. PubMed DOI PMC
Mata J., Lyne R., Burns G., Bahler J. The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 2002;32:143–147. doi: 10.1038/ng951. PubMed DOI
Dephoure N., Gould K., Gygi S.P., Kellogg D.R. Mapping and analysis of phosphorylation sites: A quick guide for cell biologists. Mol. Biol. Cell. 2013;24:535–542. doi: 10.1091/mbc.e12-09-0677. PubMed DOI PMC
Huraiova B., Kanovits J., Polakova S.B., Cipak L., Benko Z., Sevcovicova A., Anrather D., Ammerer G., Duncan C.D.S., Mata J., et al. Proteomic Analysis of Meiosis and Characterization of Novel Short Open Reading Frames in the Fission Yeastschizosaccharomyces pombe. Cell Cycle. 2020;19:1777–1785. doi: 10.1080/15384101.2020.1779470. PubMed DOI PMC