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http://dx.doi.org/10.4014/jmb.1610.10074

Hed1 Promotes Meiotic Crossover Formation in Saccharomyces cerevisiae  

Kong, Yoon-Ju (Department of Life Sciences, Chung-Ang University)
Joo, Jeong-Hwan (Department of Life Sciences, Chung-Ang University)
Kim, Keun Pil (Department of Life Sciences, Chung-Ang University)
Hong, Soogil (Department of Life Sciences, Chung-Ang University)
Publication Information
Journal of Microbiology and Biotechnology / v.27, no.2, 2017 , pp. 405-411 More about this Journal
Abstract
Homologous recombination occurs between homologous chromosomes and is significantly involved in programmed double-strand break (DSB) repair. Activation of two recombinases, Rad51 and Dmc1, is essential for an interhomolog bias during meiosis. Rad51 participates in both mitotic and meiotic recombination, and its strand exchange activity is regulated by an inhibitory factor during meiosis. Thus, activities of Rad51 and Dmc1 are coordinated to promote homolog bias. It has been reported that Hed1, a meiosis-specific protein in budding yeast, regulates Rad51-dependent recombination activity. Here, we investigated the role of Hed1 in meiotic recombination by ectopic expression of the protein after pre-meiotic replication in Saccharomyces cerevisiae. DNA physical analysis revealed that the overexpression of Hed1 delays the DSB-to-joint molecule (JM) transition and promotes interhomolog JM formation. The study indicates a possible role of Hed1 in controlling the strand exchange activity of Rad51 and, eventually, meiotic crossover formation.
Keywords
Hed1; meiosis; recombination; Saccharomyces cerevisiae;
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1 Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, Lee CY, et al. 2013. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet. 9: e1003978.   DOI
2 Prieler S, Penkner A, Borde V, Klein F. 2005. The control of Spo11's interaction with meiotic recombination hotspots. Genes Dev. 19: 255-269.   DOI
3 Paull TT, Gellert M. The 3' to 5' exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell 1: 969-979.
4 Usui T, Ohta T, Oshiumi H, Tomizawa J, Ogawa H, Ogawa T. 1998. Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95: 705-716.   DOI
5 Cannavo E, Cejka P. 2014. Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature 514: 122-125.   DOI
6 Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK. 1998. Rad52 associates with RPA and functions with Rad55 and Rad57 to assemble meiotic recombination complexes. Genes Dev. 12: 2208-2221.   DOI
7 Hays SL, Firmenich AA, Berg P. 1995. Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl. Acad. Sci. USA 92: 6925-6929.   DOI
8 Sugiyama T, Zaitseva EM, Kowalczykowski SC. 1997. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 272: 7940-7945.   DOI
9 Sung P. 1997. Function of yeast Rad52 protein as a mediator between replication protein A and the R ad51 recombinase. J. Biol. Chem. 272: 28194-28197.   DOI
10 Hong EL, Shinohara A, Bishop DK. 2001. Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA. J. Biol. Chem. 276: 41906-41912.   DOI
11 Bishop DK. 1994. RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79: 1081-1092.   DOI
12 Arora C, Kee K, Maleki S, Keeney S. 2004. Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol. Cell 13: 549-559.   DOI
13 Roeder GS. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev. 11: 2600-2621.   DOI
14 Kleckner N, Zhang L, Weiner B, Zickler D. 2011. Meiotic chromosome dynamics. In Rippe K (ed.). Genome Organization and Function in the Cell Nucleus, Ch. 19. WileyVCH, Weinheim Germany.
15 Zickler D, Kleckner N. 1999. Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33: 603-754.   DOI
16 Kee K, Protacio RU, Arora C, Keeney S. 2004. Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO J. 23: 1815-1824.   DOI
17 Keeney S. 2001. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52: 1-53.
18 Hong S, Sung Y, Yu M, Lee M, Kleckner N, Kim KP. 2013. The logic and mechanism of homologous recombination partner choice. Mol. Cell 51: 440-453.   DOI
19 Shinohara A, Ogawa H, Ogawa T. 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69: 457-470.   DOI
20 Krejci L, Altmannova V, Spirek M, Zhao X. 2012. Homologous recombination and its regulation. Nucleic Acids Res. 40: 5795-5818.   DOI
21 Bishop DK, Park D, Xu L, Kleckner N. 1992. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69: 439-456.   DOI
22 Jiang H, Xie Y, Houston P, Stemke-Hale K, Mortensen UH, Rothstein R, Kodadek T. 1996. Direct association between the yeast Rad51 and Rad54 recombination proteins. J. Biol. Chem. 271: 33181-33186.   DOI
23 Sehorn MG, Sung P. 2004. Meiotic recombination: an affair of two recombinases. Cell Cycle 3: 1375-1377.   DOI
24 Sung P. 1994. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast Rad51 protein. Science 265: 1241-1243.   DOI
25 Bishop DK, Zickler D. 2004. Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9-15.   DOI
26 Sasanuma H, Tawaramoto MS, Lao JP, Hosaka H, Sanda E, Suzuki M, et al. 2013. A new protein complex promoting the assembly of Rad51 filaments. Nat. Commun. 4: 1676.   DOI
27 Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, Sung P. 2008. Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev. 22: 786-795.   DOI
28 Tsubouchi H, Roeder GS. 2006. Budding yeast Hed1 downregulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev. 20: 1766-1775.   DOI
29 Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, et al. 2004. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962.   DOI
30 Hong S, Kim KP. 2013. Shu1 promotes homolog bias of meiotic recombination in Saccharomyces cerevisiae. Mol. Cells 36: 446-454.   DOI
31 Lee MS, Yoon SW, Kim KP. 2015. Mitotic cohesin subunit Mcd1 regulates the progression of meiotic recombination in budding yeast. J. Microbiol. Biotechnol. 25: 598-605.   DOI
32 Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, Kleckner N. 2010. Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924-937.   DOI
33 Schwacha A, Kleckner N. 1994. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51-63.   DOI
34 Cho HR, Kong YJ, Hong SG, Kim KP. 2016. Hop2 and Sae3 are required for Dmc1-mediated double-strand break repair via homolog bias during meiosis. Mol. Cells 39: 550-556.   DOI
35 Hong S, Choi EH, Kim KP. 2015. Ycs4 is required for efficient double-strand break formation and homologous recombination during meiosis. J. Microbiol. Biotechnol. 25: 1026-1035.   DOI
36 Lee MS, Yu M, Kim KY, Park GH, Kim KP. 2015. Functional validation of rare human genetic variants involved in homologous recombination using Saccharomyces cerevisiae. PLoS One 10: e0124152.   DOI
37 Yoon SW, Lee MS, Xaver M, Zhang L, Hong SG, Kong YJ, et al. 2016. Meiotic prophase roles of Rec8 in crossover recombination and chromosome structure. Nucleic Acids Res. 44: 9296-9314.