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Journal of Microbiology

, Volume 57, Issue 4, pp 221–231 | Cite as

The nature of meiotic chromosome dynamics and recombination in budding yeast

  • Soogil Hong
  • Jeong Hwan Joo
  • Hyeseon Yun
  • Keunpil KimEmail author
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Abstract

During meiosis, crossing over allows for the exchange of genes between homologous chromosomes, enabling their segregation and leading to genetic variation in the resulting gametes. Spo11, a topoisomerase-like protein expressed in eukaryotes, and diverse accessory factors induce programmed double-strand breaks (DSBs) to initiate meiotic recombination during the early phase of meiosis after DNA replication. DSBs are further repaired via meiosis-specific homologous recombination. Studies on budding yeast have provided insights into meiosis and genetic recombination and have improved our understanding of higher eukaryotic systems. Cohesin, a chromosome-associated multiprotein complex, mediates sister chromatid cohesion (SCC), and is conserved from yeast to humans. Diverse cohesin subunits in budding yeast have been identified in DNA metabolic pathways, such as DNA replication, chromosome segregation, recombination, DNA repair, and gene regulation. During cell cycle, SCC is established by multiple cohesin subunits, which physically bind sister chromatids together and modulate proteins that involve in the capturing and separation of sister chromatids. Cohesin components include at least four core subunits that establish and maintain SCC: two structural maintenance chromosome subunits (Smc1 and Smc3), an α-kleisin subunit (Mcd1/Scc1 during mitosis and Rec8 during meiosis), and Scc3/Irr1 (SA1 and SA2). In addition, the cohesin-associated factors Pds5 and Rad61 regulate structural modifications and cell cyclespecific dynamics of chromatin to ensure accurate chromosome segregation. In this review, we discuss SCC and the recombination pathway, as well as the relationship between the two processes in budding yeast, and we suggest a possible conserved mechanism for meiotic chromosome dynamics from yeast to humans.

Keywords

meiosis yeast recombination sister chromatid cohesion cohesin 

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References

  1. Agarwal, S. and Roeder, G.S. 2000. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102, 245–255.Google Scholar
  2. Bishop, D.K. and Zickler, D. 2004. Early decision: Meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117, 9–15.Google Scholar
  3. Börner, G.V., Kleckner, N., and Hunter, N. 2004. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117, 29–45.Google Scholar
  4. Brar, G.A., Kiburz, B.M., Zhang, Y., Kim, J.E., White, F., and Amon, A. 2006. Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441, 532–536.Google Scholar
  5. Brooker, A.S. and Berkowitz, K.M. 2014. The roles of cohesins in mitosis, meiosis, and human health and disease. Methods Mol. Biol. 1170, 229–266.Google Scholar
  6. Brown, M.S., Grubb, J., Zhang, A., Rust, M.J., and Bishop, D.K. 2015. Small Rad51 and Dmc1 complexes often co-occupy both ends of a meiotic DNA double strand break. PLoS Genet. 11, e1005653.Google Scholar
  7. Cejka, P., Cannavo, E., Polaczek, P., Masuda-Sasa, T., Pokharel, S., Campbell, J.L., and Kowalczykowski, S.C. 2010. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467, 112–116.Google Scholar
  8. Challa, K., Lee, M.S., Shinohara, M., Kim, K.P., and Shinohara, A. 2016. Rad61/Wpl1 (Wapl), a cohesin regulator, controls chromosome compaction during meiosis. Nucleic Acids Res. 44, 3190–3203.Google Scholar
  9. Chan, K.L., Gligoris, T., Upcher, W., Kato, Y., Shirahige, K., Nasmyth, K., and Beckouët, F. 2013. Pds5 promotes and protects cohesin acetylation. Proc. Natl. Acad. Sci. USA 110, 13020–13025.Google Scholar
  10. Cheng, C.H., Lo, Y.H., Liang, S.S., Ti, S.C., Lin, F.M., Yeh, C.H., Huang, H.Y., and Wang, T.F. 2006. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev. 20, 2067–2081.Google Scholar
  11. Choi, D.H., Lee, R., Kwon, S.H., and Bae, S.H. 2013. Hrq1 functions independently of Sgs1 to preserve genome integrity in Saccharomyces cerevisiae. J. Microbiol. 51, 105–112.Google Scholar
  12. Chua, P.R. and Roeder, G.S. 1998. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93, 349–359.Google Scholar
  13. Chung, W.H. 2014. To peep into Pif1 helicase: Multifaceted all the way from genome stability to repair-associated DNA synthesis. J. Microbiol. 52, 89–98.Google Scholar
  14. Cloud, V., Chan, Y.L., Grubb, J., Budke, B., and Bishop, D.K. 2012. Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337, 1222–1225.Google Scholar
  15. Deardorff, M.A., Wilde, J.J., Albrecht, M., Dickinson, E., Tennstedt, S., Braunholz, D., Mönnich, M., Yan, Y., Xu, W., Gil-Rodríguez, M.C., et al. 2012. RAD21 mutations cause a human cohesinopathy. Am. J. Hum. Genet. 90, 1014–1027.Google Scholar
  16. DeMare, L.E., Leng, J., Cotney, J., Reilly, S.K., Yin, J., Sarro, R., and Noonan, J.P. 2013. The genomic landscape of cohesin-associated chromatin interactions. Genome Res. 23, 1224–1234.Google Scholar
  17. Denison, S.H., Käfer, E., and May, G.S. 1993. Mutation in the bimD gene of Aspergillus nidulans confers a conditional mitotic block and sensitivity to DNA damaging agents. Genetics 134, 1085–1096.Google Scholar
  18. Gligoris, T.G., Scheinost, J.C., Bürmann, F., Petela, N., Chan, K.L., Uluocak, P., Beckouët, F., Gruber, S., Nasmyth, K., and Löwe, J. 2014. Closing the cohesin ring: structure and function of its Smc3- kleisin interface. Science 346, 963–967.Google Scholar
  19. Gruber, S., Haering, C.H., and Nasmyth, K. 2003. Chromosomal cohesin forms a ring. Cell 112, 765–777.Google Scholar
  20. Guacci, V., Yamamoto, A., Strunnikov, A., Kingsbury, J., Hogan, E., Meluh, P., and Koshland, D. 1993. Structure and function of chromosomes in mitosis of budding yeast, pp. 677–685. In Cold spring harbor symposia on quantitative biology Vol. 58. Cold Spring Harbor Laboratory Press.Google Scholar
  21. Gullerova, M. and Proudfoot, N.J. 2008. Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell 132, 983–995.Google Scholar
  22. Haering, C.H., Farcas, A.M., Arumugam, P., Metson, J., and Nasmyth, K. 2008. The cohesin ring concatenates sister DNA molecules. Nature 454, 297–301.Google Scholar
  23. Haering, C.H., Löwe, J., Hochwagen, A., and Nasmyth, K. 2002. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9, 773–788.Google Scholar
  24. Haering, C.H., Schoffnegger, D., Nishino, T., Helmhart, W., Nasmyth, K., and Löwe, J. 2004. Structure and stability of cohesin’s Smc1-kleisin interaction. Mol. Cell 15, 951–964.Google Scholar
  25. Hartman, T., Stead, K., Koshland, D., and Guacci, V. 2000. Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae. J. Cell Biol. 151, 613–626.Google Scholar
  26. Hirano, M. and Hirano, T. 2002. Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J. 21, 5733–5744.Google Scholar
  27. Hong, S., Sung, Y., Yu, M., Lee, M., Kleckner, N., and Kim, K.P. 2013. The logic and mechanism of homologous recombination partner choice. Mol. Cell 51, 440–453.Google Scholar
  28. Horsfield, J.A., Print, C.G., and Mönnich, M. 2012. Diverse developmental disorders from the one ring: distinct molecular pathways underlie the cohesinopathies. Front. Genet. 3, 171.Google Scholar
  29. Hunter, N. and Kleckner, N. 2001. The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106, 59–70.Google Scholar
  30. Jin, H., Guacci, V., and Yu, H.G. 2009. Pds5 is required for homologue pairing and inhibits synapsis of sister chromatids during yeast meiosis. J. Cell Biol. 186, 713–725.Google Scholar
  31. Katis, V.L., Lipp, J.J., Imre, R., Bogdanova, A., Okaz, E., Habermann, B., Mechtler, K., Nasmyth, K., and Zachariae, W. 2010. Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev. Cell 18, 397–409.Google Scholar
  32. Keeney, S. 2001. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52, 1–53.Google Scholar
  33. Kim, K.P. and Mirkin, E.V. 2018. So similar yet so different: The two ends of a double strand break. Mutat. Res. 809, 70–80.Google Scholar
  34. Kim, K.P., Weiner, B.M., Zhang, L., Jordan, A., Dekker, J., and Kleckner, N. 2010. Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143, 924–937.Google Scholar
  35. Klein, F., Mahr, P., Galova, M., Buonomo, S.B., Michaelis, C., Nairz, K., and Nasmyth, K. 1999. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98, 91–103.Google Scholar
  36. Kowalec, P., Fronk, J., and Kurlandzka, A. 2017. The Irr1/Scc3 protein implicated in chromosome segregation in Saccharomyces cerevisiae has a dual nuclear-cytoplasmic localization. Cell Div. 12, 1.Google Scholar
  37. Krantz, I.D., McCallum, J., DeScipio, C., Kaur, M., Gillis, L.A., Yaeger, D., Jukofsky, L., Wasserman, N., Bottani, A., Morris, C.A., et al. 2004. Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped- B. Nat. Genet. 36, 631–635.Google Scholar
  38. Kueng, S., Hegemann, B., Peters, B.H., Lipp, J.J., Schleiffer, A., Mechtler, K., and Peters, J.M. 2006. Wapl controls the dynamic association of cohesin with chromatin. Cell 127, 955–967.Google Scholar
  39. Kulemzina, I., Schumacher, M.R., Verma, V., Reiter, J., Metzler, J., Failla, A.V., Lanz, C., Sreedharan, V.T., Rätsch, G., and Ivanov, D. 2012. Cohesin rings devoid of Scc3 and Pds5 maintain their stable association with the DNA. PLoS Genet. 8, e1002856.Google Scholar
  40. Lao, J.P., Cloud, V., Huan, C.C., Grubb, J., Thacker, D., Lee, C.Y., Dresser, M.E., Hunter, N., and Bishop, D.K. 2013. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet. 9, e1003978.Google Scholar
  41. Lao, O., Lu, T.T., Nothnagel, M., Junge, O., Freitag-Wolf, S., Caliebe, A., Balascakova, M., Bertranpetit, J., Bindoff, L.A., Comas, D., et al. 2008. Correlation between genetic and geographic structure in Europe. Curr. Biol. 18, 1241–1248.Google Scholar
  42. Lara-Pezzi, E., Pezzi, N., Prieto, I., Barthelemy, I., Carreiro, C., Martínez, A., Maldonado-Rodríguez, A., López-Cabrera, M., and Barbero, J.L. 2004. Evidence of a transcriptional co-activator function of cohesin STAG/SA/Scc3. J. Biol. Chem. 279, 6553–6559.Google Scholar
  43. Larionov, V., Karpova, T., Kouprina, N., and Jouravleva, G. 1985. A mutant of Saccharomyces cerevisiae with impaired maintenance of centromeric plasmids. Curr. Genet. 10, 15–20.Google Scholar
  44. Laurent, J.M., Young, J.H., Kachroo, A.H., and Marcotte, E.M. 2016. Efforts to make and apply humanized yeast. Brief Funct. Genomics 15, 155–163.Google Scholar
  45. Lee, J., Okada, K., Ogushi, S., Miyano, T., Miyake, M., and Yamashita, M. 2006. Loss of Rec8 from chromosome arm and centromere region is required for homologous chromosome separation and sister chromatid separation, respectively, in mammalian meiosis. Cell Cycle 5, 1448–1455.Google Scholar
  46. Li, Y., Muir, K.W., Bowler, M.W., Metz, J., Haering, C.H., and Panne, D. 2018. Structural basis for Scc3-dependent cohesin recruitment to chromatin. Elife 7, e38356.Google Scholar
  47. Lin, W., Jin, H., Liu, X., Hampton, K., and Yu, H.G. 2011. Scc2 regulates gene expression by recruiting cohesin to the chromosome as a transcriptional activator during yeast meiosis. Mol. Biol. Cell 22, 1985–1996.Google Scholar
  48. Liu, J., Feldman, R., Zhang, Z., Deardorff, M.A., Haverfield, E.V., Kaur, M., Li, J.R., Clark, D., Kline, A.D., Waggoner, D.J., et al. 2009. SMC1A expression and mechanism of pathogenicity in probands with X-linked Cornelia de Lange syndrome. Hum. Mutat. 30, 1535–1542.Google Scholar
  49. Longhese, M.P., Bonetti, D., Guerini, I., Manfrini, N., and Clerici, M. 2009. DNA double-strand breaks in meiosis: checking their formation, processing and repair. DNA Repair (Amst.) 8, 1127–1138.Google Scholar
  50. Lopez-Serra, L., Lengronne, A., Borges, V., Kelly, G., and Uhlmann, F. 2013. Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Curr. Biol. 23, 64–69.Google Scholar
  51. Losada, A. and Hirano, T. 2005. Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev. 19, 1269–1287.Google Scholar
  52. Lukaszewicz, A., Shodhan, A., and Loidl, J. 2015. Exo1 and Mre11 execute meiotic DSB end resection in the protist Tetrahymena. DNA Repair 35, 137–143.Google Scholar
  53. Makrantoni, V. and Marston, A.L. 2018. Cohesin and chromosome segregation. Curr. Biol. 28, R688–R693.Google Scholar
  54. Mannini, L., Liu, J., Krantz, I.D., and Musio, A. 2010. Spectrum and consequences of SMC1A mutations: the unexpected involvement of a core component of cohesin in human disease. Hum. Mutat. 31, 5–10.Google Scholar
  55. Marcon, E. and Moens, P.B. 2005. The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins. Bioessays 27, 795–808.Google Scholar
  56. Markowitz, T.E., Suarez, D., Blitzblau, H.G., Patel, N.J., Markhard, A.L., MacQueen, A.J., and Hochwagen, A. 2017. Reduced dosage of the chromosome axis factor Red1 selectively disrupts the meiotic recombination checkpoint in Saccharomyces cerevisiae. PLoS Genet. 13, e1006928.Google Scholar
  57. Marston, A.L. 2014. Chromosome segregation in budding yeast: sister chromatid cohesion and related mechanisms. Genetics 196, 31–63.Google Scholar
  58. Melby, T.E., Ciampaglio, C.N., Briscoe, G., and Erickson, H.P. 1998. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J. Cell Biol. 142, 1595–1604.Google Scholar
  59. Misulovin, Z., Pherson, M., Gause, M., and Dorsett, D. 2018. Brca2, Pds5 and Wapl differentially control cohesin chromosome association and function. PLoS Genet. 14, e1007225.Google Scholar
  60. Molnar, M., Bahler, J., Sipiczki, M., and Kohli, J. 1995. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics 141, 61–73.Google Scholar
  61. Monnich, M., Kuriger, Z., Print, C.G., and Horsfield, J.A. 2011. A zebrafish model of Roberts syndrome reveals that Esco2 depletion interferes with development by disrupting the cell cycle. PLoS One 6, e20051.Google Scholar
  62. Morin, I., Ngo, H.P., Greenall, A., Zubko, M.K., Morrice, N., and Lydall, D. 2008. Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J. 27, 2400–2410.Google Scholar
  63. Moynahan, M.E. and Jasin, M. 2010. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 11, 196–207.Google Scholar
  64. Muir, K.W., Kschonsak, M., Li, Y., Metz, J., Haering, C.H., and Panne, D. 2016. Structure of the Pds5-Scc1 complex and implications for cohesin function. Cell Rep. 14, 2116–2126.Google Scholar
  65. Musio, A., Selicorni, A., Focarelli, M.L., Gervasini, C., Milani, D., Russo, S., Vezzoni, P., and Larizza, L. 2006. X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat. Genet. 38, 528–530.Google Scholar
  66. Nanbu, T., Nguyễn, L.C., Habib, A.G., Hirata, N., Ukimori, S., Tanaka, D., Masuda, K., Takahashi, K., Yukawa, M., Tsuchiya, E., et al. 2015. Fission yeast Exo1 and Rqh1-Dna2 redundantly contribute to resection of uncapped telomeres. PLoS One 10, e0140456.Google Scholar
  67. Nasmyth, K. and Haering, C.H. 2009. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 43, 525–558.Google Scholar
  68. Nasmyth, K., Peters, J.M., and Uhlmann, F. 2000. Splitting the chromosome: Cutting the ties that bind sister chromatids. Science 288, 1379–1385.Google Scholar
  69. Neale, M.J., Pan, J., and Keeney, S. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436, 1053–1057.Google Scholar
  70. New, J.H., Sugiyama, T., Zaitseva, E., and Kowalczykowski, S.C. 1998. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391, 407–410.Google Scholar
  71. Niu, H., Chung, W.H., Zhu, Z., Kwon, Y., Zhao, W., Chi, P., Prakash, R., Seong, C., Liu, D., Lu, L., et al. 2010. Mechanism of the ATPdependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467, 108–111.Google Scholar
  72. Orgil, O., Matityahu, A., Eng, T., Guacci, V., Koshland, D., and Onn, I. 2015. A conserved domain in the Scc3 subunit of cohesin mediates the interaction with both Mcd1 and the cohesin loader complex. PLoS Genet. 11, e1005036.Google Scholar
  73. Panizza, S., Tanaka, T., Hochwagen, A., Eisenhaber, F., and Nasmyth, K. 2000. Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr. Biol. 10, 1557–1564.Google Scholar
  74. Remeseiro, S., Cuadrado, A., Kawauchi, S., Calof, A.L., Lander, A.D., and Losada, A. 2013. Reduction of Nipbl impairs cohesin loading locally and affects transcription but not cohesion-dependent functions in a mouse model of Cornelia de Lange Syndrome. Biochim. Biophys. Acta 1831, 2097–2102.Google Scholar
  75. Remeseiro, S. and Losada, A. 2013. Cohesin, a chromatin engagement ring. Curr. Opin. Cell Biol. 25, 63–71.Google Scholar
  76. Rogacheva, M.V., Manhart, C.M., Chen, C., Guarne, A., Surtees, J., and Alani, E. 2014. Mlh1-Mlh3, a meiotic crossover and DNA mismatch repair factor, is a Msh2-Msh3-stimulated endonuclease. J. Biol. Chem. 289, 5664–5673.Google Scholar
  77. Rowland, B.D., Roig, M.B., Nishino, T., Kurze, A., Uluocak, P., Mishra, A., Beckouët, F., Underwood, P., Metson, J., Imre, R., et al. 2009. Building sister chromatid cohesion: Smc3 acetylation counteracts an antiestablishment activity. Mol. Cell 33, 763–774.Google Scholar
  78. Sasanuma, H., Tawaramoto, M.S., Lao, J.P., Hosaka, H., Sanda, E., Suzuki, M., Yamashita, E., Hunter, N., Shinohara, M., Nakagawa, A., et al. 2013. A new protein complex promoting the assembly of Rad51 filaments. Nat. Commun. 4, 1676.Google Scholar
  79. Sekigawa, M., Kunoh, T., Wada, S., Mukai, Y., Ohshima, K., Ohta, S., Goshima, N., Sasaki, R., and Mizukami, T. 2010. Comprehensive screening of human genes with inhibitory effects on yeast growth and validation of a yeast cell-based system for screening chemicals. J. Biomol. Screen 15, 368–378.Google Scholar
  80. Serrentino, M.E., Chaplais, E., Sommermeyer, V., and Borde, V. 2013. Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet. 9, e1003416.Google Scholar
  81. Shinohara, M., Oh, S.D., Hunter, N., and Shinohara, A. 2008. Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat. Genet. 40, 299–309.Google Scholar
  82. Storlazzi, A., Tesse, S., Ruprich-Robert, G., Gargano, S., Pöggeler, S., Kleckner, N., and Zickler, D. 2008. Coupling meiotic chromosome axis integrity to recombination. Genes Dev. 22, 796–809.Google Scholar
  83. Strunnikov, A.V., Larionov, V.L., and Koshland, D. 1993. SMC1: An essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous family. J. Cell Biol. 123, 1635–1648.Google Scholar
  84. Sugiyama, T., Zaitseva, E.M., and Kowalczykowski, S.C. 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.Google Scholar
  85. Sumara, I., Vorlaufer, E., Gieffers, C., Peters, B.H., and Peters, J.M. 2000. Characterization of vertebrate cohesin complexes and their regulation in prophase. J. Cell Biol. 151, 749–762.Google Scholar
  86. Sun, X., Huang, L., Markowitz, T.E., Blitzblau, H.G., Chen, D., Klein, F., and Hochwagen, A. 2015. Transcription dynamically patterns the meiotic chromosome-axis interface. Elife 10, 4.Google Scholar
  87. Sung, P. 1994. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265, 1241–1243.Google Scholar
  88. Sutani, T., Kawaguchi, T., Kanno, R., Itoh, T., and Shirahige, K. 2009. Budding yeast Wpl1(Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr. Biol. 19, 492–427.Google Scholar
  89. Sym, M., Engebrecht, J.A., and Roeder, G.S. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72, 365–378.Google Scholar
  90. Symington, L.S., Rothstein, R., and Lisby, M. 2014. Mechanisms and regulation of mitotic recombination in Saccharomyces cerevisiae. Genetics 198, 795–835.Google Scholar
  91. Szankasi, P. and Smith, G.R. 1995. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267, 1166–1169.Google Scholar
  92. Tanaka, K., Hao, Z., Kai, M., and Okayama, H. 2001. Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J. 20, 5779–5790.Google Scholar
  93. Tonkin, E.T., Wang, T.J., Lisgo, S., Bamshad, M.J., and Strachan, T. 2004. NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat. Genet. 36, 636–641.Google Scholar
  94. Tran, P.T., Erdeniz, N., Symington, L.S., and Liskay, R.M. 2004. EXO1- A multi-tasking eukaryotic nuclease. DNA Repair 3, 1549–1559.Google Scholar
  95. Tsubouchi, H. and Ogawa, H. 2000. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell 11, 2221–2233.Google Scholar
  96. Tsutsumi, M., Fujiwara, R., Nishizawa, H., Ito, M., Kogo, H., Inagaki, H., Ohye, T., Kato, T., Fujii, T., and Kurahashi, H. 2014. Age-related decrease of meiotic cohesins in human oocytes. PLoS One 9, e96710.Google Scholar
  97. van Heemst, D., James, F., Pöggeler, S., Berteaux-Lecellier, V., and Zickler, D. 1999. Spo76p is a conserved chromosome morphogenesis protein that links the mitotic and meiotic programs. Cell 98, 261–271.Google Scholar
  98. Vega, H., Waisfisz, Q., Gordillo, M., Sakai, N., Yanagihara, I., Yamada, M., van Gosliga, D., Kayserili, H., Xu, C., Ozono, K., et al. 2005. Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat. Genet. 37, 468–470.Google Scholar
  99. Wold, M.S. 1997. Replication protein A: a heterotrimeric, singlestranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66, 61–92.Google Scholar
  100. Xu, B., Lu, S., and Gerton, J.L. 2014. A deficit in acetylated cohesin leads to nucleolar dysfunction. Rare Dis. 2, e27743.Google Scholar
  101. Yoon, S.W., Lee, M.S., Xaver, M., Zhang, L., Hong, S.G., Kong, Y.J., Cho, H.R., Kleckner, N., and Kim, K.P. 2016. Meiotic prophase roles of Rec8 in crossover recombination and chromosome structure. Nucleic Acids Res. 44, 9296–9314.Google Scholar
  102. Yu, H.G. and Koshland, D.E. 2003. Meiotic condensin is required for proper chromosome compaction, SC assembly, and resolution of recombination-dependent chromosome linkages. J. Cell Biol. 163, 937–947.Google Scholar
  103. Zakharyevich, K., Ma, Y., Tang, S., Hwang, P.Y., Boiteux, S., and Hunter, N. 2010. Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double holliday junctions. Mol. Cell 40, 1001–1015.Google Scholar
  104. Zhang, B., Chang, J., Fu, M., Huang, J., Kashyap, R., Salavaggione, E., Jain, S., Shashikant, K., Deardorff, M.A., Uzielli, M.L., et al. 2009. Dosage effects of cohesin regulatory factor PDS5 on mammalian development: implications for cohesinopathies. PLoS One 4, e5232.Google Scholar
  105. Zhang, B., Jain, S., Song, H., Fu, M., Heuckeroth, R.O., Erlich, J.M., Jay, P.Y., and Milbrandt, J. 2007. Mice lacking sister chromatid cohesion protein PDS5B exhibit developmental abnormalities reminiscent of Cornelia de Lange syndrome. Development 134, 3191–3201.Google Scholar
  106. Zhang, Z., Ren, Q., Yang, H., Conrad, M.N., Guacci, V., Kateneva, A., and Dresser, M.E. 2005. Budding yeast PDS5 plays an important role in meiosis and is required for sister chromatid cohesion. Mol. Microbiol. 56, 670–680.Google Scholar

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© The Microbiological Society of Korea 2019

Authors and Affiliations

  • Soogil Hong
    • 1
  • Jeong Hwan Joo
    • 1
  • Hyeseon Yun
    • 1
  • Keunpil Kim
    • 1
    Email author
  1. 1.Department of Life ScienceChung-Ang UniversitySeoulRepublic of Korea

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