Erratum: Mek1 Down Regulates Rad51 Activity during Yeast Meiosis by Phosphorylation of Hed1 (PLoS Genetics (2016) 12:8 (e1006226) DOI: 10.1371/journal.pgen.1006226);Mek1 Down Regulates Rad51 Activity during Yeast Meiosis by Phosphorylation of Hed1

PLoS Genetics

Volumn 12, Issue 8, 2016, Pages

  Callender, Tracy L ^a,f   Laureau, Raphaelle ^b,c   Wan, Lihong ^a   Chen, Xiangyu ^a   Sandhu, Rima ^d   Laljee, Saif ^a   Zhou, Sai ^a   Suhandynata, Ray T ^a   Prugar, Evelyn ^a   Gaines, William A ^e   Kwon, YoungHo ^e   Börner, G Valentin ^d   Nicolas, Alain ^b,c   Neiman, Aaron M ^a   Hollingsworth, Nancy M ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b Institut Curie   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d CLEVELAND STATE UNIVERSITY   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f LONG ISLAND UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PEPTIDES AND PROTEINS; PROTEIN HED1; RAD51 PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DMC1 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; DNA HELICASE; DNA LIGASE; HED1 PROTEIN, S CEREVISIAE; MUTANT PROTEIN; RAD54 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME REPRESSION; MEIOSIS; MEIOTIC RECOMBINATION; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; DNA REPAIR; GENETICS; HOMOLOGOUS RECOMBINATION; MITOSIS; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; HOMOLOGOUS RECOMBINATION; MAP KINASE KINASE 1; MEIOSIS; MITOSIS; MUTANT PROTEINS; PHOSPHORYLATION; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84984889131     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/JOURNAL.PGEN.1006283     Document Type: Erratum

References (85)

1. Bzymek M, Thayer NH, Oh SD, Kleckner N, Hunter N, Double Holliday junctions are intermediates of DNA break repair. Nature. 2010;464(7290):937–41. Epub 2010/03/30. doi: 10.1038/nature0886820348905
2. Kadyk LC, Hartwell LH, Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics. 1992;132(2):387–402. 1427035
3. Krejci L, Altmannova V, Spirek M, Zhao X, Homologous recombination and its regulation. Nuc Acids Res2012;40(13):5795–818.
4. Lam I, Keeney S, Mechanism and regulation of meiotic recombination initiation. Cold Spring Harbor Perspect Biol. 2015;7:a016634.
5. Szekvolgyi L, Ohta K, Nicolas A, Initiation of meiotic homologous recombination: flexibility, impact of histone modifications, and chromatin remodeling. Cold Spring Harbor Perspect Biol. 2015;7:a016527.
6. Zickler D, Kleckner N, Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harbor Perspect Biol. 2015;7:a016626.
7. Blat Y, Kleckner N, Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell. 1999;98(2):249–59. 10428036
8. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, et al. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell. 2011;146(3):372–83. Epub 2011/08/06. doi: 10.1016/j.cell.2011.07.00321816273
9. Klein F, Mahr P, Galova M, Buonomo SBC, Michaelis C, Nairz K, et al. A central role for cohesins in sister chromatid cohesion, formation of axial elements and recombination during meiosis. Cell. 1999;98:91–103. 10412984
10. Smith AV, Roeder GS, The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol. 1997;136:957–67. 9060462
11. Hollingsworth NM, Goetsch L, Byers B, The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990;61:73–84. 2107981
12. Acquaviva L, Szekvolgyi L, Dichtl B, Dichtl BS, de La Roche Saint Andre C, Nicolas A, et al. The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science. 2013;339(6116):215–8. doi: 10.1126/science.122573923160953
13. Keeney S, Lange J, Mohibullah N, Self-organization of meiotic recombination initiation: general principles and molecular pathways. Annu Rev Genet. 2014;48:187–214. doi: 10.1146/annurev-genet-120213-09230425421598
14. Sommermeyer V, Beneut C, Chaplais E, Serrentino ME, Borde V, Spp1, a member of the Set1 Complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol Cell. 2013;49(1):43–54. doi: 10.1016/j.molcel.2012.11.00823246437
15. Carballo JA, Johnson AL, Sedgwick SG, Cha RS, Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell. 2008;132:758–70. doi: 10.1016/j.cell.2008.01.03518329363
16. Niu H, Li X, Job E, Park C, Moazed D, Gygi SP, et al. Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis. Mol Cell Biol. 2007;27(15):5456–67. 17526735
17. Subramanian VV, Hochwagen A, The meiotic checkpoint network: step-by-step through meiotic prophase. Cold Spring Harbor Perspect Biol. 2014;6(10):a016675.
18. Xu L, Weiner BM, Kleckner N, Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 1997;11:106–18. 9000054
19. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, Kleckner N, Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell. 2010;143(6):924–37. Epub 2010/12/15. doi: 10.1016/j.cell.2010.11.01521145459
20. Niu H, Wan L, Baumgartner B, Schaefer D, Loidl J, Hollingsworth NM, Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol Biol Cell. 2005;16:5804–18. 16221890
21. Thompson DA, Stahl FW, Genetic control of recombination partner preference in yeast meiosis. Isolation and characterization of mutants elevated for meiotic unequal sister-chromatid recombination. Genetics. 1999;153(2):621–41. 10511544
22. Chen X, Suhandynata RT, Sandhu R, Rockmill B, Mohibullah N, Niu H, et al. Phosphorylation of the synaptonemal complex protein Zip1 regulates the crossover/noncrossover decision during yeast meiosis. PLoS Biol. 2015;13(12):e1002329. doi: 10.1371/journal.pbio.100232926682552
23. Brown MS, Bishop DK, DNA strand exchange and RecA homologs in meiosis. Cold Spring Harbor Perspect Biol. 2015;7(1):a016659.
24. Bishop DK, RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell. 1994;79:1081–92. 7528104
25. Kurzbauer MT, Uanschou C, Chen D, Schlogelhofer P, The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell. 2012;24(5):2058–70. Epub 2012/05/17. doi: 10.1105/tpc.112.09845922589466
26. Brown MS, Grubb J, Zhang A, Rust MJ, Bishop DK, Small Rad51 and Dmc1 complexes often co-occupy both ends of a meiotic DNA double strand break. PLoS Genet. 2015;11(12):e1005653. doi: 10.1371/journal.pgen.100565326719980
27. Cloud V, Chan Y-L, Grubb J, Budke B, Bishop DK, Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science. 2012;337:1222–5. doi: 10.1126/science.121937922955832
28. Hong S, Sung Y, Yu M, Lee M, Kleckner N, Kim KP, The logic and mechanism of homologous recombination partner choice. Mol Cell. 2013;51(4):440–53. doi: 10.1016/j.molcel.2013.08.00823973374
29. Lao JP, Oh SD, Shinohara M, Shinohara A, Hunter N, Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol Cell. 2008;29:517–24. doi: 10.1016/j.molcel.2007.12.01418313389
30. Schwacha A, Kleckner N, Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell. 1997;90:1123–35. 9323140
31. Da Ines O, Degroote F, Goubely C, Amiard S, Gallego ME, White CI, Meiotic recombination in Arabidopsis is catalysed by DMC1, with RAD51 playing a supporting role. PLoS Genet. 2013;9(9):e1003787. doi: 10.1371/journal.pgen.100378724086145
32. Bishop DK, 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;69:439–56. 1581960
33. Lydall D, Nikolsky Y, Bishop DK, Weinert T, A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature. 1996;383:840–3. 8893012
34. Arbel A, Zenvirth D, Simchen G, Sister chromatid-based DNA repair is mediated by RAD54, not by DMC1 or TID1. Embo J. 1999;18(9):2648–58. 10228176
35. Busygina V, Gaines W, Xu Y, Kwon Y, Williams G, Lin S, et al. Functional attributes of the S. cerevisiae meiotic recombinase Dmc1. DNA Repair. 2013;12:707–12. doi: 10.1016/j.dnarep.2013.05.00423769192
36. Nimonkar AV, Dombrowski CC, Siino JS, Stasiak AZ, Stasiak A, Kowalczykowski SC, Saccharomyces cerevisiae Dmc1 and Rad51 preferentially function with Tid1 and Rad54, respectively, to promote DNA strand invasion during genetic recombination. J Biol Chem. 2012;287:28727–37. Epub 2012/07/05. doi: 10.1074/jbc.M112.37329022761450
37. Petukhova G, Stratton S, Sung P, Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature. 1998;393(6680):91–4. Epub 1998/05/20. 9590697
38. Shinohara M, Shita-Yamaguchi E, Buerstedde J-M, Shinagawa H, Ogawa H, Shinohara A, Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homolog of RAD54, RDH54/TID1 in mitosis and meiosis. Genetics. 1997;147:1545–56. 9409820
39. Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, Sung P, Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev. 2008;22:786–95. doi: 10.1101/gad.163870818347097
40. Tsubouchi H, Roeder GS, Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev. 2006;20(13):1766–75. 16818607
41. Niu H, Wan L, Busygina V, Kwon Y, Allen JA, Li X, et al. Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol Cell. 2009;36(3):393–404. doi: 10.1016/j.molcel.2009.09.02919917248
42. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, Lee CY, et al. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet. 2013;9(12):e1003978. doi: 10.1371/journal.pgen.100397824367271
43. Liu Y, Gaines WA, Callender T, Busygina V, Oke A, Sung P, et al. Down-regulation of Rad51 activity during meiosis in yeast prevents competition with Dmc1 for repair of double-strand breaks. PLoS Genet. 2014;10(1):e1004005. doi: 10.1371/journal.pgen.100400524465215
44. Callender TL, Hollingsworth NM, Mek1 suppression of meiotic double-strand break repair is specific to sister chromatids, chromosome autonomous and independent of Rec8 cohesin complexes. Genetics. 2010;185(3):771–82. doi: 10.1534/genetics.110.11752320421598
45. Benjamin KR, Zhang C, Shokat KM, Herskowitz I, Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev. 2003;17(12):1524–39. 12783856
46. Carlile TM, Amon A, Meiosis I is established through division-specific translational control of a cyclin. Cell. 2008;133:280–91. doi: 10.1016/j.cell.2008.02.03218423199
47. Suhandynata R, Liang J, Albuquerque CP, Zhou H, Hollingsworth NM, A method for sporulating budding yeast cells that allows for unbiased identification of kinase substrates using stable isotope labeling by amino acids in cell culture. G3. 2014;4(11):2125–35. doi: 10.1534/g3.114.01388825168012
48. Busygina V, Saro D, Williams G, Leung WK, Say AF, Sehorn MG, et al. Novel attributes of Hed1 affect dynamics and activity of the Rad51 presynaptic filament during meiotic recombination. J Biol Chem. 2012;287(2):1566–75. doi: 10.1074/jbc.M111.29730922115747
49. Sourirajan A, Lichten M, Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev. 2008;22:2627–32. doi: 10.1101/gad.171140818832066
50. Lo HC, Hollingsworth NM, Using the semi-synthetic epitope system to identify direct substrates of the meiosis-specific budding yeast kinase, Mek1. Methods Mol Biol. 2011;745:135–49. Epub 2011/06/11. doi: 10.1007/978-1-61779-129-1_921660693
51. Govin J, Dorsey J, Gaucher J, Rousseaux S, Khochbin S, Berger SL, Systematic screen reveals new functional dynamics of histones H3 and H4 during gametogenesis. Genes Dev. 2010;24(16):1772–86. doi: 10.1101/gad.195491020713519
52. Mok J, Kim PM, Lam HY, Piccirillo S, Zhou X, Jeschke GR, et al. Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Sci Signal. 2010;3(109):ra12. doi: 10.1126/scisignal.200048220159853
53. de los Santos T, Hollingsworth NM, Red1p, a MEK1-dependent phosphoprotein that physically interacts with Hop1p during meiosis in yeast. J Biol Chem. 1999;274(3):1783–90. 9880561
54. Bishop AC, Ubersax JA, Petsch DT, Matheos DP, Gray NS, Blethrow J, et al. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature. 2000;407(6802):395–401. 11014197
55. Wan L, de los Santos T, Zhang C, Shokat K, Hollingsworth NM, Mek1 kinase activity functions downstream of RED1 in the regulation of meiotic DSB repair in budding yeast. Mol Biol Cell. 2004;15:11–23. 14595109
56. Allen JA, Li M, Brinkworth CS, Paulson JL, Wang D, Hubner A, et al. A semisynthetic epitope for kinase substrates. Nat Methods. 2007;4:511–6. 17486086
57. McKee AHZ, Kleckner N, A general method for identifying recessive diploid-specific mutations in Saccharomyces cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase and characterization of a new gene SAE2. Genetics. 1997;146:797–816. 9215888
58. Prinz S, Amon A, Klein F, Isolation of COM1, a new gene required to complete meiotic double-strand induced recombination in Saccharomyces cerevisiae. Genetics. 1997;146:781–95. 9215887
59. Hunter N, Kleckner N, The single-end invasion: an asymmetric intermediate at the double- strand break to double-holliday junction transition of meiotic recombination. Cell. 2001;106(1):59–70. 11461702
60. Kinoshita E, Takahashi M, Takeda H, Shiro M, Koike T, Recognition of phosphate monoester dianion by an alkoxide-bridged dinuclear zinc(II) complex. Dalton transactions. 2004;(8):1189–93. 15252659
61. Oh SD, Jessop L, Lao JP, Allers T, Lichten M, Hunter N, Stabilization and electrophoretic analysis of meiotic recombination intermediates in Saccharomyces cerevisiae. Methods Mol Biol. 2009;557:209–34. doi: 10.1007/978-1-59745-527-5_1419799185
62. Thacker D, Mohibullah N, Zhu X, Keeney S, Homologue engagement controls meiotic DNA break number and distribution. Nature. 2014;510(7504):241–6. doi: 10.1038/nature1312024717437
63. Wu HY, Ho HC, Burgess SM, Mek1 kinase governs outcomes of meiotic recombination and the checkpoint response. Curr Bio. 2010;20(19):1707–16. Epub 2010/10/05.
64. Chu S, Herskowitz I, Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol Cell. 1998;1(5):685–96. 9660952
65. Laureau R, Loeillet S, Salinas F, Bergstrom A, Legoix-Ne P, Liti G, et al. Extensive Recombination of a Yeast Diploid Hybrid through Meiotic Reversion. PLoS Genet. 2016;12(2):e1005781. doi: 10.1371/journal.pgen.100578126828862
66. Anderson CM, Chen SY, Dimon MT, Oke A, DeRisi JL, Fung JC, ReCombine: a suite of programs for detection and analysis of meiotic recombination in whole-genome datasets. PLoS One. 2011;6(10):e25509. Epub 2011/11/03. doi: 10.1371/journal.pone.002550922046241
67. Oke A, Anderson CM, Yam P, Fung JC, Controlling meiotic recombinational repair—specifying the roles of ZMMs, Sgs1 and Mus81/Mms4 in crossover formation. PLoS Genet. 2014;10(10):e1004690. doi: 10.1371/journal.pgen.100469025329811
68. Sturtevant AH, The linear arrangment of six sex-linked factors in Drosophila, as shown by their mode of association. J Exptl Zool. 1913;14:43–59.
69. Chen SY, Fung JC, Mapping of crossover sites using DNA microarrays. Meth Mol Biol. 2011;745:117–34. Epub 2011/06/11.
70. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell. 2011;144(5):719–31. Epub 2011/03/08. doi: 10.1016/j.cell.2011.02.00921376234
71. Chuang CN, Cheng YH, Wang TF, Mek1 stabilizes Hop1-Thr318 phosphorylation to promote interhomolog recombination and checkpoint responses during yeast meiosis. Nuc Acids Res. 2012;40(22):11416–27. Epub 2012/10/11.
72. Villeneuve AM, Hillers KJ, Whence meiosis?Cell. 2001;106(6):647–50. Epub 2001/09/27. 11572770
73. Borgogno MV, Monti MR, Zhao W, Sung P, Argarana CE, Pezza RJ, Tolerance of DNA Mismatches in Dmc1 Recombinase-mediated DNA Strand Exchange. J Biol Chem. 2016;291(10):4928–38. doi: 10.1074/jbc.M115.70471826709229
74. Lee JY, Terakawa T, Qi Z, Steinfeld JB, Redding S, Kwon Y, et al. Base triplet stepping by the Rad51/RecA family of recombinases. Science. 2015;349(6251):977–81. doi: 10.1126/science.aab266626315438
75. Goldstein AL, McCusker JH, Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast. 1999;15:1541–53. 10514571
76. Longtine MS, McKenzie A, 3rdDemarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 1998;14(10):953–61. 9717241
77. Tong A, Boone C, Totowa NJ, Synthetic Genetic Array (SGA) analysis in Saccharomyces cerevisiae. Yeast Protocols, Meth Mol Biol. 313. Second ed. USA: The Humana Press, Inc.; 2005. p. 171–92.
78. de los Santos T, Hollingsworth NM, Red1p: A MEK1-dependent phosphoprotein that physically interacts with Hop1p during meiosis in yeast. J Biol Chem. 1999;274:1783–90. 9880561
79. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, et al. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast. 1998;14:115–32. 9483801
80. Acosta I, Ontoso D, San-Segundo PA, The budding yeast polo-like kinase Cdc5 regulates the Ndt80 branch of the meiotic recombination checkpoint pathway. Molecular biology of the cell. 2011;22(18):3478–90. doi: 10.1091/mbc.E11-06-048221795394
81. Ontoso D, Acosta I, van Leeuwen F, Freire R, San-Segundo PA, Dot1-dependent histone H3K79 methylation promotes activation of the Mek1 meiotic checkpoint effector kinase by regulating the Hop1 adaptor. PLoS Genet. 2013;9(1):e1003262. doi: 10.1371/journal.pgen.100326223382701
82. Falk JE, Chan AC, Hoffmann E, Hochwagen A, A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell. 2010;19(4):599–611. Epub 2010/10/19. doi: 10.1016/j.devcel.2010.09.00620951350
83. Chi P, Kwon Y, Seong C, Epshtein A, Lam I, Sung P, et al. Yeast recombination factor Rdh54 functionally interacts with the Rad51 recombinase and catalyzes Rad51 removal from DNA. J Biol Chem. 2006;281:26268–79. 16831867
84. Serero A, Jubin C, Loeillet S, Legoix-Ne P, Nicolas AG, Mutational landscape of yeast mutator strains. Proc Natl Acad Sci U S A. 2014;111(5):1897–902. doi: 10.1073/pnas.131442311124449905
85. Li H, Durbin R, Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60. doi: 10.1093/bioinformatics/btp32419451168