Small Rad51 and Dmc1 Complexes Often Co-occupy Both Ends of a Meiotic DNA Double Strand Break

PLoS Genetics

Volumn 11, Issue 12, 2015, Pages

  Brown, M Scott ^a   Grubb, Jennifer ^a   Zhang, Annie ^a   Rust, Michael J ^a   Bishop, Douglas K ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; DMC1 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX; RAD51 PROTEIN; RAD51 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SINGLE STRANDED DNA;

CHROMOSOME PAIRING; DOUBLE STRANDED DNA BREAK; GENETICS; MEIOSIS; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID EXCHANGE;

CELL CYCLE PROTEINS; CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; MEIOSIS; MULTIPROTEIN COMPLEXES; MUTATION; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SISTER CHROMATID EXCHANGE;

EID: 84953255734     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005653     Document Type: Article

References (69)

1. Hunter N, Meiotic recombination. Molecular genetics of recombination. Berlin, Heidelberg: Springer Berlin Heidelberg; 2007. pp. 381–442.
2. Brown MS, Bishop DK, DNA Strand Exchange and RecA Homologs in Meiosis. Cold Spring Harb Perspect Biol. 2015 Jan 5;7(1):a016659.
3. Sung P, Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science. 1994 Aug 26;265(5176):1241–3. 8066464
4. Baumann P, Benson FE, West SC, Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell. 1996 Nov 15;87(4):757–66. 8929543
5. Li Z, Golub EI, Gupta R, Radding CM, Recombination activities of HsDmc1 protein, the meiotic human homolog of RecA protein. Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11221–6. 9326590
6. Hong EL, Shinohara A, Bishop DK, Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA. J Biol Chem. 2001 Nov 9;276(45):41906–12. 11551925
7. Shinohara A, Ogawa H, Ogawa T, Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 1992 May 1;69(3):457–70. 1581961
8. 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 May 1;69(3):439–56. 1581960
9. Cloud V, Chan YL, Grubb J, Budke B, Bishop DK, Rad51 Is an Accessory Factor for Dmc1-Mediated Joint Molecule Formation During Meiosis. Science. 2012 Sep 6;337(6099):1222–5. doi: 10.1126/science.1219379 22955832
10. 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. Public Library of Science; 2013 Sep 26;9(9):e1003787. doi: 10.1371/journal.pgen.1003787 24086145
11. Tsubouchi H, Roeder GS, Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes & Development. 2006 Jul 1;20(13):1766–75.
12. Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, Sung P, Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes & Development. 2008;22(6):786–95.
13. Schwacha A, Kleckner N, Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell. 1997 Sep 19;90(6):1123–35. 9323140
14. Lao JP, Cloud V, Huang C-C, Grubb J, Thacker D, Lee C-Y, et al. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet. 2013 Dec 1;9(12):e1003978–8. doi: 10.1371/journal.pgen.1003978 24367271
15. Hong S, Sung Y, Yu M, Lee M, Kleckner N, Kim KP, The logic and mechanism of homologous recombination partner choice. Mol Cell. 2013 Aug 22;51(4):440–53. doi: 10.1016/j.molcel.2013.08.008 23973374
16. Bishop DK, RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell. 1994 Dec 16;79(6):1081–92. 7528104
17. Shinohara M, Gasior SL, Bishop DK, Shinohara A, Tid1/Rdh54 promotes colocalization of Rad51 and Dmc1 during meiotic recombination. Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):10814–9. 11005857
18. Kurzbauer M- T, Uanschou C, Chen D, Schlögelhofer P, The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell. 2012 May;24(5):2058–70. doi: 10.1105/tpc.112.098459 22589466
19. Dresser ME, Ewing DJ, Conrad MN, Dominguez AM, Barstead R, Jiang H, et al. DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics. 1997 Oct;147(2):533–44. 9335591
20. Masson J- Y, Davies AA, Hajibagheri N, Van Dyck E, Benson FE, Stasiak AZ, et al. The meiosis-specific recombinase hDmc1 forms ring structures and interacts with hRad51. The EMBO Journal. 1999 Nov 15;18(22):6552–60. 10562567
21. Tarsounas M, Morita T, Pearlman RE, Moens PB, RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes. J Cell Biol. 1999 Oct 18;147(2):207–20. 10525529
22. Shinohara A, Gasior S, Ogawa T, Kleckner N, Bishop DK, Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes to Cells. 2003 Nov 14;2(10):615–29.
23. Oh SD, Lao JP, Hwang PY- H, Taylor AF, Smith GR, Hunter N, BLM Ortholog, Sgs1, Prevents Aberrant Crossing-over by Suppressing Formation of Multichromatid Joint Molecules. Cell. 2007 Jul;130(2):259–72. 17662941
24. Henderson KA, Keeney S, Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc Natl Acad Sci U S A. 2004;101:4519–24. 15070750
25. Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P, An atypical topoisomerase II from archaea with implications for meiotic recombination. Nature. 1997 Mar 27;386(6623):414–7. 9121560
26. Keeney S, Giroux CN, Kleckner N, Meiosis-Specific DNA Double-Strand Breaks Are Catalyzed by Spo11, a Member of a Widely Conserved Protein Family. Cell. 1997 Feb;88(3):375–84. 9039264
27. Cole F, Kauppi L, Lange J, Roig I, Wang R, Keeney S, et al. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol. 2012 Apr;14(4):424–30. doi: 10.1038/ncb2451 22388890
28. Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S, ATM controls meiotic double-strand-break formation. Nature. 2011 Nov 10;479(7372):237–40. doi: 10.1038/nature10508 22002603
29. Martini E, Diaz RL, Hunter N, Keeney S, Crossover homeostasis in yeast meiosis. Cell. 2006 Jul 28;126(2):285–95. 16873061
30. Fukuda T, Nogami S, Ohya Y, VDE-initiated intein homing in Saccharomyces cerevisiae proceeds in a meiotic recombination-like manner. Genes to Cells. 2003 Jul;8(7):587–602. 12839620
31. Johnson R, Borde V, Neale MJ, Bishop-Bailey A, North M, Harris S, et al. Excess single-stranded DNA inhibits meiotic double-strand break repair. PLoS Genet. 2007 Nov;3(11):e223. 18081428
32. Gerton JL, DeRisi JL, Mnd1p: An evolutionarily conserved protein required for meiotic recombination. Proc Natl Acad Sci U S A. 2002 May 14;99(10):6895–900. 12011448
33. Tsubouchi H, Roeder GS, The Mnd1 protein forms a complex with Hop2 to promote homologous chromosome pairing and meiotic double-strand break repair. Mol Cell Biol. 2002 May;22(9):3078–88. 11940665
34. Zierhut C, Berlinger M, Rupp C, Shinohara A, Klein F, Mnd1 Is Required for Meiotic Interhomolog Repair. Current Biology. 2004 May;14(9):752–62. 15120066
35. Zhang L, Kim KP, Kleckner NE, Storlazzi A, Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. Proc Natl Acad Sci U S A. 2011;108:20036–41. doi: 10.1073/pnas.1117937108 22123968
36. Börner GV, Kleckner N, Hunter N, Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell. 2004;117(1):29–45. 15066280
37. Rockmill B, Sym M, Scherthan H, Roeder GS, Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes & Development. 1995 Nov 1;9(21):2684–95.
38. Sym M, Engebrecht JA, Roeder GS, ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell. 1993 Feb 12;72(3):365–78. 7916652
39. Fölling J, Bossi M, Bock H, Medda R, Wurm CA, Hein B, et al. Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat Methods. 2008 Sep 15;5(11):943–5. doi: 10.1038/nmeth.1257 18794861
40. Heilemann M, van de Linde S, Schüttpelz M, Kasper R, Seefeldt B, Mukherjee A, et al. Subdiffraction-Resolution Fluorescence Imaging with Conventional Fluorescent Probes. Angew Chem Int Ed. 2008 Aug 4;47(33):6172–6.
41. Ogawa T, Yu X, Shinohara A, Egelman EH, Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science. 1993 Mar 26;259(5103):1896–9. 8456314
42. Sehorn MG, Sigurdsson S, Bussen W, Unger VM, Sung P, Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature. 2004 May 27;429(6990):433–7. 15164066
43. Sheridan SD, Yu X, Roth R, Heuser JE, Sehorn MG, Sung P, et al. A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic Acids Research. 2008 May 23;36(12):4057–66. doi: 10.1093/nar/gkn352 18535008
44. Holzen TM, Shah PP, Olivares HA, Bishop DK, Tid1/Rdh54 promotes dissociation of Dmc1 from nonrecombinogenic sites on meiotic chromatin. Genes & Development. 2006;20(18):2593–604.
45. Li X, Heyer WD, RAD54 controls access to the invading 3'-OH end after RAD51-mediated DNA strand invasion in homologous recombination in Saccharomyces cerevisiae. Nucleic Acids Research. 2008 Nov 28;37(2):638–46. doi: 10.1093/nar/gkn980 19074197
46. Shah PP. Characterization of in vivo recombinase dynamics in S. cerevisiae and E. coli. Ph.D. dissertation, The University of Chicago. 2008. http://gradworks.umi.com/33/09/3309107.html
47. Chen Z, Yang H, Pavletich NP, Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature. 2008 May 22;453(7194):489–484. doi: 10.1038/nature06971 18497818
48. Zakharyevich K, Ma Y, Tang S, Hwang PY- H, Boiteux S, Hunter N, Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions. Mol Cell. 2010 Dec 22;40(6):1001–15. doi: 10.1016/j.molcel.2010.11.032 21172664
49. Roca AI, Cox MM, Brenner SL, The RecA Protein: Structure and Function. Critical reviews in biochemistry and molecular biology. 1990;25(6):415–56. 2292186
50. Hsieh P, Camerini-Otero CS, The synapsis event in the homologous pairing of DNAs: RecA recognizes and pairs less than one helical repeat of DNA. Proc Natl Acad Sci U S A.1992;89:6492–6. 1631148
51. Qi Z, Redding S, Lee JY, Gibb B, Kwon Y, Niu H, et al. DNA Sequence Alignment by Microhomology Sampling during Homologous Recombination. Cell. 2015 Feb 26;160(5):856–69. doi: 10.1016/j.cell.2015.01.029 25684365
52. Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK, Rad52 associates with RPA and functions with Rad55 and Rad57 to assemble meiotic recombination complexes. Genes & Development. 1998 Jul 15;12(14):2208–21.
53. Hayase A, Takagi M, Miyazaki T, Oshiumi H, Shinohara M, Shinohara A, A Protein Complex Containing Mei5 and Sae3 Promotes the Assembly of the Meiosis-Specific RecA Homolog Dmc1. Cell. 2004 Dec 29;119(7):927–40. 15620352
54. Tsubouchi H, Roeder GS, The Budding Yeast Mei5 and Sae3 Proteins Act Together With Dmc1 During Meiotic Recombination. Genetics. 2004 Nov 1;168(3):1219–30. 15579681
55. 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 Jul 13;106(1):59–70. 11461702
56. Blat Y, Protacio RU, Hunter N, Kleckner N, Physical and Functional Interactions among Basic Chromosome Organizational Features Govern Early Steps of Meiotic Chiasma Formation. Cell. 2002 Dec;111(6):791–802. 12526806
57. Zickler D, Kleckner N, Meiotic Chromosomes: Integrating Structure and Function. Annu Rev Genet. 1999 Dec;33(1):603–754.
58. Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, Kleckner N, et al. Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell. 2010 Apr 2;141(1):94–106. doi: 10.1016/j.cell.2010.02.041 20371348
59. Franklin AE, McElver J, Sunjevaric I, Rothstein R, Bowen B, Cande WZ, Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase. Plant Cell. 1999 May;11(5):809–24. 10330467
60. Sym M, Roeder GS, Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol. 1995 Feb;128(4):455–66. 7860625
61. Moens PB, Pearlman RE, Chromatin organization at meiosis. Bioessays. 1988 Nov;9(5):151–3. 3071365
62. 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 Dec;143(6):924–37. doi: 10.1016/j.cell.2010.11.015 21145459
63. Storchová Z, Breneman A, Cande J, Dunn J, Burbank K, O'Toole E, et al. Genome-wide genetic analysis of polyploidy in yeast. Nature. 2006 Oct 5;443(7111):541–7. 17024086
64. Joshi N, Brown MS, Bishop DK, Börner GV, Gradual implementation of the meiotic recombination program via checkpoint pathways controlled by global DSB levels. Mol Cell. 2015 Mar 5;57(5):797–811. doi: 10.1016/j.molcel.2014.12.027 25661491
65. Rohner S, Gasser SM, Meister P, Modules for cloning-free chromatin tagging in Saccharomyces cerevisae. Yeast. 2008 Mar;25(3):235–9. doi: 10.1002/yea.1580 18302313
66. Henriques R, Lelek M, Fornasiero EF, Valtorta F, Zimmer C, Mhlanga MM, QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ. Nat Methods. 2010 May;7(5):339–40. doi: 10.1038/nmeth0510-339 20431545
67. Shah PP, Zheng X, Epshtein A, Carey JN, Bishop DK, Klein HL, Swi2/Snf2-Related Translocases Prevent Accumulation of Toxic Rad51 Complexes during Mitotic Growth. Mol Cell. 2010 Sep;39(6):862–72. doi: 10.1016/j.molcel.2010.08.028 20864034
68. Busygina V, Saro D, Williams G, Leung W- K, Say AF, Sehorn MG, et al. Novel Attributes of Hed1 Affect Dynamics and Activity of the Rad51 Presynaptic Filament during Meiotic Recombination. Journal of Biological Chemistry. 2012;287(2):1566–75. doi: 10.1074/jbc.M111.297309 22115747
69. Joo C, Ha T, Single-molecule FRET with total internal reflection microscopy. Cold Spring Harb Protoc. 2012 Dec;2012(12).