DNA damage response clamp 9-1-1 promotes assembly of ZMM proteins for formation of crossovers and synaptonemal complex

Journal of Cell Science

Volumn 128, Issue 8, 2015, Pages 1494-1506

  Shinohara, Miki ^a   Hayashihara, Kayoko ^a   Grubb, Jennifer T ^b   Bishop, Douglas K ^b   Shinohara, Akira ^a  

^a OSAKA UNIVERSITY   (Japan)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Checkpoint clamp; Meiosis; Recombination; SIC; ZMM

Indexed keywords

DCD1 PROTEIN; FUNGAL DNA; FUNGAL PROTEIN; MEC3 PROTEIN; RAD17 PROTEIN; UNCLASSIFIED DRUG; ZMM PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL FREE SYSTEM; CELL MUTANT; CENTROMERE; CHROMOSOME; COMPLEX FORMATION; CONTROLLED STUDY; CROSSING OVER; CYTOLOGY; DELETION MUTANT; DNA DAMAGE; HOMOLOGOUS RECOMBINATION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MEIOSIS; MEIOTIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; STEADY STATE; SYNAPTONEMAL COMPLEX; TWO DIMENSIONAL GEL ELECTROPHORESIS; WILD TYPE; YEAST; YEAST CELL; DNA REPAIR; GENETICS; METABOLISM; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCETALES;

CELL-FREE SYSTEM; CHROMOSOMES, FUNGAL; CROSSING OVER, GENETIC; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; HOMOLOGOUS RECOMBINATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SYNAPTONEMAL COMPLEX;

EID: 84928532573     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.161554     Document Type: Article

References (59)

1. Agarwal, S. and Roeder, G. S. (2000). Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102, 245-255.
2. Alani, E., Padmore, R. and Kleckner, N. (1990). Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61, 419-436.
3. Allers, T. and Lichten, M. (2001). Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106, 47-57.
4. Bishop, D. K. (1994). RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79, 1081-1092.
5. Bishop, D. K., Park, D., Xu, L. and 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.
6. 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.
7. Carballo, J. A., Johnson, A. L., Sedgwick, S. G. and Cha, R. S. (2008). Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132, 758-770.
8. 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.
9. Chu, S. and Herskowitz, I. (1998). Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol. Cell 1, 685-696.
10. Chua, P. R. and Roeder, G. S. (1998). Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93, 349-359.
11. De Antoni, A. and Gallwitz, D. (2000). A novel multi-purpose cassette for repeated integrative epitope tagging of genes in Saccharomyces cerevisiae. Gene 246, 179-185.
12. Eichinger, C. S. and Jentsch, S. (2010). Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1. Proc. Natl. Acad. Sci. USA 107, 11370-11375.
13. Freire, R., Murguía, J. R., Tarsounas, M., Lowndes, N. F., Moens, P. B. and Jackson, S. P. (1998). Human and mouse homologs of Schizosaccharomyces pombe rad1(+) and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis. Genes Dev. 12, 2560-2573.
14. Gasior, S. L., Wong, A. K., Kora, Y., Shinohara, A. and Bishop, D. K. (1998). Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev. 12, 2208-2221.
15. Goldfarb, T. and Lichten, M. (2010). Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol. 8, e1000520.
16. Gotta, M., Laroche, T., Formenton, A., Maillet, L., Scherthan, H. and Gasser, S. M. (1996). The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. J. Cell Biol. 134, 1349-1363.
17. Gray, S., Allison, R. M., Garcia, V., Goldman, A. S. and Neale, M. J. (2013). Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR). Open Biol. 3, 130019.
18. Grushcow, J. M., Holzen, T. M., Park, K. J., Weinert, T., Lichten, M. and Bishop, D. K. (1999). Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics 153, 607-620.
19. Heyer, W. D., Ehmsen, K. T. and Liu, J. (2010). Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44, 113-139.
20. Ho, H. C. and Burgess, S. M. (2011). Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet. 7, e1002351.
21. Hochwagen, A. and Amon, A. (2006). Checking your breaks: surveillance mechanisms of meiotic recombination. Curr. Biol. 16, R217-R228.
22. Hollingsworth, N. M., Ponte, L. and Halsey, C. (1995). MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev. 9, 1728-1739.
23. Hong, E. J. and Roeder, G. S. (2002). A role for Ddc1 in signaling meiotic double-strand breaks at the pachytene checkpoint. Genes Dev. 16, 363-376.
24. 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.
25. 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.
26. Keeney, S. (2001). Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52, 1-53.
27. Keeney, S., Giroux, C. N. and Kleckner, N. (1997). Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88, 375-384.
28. 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.
29. Lao, J. P., Oh, S. D., Shinohara, M., Shinohara, A. and Hunter, N. (2008). Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol. Cell 29, 517-524.
30. Lao, J. P., Cloud, V., Huang, 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.
31. Li, M. Z. and Elledge, S. J. (2007). Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat. Methods 4, 251-256.
32. Lydall, D., Nikolsky, Y., Bishop, D. K. and Weinert, T. (1996). A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383, 840-843.
33. Lyndaker, A. M., Lim, P. X., Mleczko, J. M., Diggins, C. E., Holloway, J. K., Holmes, R. J., Kan, R., Schlafer, D. H., Freire, R., Cohen, P. E. et al. (2013). Conditional inactivation of the DNA damage response gene Hus1 in mouse testis reveals separable roles for components of the RAD9-RAD1-HUS1 complex in meiotic chromosome maintenance. PLoS Genet. 9, e1003320.
34. MacQueen, A. J. and Hochwagen, A. (2011). Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol. 21, 393-400.
35. Majka, J. and Burgers, P. M. (2003). Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc. Natl. Acad. Sci. USA 100, 2249-2254.
36. Miyazaki, T., Bressan, D. A., Shinohara, M., Haber, J. E. and Shinohara, A. (2004). In vivo assembly and disassembly of Rad51 and Rad52 complexes during double-strand break repair. EMBO J. 23, 939-949.
37. Sancar, A., Lindsey-Boltz, L. A., Unsal-Kaçmaz, K. and Linn, S. (2004). Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39-85.
38. Sangawa, T., Tabata, S., Suzuki, K., Saheki, Y., Tanaka, K. and Takagi, J. (2013). A multipurpose fusion tag derived from an unstructured and hyperacidic region of the amyloid precursor protein. Protein Sci. 22, 840-850.
39. 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.
40. Schwacha, A. and Kleckner, N. (1994). Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76, 51-63.
41. Schwacha, A. and Kleckner, N. (1995). Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83, 783-791.
42. Schwacha, A. and Kleckner, N. (1997). Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomologonly pathway. Cell 90, 1123-1135.
43. 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.
44. Shimada, M., Nabeshima, K., Tougan, T. and Nojima, H. (2002). The meiotic recombination checkpoint is regulated by checkpoint rad+ genes in fission yeast. EMBO J. 21, 2807-2818.
45. Shinohara, A. and Ogawa, T. (1998). Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391, 404-407.
46. Shinohara, A., Gasior, S., Ogawa, T., Kleckner, N. and Bishop, D. K. (1997). Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2, 615-629.
47. Shinohara, M., Gasior, S. L., Bishop, D. K. and Shinohara, A. (2000). Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination. Proc. Natl. Acad. Sci. USA 97, 10814-10819.
48. Shinohara, M., Sakai, K., Ogawa, T. and Shinohara, A. (2003a). The mitotic DNA damage checkpoint proteins Rad17 and Rad24 are required for repair of double-strand breaks during meiosis in yeast. Genetics 164, 855-865.
49. Shinohara, M., Sakai, K., Shinohara, A. and Bishop, D. K. (2003b). Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. Genetics 163, 1273-1286.
50. 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.
51. Snowden, T., Acharya, S., Butz, C., Berardini, M. and Fishel, R. (2004). hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol. Cell 15, 437-451.
52. 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.
53. Thacker, D., Mohibullah, N., Zhu, X. and Keeney, S. (2014). Homologue engagement controls meiotic DNA break number and distribution. Nature 510, 241-246.
54. Thompson, D. A. and Stahl, F.W. (1999). Genetic control of recombination partner preference in yeast meiosis. Isolation and characterization of mutants elevated for meiotic unequal sister-chromatid recombination. Genetics 153, 621-641.
55. Tsubouchi, T. and Roeder, G. S. (2005). A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308, 870-873.
56. Tsubouchi, T., Zhao, H. and Roeder, G. S. (2006). The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2. Dev. Cell 10, 809-819.
57. Zhu, Z., Mori, S., Oshiumi, H., Matsuzaki, K., Shinohara, M. and Shinohara, A. (2010). Cyclin-dependent kinase promotes formation of the synaptonemal complex in yeast meiosis. Genes Cells 15, 1036-1050.
58. Zickler, D. and Kleckner, N. (1999). Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603-754.
59. Zou, L. and Elledge, S. J. (2003). Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548.