The logic and mechanism of homologous recombination partner choice

Molecular Cell

Volumn 51, Issue 4, 2013, Pages 440-453

  Hong, Soogil ^a   Sung, Youngjin ^a   Yu, Mi ^a   Lee, Minsu ^a   Kleckner, Nancy ^b   Kim, KeunP ^a  

^a Chung Ang University   (South Korea)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; RAD51 PROTEIN;

ARTICLE; DOUBLE STRANDED DNA BREAK; HOMOLOGOUS RECOMBINATION; MEIOSIS; NONHUMAN; PHENOTYPE; RECOMBINATION REPAIR; SISTER CHROMATID; YEAST;

EID: 84882718761     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.08.008     Document Type: Article

References (36)

1. Ball L.G., Zhang K., Cobb J.A., Boone C., Xiao W. The yeast Shu complex couples error-free post-replication repair to homologous recombination. Mol. Microbiol. 2009, 73:89-102.
2. Beumer K.J., Pimpinelli S., Golic K.G. Induced chromosomal exchange directs the segregation of recombinant chromatids in mitosis of Drosophila. Genetics 1998, 150:173-188.
3. Brar G.A., Hochwagen A., Ee L.S., Amon A. The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol. Biol. Cell 2009, 20:1030-1047.
4. Busygina V., Saro D., Williams G., Leung W.K., Say A.F., Sehorn M.G., Sung P., Tsubouchi H. Novel attributes of Hed1 affect dynamics and activity of the Rad51 presynaptic filament during meiotic recombination. J.Biol. Chem. 2012, 287:1566-1575.
5. Bzymek M., Thayer N.H., Oh S.D., Kleckner N., Hunter N. Double Holliday junctions are intermediates of DNA break repair. Nature 2010, 464:937-941.
6. Chung W.H., Zhu Z., Papusha A., Malkova A., Ira G. Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet. 2010, 6:e1000948.
7. Cloud V., Chan Y.L., Grubb J., Budke B., Bishop D.K. Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 2012, 337:1222-1225.
8. Covo S., Westmoreland J.W., Gordenin D.A., Resnick M.A. Cohesin Is limiting for the suppression of DNA damage-induced recombination between homologous chromosomes. PLoS Genet. 2010, 6:e1001006.
9. Goldfarb T., Lichten M. Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol. 2010, 8:e1000520.
10. Hochwagen A., Tham W.H., Brar G.A., Amon A. The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 2005, 122:861-873.
11. Hunter N. Meiotic Recombination. Molecular Genetics of Recombination 2006, 381-442. Topics in Current Genetics, Springer-Verlag, Heidelberg. A. Aguilera, R. Rothstein (Eds.).
12. 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, 106:59-70.
13. Johnson R.D., Jasin M. Double-strand-break-induced homologous recombination in mammalian cells. Biochem. Soc. Trans. 2001, 29:196-201.
14. Kadyk L.C., Hartwell L.H. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 1992, 132:387-402.
15. Kateneva A.V., Konovchenko A.A., Guacci V., Dresser M.E. Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae. J.Cell Biol. 2005, 171:241-253.
16. Kim K.P., Weiner B.M., Zhang L., Jordan A., Dekker J., Kleckner N. Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 2010, 143:924-937.
17. Kleckner N., Zhang L., Weiner B., Zickler D. genome organization and function in the cell nucleus 2011, Chapter 19. Wiley-VCH, Weinheim, Germany.
18. Krejci L., Altmannova V., Spirek M., Zhao X. Homologous recombination and its regulation. Nucleic Acids Res. 2012, 40:5795-5818.
19. 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, 24:2058-2070.
20. Mankouri H.W., Ngo H.P., Hickson I.D. Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3. Mol. Biol. Cell 2007, 18:4062-4073.
21. Nimonkar A.V., Dombrowski C.C., Siino J.S., Stasiak A.Z., Stasiak A., Kowalczykowski S.C. Saccharomyces cerevisiae Dmc1 and Rad51 proteins preferentially function with Tid1 and Rad54 proteins, respectively, to promote DNA strand invasion during genetic recombination. J.Biol. Chem. 2012, 287:28727-28737.
22. Oh S.D., Lao J.P., Hwang P.Y., Taylor A.F., Smith G.R., Hunter N. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 2007, 130:259-272.
23. Pezza R.J., Voloshin O.N., Vanevski F., Camerini-Otero R.D. Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing. Genes Dev. 2007, 21:1758-1766.
24. Qing Y., Yamazoe M., Hirota K., Dejsuphong D., Sakai W., Yamamoto K.N., Bishop D.K., Wu X., Takeda S. The epistatic relationship between BRCA2 and the other RAD51 mediators in homologous recombination. PLoS Genet. 2011, 7:e1002148.
25. Rong Y.S., Golic K.G. The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila. Genetics 2003, 165:1831-1842.
26. Sasanuma H., Tawaramoto M.S., Lao J.P., Hosaka H., Sanda E., Suzuki M., Yamashita E., Hunter N., Shinohara M., Nakagawa A., Shinohara A. A new protein complex promoting the assembly of Rad51 filaments. Nat. Commun. 2013, 4:1676.
27. Schwacha A., Kleckner N. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 1994, 76:51-63.
28. Schwacha A., Kleckner N. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 1997, 90:1123-1135.
29. Sheridan S., Bishop D.K. Red-Hed regulation: recombinase Rad51, though capable of playing the leading role, may be relegated to supporting Dmc1 in budding yeast meiosis. Genes Dev. 2006, 20:1685-1691.
30. Shinohara M., Gasior S.L., Bishop D.K., Shinohara A. Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination. Proc. Natl. Acad. Sci. USA 2000, 97:10814-10819.
31. Shor E., Weinstein J., Rothstein R. A genetic screen for top3 suppressors in Saccharomyces cerevisiae identifies SHU1, SHU2, PSY3 and CSM2: four genes involved in error-free DNA repair. Genetics 2005, 169:1275-1289.
32. Storlazzi A., Gargano S., Ruprich-Robert G., Falque M., David M., Kleckner N., Zickler D. Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 2010, 141:94-106.
33. Tao Y., Li X., Liu Y., Ruan J., Qi S., Niu L., Teng M. Structural analysis of Shu proteins reveals a DNA binding role essential for resisting damage. J.Biol. Chem. 2012, 287:20231-20239.
34. Tsubouchi H., Roeder G.S. Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev. 2006, 20:1766-1775.
35. Wan L., de los Santos T., Zhang C., Shokat K., Hollingsworth N. Mek1 kinase activity functions downstream of RED1 in the regulation of meiotic double strand break repair in budding yeast. Mol. Biol. Cell 2004, 15:11-23.
36. Zenvirth D., Loidl J., Klein S., Arbel A., Shemesh R., Simchen G. Switching yeast from meiosis to mitosis: double-strand break repair, recombination and synaptonemal complex. Genes Cells 1997, 2:487-498.