Saccharomyces cerevisiae Dmc1 and Rad51 proteins preferentially function with Tid1 and Rad54 proteins, respectively, to promote DNA strand invasion during genetic recombination

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 28727-28737

  Nimonkar, Amitabh V ^a   Dombrowski, Christopher C ^a   Siino, Joseph S ^a,c   Stasiak, Alicja Z ^b   Stasiak, Andrzej ^b   Kowalczykowski, Stephen C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c BIO RAD LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIRECT INTERACTIONS; DNA STRANDS; GENETIC RECOMBINATIONS; HOMOLOGOUS CHROMOSOMES; MEIOTIC RECOMBINATIONS; NUCLEOPROTEIN FILAMENTS; PARALOGS; PHYSICAL INTERACTIONS;

CHROMOSOMES; DNA; PROTEINS;

YEAST;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BUFFER; CALCIUM ION; FUNGAL PROTEIN; PROTEIN DMC1; PROTEIN TID1; RAD51 PROTEIN; RAD54 PROTEIN; RECOMBINANT PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BASE PAIRING; CONTROLLED STUDY; DNA HELIX; DNA STRAND; ELECTRON MICROSCOPY; GENETIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; CHROMOSOMES, FUNGAL; DNA HELICASES; DNA REPAIR ENZYMES; DNA TOPOISOMERASES; DNA, FUNGAL; DNA-BINDING PROTEINS; MEIOSIS; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84865230072     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.373290     Document Type: Article

References (62)

1. Ehmsen, K. T., and Heyer, W. D. (2008) Biochemistry of meiotic recombination: formation, processing, and resolution of recombination intermediates. Genome Dyn. Stab. 3, 91-164
2. Roeder, G. S. (1997) Meiotic chromosomes: it takes two to tango. Genes Dev. 11, 2600-2621
3. Hassold, T., and Hunt, P. (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280-291 (Pubitemid 33674776)
4. Baudat, F., Manova, K., Yuen, J. P., Jasin, M., and Keeney, S. (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol. Cell 6, 989-998
5. Romanienko, P. J., and Camerini-Otero, R. D. (2000) The mouse spo11 gene is required for meiotic chromosome synapsis. Mol. Cell 6, 975-987
6. Heyer, W. D., Ehmsen, K. T., and Liu, J. (2010) Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44, 113-139
7. Keeney, S., and Neale, M. J. (2006) Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans. 34, 523-525 (Pubitemid 44230753)
8. Mimitou, E. P., and Symington, L. S. (2009) Nucleases and helicases take center stage in homologous recombination. Trends Biochem. Sci. 34, 264-272
9. Sun, H., Treco, D., Schultes, N. P., and Szostak, J. W. (1989) Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338, 87-90 (Pubitemid 19076790)
10. Cao, L., Alani, E., and Kleckner, N. (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61, 1089-1101
11. San Filippo, J., Sung, P., and Klein, H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257
12. Hunter, N. (2007) in Molecular Genetics of Recombination (Aguilera, A., and Rothstein, R., eds) pp. 381-442, Springer-Verlag, Berlin
13. 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 (Pubitemid 32709958)
14. McIlwraith, M. J., and West, S. C. (2008) DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. Mol. Cell 29, 510-516 (Pubitemid 351282535)
15. Li, X., Stith, C. M., Burgers, P. M., and Heyer, W. D. (2009) PCNA is required for initiation of recombination-associated DNA synthesis by DNA polymerase δ. Mol. Cell 36, 704-713
16. Allers, T., and Lichten, M. (2001) Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol. Cell 8, 225-231 (Pubitemid 32772920)
17. Schwacha, A., and Kleckner, N. (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83, 783-791 (Pubitemid 3006321)
18. Dresser, M. E., Ewing, D. J., Conrad, M. N., Dominguez, A. M., Barstead, R., Jiang, H., and Kodadek, T. (1997) DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics 147, 533-544 (Pubitemid 27418564)
19. Arbel, A., Zenvirth, D., and Simchen, G. (1999) Sister chromatid-based DNA repair is mediated by RAD54, not by DMC1 or TID1. EMBO J. 18, 2648-2658 (Pubitemid 29213294)
20. Klein, H. L. (1997) RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. Genetics 147, 1533-1543
21. Shinohara, M., Shita-Yamaguchi, E., Buerstedde, J. M., Shinagawa, H., Ogawa, H., and Shinohara, A. (1997) Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. Genetics 147, 1545-1556
22. Shinohara, M., Sakai, K., Shinohara, A., and Bishop, D. K. (2003) Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. Genetics 163, 1273-1286 (Pubitemid 36523381)
23. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Second Edition, pp. 92-96 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
24. Kiianitsa, K., Solinger, J. A., and Heyer, W. D. (2002) Rad54 protein exerts diverse modes of ATPase activity on duplex DNA partially and fully covered with Rad51 protein. J. Biol. Chem. 277, 46205-46215 (Pubitemid 35417612)
25. Zaitseva, E. M., Zaitsev, E. N., and Kowalczykowski, S. C. (1999) The DNA binding properties of Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 274, 2907-2915 (Pubitemid 29075377)
26. Mazin, A. V., Bornarth, C. J., Solinger, J. A., Heyer, W. D., and Kowalczykowski, S. C. (2000) Rad54 protein is targeted to pairing loci by the Rad51 nucleoprotein filament. Mol. Cell 6, 583-592
27. Hong, E. L., Shinohara, A., and Bishop, D. K. (2001) Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA. J. Biol. Chem. 276, 41906-41912
28. Roman, L. J., and Kowalczykowski, S. C. (1989) Characterization of the adenosinetriphosphatase activity of the Escherichia coli RecBCD enzyme: relationship of ATP hydrolysis to the unwinding of duplex DNA. Biochemistry 28, 2873-2881 (Pubitemid 19099464)
29. Menetski, J. P., Varghese, A., and Kowalczykowski, S. C. (1988) Properties of the high-affinity single-stranded DNA binding state of the Escherichia coli recA protein. Biochemistry 27, 1205-1212
30. Menetski, J. P., and Kowalczykowski, S. C. (1985) Interaction of recA protein with single-stranded DNA. Quantitative aspects of binding affinity modulation by nucleotide cofactors. J. Mol. Biol. 181, 281-295
31. Sogo, J., Stasiak, A., DeBernardin, W., Losa, R., and Koller, T. (1987) in Electron Microscopy in Molecular Biology (Sommerville, J., and Scheer, U., eds) pp. 61-79, IRL Press, Oxford
32. Nimonkar, A. V., Amitani, I., Baskin, R. J., and Kowalczykowski, S. C. (2007) Single molecule imaging of Tid1/Rdh54, a Rad54 homolog that translocates on duplex DNA and can disrupt joint molecules. J. Biol. Chem. 282, 30776-30784 (Pubitemid 350035166)
33. Petukhova, G., Sung, P., and Klein, H. (2000) Promotion of Rad51-dependent D-loop formation by yeast recombination factor Rdh54/Tid1. Genes Dev. 14, 2206-2215
34. Lee, M. H., Chang, Y. C., Hong, E. L., Grubb, J., Chang, C. S., Bishop, D. K., and Wang, T. F. (2005) Calcium ion promotes yeast Dmc1 activity via formation of long and fine helical filaments with single-stranded DNA. J. Biol. Chem. 280, 40980-40984 (Pubitemid 41780593)
35. Bugreev, D. V., Golub, E. I., Stasiak, A. Z., Stasiak, A., and Mazin, A. V. (2005) Activation of human meiosis-specific recombinase Dmc1 by Ca2+. J. Biol. Chem. 280, 26886-26895 (Pubitemid 41040723)
36. Record, M. T., Jr., Lohman, M. L., and De Haseth, P. (1976) Ion effects on ligand-nucleic acid interactions. J. Mol. Biol. 107, 145-158
37. Menetski, J. P., Varghese, A., and Kowalczykowski, S. C. (1992) The physical and enzymatic properties of Escherichia coli recA protein display anion- specific inhibition. J. Biol. Chem. 267, 10400-10404
38. Seitz, E. M., Brockman, J. P., Sandler, S. J., Clark, A. J., and Kowalczykowski, S. C. (1998) RadA protein is an archaeal RecA protein homolog that catalyzes DNA strand exchange. Genes Dev. 12, 1248-1253 (Pubitemid 28213400)
39. Yu, X., Jacobs, S. A., West, S. C., Ogawa, T., and Egelman, E. H. (2001) Domain structure and dynamics in the helical filaments formed by RecA and Rad51 on DNA. Proc. Natl. Acad. Sci. U.S.A. 98, 8419-8424 (Pubitemid 32678044)
40. Yang, S., Yu, X., Seitz, E. M., Kowalczykowski, S. C., and Egelman, E. H. (2001) Archaeal RadA protein binds DNA as both helical filaments and octameric rings. J. Mol. Biol. 314, 1077-1085 (Pubitemid 34073071)
41. Sheridan, S. D., Yu, X., Roth, R., Heuser, J. E., Sehorn, M. G., Sung, P., Egelman, E. H., and Bishop, D. K. (2008) A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic Acids Res. 36, 4057-4066 (Pubitemid 351984821)
42. Bugreev, D. V., and Mazin, A. V. (2004) Ca2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proc. Natl. Acad. Sci. U.S.A. 101, 9988-9993 (Pubitemid 38891183)
43. Petukhova, G., Stratton, S., and Sung, P. (1998) Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393, 91-94 (Pubitemid 28240262)
44. Mazin, A. V., Alexeev, A. A., and Kowalczykowski, S. C. (2003) A novel function of Rad54 protein: stabilization of the Rad51 nucleoprotein filament. J. Biol. Chem. 278, 14029-14036 (Pubitemid 36799947)
45. Fornander, L. H., Frykholm, K., Reymer, A., Renodon-Cornière, A., Takahashi, M., and Nordén, B. (2012) Ca2+ improves organization of singlestranded DNA bases in human Rad51 filament, explaining stimulatory effect on gene recombination. Nucleic Acids Res. 40, 4904-4913
46. Carreira, A., Hilario, J., Amitani, I., Baskin, R. J., Shivji, M. K., Venkitaraman, A. R., and Kowalczykowski, S. C. (2009) The BRC repeats of BRCA2 modulate the DNA-binding selectivity of RAD51. Cell 136, 1032-1043
47. Carreira, A., and Kowalczykowski, S. C. (2011) Two classes of BRC repeats in BRCA2 promote RAD51 nucleoprotein filament function by distinct mechanisms. Proc. Natl. Acad. Sci. U.S.A. 108, 10448-10453
48. Jensen, R. B., Carreira, A., and Kowalczykowski, S. C. (2010) Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467, 678-683
49. Petalcorin, M. I., Sandall, J., Wigley, D. B., and Boulton, S. J. (2006) Ce- BRC-2 stimulates D-loop formation by RAD-51 and promotes DNA single-strand annealing. J. Mol. Biol. 361, 231-242 (Pubitemid 44092785)
50. Whitaker, M. (2006) Calcium at fertilization and in early development. Physiol. Rev. 86, 25-88
51. Keith, C. H., Maxfield, F. R., and Shelanski, M. L. (1985) Intracellular free calcium levels are reduced in mitotic Pt K2 epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 82, 800-804 (Pubitemid 15142766)
52. Schmuckli-Maurer, J., and Heyer, W. D. (2000) Meiotic recombination in RAD54 mutants of Saccharomyces cerevisiae. Chromosoma 109, 86-93 (Pubitemid 30433300)
53. Tsubouchi, H., and Roeder, G. S. (2003) The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev. Cell 5, 915-925 (Pubitemid 37527691)
54. Schwacha, A., and Kleckner, N. (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90, 1123-1135 (Pubitemid 27408526)
55. Kaback, D. B., Barber, D., Mahon, J., Lamb, J., and You, J. (1999) Chromosome size-dependent control of meiotic reciprocal recombination in Saccharomyces cerevisiae: the role of crossover interference. Genetics 152, 1475-1486 (Pubitemid 29370330)
56. Tsubouchi, H., and Roeder, G. S. (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev. 20, 1766-1775 (Pubitemid 43992885)
57. 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. U.S.A. 97, 10814-10819
58. Niu, H., Wan, L., Baumgartner, B., Schaefer, D., Loidl, J., and Hollingsworth, N. M. (2005) Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol. Biol. Cell 16, 5804-5818 (Pubitemid 41752228)
59. Busygina, V., Sehorn, M. G., Shi, I. Y., Tsubouchi, H., Roeder, G. S., and Sung, P. (2008) Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev. 22, 786-795 (Pubitemid 351439109)
60. Tsubouchi, H., and Roeder, G. S. (2004) The budding yeast mei5 and sae3 proteins act together with dmc1 during meiotic recombination. Genetics 168, 1219-1230 (Pubitemid 40007343)
61. Ferrari, S. R., Grubb, J., and Bishop, D. K. (2009) The Mei5-Sae3 protein complex mediates Dmc1 activity in Saccharomyces cerevisiae. J. Biol. Chem. 284, 11766-11770
62. Bugreev, D. V., Pezza, R. J., Mazina, O. M., Voloshin, O. N., Camerini- Otero, R. D., and Mazin, A. V. (2011) The resistance of DMC1 D-loops to dissociation may account for the DMC1 requirement in meiosis. Nat. Struct. Mol. Biol. 18, 56-60