Role of replication protein a in double holliday junction dissolution mediated by the BLM-Topo IIIα-RMI1-RMI2 protein complex

Journal of Biological Chemistry

Volumn 288, Issue 20, 2013, Pages 14221-14227

  Xue, Xiaoyu ^a   Raynard, Steven ^a,b   Busygina, Valeria ^a,c   Singh, Akhilesh K ^a,d,e   Sung, Patrick ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Precision BioLogic   (Canada)

^c AxioMx Inc   (United States)

^d SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISSOLUTION REACTIONS; HOLLIDAY JUNCTIONS; HOMOLOGOUS RECOMBINATION; INTERACTION DOMAIN; PROTEIN COMPLEXES; REPLICATION PROTEIN A; SINGLE-STRANDED DNA; SINGLE-STRANDED DNA BINDING PROTEINS;

DNA; PROTEINS;

DISSOLUTION;

BLOOM SYNDROME HELICASE; BTR COMPLEX; DNA TOPOISOMERASE; MUTANT PROTEIN; PROTEIN A; REPLICATION FACTOR A; SINGLE STRANDED DNA; TOPOISOMERASE III ALPHA; TOPOISOMERASE RMI1; TOPOISOMERASE RMI2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DISSOLUTION; DNA BINDING; DNA REPLICATION; HOLLIDAY JUNCTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

CANCER BIOLOGY; DNA BINDING PROTEIN; DNA HELICASE; DNA REPAIR; DOUBLE HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; SINGLE-STRANDED DNA BINDING PROTEIN RPA;

AMINO ACID SEQUENCE; CARRIER PROTEINS; DNA; DNA REPAIR; DNA TOPOISOMERASES, TYPE I; DNA, CRUCIFORM; DNA-BINDING PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PROTEIN BINDING; RECQ HELICASES; REPLICATION PROTEIN A; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84877898746     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.465609     Document Type: Article

References (35)

1. Ellis, N. A., Groden, J., Ye, T. Z., Straughen, J., Lennon, D. J., Ciocci, S., Proytcheva, M., and German, J. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83, 655-666
2. Chaganti, R. S., Schonberg, S., and German, J. (1974) A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 71, 4508-4512
3. Kuhn, E. M., and Therman, E. (1986) Cytogenetics of Bloom's syndrome. Cancer Genet. Cytogenet. 22, 1-18 (Pubitemid 16071527)
4. Cheok, C. F., Bachrati, C. Z., Chan, K. L., Ralf, C., Wu, L., and Hickson, I. D. (2005) Roles of the Bloom's syndrome helicase in the maintenance of genome stability. Biochem. Soc. Trans. 33, 1456-1459 (Pubitemid 41779714)
5. Raynard, S., Bussen, W., and Sung, P. (2006) A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIα, and BLAP75. J. Biol. Chem. 281, 13861-13864 (Pubitemid 43848308)
6. Wu, L., Bachrati, C. Z., Ou, J., Xu, C., Yin, J., Chang, M., Wang, W., Li, L., Brown, G. W., and Hickson, I. D. (2006) BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. U.S.A. 103, 4068-4073
7. Wu, L., and Hickson, I. D. (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874 (Pubitemid 38056876)
8. Plank, J. L., Wu, J., and Hsieh, T. S. (2006) Topoisomerase IIIα and Bloom's helicase can resolve a mobile double Holliday junction substrate through convergent branch migration. Proc. Natl. Acad. Sci. U.S.A. 103, 11118-11123 (Pubitemid 44156483)
9. Raynard, S., Zhao, W., Bussen, W., Lu, L., Ding, Y. Y., Busygina, V., Meetei, A. R., and Sung, P. (2008) Functional role of BLAP75 in BLM-topoisomerase IIIα-dependent Holliday junction processing. J. Biol. Chem. 283, 15701-15708
10. Singh, T. R., Ali, A. M., Busygina, V., Raynard, S., Fan, Q., Du, C. H., Andreassen, P. R., Sung, P., and Meetei, A. R. (2008) BLAP18/RMI2, a novel OB-fold-containing protein, is an essential component of the Bloom helicase-double Holliday junction dissolvasome. Genes Dev. 22, 2856-2868
11. Xu, D., Guo, R., Sobeck, A., Bachrati, C. Z., Yang, J., Enomoto, T., Brown, G. W., Hoatlin, M. E., Hickson, I. D., and Wang, W. (2008) RMI, a new OB-fold complex essential for Bloom syndrome protein to maintain genome stability. Genes Dev. 22, 2843-2855
12. Sung, P., and Klein, H. (2006) Mechanism of homologous recombination. Mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 7, 739-750 (Pubitemid 44450458)
13. Yin, J., Sobeck, A., Xu, C., Meetei, A. R., Hoatlin, M., Li, L., and Wang, W. (2005) BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity. EMBO J. 24, 1465-1476 (Pubitemid 40593066)
14. Cejka, P., Plank, J. L., Bachrati, C. Z., Hickson, I. D., and Kowalczykowski, S. C. (2010) Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat. Struct. Mol. Biol. 17, 1377-1382
15. Niu, H., Chung, W. H., Zhu, Z., Kwon, Y., Zhao, W., Chi, P., Prakash, R., Seong, C., Liu, D., Lu, L., Ira, G., and Sung, P. (2010) Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467, 108-111
16. Cejka, P., Cannavo, E., Polaczek, P., Masuda-Sasa, T., Pokharel, S., Campbell, J. L., and Kowalczykowski, S. C. (2010) DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467, 112-116
17. Mimitou, E. P., and Symington, L. S. (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-774
18. Gravel, S., Chapman, J. R., Magill, C., and Jackson, S. P. (2008) DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22, 2767-2772
19. Nimonkar, A. V., Genschel, J., Kinoshita, E., Polaczek, P., Campbell, J. L., Wyman, C., Modrich, P., and Kowalczykowski, S. C. (2011) BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 25, 350-362
20. Nimonkar, A. V., Ozsoy, A. Z., Genschel, J., Modrich, P., and Kowalczykowski, S. C. (2008) Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc. Natl. Acad. Sci. U.S.A. 105, 16906-16911
21. Bussen, W., Raynard, S., Busygina, V., Singh, A. K., and Sung, P. (2007) Holliday junction processing activity of the BLM-Topo IIIα-BLAP75 complex. J. Biol. Chem. 282, 31484-31492 (Pubitemid 350044838)
22. Van Komen, S., Macris, M., Sehorn, M. G., and Sung, P. (2006) Purification and assays of Saccharomyces cerevisiae homologous recombination proteins. Methods Enzymol. 408, 445-463
23. Walther, A. P., Gomes, X. V., Lao, Y., Lee, C. G., and Wold, M. S. (1999) Replication protein A interactions with DNA. 1. Functions of the DNA-binding and zinc-finger domains of the 70-kDa subunit. Biochemistry 38, 3963-3973
24. Fu, T. J., Tse-Dinh, Y. C., and Seeman, N. C. (1994) Holliday junction crossover topology. J. Mol. Biol. 236, 91-105
25. Plate, I., Hallwyl, S. C., Shi, I., Krejci, L., Müller, C., Albertsen, L., Sung, P., and Mortensen, U. H. (2008) Interaction with RPA is necessary for Rad52 repair center formation and for its mediator activity. J. Biol. Chem. 283, 29077-29085
26. Bochkareva, E., Kaustov, L., Ayed, A., Yi, G. S., Lu, Y., Pineda-Lucena, A., Liao, J. C., Okorokov, A. L., Milner, J., Arrowsmith, C. H., and Bochkarev, A. (2005) Single-stranded DNA mimicry in the p53 transactivation domain interaction with replication protein A. Proc. Natl. Acad. Sci. U.S.A. 102, 15412-15417 (Pubitemid 41528071)
27. Xu, X., Vaithiyalingam, S., Glick, G. G., Mordes, D. A., Chazin, W. J., and Cortez, D. (2008) The basic cleft of RPA70N binds multiple checkpoint proteins, including RAD9, to regulate ATR signaling. Mol. Cell Biol. 28, 7345-7353
28. Cejka, P., Plank, J. L., Dombrowski, C. C., and Kowalczykowski, S. C. (2012) Decatenation of DNA by the S. cerevisiae Sgs1-Top3-Rmi1 and RPA complex. A mechanism for disentangling chromosomes. Mol. Cell 47, 886-896
29. Deans, A. J., and West, S. C. (2009) FANCM connects the genome instability disorders Bloom's Syndrome and Fanconi anemia. Mol. Cell 36, 943-953
30. Mullen, J. R., Nallaseth, F. S., Lan, Y. Q., Slagle, C. E., and Brill, S. J. (2005) Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex. Mol. Cell Biol. 25, 4476-4487 (Pubitemid 40705754)
31. Chen, S. H., Wu, C. H., Plank, J. L., and Hsieh, T. S. (2012) Essential functions of C terminus of Drosophila topoisomerase IIIα in double Holliday junction dissolution. J. Biol. Chem. 287, 19346-19353
32. Zhu, Z., Chung, W. H., Shim, E. Y., Lee, S. E., and Ira, G. (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134, 981-994
33. Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G. C., Lukas, J., and Jackson, S. P. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8, 37-45 (Pubitemid 43064795)
34. Llorente, B., and Symington, L. S. (2004) The Mre11 nuclease is not required for 5′ to 3′ resection at multiple HO-induced double-strand breaks. Mol. Cell Biol. 24, 9682-9694 (Pubitemid 39391702)
35. Tsubouchi, H., and Ogawa, H. (2000) Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell 11, 2221-2233 (Pubitemid 30489910)