A dual role for mycobacterial RecO in RecA-dependent homologous recombination and RecA-independent single-strand annealing

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2284-2295

  Gupta, Richa ^a   Ryzhikov, Mikhail ^b   Koroleva, Olga ^b   Unciuleac, Mihaela ^a   Shuman, Stewart ^a   Korolev, Sergey ^b   Glickman, Michael S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADNAB HELICASE; BACTERIAL DNA; BACTERIAL PROTEIN; DOUBLE STRANDED DNA; HELICASE; RECA PROTEIN; RECO PROTEIN; RECOMBINANT DNA; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; CONTROLLED STUDY; DNA BINDING; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; GENE DELETION; HOMOLOGOUS RECOMBINATION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR GENETICS; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECOMBINATION REPAIR; SINGLE STRAND ANNEALING; STRAIN DIFFERENCE;

BACTERIAL PROTEINS; DEOXYRIBONUCLEASES; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; EXODEOXYRIBONUCLEASE V; GENE DELETION; MICROBIAL VIABILITY; MYCOBACTERIUM SMEGMATIS; REC A RECOMBINASES; RECOMBINATIONAL DNA REPAIR; ZINC;

CORYNEBACTERINEAE; EUKARYOTA;

EID: 84876347637     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1298     Document Type: Article

References (42)

1. Gong, C., Bongiorno, P., Martins, A., Stephanou, N.C., Zhu, H., Shuman, S. and Glickman, M.S. (2005) Mechanism of nonhomologous end-joining in mycobacteria: a low-fidelity repair system driven by Ku, ligase D and ligase C. Nat. Struct. Mol. Biol., 12, 304-312.
2. Gong, C., Martins, A., Bongiorno, P., Glickman, M. and Shuman, S. (2004) Biochemical and genetic analysis of the four DNA ligases of mycobacteria. J. Biol. Chem., 279, 20594-20606.
3. Gupta, R., Barkan, D., Redelman-Sidi, G., Shuman, S. and Glickman, M.S. (2011) Mycobacteria exploit three genetically distinct DNA double-strand break repair pathways. Mol. Microbiol., 79, 316-330.
4. Shuman, S. and Glickman, M.S. (2007) Bacterial DNA repair by non-homologous end joining. Nat. Rev. Microbiol., 5, 852-861.
5. Pitcher, R.S., Green, A.J., Brzostek, A., Korycka-Machala, M., Dziadek, J. and Doherty, A.J. (2007) NHEJ protects mycobacteria in stationary phase against the harmful effects of desiccation. DNA Repair (Amst), 6, 1271-1276.
6. Stephanou, N.C., Gao, F., Bongiorno, P., Ehrt, S., Schnappinger, D., Shuman, S. and Glickman, M.S. (2007) Mycobacterial nonhomologous end joining mediates mutagenic repair of chromosomal double-strand DNA breaks. J. Bacteriol., 189, 5237-5246.
7. Aniukwu, J., Glickman, M.S. and Shuman, S. (2008) The pathways and outcomes of mycobacterial NHEJ depend on the structure of the broken DNA ends. Genes Dev., 22, 512-527.
8. Courcelle, J., Carswell-Crumpton, C. and Hanawalt, P.C. (1997) recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc. Natl Acad. Sci. USA, 94, 3714-3719.
9. Xu, L. and Marians, K.J. (2003) PriA mediates DNA replication pathway choice at recombination intermediates. Mol. Cell, 11, 817-826.
10. Cox, M.M., Goodman, M.F., Kreuzer, K.N., Sherratt, D.J., Sandler, S.J. and Marians, K.J. (2000) The importance of repairing stalled replication forks. Nature, 404, 37-41.
11. Bidnenko, V., Seigneur, M., Penel-Colin, M., Bouton, M.F., Dusko Ehrlich, S. and Michel, B. (1999) sbcB sbcC null mutations allow RecF-mediated repair of arrested replication forks in rep recBC mutants. Mol. Microbiol., 33, 846-857.
12. Fernandez, S., Kobayashi, Y., Ogasawara, N. and Alonso, J.C. (1999) Analysis of the Bacillus subtilis recO gene: RecO forms part of the RecFLOR function. Mol. Gen. Genet., 261, 567-573.
13. Bentchikou, E., Servant, P., Coste, G. and Sommer, S. (2010) A major role of the RecFOR pathway in DNA double-strand-break repair through ESDSA in Deinococcus radiodurans. PLoS Genet., 6, e1000774.
14. Satoh, K., Kikuchi, M., Ishaque, A.M., Ohba, H., Yamada, M., Tejima, K., Onodera, T. and Narumi, I. (2012) The role of Deinococcus radiodurans RecFOR proteins in homologous recombination. DNA Repair (Amst), 11, 410-418.
15. Xu, G., Wang, L., Chen, H., Lu, H., Ying, N., Tian, B. and Hua, Y. (2008) RecO is essential for DNA damage repair in Deinococcus radiodurans. J. Bacteriol., 190, 2624-2628.
16. Handa, N., Morimatsu, K., Lovett, S.T. and Kowalczykowski, S.C. (2009) Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli. Genes Dev., 23, 1234-1245.
17. Morimatsu, K. and Kowalczykowski, S.C. (2003) RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol. Cell, 11, 1337-1347.
18. Sakai, A. and Cox, M.M. (2009) RecFOR and RecOR as distinct RecA loading pathways. J. Biol. Chem., 284, 3264-3272.
19. Sandler, S.J. and Clark, A.J. (1994) RecOR suppression of recF mutant phenotypes in Escherichia coli K-12. J. Bacteriol., 176, 3661-3672.
20. Umezu, K., Chi, N.W. and Kolodner, R.D. (1993) Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded DNA binding protein. Proc. Natl Acad. Sci. USA, 90, 3875-3879.
21. Kantake, N., Madiraju, M.V., Sugiyama, T. and Kowalczykowski, S.C. (2002) Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: a common step in genetic recombination. Proc. Natl Acad. Sci. USA, 99, 15327-15332.
22. Ryzhikov, M., Koroleva, O., Postnov, D., Tran, A. and Korolev, S. (2011) Mechanism of RecO recruitment to DNA by single-stranded DNA binding protein. Nucleic Acids Res., 39, 6305-6314.
23. New, J.H., Sugiyama, T., Zaitseva, E. and Kowalczykowski, S.C. (1998) Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature, 391, 407-410.
24. Sugiyama, T., New, J.H. and Kowalczykowski, S.C. (1998) DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc. Natl Acad. Sci. USA, 95, 6049-6054.
25. Ivanov, E.L., Sugawara, N., Fishman-Lobell, J. and Haber, J.E. (1996) Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics, 142, 693-704.
26. Shiraishi, K., Hanada, K., Iwakura, Y. and Ikeda, H. (2002) Roles of RecJ, RecO, and RecR in RecET-mediated illegitimate recombination in Escherichia coli. J. Bacteriol., 184, 4715-4721.
27. Kolodner, R., Fishel, R.A. and Howard, M. (1985) Genetic recombination of bacterial plasmid DNA: effect of RecF pathway mutations on plasmid recombination in Escherichia coli. J. Bacteriol., 163, 1060-1066.
28. Sugiyama, T., Kantake, N., Wu, Y. and Kowalczykowski, S.C. (2006) Rad52-mediated DNA annealing after Rad51-mediated DNA strand exchange promotes second ssDNA capture. EMBO J., 25, 5539-5548.
29. Hobbs, M.D., Sakai, A. and Cox, M.M. (2007) SSB protein limits RecOR binding onto single-stranded DNA. J. Biol. Chem., 282, 11058-11067.
30. Unciuleac, M.C. and Shuman, S. (2010) Double strand break unwinding and resection by the mycobacterial helicase-nuclease AdnAB in the presence of single strand DNA-binding protein (SSB). J. Biol. Chem., 285, 34319-34329.
31. Rocha, E.P., Cornet, E. and Michel, B. (2005) Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet., 1, e15.
32. Mizrahi, V. and Andersen, S.J. (1998) DNA repair in Mycobacterium tuberculosis What have we learnt from the genome sequence? Mol. Microbiol., 29, 1331-1339.
33. Marsin, S., Mathieu, A., Kortulewski, T., Guerois, R. and Radicella, J.P. (2008) Unveiling novel RecO distant orthologues involved in homologous recombination. PLoS Genet., 4, e1000146.
34. Makharashvili, N., Koroleva, O., Bera, S., Grandgenett, D.P. and Korolev, S. (2004) A novel structure of DNA repair protein RecO from Deinococcus radiodurans. Structure, 12, 1881-1889.
35. Shereda, R.D., Kozlov, A.G., Lohman, T.M., Cox, M.M. and Keck, J.L. (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol., 43, 289-318.
36. Curth, U., Genschel, J., Urbanke, C. and Greipel, J. (1996) In vitro and in vivo function of the C-terminus of Escherichia coli single-stranded DNA binding protein. Nucleic Acids Res., 24, 2706-2711.
37. Reddy, M.S., Guhan, N. and Muniyappa, K. (2001) Characterization of single-stranded DNA-binding proteins from Mycobacteria. The carboxyl-terminal of domain of SSB is essential for stable association with its cognate RecA protein. J. Biol. Chem., 276, 45959-45968.
38. Costes, A., Lecointe, F., McGovern, S., Quevillon-Cheruel, S. and Polard, P. (2010) The C-terminal domain of the bacterial SSB protein acts as a DNA maintenance hub at active chromosome replication forks. PLoS Genet., 6, e1001238.
39. Courcelle, J. and Hanawalt, P.C. (1999) RecQ and RecJ process blocked replication forks prior to the resumption of replication in UV-irradiated Escherichia coli. Mol. Gen. Genet., 262, 543-551.
40. Yadav, T., Carrasco, B., Myers, A.R., George, N.P., Keck, J.L. and Alonso, J.C. (2012) Genetic recombination in Bacillus subtilis: a division of labor between two single-strand DNA-binding proteins. Nucleic Acids Res., 40, 5546-5559.
41. Manfredi, C., Suzuki, Y., Yadav, T., Takeyasu, K. and Alonso, J.C. (2010) RecO-mediated DNA homology search and annealing is facilitated by SsbA. Nucleic Acids Res., 38, 6920-6929.
42. Manfredi, C., Carrasco, B., Ayora, S. and Alonso, J.C. (2008) Bacillus subtilis RecO nucleates RecA onto SsbA-coated single-stranded DNA. J. Biol. Chem., 283, 24837-24847