Lactococcal phage p2 ORF35-Sak3 is an ATPase involved in DNA recombination and AbiK mechanism

Molecular Microbiology

Volumn 80, Issue 1, 2011, Pages 102-116

  Scaltriti, Erika ^a,b   Launay, Hélène ^c   Genois, Marie Michelle ^c   Bron, Patrick ^d   Rivetti, Claudio ^b   Grolli, Stefano ^b   Ploquin, Mickael ^c   Campanacci, Valérie ^a   Tegoni, Mariella ^a   Cambillau, Christian ^a   Moineau, Sylvain ^e   Masson, Jean Yves ^c  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF PARMA   (Italy)

^c LAVAL UNIVERSITY   (Canada)

^d CNRS   (France)

^e UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PROTEIN SAK3; RECA PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ANTIVIRAL ABORTIVE INFECTION MECHANISM; ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIOPHAGE; BINDING AFFINITY; CONTROLLED STUDY; DNA RECOMBINATION; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENE LOCATION; HOMOLOGOUS RECOMBINATION; IN VITRO STUDY; INFECTION SENSITIVITY; LACTOCOCCUS LACTIS PHAGE P2; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN INDUCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; VIRUS RESISTANCE;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; BACTERIOPHAGE P2; MICROSCOPY, ATOMIC FORCE; OPEN READING FRAMES; RECOMBINATION, GENETIC; VIRAL PROTEINS;

ESCHERICHIA COLI; LACTOCOCCUS LACTIS PHAGE P2; SIPHOVIRIDAE;

EID: 79953058659     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07561.x     Document Type: Article

References (48)

1. Albertini, A.A., Clapier, C.R., Wernimont, A.K., Schoehn, G., Weissenhorn, W., and Ruigrok, R.W. (2007) Isolation and crystallization of a unique size category of recombinant Rabies virus Nucleoprotein-RNA rings. J Struct Biol 158: 129-133.
2. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
3. Ayora, S., Missich, R., Mesa, P., Lurz, R., Yang, S., Egelman, E.H., and Alonso, J.C. (2002) Homologous-pairing activity of the Bacillus subtilis bacteriophage SPP1 replication protein G35P. J Biol Chem 277: 35969-35979.
4. Bouchard, J.D., and Moineau, S. (2000) Homologous recombination between a lactococcal bacteriophage and the chromosome of its host strain. Virology 270: 65-75.
5. Bouchard, J.D., and Moineau, S. (2004) Lactococcal phage genes involved in sensitivity to AbiK and their relation to single-strand annealing proteins. J Bacteriol 186: 3649-3652.
6. Bouchard, J.D., Dion, E., Bissonnette, F., and Moineau, S. (2002) Characterization of the two-component abortive phage infection mechanism AbiT from Lactococcus lactis. J Bacteriol 184: 6325-6332.
7. Champoux, J.J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70: 369-413.
8. Chang, Y.C., Lo, Y.H., Lee, M.H., Leng, C.H., Hu, S.M., Chang, C.S., and Wang, T.F. (2005) Molecular visualization of the yeast Dmc1 protein ring and Dmc1-ssDNA nucleoprotein complex. Biochemistry 44: 6052-6058.
9. Clamp, M., Cuff, J., Searle, S.M., and Barton, G.J. (2004) The Jalview Java alignment editor. Bioinformatics 20: 426-427.
10. Datta, S., Costantino, N., Zhou, X., and Court, D.L. (2008) Identification and analysis of recombineering functions from Gram-negative and Gram-positive bacteria and their phages. Proc Natl Acad Sci USA 105: 1626-1631.
11. Dodson, M. (1991) Electron microscopy of protein-DNA complexes. Methods Enzymol 208: 168-196.
12. Dröge, A., and Tavares, P. (2005) Bacteriophage SPP1 DNA packaging. In Viral Genome Packaging Machines: Genetics, Structure, and Mechanism. Catalano, C. (ed.). Georgetown: Landes Biosciences, pp. 89-101.
13. Egelman, E.H., Yu, X., Wild, R., Hingorani, M.M., and Patel, S.S. (1995) Bacteriophage T7 helicase/primase proteins form rings around single-stranded DNA that suggest a general structure for hexameric helicases. Proc Natl Acad Sci USA 92: 3869-3873.
14. Eggleston, A.K., Mitchell, A.H., and West, S.C. (1997) In vitro reconstitution of the late steps of genetic recombination in E. coli. Cell 89: 607-617.
15. Emond, E., Holler, B.J., Boucher, I., Vandenbergh, P.A., Vedamuthu, E.R., Kondo, J.K., and Moineau, S. (1997) Phenotypic and genetic characterization of the bacteriophage abortive infection mechanism AbiK from Lactococcus lactis. Appl Environ Microbiol 63: 1274-1283.
16. Guenther, B., Onrust, R., Sali, A., O'Donnell, M., and Kuriyan, J. (1997) Crystal structure of the delta' subunit of the clamp-loader complex of E. coli DNA polymerase III. Cell 91: 335-345.
17. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R., and Schatz, M. (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116: 17-24.
18. Jackson, D., Dhar, K., Wahl, J.K., Wold, M.S., and Borgstahl, G.E. (2002) Analysis of the human replication protein A:Rad52 complex: evidence for crosstalk between RPA32, RPA70, Rad52 and DNA. J Mol Biol 321: 133-148.
19. Kagawa, W., Kurumizaka, H., Ishitani, R., Fukai, S., Nureki, O., Shibata, T., and Yokoyama, S. (2002) Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol Cell 10: 359-371.
20. Labrie, S.L., Samson, J.E., and Moineau, S. (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8: 317-327.
21. Lopes, A., Amarir-Bouhram, J., Faure, G., Petit, M.A., and Guerois, R. (2010) Detection of novel recombinases in bacteriophage genomes unveils Rad52, Rad51 and Gp2.5 remote homologs. Nucleic Acids Res 38: 3952-3962.
22. Ludtke, S.J., Baldwin, P.R., and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97.
23. Lusetti, S.L., and Cox, M.M. (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem 71: 71-100.
24. Moineau, S. (1999) Applications of phage resistance in lactic acid bacteria. Antonie Van Leeuwenhoek 76: 377-382.
25. Moineau, S., Walker, S.A., Vedamuthu, E.R., and Vandenbergh, P.A. (1995) Cloning and sequencing of LlaDCHI [corrected] restriction/modification genes from Lactococcus lactis and relatedness of this system to the Streptococcus pneumoniae DpnII system. Appl Environ Microbiol 61: 2193-2202.
26. Mortensen, U.H., Bendixen, C., Sunjevaric, I., and Rothstein, R. (1996) DNA strand annealing is promoted by the yeast Rad52 protein. Proc Natl Acad Sci USA 93: 10729-10734.
27. Mythili, E., Kumar, K.A., and Muniyappa, K. (1996) Characterization of the DNA-binding domain of beta protein, a component of phage lambda red-pathway, by UV catalyzed cross-linking. Gene 182: 81-87.
28. Parsons, C.A., Baumann, P., Van Dyck, E., and West, S.C. (2000) Precise binding of single-stranded DNA termini by human RAD52 protein. EMBO J 19: 4175-4181.
29. Passy, S.I., Yu, X., Li, Z., Radding, C.M., Masson, J.Y., West, S.C., and Egelman, E.H. (1999) Human Dmc1 protein binds DNA as an octameric ring. Proc Natl Acad Sci USA 96: 10684-10688.
30. Ploquin, M., Bransi, A., Paquet, E.R., Stasiak, A.Z., Stasiak, A., Yu, X., etal. (2008) Functional and structural basis for a bacteriophage homolog of human RAD52. Curr Biol 18: 1142-1146.
31. Ranatunga, W., Jackson, D., Lloyd, J.A., Forget, A.L., Knight, K.L., and Borgstahl, G.E. (2001) Human RAD52 exhibits two modes of self-association. J Biol Chem 276: 15876-15880.
32. 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.
33. Rivetti, C., Walker, C., and Bustamante, C. (1998) Polymer chain statistics and conformational analysis of DNA molecules with bends or sections of different flexibility. J Mol Biol 280: 41-59.
34. Rousseau, G.M., and Moineau, S. (2009) Evolution of Lactococcus lactis phages within a cheese factory. Appl Environ Microbiol 75: 5336-5344.
35. San Martin, M.C., Gruss, C., and Carazo, J.M. (1997) Six molecules of SV40 large T antigen assemble in a propeller-shaped particle around a channel. J Mol Biol 268: 15-20.
36. Scaltriti, E., Tegoni, M., Rivetti, C., Launay, H., Masson, J.-Y., Tremblay, D., etal. (2009) Crystal structure and characterization of a new type of single stranded DNA binding protein from the lactococcal phage p2. Mol Microbiol 73: 1156-1157.
37. Scaltriti, E., Moineau, S., Launay, H., Masson, J.Y., Rivetti, C., Ramoni, R., etal. (2010) Deciphering the function of lactococcal phage ul36 Sak domains. J Struct Biol 170: 462-469.
38. Shen, Z., Cloud, K.G., Chen, D.J., and Park, M.S. (1996) Specific interactions between the human RAD51 and RAD52 proteins. J Biol Chem 271: 148-152.
39. Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S., and Ogawa, T. (1998) Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells 3: 145-156.
40. Singleton, M.R., Wentzell, L.M., Liu, Y., West, S.C., and Wigley, D.B. (2002) Structure of the single-strand annealing domain of human RAD52 protein. Proc Natl Acad Sci USA 99: 13492-13497.
41. Soding, J. (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951-960.
42. Soding, J., Biegert, A., and Lupas, A.N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33: W244-W248.
43. Stasiak, A.Z., Larquet, E., Stasiak, A., Muller, S., Engel, A., Dyck, E.V., etal. (2000) The human Rad52 protein exists as a heptameric ring. Curr Biol 10: 337-340.
44. Sulzenbacher, G., Gruez, A., Roig-Zamboni, V., Spinelli, S., Valencia, C., Pagot, F., etal. (2002) A medium-throughput crystallization approach. Acta Crystallogr D Biol Crystallogr 58: 2109-2115.
45. VanLoock, M.S., Chen, Y.J., Yu, X., Patel, S.S., and Egelman, E.H. (2001) The primase active site is on the outside of the hexameric bacteriophage T7 gene 4 helicase-primase ring. J Mol Biol 311: 951-956.
46. Vincentelli, R., Bignon, C., Gruez, A., Canaan, S., Sulzenbacher, G., Tegoni, M., etal. (2003) Medium-scale structural genomics: strategies for protein expression and crystallization. Acc Chem Res 36: 165-172.
47. Vincentelli, R., Canaan, S., Offant, J., Cambillau, C., and Bignon, C. (2005) Automated expression and solubility screening of His-tagged proteins in 96-well format. Anal Biochem 346: 77-84.
48. Yang, S., Yu, X., VanLoock, M.S., Jezewska, M.J., Bujalowski, W., and Egelman, E.H. (2002) Flexibility of the rings: structural asymmetry in the DnaB hexameric helicase. J Mol Biol 321: 839-849.