Structure and function of phage p2 0RF34P2, a new type of Single-standed DNA binding protein

Molecular Microbiology

Volumn 73, Issue 6, 2009, Pages 1156-1170

  Scaltrlti, Erika ^a,b   Tegoni, Mariella ^a   Rivetti, Claudio ^b   Launay, Hélène ^c   Masson, Jean Yves ^c   Magadan, Alfonso H ^c   Tremblay, Denise ^c   Moineau, Sylvain ^c   Ramoni, Roberto ^c   Lichlère, Julie ^c   Campanacci, Valérie ^b   Cambillau, Christian ^a   Ortiz Lombardia, Miguel ^a  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITY OF PARMA   (Italy)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; OLIGONUCLEOTIDE; OLIGOSACCHARIDE; OPEN READING FRAME 34 P2 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENETICS; BACTERIOPHAGE; CONTROLLED STUDY; ESCHERICHIA COLI; GEL ELECTROPHORESIS; LACTOCOCCUS LACTIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE;

ESCHERICHIA COLI; LACTOCOCCUS LACTIS; LACTOCOCCUS PHAGE P2; POSIBACTERIA;

EID: 70350173629     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06844.x     Document Type: Article

References (70)

1. Ayora, S., Langer, U., and Alonso, J.C. (1998) Bacillus subtilis DnaG primase stabilises the bacteriophage SPP1 G40P helicase-ssDNA complex. FEBS Lett 439: 59-62. (Pubitemid 28537863)
2. Bleuit, J.S., Xu, H., Ma, Y., Wang, T., Liu, J., and Morrical, S.W. (2001) Mediator proteins orchestrate enzyme-ssDNA assembly during T4 recombination-dependent DNA replication and repair. Proc Natl Acad Sci USA 98: 8298-8305. (Pubitemid 32678027)
3. 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.
4. Chrysogelos, S., and Griffith, J. (1982) Escherichia coli single-strand binding protein organizes single-stranded DNA in nucleosome-like units. Proc Natl Acad Sci USA 79: 5803-5807. (Pubitemid 13199978)
5. Cohen, S.X., Morris, RJ., Fernandez, FJ., Ben Jelloul, M., Kakaris, M., Parthasarathy, V, et al. (2004) Towards complete validated models in the next generation of ARP/ wARP. Acta Crystallogr D Biol Crystallogr 60: 2222-2229. (Pubitemid 41742774)
6. Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Cryst D 50: 760-763.
7. Deveau, H., Labrie, SJ., Chopin, M., and Moineau, S. (2006) Biodiversity and classification of lactococcal phages. Appl Environ Microbiol 72: 4338-4346.
8. DiDonato, M., Krishna, S.S., Schwarzenbacher, R., McMullan, D., Jaroszewski, L., Miller, M.D, et al. (2006) Crystal structure of a single-stranded DNA-binding protein (TM0604) from Thermotoga maritima at 2.60 A resolution. Proteins 63: 256-260. (Pubitemid 44420946)
9. 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.
10. 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 Mierobid 63: 1274-1283. (Pubitemid 27174828)
11. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132. (Pubitemid 41742764)
12. Folmer, R.H., Folkers, P.J., Kaan, A., Jonker, AJ., Aelen, J.M., Konings, R.N., and Hilbers, C.W. (1994) Secondary structure of the single-stranded DNA binding protein encoded by filamentous phage Pf3 as determined by NMR. Eur J Biochem 224: 663-676. (Pubitemid 24282852)
13. Folmer, R.H., Nilges, M., Konings, R.N., and Hilbers, C.W. (1995) Solution structure of the single-stranded DNA binding protein of the filamentous Pseudomonas phage Pf3: similarity to other proteins binding to single-stranded nucleic acids. EMBO J 14: 4132-4142.
14. Gasior, S.L., Olivares, H., Ear, U., Hari, D.M., Weichselbaum, R., and Bishop, D.K. (2001) Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis. Proc Natl Acad Sci USA 98: 8411-8418. (Pubitemid 32678043)
15. Gasson, M.J. (1983) Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol 154: 1-9.
16. Genschel, J., Curth, U., and Urbanke, C (2000) Interaction of E. coli single-stranded DNA binding protein (SSB) with exonuclease I. The carboxy-terminus of SSB is the recognition site for the nuclease. Biol Chem 381: 183-192. (Pubitemid 30179552)
17. Griffith, J., and Shores, C.G. (1985) RecA protein rapidly crystallizes in the presence of spermidine: a valuable step in its purification and physical characterization. Biochemistry 24: 158-162.
18. Haaber, J., Moineau, S., Fortier, L., and Hammer, K. (2008) AbiV, a novel antiphage abortive infection mechanism on the chromosome of Lactococcus lactis subsp. cremoris MG1363. Appl Environ Microbiol 74: 6528-6537.
19. Hamon, L., Pastre, D., Dupaigne, P., Le Breton, C., Le Cam, E., and Pietrement, O. (2007) High-resolution AFM imaging of single-stranded DNA-binding (SSB) protein -DNA complexes. Nucleic Acids Res 35: e58. (Pubitemid 47073694)
20. Hay, N., and Cohen, G. (1983) Requirement of E. coli DNA synthesis functions for the lytic replication of bacteriophage P1. Virology 131: 193-206. (Pubitemid 14248610)
21. He, Z., Rezende, L.F., Willcox, S., Griffith, J.D., and Richardson, C.C. (2003) The carboxyl-terminal domain of bacteriophage T7 single-stranded DNA-binding protein modulates DNA binding and interaction with T7 DNA polymerase. J Biol Chem 278: 29538-29545.
22. HoIHs, T., Stattel, J.M., Walther, D.S., Richardson, C.C., and Ellenberger, T. (2001 ) Structure of the gene 2.5 protein, a single-stranded DNA binding protein encoded by bacteriophage T7. Proc Natl Acad Sci USA 98: 9557-9562. (Pubitemid 32769342)
23. Iftode, C., Daniely, Y., sind Borowiec, J.A. (1999) Replication protein A (RPA): the eukaryotic SSB. Crit Rev Biochem Mol Biol 34: 141-180.
24. Jackson, D., Dhar, K., Wahl, J.K., Wold, M.S., and Borgstahl, G.E.O. (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. (Pubitemid 34948475)
25. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 26: 795-800.
26. Kim, Y.T., and Richardson, C.C. (1993) Bacteriophage T7 gene 2.5 protein: an essential protein for DNA replication. Proc Natl Acad Sci USA 90: 10173-10177.
27. Kowalczykowski, S.C., Clow, J., and Krupp, R.A. (1987) Properties of the duplex DNA-dependent ATPase activity of Escherichia coli RecA protein and its role in branch migration. Proc Natl Acad Sci USA 84: 3127-3131. (Pubitemid 17085357)
28. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Ada Crystallogr D Biol Crystallogr 60: 2256-2268. (Pubitemid 41742778)
29. Lohman, T.M., and Ferrari, M.E. (1994) Esdierichia coli single-stranded DNA-binding protein: multiple DNAbinding modes and cooperativities. Annu Rev Biochem 63: 527-570. (Pubitemid 24218642)
30. Lohman, T.M., and Overman, L.B. (1985) Two binding modes in Escherichia coli single strand binding proteinsingle stranded DNA complexes. Modulation by NaCI concentration. J Biol Chem 260: 3594-3603.
31. Lovell, S.C., Davis, I.W., Arendall, W.B., 3rd, de Bakker, P.I.W., Word, J.M., Prisant, M.G., et al. (2003) Structure validation by Calpha geometry: phi, psi and Cβ deviation. Proteins 50: 437-450.
32. Matsumoto, T., Morimoto, Y., Shibata, N., Kinebuchi, T., Shimamoto, N., Tsukihara, T., and Yasuoka, N. (2000) Roles of functional loops and the C-terminal segment of a single-stranded DNA binding protein elucidated by X-Ray structure analysis. J Biochem 127: 329-335. (Pubitemid 30136917)
33. Meyer, R.R., and Laine, P.S. (1990) The single-stranded DNA-binding protein of Escherichia coli. Microbiol Rev 54: 342-380.
34. Miller, E.S., Heidelberg, J.F., Eisen, J.A., Nelson, W.C., Durkin, A.S., Ciecko, A, et al. (2003) Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J Bacteriol 185: 5220-5233. (Pubitemid 37025119)
35. Moineau, S. (1999) Applications of phage resistance in lactic acid bacteria. Antonie Van Leeuwenhoek 76: 377-382. (Pubitemid 29440741)
36. Moineau, S., Walker, S.A., Vedamuthu, E.R., and Vandenbergh, P.A. (1995) Cloning and sequencing of LIaDCHI [corrected] restriction/modification genes from Lactococcus lactis and relatedness of this system to the Streptococcus pneumoniae Dpnll system. Appl Environ Microbiol 61 : 2193-2202.
37. Mosca, R., and Schneider, T.R. (2008) RAPIDO: a web server for the alignment of protein structures in the presence of conformational changes. Nucleic Adds Res 36: W42-W46.
38. Murphy, M.C., Rasnik, I., Cheng, W., Lohman, T.M., and Ha, T. (2004) Probing single-stranded DNA conformational flexibility using fluorescence spectroscopy. Biophys J 86: 2530-2537. (Pubitemid 38524439)
39. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
40. Murzin, A.G. (1993) OB(oligonucleotide/oligosaccharide binding)-fold: common structural sind functional solution for non-homologous sequences. EMBO J 12: 861-867. (Pubitemid 23095834)
41. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., and Ferrin, T.E. (2004) UCSF Chimera -a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
42. Ploquin, M., Bransi, A., Paquet, E.R., Stasiak, A.Z., Stasiak, A., Yu, X., et al. (2008) Functional and structural basis for a bacteriophage homolog of human RAD52. Curr Biol 18: 1142-1146.
43. Raghunathan, S., Ricard, C.S., Lohman, T.M., and Waksman, G. (1997) Crystal structure of the homo-tetrameric DNA binding domain of Escherichia coli single-stranded DNAbinding protein determined by multiwavelength x-ray diffraction on the selenomethionyl protein at 2.9-A resolution. Proc Natl Acad Sci USA 94: 6652-6657. (Pubitemid 27281919)
44. Raghunathan, S., Kozlov, A.G., Lohman, T.M., and Waksman, G. (2000) Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat Strud Biol 7: 648-652. (Pubitemid 30636675)
45. 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 Bid Chem 276: 45959-45968. (Pubitemid 37370841)
46. Ricagno, S., Campanacci, V., Blangy, S., Spinelli, S., Tremblay, D., Moineau, S, et al. (2006) Crystal structure of the receptor-binding protein head domain from Lactococcus ladis phage bIL170. J Virol 80: 9331-9335. (Pubitemid 44360006)
47. Rivetti, C., and Codeluppi, S. (2001) Accurate length determination of DNA molecules visualized by atomic force microscopy: evidence for a partial B- to A-form transition on mica. Ultramicroscopy 87: 55-66. (Pubitemid 32220175)
48. Saikrishnan, K., Jeyakanthan, J., Venkatesh, J., Acharya, N., Sekar, K., Varshney, U., and Vijayan, M. (2003) Structure of Mycobacterium tuberculosis single-stranded DNAbinding protein. Variability in quaternary structure and its implications. J Mol Biol 331: 385-393.
49. Sanear, A., Williams, K.R., Chase, J.W., and Rupp, W.D. (1981) Sequences of the ssb gene and protein. Proc Natl Acad Sci USA 78: 4274-4278.
50. Sawides, S.N., Raghunathan, S., Futterer, K., Kozlov, A.G., Lohman, T.M., and Waksman, G. (2004) The C-terminal domain of full-length E. coli SSB is disordered even when bound to DNA. Protein Sci 13: 1942-1947.
51. Sciara, G., Blangy, S., Siponen, M., McGrath, S., van Sinderen, D., Tegoni, M, et al. (2008) A topological model of the baseplate of lactococcal phage Tuc2009. J Biol Chem 283: 2716-2723.
52. Shamoo, Y., Friedman, A.M., Parsons, M.R., Königsberg, W.H., and Steitz, T.A. (1995) Crystal structure of a replication fork single-stranded DNA binding protein (T4 gp32) complexed to DNA. Nature 376: 362-366.
53. Sheldrick, G.M. (2002) Macromolecular phasing with SHELXE. Z Kristallogr 217: 644-650.
54. Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S., and Ogawa, T. (1998) Rad52 forms ring structures and cooperates with RPA in single-strand DNA annealing. Genes Cells 3: 145-156. (Pubitemid 28374987)
55. Skinner, M.M., Zhang, H., Leschnitzer, D.H., Guan, Y., Bellamy, H., Sweet, R.M, et al. (1994) Structure of the gene V protein of bacteriophage f1 determined by multiwavelength x-ray diffraction on the selenomethionyl protein. Proc Natl Acad Sci USA 91: 2071-2075. (Pubitemid 24092044)
56. Spinelli, S., Desmyter, A., Verrips, C.T., de Haard, H. J.W., Moineau, S., and Cambillau, C (2006) Lactococcal bacteriophage p2 receptor-binding protein structure suggests a common ancestor gene with bacterial and mammalian viruses. Nat Strud Mol Biol 13: 85-89. (Pubitemid 43049407)
57. Su, S., Gao, Y.G., Zhang, H., Terwilliger, T.C., and Wang, A.H. (1997) Analyses of the stability and function of three surface mutants (R82C, K69H, and L32R) of the gene V protein from Ff phage by X-ray crystallography. Protein Sci 6: 771-780. (Pubitemid 27154803)
58. 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: 60496054. (Pubitemid 28248962)
59. Sulzenbacher, G., Gruez, A., Roig-Zamboni, V., Spinelli, S., Valencia, C., Pagot, F, et al. (2002) A medium-throughput crystallization approach. Acta Crystallogr D Bid Crystallogr 58: 2109-2115.
60. Sun, S., and Shamoo, Y. (2003) Biochemical characterization of interactions between DNA polymerase and singlestranded DNA-binding protein in bacteriophage RB69. J Biol Chem 278: 3876-3881. (Pubitemid 36801117)
61. Sung, P. (1997) Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J Biol Chem 272: 28194-28197. (Pubitemid 27517755)
62. Szczepanska, A.K., Bidnenko, E., Plochocka, D., McGovern, S., Ehrlich, S.D., Bardowski, J, ef al. (2007) A distinct singlestranded DNA-binding protein encoded by the Lactococcus lactis bacteriophage blL67. Virology 363: 104-112.
63. Terwilliger, T.C. (2002) Automated structure solution, density modification and model building. Acta Crystallogr D Biol Crystallogr 58: 1937-1940.
64. Theobald, D.L., Mitton-Fry, R.M., and Wuttke, D.S. (2003) Nucleic acid recognition by OB-fold proteins. Annu Rev Biophys Biomol Strut 32: 115-133.
65. Uson, I., and Sheldrick, G.M. (1999) Advances in direct methods for protein crystallography. Curr Opin Strut Biol 9: 643-648. (Pubitemid 29460593)
66. Vagin, A., and Teplyakov, A. (1997) MOLREP: an Automated Program for Molecular Replacement. J Appl Crystallogr30: 1022-1025. (Pubitemid 127485985)
67. Wang, M., Mahrenholz, A., and Lee, S.H. (2000) RPA stabilizes the XPA-damaged DNA complex through proteinprotein interaction. Biochemistry 39: 6433-6439. (Pubitemid 30347148)
68. Wessel, D., and Flügge, U.I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138: 141-143. (Pubitemid 14146660)
69. Winn, M.D., Isupov, M.N., and Murshudov, G.N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57: 122-133.
70. Wold, M.S. (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66: 61-92.