The mechanism and control of DNA transfer by the conjugative relaxase of resistance plasmid pCU1

Nucleic Acids Research

Volumn 38, Issue 17, 2010, Pages 5929-5943

  Nash, Rebekah Potts ^a   Habibi, Sohrab ^a   Cheng, Yuan ^b   Lujan, Scott A ^b,c   Redinbo, Matthew R ^a,b  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL ENZYME; RELAXASE; TYROSINE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; DNA; DNA POLYMERASE; DNA RELAXASE; METAL;

AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIRULENCE; CONJUGATIVE PLASMID TRANSFER; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA NICK TRANSLATION; DNA TRANSFER; ENZYME ACTIVE SITE; ENZYME STRUCTURE; ESCHERICHIA COLI; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FOLDING; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; BACTERIUM CONJUGATION; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PLASMID; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; CONJUGATION, GENETIC; CRYSTALLOGRAPHY, X-RAY; DNA; DNA NUCLEOTIDYLTRANSFERASES; METALS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLASMIDS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; TYROSINE;

EID: 77957221192     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq303     Document Type: Article

References (62)

1. Siegel, J.D., Rhinehart, E., Jackson, M. and Chiarello, L. (2006) Management of Multidrug-Resistant Organisms in Healthcare Settings. The Centers for Disease Control and Prevention. Healthcare Infection Control Practices Advisory Committee.
2. Clatworthy, A.E., Pierson, E. and Hung, D.T. (2007) Targeting virulence: a new paradigm for antimicrobial therapy. Nat. Chem. Biol., 3, 541-548.
3. Lujan, S.A., Guogas, L.M., Ragonese, H., Matson, S.W. and Redinbo, M.R. (2007) Disrupting antibiotic resistance propagation by inhibiting the conjugative DNA relaxase. Proc. Natl Acad. Sci. USA, 104, 12282-12287.
4. Fernandez-Lopez, R., Machon, C., Longshaw, C.M., Martin, S., Molin, S., Zechner, E.L., Espinosa, M., Lanka, E. and de la Cruz, F. (2005) Unsaturated fatty acids are inhibitors of bacterial conjugation. Microbiology, 151, 3517-3626.
5. Garcillan-Barcia, M.P., Jurado, P., Gonzalez-Perez, B., Moncalian, G., Fernandez, L.A. and de la Cruz, F. (2007) Conjugative transfer can be inhibited by blocking relaxase activity within recipient cells with intrabodies. Mol. Microbiol., 63, 404-416.
6. Williams, J.J. and Hergenrother, P.J. (2008) Exposing plasmids as the Achilles' heel of drug-resistant bacteria. Curr. Opin. Chem. Biol., 12, 389-399.
7. Qiu, X.-Q., Wang, H., Lu, X.-F., Zhang, J., Li, S.-F., Cheng, G., Wan, L., Yang, L., Zuo, J.-Y., Zhou, Y.-Q. et al. (2003) An engineered multidomain bactericidal peptide as a model for targeted antibiotics against specific bacteria. Nat. Biotechnol., 21, 1480-1485.
8. Potts, R.G., Lujan, S.A. and Redinbo, M.R. (2008) Winning the asymmetric war: new strategies for combating antibacterial resistance. Future Microbiol., 3, 119-123.
9. Willetts, N. and Wilkins, B. (1984) Processing of plasmid DNA during bacterial conjugation. Microbiol. Rev., 48, 24-41.
10. Lanka, E. and Wilkins, B.M. (1995) DNA processing reactions in bacterial conjugation. Annu. Rev. Biochem., 64, 141-169.
11. de la Cruz, F. and Davies, J. (2000) Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol., 8, 128-133.
12. Llosa, M., Gomis-Ruth, F.X., Coll, M. and de la Cruz, F. (2002) Bacterial conjugation: a two-step mechanism for DNA transport. Mol. Microbiol., 45, 1-8.
13. de la Cruz, F., Frost, L.S., Meyer, R.J. and Zechner, E.L. (2009) Conjugative DNA Metabolism in Gram-negative bacteria. FEMS Microbiol. Rev., 34, 18-30.
14. Byrd, D.R.N. and Matson, S.W. (1997) Nicking by transesterification: the reaction catalysed by a relaxase. Mol. Microbiol., 25, 1011-1022.
15. Matson, S.W., Sampson, J.K. and Byrd, D.R.N. (2001) F plasmid conjugative DNA transfer: the TraI helicase activity is essential for DNA strand transfer. J. Biol. Chem., 276, 2372-2379.
16. Tatum, E.L. and Lederberg, J. (1947) Gene Recombination in the bacterium Escherichia coli. J. Bacteriol., 53, 673-684.
17. Matson, S.W., Nelson, W.C. and Morton, B.S. (1993) Characterization of the reaction product of the oriT nicking reaction catalyzed by Escherichia coli DNA helicase I. J. Bacteriol., 175, 2599-2606.
18. Sherman, J.A. and Matson, S.W. (1994) Escherichia coli DNA helicase I catalyzes a sequence-specific cleavage/ligation reaction at the F plasmid origin of transfer. J. Biol. Chem., 269, 26220-26226.
19. Howard, M.T., Nelson, W.C. and Matson, S.W. (1995) Stepwise assembly of a relaxosome at the F plasmid origin of transfer. J. Biol. Chem., 270, 28381-28386.
20. Matson, S.W. and Ragonese, H. (2005) The F-plasmid TraI protein contains three functional domains required for conjugative DNA strand transfer. J. Bacteriol., 187, 697-706.
21. Nelson, W.C., Howard, M.T., Sherman, J.A. and Matson, S.W. (1995) The traY gene product and integration host factor stimulate Escherichia coli DNA helicase I-catalyzed nicking at the F plasmid oriT. J. Biol. Chem., 270, 28374-28380.
22. Stern, J.C. and Schildbach, J.F. (2001) DNA recognition by F factor TraI36: highly sequence-specific binding of single-stranded DNA. Biochemistry, 40, 11586-11595.
23. Datta, S., Larkin, C. and Schildbach, J.F. (2003) Structural insights into single-stranded DNA binding and cleavage by F factor TraI. Structure, 11, 1369-1379.
24. Larkin, C., Datta, S., Harley, M.J., Anderson, B.J., Ebie, A., Hargreaves, V. and Schildbach, J.F. (2005) Inter- and intramolecular determinants of the specificity of single-stranded DNA binding and cleavage by the F factor relaxase. Structure, 13, 1533-1544.
25. Williams, S.L. and Schildbach, J.F. (2006) Examination of an inverted repeat within the F factor origin of transfer: context dependence of F TraI relaxase DNA specificity. Nucleic Acids Res., 34, 426-435.
26. Larkin, C., Haft, R.J.F., Harley, M.J., Traxler, B. and Schildbach, J.F. (2007) Roles of active site residues and the HUH motif of the F plasmid TraI relaxase. J. Biol. Chem., 282, 33707-33713.
27. Hekman, K., Guja, K., Larkin, C. and Schildbach, J.F. (2008) An intrastrand three-DNA-base interaction is a key specificity determinant of F transfer initiation and of F TraI relaxase DNA recognition and cleavage. Nucleic Acids Res., 36, 4565-4572.
28. Llosa, M., Bolland, S. and de la Cruz, F. (1991) Structural and functional analysis of the origin of conjugal transfer of the broad-host-range IncW plasmid R388 and comparison with the related IncN plasmid R46. Mol. General Genet., 226, 473-483.
29. Grandoso, G., Llosa, M., Zabala, J.C. and de la Cruz, F. (1994) Purification and biochemical characterization of TrwC, the helicase involved in plasmid R388 conjugal DNA transfer. Eur. J. Biochem., 226, 403-412.
30. Llosa, M., Grandoso, G. and de la Cruz, F. (1995) Nicking activity of TrwC directed against the origin of transfer of the IncW plasmid R388. J. Mol. Biol., 246, 54-62.
31. Llosa, M., Grandoso, G., Hernando, M.A. and de la Cruz, F. (1996) Functional domains in protein TrwC of plasmid R388: dissected DNA strand transferase and DNA helicase activities reconstitute protein function. J. Mol. Biol., 264, 56-67.
32. Grandoso, G., Avila, P., Cayon, A., Hernando, M.A., Llosa, M. and de la Cruz, F. (2000) Two active-site tyrosyl residues of protein TrwC act sequentially at the origin of transfer during plasmid R388 conjugation. J. Mol. Biol., 295, 1163-1172.
33. Guasch, A., Lucas, M., Moncalian, G., Cabezas, M., Perez-Luque, R., Gomis-Ruth, F.X., de la Cruz, F. and Coll, M. (2003) Recognition and processing of the origin of transfer DNA by conjugative relaxase TrwC. Nature Struct. Biol., 10, 1002-1010.
34. Boer, R., Russi, S., Guasch, A., Lucas, M., Blanco, A.G., Perez-Luque, R., Coll, M. and de la Cruz, F. (2006) Unveiling the molecular mechanism of a conjugative relaxase: the structure of TrwC complexed with a 27-mer DNA comprising the recognition hairpin and the cleavage site. J. Mol. Biol., 358, 857-869.
35. Gonzalez-Perez, B., Lucas, M., Cooke, L.A., Vyle, J.S., de la Cruz, F. and Moncalian, G. (2007) Analysis of DNA processing reactions in bacterial conjugation by using suicide oligonucleotides. EMBO J., 26, 3847-3857.
36. Gonzalez-Perez, B., Carballeira, J.D., Moncalian, G. and de la Cruz, F. (2008) Changing the recognition site of a conjugative relaxase by rational design. Biotechnol. J., 4, 554-557.
37. Lucas, M., Gonzalez-Perez, B., Cabezas, M., Moncalian, G., Rivas, G. and de la Cruz, F. (2010) Relaxase DNA binding and cleavage are two distinguishable steps in conjugative DNA processing that involve different sequence elements of the nic site. J. Biol. Chem., doi: 10.1074/jbc.M109.057539.
38. Pansegrau, W., Schroder, W. and Lanka, E. (1993) Relaxase (TraI) of IncPa plasmid RP4 catalyzes a site-specific cleaving-joining reaction of single-stranded DNA. Proc. Natl Acad. Sci. USA, 90, 2925-2929.
39. Balzer, D., Pansegrau, W. and Lanka, E. (1994) Essential motifs of relaxase (TraI) and TraG proteins involved in conjugative trasfer of plasmid RP4. J. Bacteriol., 176, 4285-4295.
40. Pansegrau, W. and Lanka, E. (1996) Mechanisms of initiation and termination reactions in conjugative DNA processing. J. Biol. Chem., 271, 13068-13076.
41. Bhattacharjee, M. and Meyer, R.J. (1993) Specific binding of MobA, a plasmid-encoded protein involved in the initiation and termination of conjugal DNA transfer, to single-stranded oriT DNA. Nucleic Acids Res., 21, 4563-4568.
42. Becker, E.C. and Meyer, R.J. (2000) Recognition of oriT for DNA processing at termination of a round of conjugal transfer. J. Mol. Biol., 300, 1067-1077.
43. Becker, E.C. and Meyer, R.J. (2003) Relaxed specificity of the R1162 nickase: a model for evolution of a system for conjugative mobilization of plasmids. J. Bacteriol., 185, 3538-3546.
44. Monzingo, A.F., Ozburn, A., Xia, S., Meyer, R.J. and Robertus, J.D. (2007) The structure of the minimal relaxase domain of MobA at 2.1Åresolution. J. Mol. Biol., 366, 165-178.
45. Meyer, R.J. (2008) The R1162 Mob proteins can promote conjugative transfer from cryptic origins in the bacterial chromosome. J. Bacteriol., 191, 1574-1580.
46. Xia, S. and Robertus, J.D. (2009) Effect of divalent ions on the minimal relaxase domain of MobA. Arch. Biochem. Biophys., 488, 42-47.
47. Harley, M.J. and Schildbach, J.F. (2003) Swapping single-stranded DNA sequence specificities of relaxases from conjugative plasmids F and R100. Proc. Natl Acad. Sci. USA, 100, 11243-11248.
48. Fekete, R.A. and Frost, L.S. (2000) Mobilization of chimeric oriT plasmids by F and R100-1: role of relaxosome formation in defining plasmid specificity. J. Bacteriol., 182, 4022-4027.
49. Khatoon, H., Iyer, R.V. and Iyer, V.N. (1972) A new filamentous bacteriophage with sex-factor specificity. Virology, 48, 145-155.
50. Konarska-Kozlowska, M. and Iyer, V.N. (1981) Physical and genetic organization of the IncN-group plasmid pCU1. Gene, 14, 195-204.
51. Paterson, E.S., More, M.I., Pillay, G., Cellini, C., Woodgate, R., Walker, G.C., Iyer, V.N. and Winans, S.C. (1999) Genetic analysis of the mobilization and leading regions of the IncN plasmids pKM101 and pCU1. J. Bacteriol., 181, 2572-2583.
52. Paterson, E.S. and Iyer, V.N. (1997) Localization of the nic site of IncN conjugative plasmid pCU1 through formation of a hybrid oriT. J. Bacteriol., 179, 5768-5776.
53. Paterson, E.S. and Iyer, V.N. (1992) The oriT region of the conjugative transfer system of plasmid pCU1 and specificity between it and the mob region of other N tra plasmids. J. Bacteriol., 174, 499-507.
54. Donnelly, M.I., Zhou, M., Millard, C.S., Clancy, S., Stols, L., Eschenfeldt, W.H., Collart, F.R. and Joachimiak, A. (2006) An expression vector tailored for large-scale, high throughput purification of recombinant proteins. Protein Expression Purif., 47, 446-454.
55. Lo Conte, L., Chothia, C. and Janin, J. (1999) The atomic structure of protein-protein recognition sites. J. Mol. Biol., 285, 2177-2198.
56. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol., 372, 774-797.
57. Barthel, D., Hirst, J., Blazewicz, J., Burke, E. and Krasnogor, N. (2007) ProCKSI: a decision support system for protein (structure) comparison, knowledge, similarity and information. BMC Bioinformatics, 8, 416.
58. Zhang, Y. and Skolnick, J. (2005) TM-align: a protein structure alignment algorithm based on TM-score. Nucleic Acids Res., 33, 2302-2309.
59. Finney, L.A. and O'Halloran, T.V. (2003) Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science, 300, 931-936.
60. Outten, C. and O'Halloran, T. (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science, 292, 2488-2492.
61. Harding, M.M. (2001) Geometry of metal-ligand interactions in proteins. Acta Crystallogr., Sect. D: Biol. Crystallogr., 57, 401-411.
62. Moncalian, G. and de la Cruz, F. (2004) DNA binding properties of protein TrwA, a possible structural variant of the Arc repressor superfamily. Biochim. Biophys. Acta, 1701, 15-23.