Structural basis of cooperative DNA recognition by the plasmid conjugation factor, TraM

Nucleic Acids Research

Volumn 39, Issue 15, 2011, Pages 6775-6788

  Wong, Joyce J W ^a   Lu, Jun ^a   Edwards, Ross A ^a   Frost, Laura S ^a   Glover, J N Mark ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; PROTEIN SBMA; PROTEIN TRAD; TETRAMER; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; F FACTOR;

AMINO TERMINAL RIBBON HELIX HELIX DOMAIN; ARTICLE; BACTERIAL STRAIN; BACTERIUM CONJUGATION; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DENATURATION; DNA SEQUENCE; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; MOLECULAR RECOGNITION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; ALLELE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS);

ALLELES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; DNA, BACTERIAL; DNA-BINDING PROTEINS; F FACTOR; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 80055090397     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr296     Document Type: Article

References (76)

1. Pallen, M.J. and Wren, B.W. (2007) Bacterial pathogenomics. Nature, 449, 835-842. (Pubitemid 47598624)
2. Lederberg, J. and Tatum, E.L. (1953) Sex in bacteria; genetic studies, 1945-1952. Science, 118, 169-175.
3. de la Cruz, F., Frost, L.S., Meyer, R.J. and Zechner, E.L. (2010) Conjugative DNA metabolism in gram-negative bacteria. FEMS Microbiol. Rev., 34, 18-40.
4. Watanabe, T. (1963) Infective heredity of multiple drug resistance in bacteria. Bacteriol. Rev., 27, 87-115.
5. Coque, T.M., Novais, A., Carattoli, A., Poirel, L., Pitout, J., Peixe, L., Baquero, F., Canton, R. and Nordmann, P. (2008) Dissemination of clonally related escherichia coli strains expressing extended-spectrum beta-lactamase CTX-M-15. Emerg. Infect. Dis., 14, 195-200. (Pubitemid 351213667)
6. Strahilevitz, J., Jacoby, G.A., Hooper, D.C. and Robicsek, A. (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin. Microbiol. Rev., 22, 664-689.
7. Willetts, N. and Wilkins, B. (1984) Processing of plasmid DNA during bacterial conjugation. Microbiol. Rev., 48, 24-41. (Pubitemid 14150424)
8. Lanka, E. and Wilkins, B.M. (1995) DNA processing reactions in bacterial conjugation. Annu. Rev. Biochem., 64, 141-169.
9. Lawley, T.D., Klimke, W.A., Gubbins, M.J. and Frost, L.S. (2003) F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett., 224, 1-15. (Pubitemid 36830816)
10. Kupelwieser, G., Schwab, M., Hogenauer, G., Koraimann, G. and Zechner, E.L. (1998) Transfer protein TraM stimulates TraI-catalyzed cleavage of the transfer origin of plasmid R1 in vivo. J. Mol. Biol., 275, 81-94. (Pubitemid 28022389)
11. Ragonese, H., Haisch, D., Villareal, E., Choi, J.H. and Matson, S.W. (2007) The F plasmid-encoded TraM protein stimulates relaxosome-mediated cleavage at oriT through an interaction with TraI. Mol. Microbiol., 63, 1173-1184. (Pubitemid 46184520)
12. 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. (Pubitemid 30436564)
13. 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.
14. Karl, W., Bamberger, M. and Zechner, E.L. (2001) Transfer protein TraY of plasmid R1 stimulates TraI-catalyzed oriT cleavage in vivo. J. Bacteriol., 183, 909-914. (Pubitemid 32095299)
15. 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.
16. Abo, T., Inamoto, S. and Ohtsubo, E. (1991) Specific DNA binding of the TraM protein to the oriT region of plasmid R100. J. Bacteriol., 173, 6347-6354.
17. Di Laurenzio, L., Frost, L.S., Finlay, B.B. and Paranchych, W. (1991) Characterization of the oriT region of the IncFV plasmid pED208. Mol. Microbiol., 5, 1779-1790. (Pubitemid 21896209)
18. Di Laurenzio, L., Frost, L.S. and Paranchych, W. (1992) The TraM protein of the conjugative plasmid F binds to the origin of transfer of the F and ColE1 plasmids. Mol. Microbiol., 6, 2951-2959.
19. Schwab, M., Gruber, H. and Hogenauer, G. (1991) The TraM protein of plasmid R1 is a DNA-binding protein. Mol. Microbiol., 5, 439-446. (Pubitemid 21896064)
20. Byrd, D.R. and Matson, S.W. (1997) Nicking by transesterification: The reaction catalysed by a relaxase. Mol. Microbiol., 25, 1011-1022. (Pubitemid 27410183)
21. Byrd, D.R., Sampson, J.K., Ragonese, H.M. and Matson, S.W. (2002) Structure-function analysis of escherichia coli DNA helicase I reveals non-overlapping transesterase and helicase domains. J. Biol. Chem., 277, 42645-42653. (Pubitemid 35285633)
22. Frost, L.S., Ippen-Ihler, K. and Skurray, R.A. (1994) Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol. Rev., 58, 162-210.
23. Matson, S.W., Sampson, J.K. and Byrd, D.R. (2001) F plasmid conjugative DNA transfer: the TraI helicase activity is essential for DNA strand transfer. J. Biol. Chem., 276, 2372-2379.
24. Fekete, R.A. and Frost, L.S. (2002) Characterizing the DNA contacts and cooperative binding of F plasmid TraM to its cognate sites at oriT. J. Biol. Chem., 277, 16705-16711. (Pubitemid 34967690)
25. Penfold, S.S., Simon, J. and Frost, L.S. (1996) Regulation of the expression of the traM gene of the F sex factor of escherichia coli. Mol. Microbiol., 20, 549-558. (Pubitemid 26151896)
26. Fu, Y.H., Tsai, M.M., Luo, Y.N. and Deonier, R.C. (1991) Deletion analysis of the F plasmid oriT locus. J. Bacteriol., 173, 1012-1020.
27. Miller, D.L. and Schildbach, J.F. (2003) Evidence for a monomeric intermediate in the reversible unfolding of F factor TraM. J. Biol. Chem., 278, 10400-10407. (Pubitemid 36800305)
28. Lu, J., Zhao, W. and Frost, L.S. (2004) Mutational analysis of TraM correlates oligomerization and DNA binding with autoregulation and conjugative DNA transfer. J. Biol. Chem., 279, 55324-55333. (Pubitemid 40066530)
29. Schwab, M., Reisenzein, H. and Hogenauer, G. (1993) TraM of plasmid R1 regulates its own expression. Mol. Microbiol., 7, 795-803. (Pubitemid 23090361)
30. Verdino, P., Keller, W., Strohmaier, H., Bischof, K., Lindner, H. and Koraimann, G. (1999) The essential transfer protein TraM binds to DNA as a tetramer. J. Biol. Chem., 274, 37421-37428.
31. Lu, J., Edwards, R.A., Wong, J.J., Manchak, J., Scott, P.G., Frost, L.S. and Glover, J.N. (2006) Protonation-mediated structural flexibility in the F conjugation regulatory protein, TraM. EMBO J., 25, 2930-2939. (Pubitemid 43980399)
32. Lu, J. and Frost, L.S. (2005) Mutations in the C-terminal region of TraM provide evidence for in vivo TraM-TraD interactions during F-plasmid conjugation. J. Bacteriol., 187, 4767-4773. (Pubitemid 40962194)
33. Lu, J., Wong, J.J., Edwards, R.A., Manchak, J., Frost, L.S. and Glover, J.N. (2008) Structural basis of specific TraD-TraM recognition during F plasmid-mediated bacterial conjugation. Mol. Microbiol., 70, 89-99.
34. Beranek, A., Zettl, M., Lorenzoni, K., Schauer, A., Manhart, M. and Koraimann, G. (2004) Thirty-eight C-terminal amino acids of the coupling protein TraD of the F-like conjugative resistance plasmid R1 are required and sufficient to confer binding to the substrate selector protein TraM. J. Bacteriol., 186, 6999-7006. (Pubitemid 39332138)
35. Disque-Kochem, C. and Dreiseikelmann, B. (1997) The cytoplasmic DNA-binding protein TraM binds to the inner membrane protein TraD in vitro. J. Bacteriol., 179, 6133-6137. (Pubitemid 27419040)
36. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326. (Pubitemid 27085611)
37. Vagin, A. and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr., 66, 22-25.
38. Rafferty, J.B., Somers, W.S., Saint-Girons, I. and Phillips, S.E. (1989) Three-dimensional crystal structures of escherichia coli met repressor with and without corepressor. Nature, 341, 705-710. (Pubitemid 19260883)
39. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132. (Pubitemid 41742764)
40. 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. (Pubitemid 27235885)
41. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S. et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
42. Cohen, S.X., Ben Jelloul, M., Long, F., Vagin, A., Knipscheer, P., Lebbink, J., Sixma, T.K., Lamzin, V.S., Murshudov, G.N. and Perrakis, A. (2008) ARP/wARP and molecular replacement: The next generation. Acta Crystallogr. D Biol. Crystallogr., 64, 49-60.
43. Lu, X.J. and Olson, W.K. (2008) 3DNA: A versatile, integrated software system for the analysis, rebuilding and visualization of three-dimensional nucleic-acid structures. Nat. Protoc., 3, 1213-1227.
44. Lu, J., Manchak, J., Klimke, W., Davidson, C., Firth, N., Skurray, R.A. and Frost, L.S. (2002) Analysis and characterization of the IncFV plasmid pED208 transfer region. Plasmid, 48, 24-37.
45. Stockner, T., Plugariu, C., Koraimann, G., Hogenauer, G., Bermel, W., Prytulla, S. and Sterk, H. (2001) Solution structure of the DNA-binding domain of TraM. Biochemistry, 40, 3370-3377. (Pubitemid 32221640)
46. Schreiter, E.R. and Drennan, C.L. (2007) Ribbon-helix-helix transcription factors: Variations on a theme. Nat. Rev. Microbiol., 5, 710-720. (Pubitemid 47278864)
47. 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. (Pubitemid 39140782)
48. Falkow, S. and Baron, L.S. (1962) Episomic element in a strain of salmonella typhosa. J. Bacteriol., 84, 581-589.
49. Finlay, B.B., Paranchych, W. and Falkow, S. (1983) Characterization of conjugative plasmid EDP208. J. Bacteriol., 156, 230-235. (Pubitemid 14227373)
50. Luscombe, N.M., Laskowski, R.A. and Thornton, J.M. (2001) Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res., 29, 2860-2874. (Pubitemid 32685051)
51. Inamoto, S., Fukuda, H., Abo, T. and Ohtsubo, E. (1994) Site- and strand-specific nicking at oriT of plasmid R100 in a purified system: Enhancement of the nicking activity of TraI (helicase I) with TraY and IHF. J. Biochem., 116, 838-844. (Pubitemid 24323666)
52. Llosa, M., Zunzunegui, S. and de la Cruz, F. (2003) Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc. Natl Acad. Sci. USA, 100, 10465-10470. (Pubitemid 37071901)
53. Tato, I., Matilla, I., Arechaga, I., Zunzunegui, S., de la Cruz, F. and Cabezon, E. (2007) The ATPase activity of the DNA transporter TrwB is modulated by protein TrwA: Implications for a common assembly mechanism of DNA translocating motors. J. Biol. Chem., 282, 25569-25576. (Pubitemid 47372773)
54. Gomis-Ruth, F.X., Sola, M., Acebo, P., Parraga, A., Guasch, A., Eritja, R., Gonzalez, A., Espinosa, M., del Solar, G. and Coll, M. (1998) The structure of plasmid-encoded transcriptional repressor CopG unliganded and bound to its operator. EMBO J., 17, 7404-7415. (Pubitemid 29002708)
55. Lu, J., den Dulk-Ras, A., Hooykaas, P.J. and Glover, J.N. (2009) Agrobacterium tumefaciens VirC2 enhances T-DNA transfer and virulence through its C-terminal ribbon-helix-helix DNA-binding fold. Proc. Natl Acad. Sci. USA, 106, 9643-9648.
56. Bolinger, D., Sulkowska, J.I., Hsu, H.P., Mirny, L.A., Kardar, M., Onuchic, J.N. and Virnau, P. (2010) A stevedore's protein knot. PLoS Comput. Biol., 6, e1000731.
57. Stayrook, S., Jaru-Ampornpan, P., Ni, J., Hochschild, A. and Lewis, M. (2008) Crystal structure of the lambda repressor and a model for pairwise cooperative operator binding. Nature, 452, 1022-1025. (Pubitemid 351589614)
58. Lu, D., Fillet, S., Meng, C., Alguel, Y., Kloppsteck, P., Bergeron, J., Krell, T., Gallegos, M.T., Ramos, J. and Zhang, X. (2010) Crystal structure of TtgV in complex with its DNA operator reveals a general model for cooperative DNA binding of tetrameric gene regulators. Genes Dev., 24, 2556-2565.
59. Schumacher, M.A., Miller, M.C., Grkovic, S., Brown, M.H., Skurray, R.A. and Brennan, R.G. (2002) Structural basis for cooperative DNA binding by two dimers of the multidrug-binding protein QacR. EMBO J., 21, 1210-1218. (Pubitemid 34206194)
60. Jeng, W.Y., Ko, T.P., Liu, C.I., Guo, R.T., Liu, C.L., Shr, H.L. and Wang, A.H. (2008) Crystal structure of IcaR, a repressor of the TetR family implicated in biofilm formation in staphylococcus epidermidis. Nucleic Acids Res., 36, 1567-1577. (Pubitemid 351426109)
61. Itou, H., Watanabe, N., Yao, M., Shirakihara, Y. and Tanaka, I. (2010) Crystal structures of the multidrug binding repressor corynebacteriumglutamicum CgmR in complex with inducers and with an operator. J. Mol. Biol., 403, 174-184.
62. Wisedchaisri, G., Holmes, R.K. and Hol, W.G. (2004) Crystal structure of an IdeR-DNA complex reveals a conformational change in activated IdeR for base-specific interactions. J. Mol. Biol., 342, 1155-1169. (Pubitemid 39207894)
63. Pohl, E., Holmes, R.K. and Hol, W.G. (1999) Crystal structure of a cobalt-activated diphtheria toxin repressor-DNA complex reveals a metal-binding SH3-like domain. J. Mol. Biol., 292, 653-667. (Pubitemid 29457326)
64. Pohl, E., Holmes, R.K. and Hol, W.G. (1999) Crystal structure of the iron-dependent regulator (IdeR) from mycobacterium tuberculosis shows both metal binding sites fully occupied. J. Mol. Biol., 285, 1145-1156. (Pubitemid 29054322)
65. White, A., Ding, X., vanderSpek, J.C., Murphy, J.R. and Ringe, D. (1998) Structure of the metal-ion-activated diphtheria toxin repressor/tox operator complex. Nature, 394, 502-506. (Pubitemid 28373964)
66. Alvarez-Martinez, C.E. and Christie, P.J. (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev., 73, 775-808.
67. Lang, S., Gruber, K., Mihajlovic, S., Arnold, R., Gruber, C.J., Steinlechner, S., Jehl, M.A., Rattei, T., Frohlich, K.U. and Zechner, E.L. (2010) Molecular recognition determinants for type IV secretion of diverse families of conjugative relaxases. Mol. Microbiol., 78, 1539-1555.
68. Sastre, J.I., Cabezon, E. and de la Cruz, F. (1998) The carboxyl terminus of protein TraD adds specificity and efficiency to F-plasmid conjugative transfer. J. Bacteriol., 180, 6039-6042. (Pubitemid 28514224)
69. Salje, J. and Lowe, J. (2008) Bacterial actin: Architecture of the ParMRC plasmid DNA partitioning complex. EMBO J., 27, 2230-2238.
70. Schumacher, M.A., Glover, T.C., Brzoska, A.J., Jensen, S.O., Dunham, T.D., Skurray, R.A. and Firth, N. (2007) Segrosome structure revealed by a complex of ParR with centromere DNA. Nature, 450, 1268-1271.
71. Rice, P.A., Yang, S., Mizuuchi, K. and Nash, H.A. (1996) Crystal structure of an IHF-DNA complex: A protein-induced DNA U-turn. Cell, 87, 1295-1306. (Pubitemid 27010112)
72. Di Laurenzio, L., Scraba, D.G., Paranchych, W. and Frost, L.S. (1995) Studies on the binding of integration host factor (IHF) and TraM to the origin of transfer of the IncFV plasmid pED208. Mol. Gen. Genet., 247, 726-734.
73. Csitkovits, V.C. and Zechner, E.L. (2003) Extent of single-stranded DNA required for efficient TraI helicase activity in vitro. J. Biol. Chem., 278, 48696-48703. (Pubitemid 41079510)
74. Dostal, L. and Schildbach, J.F. (2010) Single-stranded DNA binding by F TraI relaxase and helicase domains are coordinately regulated. J. Bacteriol., 192, 3620-3628.
75. 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. (Pubitemid 37412419)
76. 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 M TraI relaxase DNA recognition and cleavage. Nucleic Acids Res., 36, 4565-4572.