The structure of the KlcA and ArdB proteins reveals a novel fold and antirestriction activity against type I DNA restriction systems in vivo but not in vitro

Nucleic Acids Research

Volumn 38, Issue 5, 2009, Pages 1723-1737

  Serfiotis Mitsa, Dimitra ^a   Herbert, Andrew P ^a   Roberts, Gareth A ^a   Soares, Dinesh C ^a   White, John H ^a   Blakely, Garry W ^a   Uhrín, Dušan ^a   Dryden, David T F ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; PROTEIN ARDB; PROTEIN KLCA; RESTRICTION ENDONUCLEASE; UNCLASSIFIED DRUG; ARDB PROTEIN, E COLI; CLPXP PROTEASE, E COLI; DNA MODIFICATION METHYLASE ECOKI; ENDODEOXYRIBONUCLEASE ECOKI; ENDOPEPTIDASE CLP; ESCHERICHIA COLI PROTEIN; SITE SPECIFIC DNA METHYLTRANSFERASE (ADENINE SPECIFIC); TYPE I SITE SPECIFIC DEOXYRIBONUCLEASE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIOPHAGE; BORDETELLA PERTUSSIS; CONTROLLED STUDY; DNA MODIFICATION; DNA RESTRICTION; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOGENICITY ISLAND; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; TRANSPOSON; UROPATHOGENIC ESCHERICHIA COLI; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; ESCHERICHIA COLI; GENETICS; HYDROPHOBICITY; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; SEQUENCE HOMOLOGY;

BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS; ESCHERICHIA COLI;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BORDETELLA PERTUSSIS; DEOXYRIBONUCLEASES, TYPE I SITE-SPECIFIC; DNA RESTRICTION ENZYMES; ENDOPEPTIDASE CLP; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROPHOBICITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; SEQUENCE HOMOLOGY, AMINO ACID; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC);

EID: 77950485049     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1144     Document Type: Article

References (78)

1. Thomas, C.M. and Nielsen, K.M. (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev., 3, 711-721.
2. Tock, M.R. and Dryden, D.T.F. (2005) The biology of restriction and anti-restriction. Curr. Opin. Microbiol., 8, 466-472.
3. Wilkins, B.M. (2002) Plasmid promiscuity: meeting the challenge of DNA immigration control. Env. Microbiol., 4, 495-500.
4. Murray, N.E. (2000) Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol. Mol. Biol. Rev., 64, 412-434.
5. Roberts, R.J., Vincze, T., Posfai, J. and Macelis, D. (2007) REBASE-enzymes and genes for DNA restriction and modification. Nucleic Acids Res., 35, D269-D270.
6. Webb, J.L., King, G., Ternent, D., Titheradge, A.J. and Murray, N.E. (1996) Restriction by EcoKI is enhanced by co-operative interactions between target sequences and is dependent on DEAD box motifs. EMBO J., 15, 2003-2009.
7. Zavilgelsky, G.B. (2000) Antirestriction. Mol. Biol., 34, 724-732
8. McMahon, S.A., Roberts, G.A., Johnson, K.A., Cooper, L.P., Liu, H., White, J.H., Carter, L.G., Sanghvi, B., Oke, M., Walkinshaw, M.D. et al. (2009) Extensive DNA mimicry by the ArdA anti-restriction protein and its role in the spread of antibiotic resistance. Nucleic Acids Res., 37, 4887-4897.
9. Walkinshaw, M.D., Taylor, P., Sturrock, S.S., Atanasiu, C., Berge, T., Henderson, R.M., Edwardson, J.M. and Dryden, D.T.F. (2002) Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. Mol. Cell, 9, 187-194.
10. Stephanou, A.S., Roberts, G.A., Tock, M.R., Pritchard, E.H.,Turkington, R., Nutley, M., Cooper, A. and Dryden, D.T.F. (2009) A mutational analysis of DNA mimicry by ocr, the gene 0.3 antirestriction protein of bacteriophage T7. Biochem. Biophys. Res. Commun., 378, 129-132.
11. Belogurov, A.A., Delver, E.P. and Rodzevich, O.V. (1993) Plasmid pKM101 encodes two nonhomologous antirestriction proteins (ArdA and ArdB) whose expression is controlled by homologous regulatory sequences. J. Bacteriol., 175, 4843-4850.
12. Nekrasov, S.V., Agafonova, O.V., Belogurova, N.G., Delver, E.P. and Belogurov, A.A. (2007) Plasmid-encoded antirestriction protein ArdA can discriminate between type I methyltransferase and complete restriction-modification system. J. Mol. Biol., 365, 284-297.
13. Serfiotis-Mitsa, D., Roberts, G.A., Cooper, L.P., White, J.H.,Nutley, M., Cooper, A., Blakely, G.W. and Dryden, D.T.F. (2008) The Orf18 gene product from conjugative transposon Tn916 is an ArdA antirestriction protein that inhibits type I DNA restriction-modification systems. J. Mol. Biol., 383, 970-981.
14. Thomas, A.T., Brammar, W.J. and Wilkins, B.M. (2003) Plasmid R16 ArdA protein preferentially targets restriction activity of the type I restriction-modification system EcoKI. J. Bacteriol., 185, 2022-2025.
15. Zavilgelsky, G.B., Kotova, V.Y. and Rastorguev, S.M. (2008) Comparative analysis of anti-restriction activities of ArdA (ColIb-P9) and Ocr (T7) proteins. Biochemistry, 73, 906-911
16. Atanasiu, C., Su, T.J., Sturrock, S.S. and Dryden, D.T.F. (2002) Interaction of the ocr gene 0.3 protein of bacteriophage T7 with EcoKI restriction/modification enzyme. Nucleic Acids Res., 30, 3936-3944.
17. Kennaway, C.K., Obarska-Kosinska, A., White, J.H., Tuszynska, I., Cooper, L.P., Bujnicki, J.M., Trinick, J. and Dryden, D.T.F. (2009) The structure of M.EcoKI Type I DNA methyltransferase with a DNA mimic antirestriction protein. Nucleic Acids Res., 37, 762-770.
18. Belogurov, A.A., Delver, E.P., Agafonova, O.V., Belogurova, N.G., Lee, L.Y. and Kado, C.I. (2000) Antirestriction protein Ard (Type C) encoded by IncW plasmid pSa has a high similarity to the"protein transport" domain of TraC1 primase of promiscuous plasmid RP4. J. Mol. Biol., 296, 969-977.
19. Kamachi, K., Sota, M., Tamai, Y., Nagata, N., Konda, T., Inoue, T., Top, E.M. and Arakawa, Y. (2006) Plasmid pBP136 from Bordetella pertussis represents an ancestral form of IncP-1beta plasmids without accessory mobile elements. Microbiology, 152, 3477-3484.
20. Larsen, M.H. and Figurski, D.H. (1994) Structure, expression, and regulation of the kilC operon of promiscuous IncP alpha plasmids. J. Bacteriol., 176, 5022-5032.
21. Riley, M., Abe, T., Arnaud, M.B., Berlyn, M.K., Blattner, F.R., Chaudhuri, R.R., Glasner, J.D., Horiuchi, T., Keseler, I.M.,Kosuge, T. et al. (2006) Escherichia coli K-12: a cooperatively developed annotation snapshot-2005. Nucleic Acids Res., 34, 1-9
22. Rasko, D.A., Phillips, J.A., Li, X. and Mobley, H.L. (2001) Identification of DNA sequences from a second pathogenicity island of uropathogenic Escherichia coli CFT073: probes specific for uropathogenic populations. J. Infectious Diseases, 184, 1041-1049.
23. Welch, R.A., Burland, V., Plunkett, G. III, Redford, P., Roesch, P., Rasko, D., Buckles, E.L., Liou, S.R., Boutin, A., Hackett, J. et al. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl Acad. Sci. USA, 99, 17020-17024.
24. Cazalet, C., Rusniok, C., Bruggemann, H., Zidane, N., Magnier, A., Ma, L., Tichit, M., Jarraud, S., Bouchier, C., Vandenesch, F. et al. (2004) Evidence in the Legionella pneumophila genome forexploitation of host cell functions and high genome plasticity. Nat. Genet., 36, 1165-1173.
25. Vedler, E., Vahter, M. and Heinaru, A. (2004) The completely sequenced plasmid pEST4011 contains a novel IncP1 backbone and a catabolic transposon harboring tfd genes for 2, 4-dichlorophenoxyacetic acid degradation. J. Bacteriol., 186, 7161-7174.
26. Belogurov, A.A. and Delver, E.P. (1995) A motif conserved among the type I restriction-modification enzymes and antirestriction proteins: a possible basis for mechanism of action of plasmid-encoded antirestriction functions. Nucleic Acids Res., 23, 785-787
27. Adamczyk, M. and Jagura-Burdzy, G. (2003) Spread and survival of promiscuous IncP-1 plasmids. Acta Biochimica Polonica, 50, 425-453.
28. Burlage, R.S., Bemis, L.A., Layton, A.C., Sayler, G.S. and Larimer, F. (1990) Comparative genetic organization of incompatibility group P degradative plasmids. J. Bacteriol., 172, 6818-6825.
29. Harada, K.M., Aso, Y., Hashimoto, W., Mikami, B. and Murata, K. (2006) Sequence and analysis of the 46.6-kb plasmid pA1 from Sphingomonas sp. A1 that corresponds to the typical IncP-1beta plasmid backbone without any accessory gene. Plasmid, 56, 11-23.
30. Blakely, G.W. and Murray, N.E. (2006) Control of the endonuclease activity of type I restriction-modification systems is required to maintain chromosome integrity following homologous recombination. Mol. Microbiol., 60, 883-893.
31. Gill, S.C. and von Hippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem., 182, 319-326.
32. Makovets, S., Powell, L.M., Titheradge, A.J., Blakely, G.W. and Murray, N.E. (2004) Is modification sufficient to protect a bacterial chromosome from a resident restriction endonuclease? Mol. Microbiol., 51, 135-147.
33. Stephanou, A.S., Roberts, G.A., Cooper, L.P., Clarke, D.J., Thomson, A.R., MacKay, C.L., Nutley, M., Cooper, A. and Dryden, D.T.F. (2009) Dissection of the DNA mimicry of the bacteriophage T7 Ocr protein using chemical modification. J. Mol. Biol., 391, 565-576.
34. Dryden, D.T.F., Cooper, L.P., Thorpe, P.H. and Byron, O. (1997) The in vitro assembly of the EcoKI type I DNA restriction/ modification enzyme and its in vivo implications. Biochemistry, 36, 1065-1076.
35. Uhrinova, S., Uhrin, D., Denton, H., Smith, M., Sawyer, L. and Barlow, P.N. (1998) Complete assignment of 1H, 13C and 15N chemical shifts for bovine beta-lactoglobulin: secondary structure and topology of the native state is retained in a partially unfolded form. J. Biomol. NMR, 12, 89-107.
36. Muhandiram, D.R., Farrow, N.A., Xu, G.Y., Smallcombe, S.H. and Kay, L.E. (1993) A gradient C-13 Noesy-Hsqc experiment for recording Noesy spectra of C-13-labeled proteins dissolved in H2O. J. Mag. Res. Series B, 102, 317-321.
37. Sklenar, V., Piotto, M., Leppik, R. and Saudek, V. (1993) Gradient-tailored water suppression for H-1-N-15 Hsqc experiments optimized to retain full sensitivity. J. Mag. Res. Series A, 102, 241-245.
38. Yamazaki, T., Forman-Kay, J.D. and Kay, L.E. (1993) Two-dimensional NMR experiments for correlating 13Cβ and 1Hδ/ε chemical shifts of aromatic residues in 13C-labeled proteins via scalar couplings. J. Am. Chem. Soc., 115, 11054-11055.
39. Vranken, W.F., Boucher, W., Stevens, T.J., Fogh, R.H., Pajon, A., Llinas, M., Ulrich, E.L., Markley, J.L., Ionides, J. and Laue, E.D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins, 59, 687-696.
40. Herrmann, T., Guntert, P. and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 319, 209-227.
41. Guntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol., 278, 353-378.
42. Cornilescu, G., Delaglio, F. and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR, 13, 289-302.
43. 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., 54, 905-921.
44. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R. and Thornton, J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486.
45. Vriend, G. (1990) What if - a molecular modeling and drug design program. J. Mol. Graphics, 8, 52-56.
46. Koradi, R., Billeter, M. and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics, 14, 51-55, 29-32.
47. Ottiger, M., Delaglio, F. and Bax, A. (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson., 131, 373-378.
48. Valafar, H. and Prestegard, J.H. (2004) REDCAT: a residual dipolar coupling analysis tool. J. Magn. Reson., 167, 228-241.
49. Grzesiek, S. and Bax, A. (1993) The importance of not saturating water in protein NMR. Application to sensitivity enhancement and NOE measurements. J. Am. Chem. Soc., 115, 12593-12594
50. Yip, G.N. and Zuiderweg, E.R. (2005) Improvement of duty-cycle heating compensation in NMR spin relaxation experiments. J. Magn. Reson., 176, 171-178.
51. Dosset, P., Hus, J.C., Blackledge, M. and Marion, D. (2000) Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR, 16, 23-28
52. Tjandra, N., Feller, S.E., Pastor, R.W. and Bax, A. (1995) Rotational diffusion anisotropy of human ubiquitin from 15N NMR relaxation. J. Am. Chem. Soc., 117, 12562-12566.
53. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N.,Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The Protein Data Bank. Nucleic Acids Res., 28, 235-242.
54. Frishman, D. and Argos, P. (1995) Knowledge-based protein secondary structure assignment. Proteins, 23, 566-579.
55. Hutchinson, E.G. and Thornton, J.M. (1990) HERA-a program to draw schematic diagrams of protein secondary structures. Proteins, 8, 203-212.
56. Hutchinson, E.G. and Thornton, J.M. (1996) PROMOTIF-a program to identify and analyze structural motifs in proteins. Protein Sci., 5, 212-220.
57. Bond, C.S. (2003) TopDraw: a sketchpad for protein structure topology cartoons. Bioinformatics, 19, 311-312.
58. 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.
59. Bennett-Lovsey, R.M., Herbert, A.D., Sternberg, M.J. and Kelley, L.A. (2008) Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins, 70, 611-625.
60. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol., 233, 123-138.
61. Krissinel, E. and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr., 60, 2256-2268.
62. Bairoch, A., Apweiler, R., Wu, C.H., Barker, W.C., Boeckmann, B., Ferro, S., Gasteiger, E., Huang, H., Lopez, R., Magrane, M. et al. (2005) The Universal Protein Resource (UniProt). Nucleic Acids Res., 33, D154-159.
63. Combet, C., Blanchet, C., Geourjon, C. and Deleage, G. (2000) NPS@:networkproteinsequenceanalysis. Trends Biochem. Sci., 25, 147-150.
64. Pei, J., Kim, B.H. and Grishin, N.V. (2008) PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res., 36, 2295-2300.
65. Glaser, F., Pupko, T., Paz, I., Bell, R.E., Bechor-Shental, D.,Martz, E. and Ben-Tal, N. (2003) ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics, 19, 163-164.
66. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
67. Heiden, W., Moeckel, G. and Brickmann, J. (1993) A new approach to analysis and display of local lipophilicity hydrophilicity mapped on molecular-surfaces. J. Comput. Aided Mol. Des., 7, 503-514.
68. Fraczkiewicz, R. and Braun, W. (1998) Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comp. Chem., 19, 319-333
69. Saltman, L.H., Kim, K.S. and Figurski, D.H. (1991) The kilA operon of promiscuous plasmid RK2: the use of a transducing phage (lambda pklaA-1) to determine the effects of the lethal klaA gene on Escherichia coli cells. Mol. Microbiol., 5, 2673-2683.
70. Dunn, J.J., Elzinga, M., Mark, K.K. and Studier, F.W. (1981) Amino acid sequence of the gene 0.3 protein of bacteriophage T7 and nucleotide sequence of its mRNA. J. Biol. Chem., 256, 2579-2585.
71. Makovets, S., Doronina, V.A. and Murray, N.E. (1999) Regulation of endonuclease activity by proteolysis prevents breakage of unmodified bacterial chromosomes by type I restriction enzymes. Proc. Natl Acad. Sci. USA, 96, 9757-9762.
72. Bandyopadhyay, P.K., Studier, F.W., Hamilton, D.L. and Yuan, R. (1985) Inhibition of the type I restriction-modification enzymes EcoB and EcoK by the gene 0.3 protein of bacteriophage T7. J. Mol. Biol., 182, 567-578.
73. Alexandrov, N. and Shindyalov, I. (2003) PDP: protein domain parser. Bioinformatics, 19, 429-430.
74. Ulrich, E.L., Akutsu, H., Doreleijers, J.F., Harano, Y.,Ioannidis, Y.E., Lin, J., Livny, M., Mading, S., Maziuk, D., Miller, Z. et al. (2008) BioMagResBank. Nucleic Acids Res., 36, D402-408
75. Kumar, S. and Nussinov, R. (1999) Salt bridge stability in monomeric proteins. J. Mol. Biol., 293, 1241-1255.
76. Kay, L.E., Torchia, D.A. and Bax, A. (1989) Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry, 28, 8972-8979.
77. Studier, F.W. and Movva, N.R. (1976) SAMase gene of bacteriophage T3 is responsible for overcoming host restriction. J. Virol., 19, 136-145.
78. Loenen, W.A. and Murray, N.E. (1986) Modification enhancement by the restriction alleviation protein (Ral) of bacteriophage lambda. J. Mol. Biol., 190, 11-22.