CdiA from enterobacter cloacae delivers a toxic ribosomal RNase into target bacteria

Structure

Volumn 22, Issue 5, 2014, Pages 707-718

  Beck, Christina M ^a   Morse, Robert P ^b   Cunningham, David A ^a   Iniguez, Angelina ^b   Low, David A ^a   Goulding, Celia W ^b   Hayes, Christopher S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; CDIA PROTEIN; COLICIN E3; NUCLEASE; RIBONUCLEASE; RNA 16S; UNCLASSIFIED DRUG; COLICIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENTEROBACTER CLOACAE; ENZYME ACTIVITY; ENZYME METABOLISM; GROWTH INHIBITION; IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; STRUCTURAL HOMOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; CONTACT INHIBITION; ESCHERICHIA COLI; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); ENTEROBACTER CLOACAE;

BACTERIAL PROTEINS; BACTERIAL TOXINS; BINDING SITES; COLICINS; CONTACT INHIBITION; CRYSTALLOGRAPHY, X-RAY; ENTEROBACTER CLOACAE; ESCHERICHIA COLI; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASES; RNA, RIBOSOMAL, 16S; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84899890856     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.02.012     Document Type: Article

References (46)

1. S.K. Aoki, R. Pamma, A.D. Hernday, J.E. Bickham, B.A. Braaten, and D.A. Low Contact-dependent inhibition of growth in Escherichia coli Science 309 2005 1245 1248
2. S.K. Aoki, J.C. Malinverni, K. Jacoby, B. Thomas, R. Pamma, B.N. Trinh, S. Remers, J. Webb, B.A. Braaten, T.J. Silhavy, and D.A. Low Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB Mol. Microbiol. 70 2008 323 340
3. S.K. Aoki, E.J. Diner, C.T. de Roodenbeke, B.R. Burgess, S.J. Poole, B.A. Braaten, A.M. Jones, J.S. Webb, C.S. Hayes, P.A. Cotter, and D.A. Low A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria Nature 468 2010 439 442
4. G.N. Basturea, K.E. Rudd, and M.P. Deutscher Identification and characterization of RsmE, the founding member of a new RNA base methyltransferase family RNA 12 2006 426 434
5. C.M. Bowman, J.E. Dahlberg, T. Ikemura, J. Konisky, and M. Nomura Specific inactivation of 16S ribosomal RNA induced by colicin E3 in vivo Proc. Natl. Acad. Sci. USA 68 1971 964 968
6. S. Carr, D. Walker, R. James, C. Kleanthous, and A.M. Hemmings Inhibition of a ribosome-inactivating ribonuclease: the crystal structure of the cytotoxic domain of colicin E3 in complex with its immunity protein Structure 8 2000 949 960
7. E. Cascales, S.K. Buchanan, D. Duché, C. Kleanthous, R. Lloubès, K. Postle, M. Riley, S. Slatin, and D. Cavard Colicin biology Microbiol. Mol. Biol. Rev. 71 2007 158 229
8. L. Chao, and B.R. Levin Structured habitats and the evolution of anticompetitor toxins in bacteria Proc. Natl. Acad. Sci. USA 78 1981 6324 6328
9. T.L. Czárán, R.F. Hoekstra, and L. Pagie Chemical warfare between microbes promotes biodiversity Proc. Natl. Acad. Sci. USA 99 2002 786 790
10. D. Desveaux, A. Maréchal, and N. Brisson Whirly transcription factors: defense gene regulation and beyond Trends Plant Sci. 10 2005 95 102
11. E.J. Diner, and C.S. Hayes Recombineering reveals a diverse collection of ribosomal proteins L4 and L22 that confer resistance to macrolide antibiotics J. Mol. Biol. 386 2009 300 315
12. E.J. Diner, C.M. Beck, J.S. Webb, D.A. Low, and C.S. Hayes Identification of a target cell permissive factor required for contact-dependent growth inhibition (CDI) Genes Dev. 26 2012 515 525
13. S. Gite, G. Reddy, and V. Shankar Active-site characterization of S1 nuclease. I. Affinity purification and influence of amino-group modification Biochem. J. 285 1992 489 494
14. D.M. Gordon, M.A. Riley, and T. Pinou Temporal changes in the frequency of colicinogeny in Escherichia coli from house mice Microbiology 144 1998 2233 2240
15. C.W. Goulding, and L.J. Perry Protein production in Escherichia coli for structural studies by X-ray crystallography J. Struct. Biol. 142 2003 133 143
16. C.S. Hayes, B. Bose, and R.T. Sauer Proline residues at the C terminus of nascent chains induce SsrA tagging during translation termination J. Biol. Chem. 277 2002 33825 33832
17. L.E. Holberger, F. Garza-Sánchez, J. Lamoureux, D.A. Low, and C.S. Hayes A novel family of toxin/antitoxin proteins in Bacillus species FEBS Lett. 586 2012 132 136
18. L. Holm, and P. Rosenström Dali server: conservation mapping in 3D Nucleic Acids Res. 38 Web Server issue 2010 W545 W549
19. R.D. Hood, P. Singh, F. Hsu, T. Güvener, M.A. Carl, R.R. Trinidad, J.M. Silverman, B.B. Ohlson, K.G. Hicks, and R.L. Plemel et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria Cell Host Microbe 7 2010 25 37
20. S. Koskiniemi, J.G. Lamoureux, K.C. Nikolakakis, C. t'Kint de Roodenbeke, M.D. Kaplan, D.A. Low, and C.S. Hayes Rhs proteins from diverse bacteria mediate intercellular competition Proc. Natl. Acad. Sci. USA 110 2013 7032 7037
21. L.E. Lancaster, A. Savelsbergh, C. Kleanthous, W. Wintermeyer, and M.V. Rodnina Colicin E3 cleavage of 16S rRNA impairs decoding and accelerates tRNA translocation on Escherichia coli ribosomes Mol. Microbiol. 69 2008 390 401
22. D.L. MacIntyre, S.T. Miyata, M. Kitaoka, and S. Pukatzki The Vibrio cholerae type VI secretion system displays antimicrobial properties Proc. Natl. Acad. Sci. USA 107 2010 19520 19524
23. R.P. Morse, K.C. Nikolakakis, J.L. Willett, E. Gerrick, D.A. Low, C.S. Hayes, and C.W. Goulding Structural basis of toxicity and immunity in contact-dependent growth inhibition (CDI) systems Proc. Natl. Acad. Sci. USA 109 2012 21480 21485
24. C.L. Ng, K. Lang, N.A. Meenan, A. Sharma, A.C. Kelley, C. Kleanthous, and V. Ramakrishnan Structural basis for 16S ribosomal RNA cleavage by the cytotoxic domain of colicin E3 Nat. Struct. Mol. Biol. 17 2010 1241 1246
25. K. Nikolakakis, S. Amber, J.S. Wilbur, E.J. Diner, S.K. Aoki, S.J. Poole, A. Tuanyok, P.S. Keim, S. Peacock, C.S. Hayes, and D.A. Low The toxin/immunity network of Burkholderia pseudomallei contact-dependent growth inhibition (CDI) systems Mol. Microbiol. 84 2012 516 529
26. T. Ogawa, K. Tomita, T. Ueda, K. Watanabe, T. Uozumi, and H. Masaki A cytotoxic ribonuclease targeting specific transfer RNA anticodons Science 283 1999 2097 2100
27. A. Pérez, D. Canle, C. Latasa, M. Poza, A. Beceiro, Mdel.M. Tomás, A. Fernández, S. Mallo, S. Pérez, and F. Molina et al. Cloning, nucleotide sequencing, and analysis of the AcrAB-TolC efflux pump of Enterobacter cloacae and determination of its involvement in antibiotic resistance in a clinical isolate Antimicrob. Agents Chemother. 51 2007 3247 3253
28. A. Pingoud, and A. Jeltsch Structure and function of type II restriction endonucleases Nucleic Acids Res. 29 2001 3705 3727
29. S.J. Poole, E.J. Diner, S.K. Aoki, B.A. Braaten, C. t'Kint de Roodenbeke, D.A. Low, and C.S. Hayes Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems PLoS Genet. 7 2011 e1002217
30. R.M. Richardson, X. Parés, and C.M. Cuchillo Chemical modification by pyridoxal 5′-phosphate and cyclohexane-1,2-dione indicates that Lys-7 and Arg-10 are involved in the p2 phosphate-binding subsite of bovine pancreatic ribonuclease A Biochem. J. 267 1990 593 599
31. M.A. Riley Positive selection for colicin diversity in bacteria Mol. Biol. Evol. 10 1993 1048 1059
32. M.A. Riley, and D.M. Gordon A survey of Col plasmids in natural isolates of Escherichia coli and an investigation into the stability of Col-plasmid lineages J. Gen. Microbiol. 138 1992 1345 1352
33. C.M. Rojas, J.H. Ham, W.L. Deng, J.J. Doyle, and A. Collmer HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings Proc. Natl. Acad. Sci. USA 99 2002 13142 13147
34. C.M. Rojas, J.H. Ham, L.M. Schechter, J.F. Kim, S.V. Beer, and A. Collmer The Erwinia chrysanthemi EC16 hrp/hrc gene cluster encodes an active Hrp type III secretion system that is flanked by virulence genes functionally unrelated to the Hrp system Mol. Plant Microbe Interact. 17 2004 644 653
35. Z.C. Ruhe, D.A. Low, and C.S. Hayes Bacterial contact-dependent growth inhibition Trends Microbiol. 21 2013 230 237
36. Z.C. Ruhe, A.B. Wallace, D.A. Low, and C.S. Hayes Receptor polymorphism restricts contact-dependent growth inhibition to members of the same species MBio. 4 2013 e00480-13
37. K. Schaller, and M. Nomura Colicin E2 is DNA endonuclease Proc. Natl. Acad. Sci. USA 73 1976 3989 3993
38. B.W. Senior, and I.B. Holland Effect of colicin E3 upon the 30S ribosomal subunit of Escherichia coli Proc. Natl. Acad. Sci. USA 68 1971 959 963
39. J.M. Silverman, Y.R. Brunet, E. Cascales, and J.D. Mougous Structure and regulation of the type VI secretion system Annu. Rev. Microbiol. 66 2012 453 472
40. S. Soelaiman, K. Jakes, N. Wu, C. Li, and M. Shoham Crystal structure of colicin E3: implications for cell entry and ribosome inactivation Mol. Cell 8 2001 1053 1062
41. Y. Tan, and M.A. Riley Positive selection and recombination: major molecular mechanisms in colicin diversification Trends Ecol. Evol. 12 1997 348 351
42. D. Walker, L. Lancaster, R. James, and C. Kleanthous Identification of the catalytic motif of the microbial ribosome inactivating cytotoxin colicin E3 Protein Sci. 13 2004 1603 1611
43. J.S. Webb, K.C. Nikolakakis, J.L. Willett, S.K. Aoki, C.S. Hayes, and D.A. Low Delivery of CdiA nuclease toxins into target cells during contact-dependent growth inhibition PLoS ONE 8 2013 e57609
44. D. Zhang, L.M. Iyer, and L. Aravind A novel immunity system for bacterial nucleic acid degrading toxins and its recruitment in various eukaryotic and DNA viral systems Nucleic Acids Res. 39 2011 4532 4552
45. D. Zhang, R.F. de Souza, V. Anantharaman, L.M. Iyer, and L. Aravind Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics Biol. Direct 7 2012 18
46. J. Zheng, B. Ho, and J.J. Mekalanos Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae PLoS ONE 6 2011 e23876