The unstructured domain of colicin N kills Escherichia coli

Molecular Microbiology

Volumn 89, Issue 1, 2013, Pages 84-95

  Johnson, Christopher L ^a   Ridley, Helen ^a   Pengelly, Robert J ^a   Salleh, Mohd Zulkifli ^a   Lakey, Jeremy H ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLICIN N; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN F; POLYPEPTIDE ANTIBIOTIC AGENT; TOLA PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DRUG TARGETING; ESCHERICHIA COLI; MEMBRANE BINDING; MEMBRANE DAMAGE; MEMBRANE PERMEABILITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROCESSING;

CELL MEMBRANE; COLICINS; DNA MUTATIONAL ANALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MICROBIAL VIABILITY; PORINS; PROTEIN STRUCTURE, TERTIARY;

ESCHERICHIA COLI; GOSSWEILERODENDRON BALSAMIFERUM;

EID: 84879507354     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12260     Document Type: Article

References (53)

1. Arnold, T., Zeth, K., and Linke, D. (2009) Structure and function of colicin S4, a colicin with a duplicated receptor-binding domain. J Biol Chem 284: 6403-6413.
2. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006-0008.
3. Benedetti, H., Frenette, M., Baty, D., Knibiehler, M., Pattus, F., and Lazdunski, C. (1991) Individual domains of colicins confer specificity in colicin uptake, in pore-properties and in immunity requirement. J Mol Biol 217: 429-439.
4. Bourdineaud, J.P., Boulanger, P., Lazdunski, C., and Letellier, L. (1990) In vivo properties of colicin A: channel activity is voltage dependent but translocation may be voltage independent. Proc Natl Acad Sci USA 87: 1037-1041.
5. Braun, V., Patzer, S.I., and Hantke, K. (2002) Ton-dependent colicins and microcins: modular design and evolution. Biochimie 84: 365-380.
6. Brogden, K.A. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3: 238-250.
7. Buchanan, S.K., Lukacik, P., Grizot, S., Ghirlando, R., Ali, M.M., Barnard, T.J., etal. (2007) Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. EMBO J 26: 2594-2604.
8. Cascales, E., Buchanan, S.K., Duche, D., Kleanthous, C., Lloubes, R., Postle, K., etal. (2007) Colicin biology. Microbiol Mol Biol Rev 71: 158-229.
9. Clifton, L.A., Johnson, C.L., Solovyova, A.S., Callow, P., Weiss, K.L., Ridley, H., etal. (2012) Low resolution structure and dynamics of a colicin-receptor complex determined by neutron scattering. J Biol Chem 287: 337-346.
10. Csonka, L.N., and Hanson, A.D. (1991) Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol 45: 569-606.
11. Dunker, A.K., and Kriwacki, R.W. (2011) The orderly chaos of proteins. Sci Am 304: 68-73.
12. Duquesne, S., Destoumieux-Garzon, D., Peduzzi, J., and Rebuffat, S. (2007) Microcins, gene-encoded antibacterial peptides from enterobacteria. Nat Prod Rep 24: 708-734.
13. El Kouhen, R., and Pages, J.M. (1996) Dynamic aspects of colicin N translocation through the Escherichia coli outer membrane. J Bacteriol 178: 5316-5319.
14. El Kouhen, R., Fierobe, H., Scianimanico, S., Steiert, M., Pattus, F., and Pages, J.M. (1993) Characterization of the receptor and translocator domains of colicin N. Eur J Biochem 214: 635-639.
15. Evans, L.J., Cooper, A., and Lakey, J.H. (1996a) Direct measurement of the association of a protein with a family of membrane receptors. J Mol Biol 255: 559-563.
16. Evans, L.J.A., Labeit, S., Cooper, A., Bond, L.H., and Lakey, J.H. (1996b) The central domain of colicin N possesses the receptor recognition site but not the binding affinity of the whole toxin. Biochemistry 35: 15143-15148.
17. Fourel, D., Hikita, C., Bolla, J.M., Mizushima, S., and Pages, J.M. (1990) Characterization of ompF domains involved in Escherichia coli K-12 sensitivity to colicins A and N. J Bacteriol 172: 3675-3680.
18. Fridd, S.L., Gokce, I., and Lakey, J.H. (2002) High level expression of His-tagged colicin pore-forming domains and reflections on the sites for pore formation in the inner membrane. Biochimie 84: 477-483.
19. Fuxreiter, M., Simon, I., Friedrich, P., and Tompa, P. (2004) Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J Mol Biol 338: 1015-1026.
20. Garinot-Schneider, C., Pommer, A.J., Moore, G.R., Kleanthous, C., and James, R. (1996) Identification of putative active-site residues in the DNase domain of colicin E9 by random mutagenesis. J Mol Biol 260: 731-742.
21. Garner, E., Cannon, P., Romero, P., Obradovic, Z., and Dunker, A.K. (1998) Predicting disordered regions from amino acid sequence: common themes despite differing structural characterization. Genome Inform Ser Workshop Genome Inform 9: 201-213.
22. Gerding, M.A., Ogata, Y., Pecora, N.D., Niki, H., and de Boer, P.A. (2007) The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol Microbiol 63: 1008-1025.
23. Gillor, O., Kirkup, B.C., and Riley, M.A. (2004) Colicins and microcins: the next generation antimicrobials. Adv Appl Microbiol 54: 129-146.
24. Gordon, D.M., and O'Brien, C.L. (2006) Bacteriocin diversity and the frequency of multiple bacteriocin production in Escherichia coli. Microbiology 152: 3239-3244.
25. Hecht, O., Ridley, H., Lakey, J.H., and Moore, G.R. (2009) A common interaction for the entry of colicin N and filamentous phage into Escherichia coli. J Mol Biol 388: 880-893.
26. Heddle, J.G., Blance, S.J., Zamble, D.B., Hollfelder, F., Miller, D.A., Wentzell, L.M., etal. (2001) The antibiotic microcin B17 is a DNA gyrase poison: characterisation of the mode of inhibition. J Mol Biol 307: 1223-1234.
27. Housden, N.G., Loftus, S.R., Moore, G.R., James, R., and Kleanthous, C. (2005) Cell entry mechanism of enzymatic bacterial colicins: porin recruitment and the thermodynamics of receptor binding. Proc Natl Acad Sci USA 102: 13849-13854.
28. Housden, N.G., Wojdyla, J.A., Korczynska, J., Grishkovskaya, I., Kirkpatrick, N., Brzozowski, A.M., and Kleanthous, C. (2011) Directed epitope delivery across the Escherichia coli outer membrane through the porin OmpF. Proc Natl Acad Sci USA 107: 21412-21417.
29. Jakes, K.S., and Finkelstein, A. (2010) The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Mol Microbiol 75: 567-578.
30. Johnson, T.J., Johnson, S.J., and Nolan, L.K. (2006) Complete DNA sequence of a ColBM plasmid from avian pathogenic Escherichia coli suggests that it evolved from closely related ColV virulence plasmids. J Bacteriol 188: 5975-5983.
31. Kleanthous, C. (2010) Swimming against the tide: progress and challenges in our understanding of colicin translocation. Nat Rev Microbiol 8: 843-848.
32. Konisky, J., and Cowell, B.S. (1972) Interaction of colicin Ia with bacterial cells. Direct measurement of Ia-receptor interaction. J Biol Chem 247: 6524-6529.
33. Lakey, J.H., Watts, J.P., and Lea, E.J. (1985) Characterisation of channels induced in planar bilayer membranes by detergent solubilised Escherichia coli porins. Biochim Biophys Acta 817: 208-216.
34. Li, X., Romero, P., Rani, M., Dunker, A.K., and Obradovic, Z. (1999) Predicting protein disorder for N-, C-, and internal regions. Genome Inform Ser Workshop Genome Inform 10: 30-40.
35. Melo, M.N., Ferre, R., and Castanho, M.A. (2009) Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations. Nat Rev Microbiol 7: 245-250.
36. Meszaros, B., Simon, I., and Dosztanyi, Z. (2011) The expanding view of protein-protein interactions: complexes involving intrinsically disordered proteins. Phys Biol 8: 035003.
37. Oldfield, C.J., Meng, J., Yang, J.Y., Yang, M.Q., Uversky, V.N., and Dunker, A.K. (2008) Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. BMC Genomics 9 (Suppl. 1): S1.
38. Penfold, C.N., Healy, B., Housden, N.G., Boetzel, R., Vankemmelbeke, M., Moore, G.R., etal. (2004) Flexibility in the receptor-binding domain of the enzymatic colicin E9 is required for toxicity against Escherichia coli cells. J Bacteriol 186: 4520-4527.
39. Pugsley, A.P. (1987) Nucleotide sequencing of the structural gene for colicin N reveals homology between the catalytic, C-terminal domains of colicins A and N. Mol Microbiol 1: 317-325.
40. Pugsley, A.P., and Schnaitman, C.A. (1978) Identification of three genes controlling production of new outer membrane pore proteins in Escherichia coli K-12. J Bacteriol 135: 1118-1129.
41. Riley, M.A., and Wertz, J.E. (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56: 117-137.
42. Robinson, N.E., Robinson, A.B., and Merrifield, R.B. (2001) Mass spectrometric evaluation of synthetic peptides as primary structure models for peptide and protein deamidation. J Pept Res 57: 483-493.
43. Rodriguez, E., and Lavina, M. (2003) The proton channel is the minimal structure of ATP synthase necessary and sufficient for microcin h47 antibiotic action. Antimicrob Agents Chemother 47: 181-187.
44. Romero, Obradovic, and Dunker, K. (1997) Sequence data analysis for long disordered regions prediction in the Calcineurin family. Genome Inform Ser Workshop Genome Inform 8: 110-124.
45. Romero, P., Obradovic, Z., Li, X., Garner, E.C., Brown, C.J., and Dunker, A.K. (2001) Sequence complexity of disordered protein. Proteins 42: 38-48.
46. Sharma, O., Yamashita, E., Zhalnina, M.V., Zakharov, S.D., Datsenko, K.A., Wanner, B.L., and Cramer, W.A. (2007) Structure of the complex of the colicin E2 R-domain and its BtuB receptor. The outer membrane colicin translocon. J Biol Chem 282: 23163-23170.
47. Sharma, O., Datsenko, K.A., Ess, S.C., Zhalnina, M.V., Wanner, B.L., and Cramer, W.A. (2009) Genome-wide screens: novel mechanisms in colicin import and cytotoxicity. Mol Microbiol 73: 571-585.
48. Sodergren, E.J., Davidson, J., Taylor, R.K., and Silhavy, T.J. (1985) Selection for mutants altered in the expression or export of outer membrane porin OmpF. J Bacteriol 162: 1047-1053.
49. Stora, T., Lakey, J.H., and Vogel, H. (1999) Ion-channel gating in transmembrane receptor proteins: functional activity in tethered lipid membranes. Angew Chem Int Ed Engl 38: 389-392.
50. Strahsburger, E., Baeza, M., Monasterio, O., and Lagos, R. (2005) Cooperative uptake of microcin E492 by receptors FepA, Fiu, and Cir and inhibition by the siderophore enterochelin and its dimeric and trimeric hydrolysis products. Antimicrob Agents Chemother 49: 3083-3086.
51. Strom, M.B., Haug, B.E., Skar, M.L., Stensen, W., Stiberg, T., and Svendsen, J.S. (2003) The pharmacophore of short cationic antibacterial peptides. J Med Chem 46: 1567-1570.
52. Udho, E., Jakes, K.S., Buchanan, S.K., James, K.J., Jiang, X., Klebba, P.E., and Finkelstein, A. (2009) Reconstitution of bacterial outer membrane TonB-dependent transporters in planar lipid bilayer membranes. Proc Natl Acad Sci USA 106: 21990-21995.
53. Yang, C.C., and Konisky, J. (1984) Colicin V-treated Escherichia coli does not generate membrane potential. J Bacteriol 158: 757-759.