Discovery of critical Tol A-binding residues in the bactericidal toxin colicin N: A biophysical approach

Molecular Microbiology

Volumn 28, Issue 6, 1998, Pages 1335-1343

  Raggett, Elaine M ^a   Bainbridge, Graeme ^a   Evans, Lucy J A ^a   Cooper, Alan ^b   Lakey, Jeremy H ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIUM PROTEIN TOL A; COLICIN N; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; ESCHERICHIA COLI; FLUORESCENCE; MICROCALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BIOPHYSICS; CALORIMETRY; CIRCULAR DICHROISM; COLICINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PORINS; THERMODYNAMICS; TRYPTOPHAN;

BACTERIA (MICROORGANISMS); ENTEROBACTERIA PHAGE FD; ESCHERICHIA COLI; GOSSWEILERODENDRON BALSAMIFERUM; NEGIBACTERIA;

EID: 0031799096     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.00899.x     Document Type: Article

References (45)

1. Benedetti, H., Lazdunski, C., and Lloubes, R. (1991) Protein import into Escherichia coli: colicins A and E1 interact with a component of their translocation system. EMBO J 10: 1989-1995.
2. Benedetti, H., Lloubes, R., Lazdunski, C., and Letellier, L. (1992) Colicin A unfolds during its translocation in Escherichia coli cells and spans the whole cell envelope when its pore has formed. EMBO J 11: 441-447.
3. Bouveret, E., Rigal, A., Lazdunski, C., and Benedetti, H. (1997) The N-terminal domain of colicin E3 interacts with ToIB which is involved in the colicin translocation step. Mol Microbiol 23: 909-920.
4. Bouveret, E., Rigal, A., Lazdunski, C., and Benedetti, H. (1998) Distinct regions of the colicin A translocation domain are involved in the interaction with TolA and TolB proteins upon import into Escherichia coli. Mol Microbiol 27: 143-157.
5. Connelly, P.R., Varadarajan, R., Sturtevant, J.M., and Richards, F.M. (1990) Thermodynamics of protein peptide interactions in the ribonuclease S system studied by titration microcalorimetry. Biochemistry 29: 6108-6114.
6. Cooper, A., and Johnson, C.M. (1994) Isothermal titration calorimetry. In Microscopy, Optical Spectroscopy, and Macroscopic Techniques. Jones, C., Mulloy, B., and Thomas, A.H. (eds). pp. 137-150. Totowa, NJ: Humana Press.
7. Davies, J.K., and Reeves, P. (1975) Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group A. J Bacteriol 123: 102-117.
8. Derouiche, R., Gavioli, M., Benedetti, H., Prilipov, A., Lazdunski, C., and Lloubes, R. (1996) TolA central domain interacts with Escherichia coli porins. EMBO J 15: 6408-6415.
9. Derouiche, R., Zeder-Lutz, G., Benedetti, H., Gavioli, M., Rigal, A., Lazdunski, C., et al. (1997) Binding of colicins A and E1 to purified TolA domains. Microbiology 143: 3185-3192.
10. Dill, K.A. (1997) Additivity principles in biochemistry. J Biol Chem 272: 701-704.
11. 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.
12. El-Kouhen, R., Fierobe, H.P., 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.
13. Escuyer, V., and Mock, M. (1987) DNA-sequence analysis of 3 missense mutations affecting colicin-E3 bactericidal activity. Mol Microbiol 1: 82-85.
14. Evans, L.J.A., Labeit, S., Cooper, A., Bond, L.H., and Lakey, J.H. (1996a) The central domain of colicin N possesses the receptor recognition site but not the binding affinity of the whole toxin. Biochemistry 35: 15143-15148.
15. Evans, L.J.A., Cooper, A., and Lakey, J.H. (1996b) Direct measurement of the association of a protein with a family of membrane receptors. J Mol Biol 255: 559-563.
16. Garavito, R.M., and Rosenbusch, J.P. (1986) Isolation and crystallisation of bacterial porin. Methods Enzymol 125: 309-315.
17. Garinot-Schneider, C., Penfold, C.N., Moore, G.R., Kleanthous, C., and James, R. (1997) Identification of residues in the putative TolA box which are essential for the toxicity of the endonuclease toxin colicin E9. Microbiology 143: 2931-2938.
18. Graziano, G., Catazano, F., Giancola, C., and Barone, G. (1996) DSC study of the thermal stability of S-protein and S-protein/S-peptide complexes. Biochemistry 35: 13386-13392.
19. Guihard, G., Boulanger, P., Benedetti, H., Lloubes, R., Besnard, M., and Letellier, L. (1994) Colicin A and the ToI proteins involved in its translocation are preferentially located in the contact sites between the inner and outer membranes of Escherichia coli cells. J Biol Chem 269: 5874-5880.
20. Hearn, R.P., Richards, F.M., Sturtevant, J.M., and Watt, G.D. (1971) The thermodynamics of the binding of S-peptide to S-protein to form ribonuclease S′. Biochemistry 10: 806-817.
21. Holliger, P., and Riechmann, L. (1997) A conserved infection pathway for filamentous bacteriophages is suggested by the structure of the membrane penetration domain of the minor coat protein g3p from phage fd. Structure 5: 265-275.
22. Jakes, K.S., Davis, N.G., and Zinder, N.D. (1988) A hybrid toxin from bacteriophage f1 attachment protein and colicin E3 has altered cell receptor specificity. J Bacteriol 170: 4231-4238.
23. Johnson, Jr, W. (1990) Protein secondary structure and circular dichroism: a practical guide. Proteins 7: 205-214.
24. Lakey, J.H., van der Goot, F.G., and Pattus, F. (1994) All in the family: the toxic activity of colicins. Toxicology 87: 85-108.
25. Lakey, J.H., Watts, J.P., and Lea, E.J.A. (1985) Characterization of channels induced in planar bilayer-membranes by detergent solubilized Escherichia coli porins. Biochim Biophys Acta 817: 208-216.
26. Lehrer, S.S. (1971) Solute perturbation of protein fluorescence. The quenching of the tryptophyl fluorescence of model compounds and of lysozyme by iodide ions. Biochemistry 10: 3254-3263.
27. Levengood, S.K., Beyer, W.J., and Webster, R.E. (1991) TolA: a membrane protein involved in colicin uptake contains an extended helical region. Proc Natl Acad Sci USA 88: 5939-5943.
28. MacMillan-Crow, L.A., and Lincoln, T.M. (1994) High-affinity binding and localisation of the cyclic GMP-dependent protein kinase with the intermediate filament protein vimentin. Biochemistry 33: 8035-8043.
29. Minn, A.J., Velez, P., Schendel, S.L., Liang, H., Muchmore, S.W., Fesik, S.W., et al. (1997) Bcl-x (L) forms an ion channel in synthetic lipid membranes. Nature 385: 353-357.
30. Pilsl, H., and Braun, V. (1995) Novel colicin-10 - assignment of 4 domains to tonb-dependent and tolc-dependent uptake via the tsx receptor and to pore formation. Mol Microbiol 16: 57-67.
31. Politou, A.S., Gautel, M., Pfuhl, M., Labeit, S., and Pastore, A. (1994) Immunoglobulin-type domains of titin - same fold, different stability. Biochemistry 33: 4730-4737.
32. 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 B. Mol Microbiol 1: 317-325.
33. Rakin, A., Boolgakowa, E., and Heesemann, J. (1996) Structural and functional organization of the Yersinia pestis bacteriocin pesticin gene cluster. Microbiology 142: 3415-3424.
34. Riechmann, L., and Holliger, P. (1997) The C-terminal domain of TolA is the coreceptor for filamentous phage infection of E. coli. Cell 90: 351-360.
35. Salwinski, L., Levinthal, C., Levinthal, F., and Hubbell, W.L. (1993) Site-directed spin labeling studies of colicin-e1 - interactions between the C and N-terminal domains and some topological features of the membrane-bound state. Biophys J 64: 183.
36. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
37. Sarkar, G., and Sommer, S.S. (1990) The megaprimer method of site-directed mutagenesis. BioTechniques 8: 404-407.
38. Schendel, S.L., Click, E.M., Webster, R.E., and Cramer, W.A. (1997) The TolA protein interacts with colicin E1 differently than with other group A colicins. J Bacteriol 179: 3683-3690.
39. Sturtevant, J.M. (1994) The thermodynamic effects of protein mutations. Curr Opin Struct Biol 4: 69-78.
40. Tan, Y., and Riley, M.A. (1996) Rapid invasion by colicinogenic Escherichia coli novel immunity functions. Microbiology 142: 2175-2180.
41. Varadarajan, R., Connelly, P.R., Sturtevant, J.M., and Richards, F.M. (1992) Heat capacity changes for peptide-protein interactions in the ribonuclease S system. Biochemistry 31: 1421-1436.
42. Vetter, I.R., Parker, M.W., Pattus, P., and Tsernoglou, D. (1996) Insights into membrane insertion based on studies of colicins. In Protein Toxin Structure. Parker, M.W. (ed.). pp. 5-24.Austin TX: R.G. Landes Company.
43. Webster, R.E. (1991) The tol gene products and the import of macromolecules into Escherichia coli. Mol Microbiol 5: 1005-1011.
44. Wiener, M., Freymann, D., Ghosh, P., and Stroud, R.M. (1997) Crystal structure of colicin la. Nature 385: 461-464.
45. Wiseman, T., Williston, S., Brandts, J.F., and Lin, L.-N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179: 131-137.