The antibacterial toxin colicin N binds to the inner core of lipopolysaccharide and close to its translocator protein

Molecular Microbiology

Volumn 92, Issue 3, 2014, Pages 440-452

  Johnson, Christopher L ^a   Ridley, Helen ^a   Marchetti, Roberta ^b   Silipo, Alba ^b   Griffin, David C ^c   Crawford, Lucy ^a   Bonev, Boyan ^c   Molinaro, Antonio ^b   Lakey, Jeremy H ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLICIN N; LIPOPOLYSACCHARIDE; OLIGOSACCHARIDE; OUTER MEMBRANE PROTEIN F; COLICIN; PORIN; PROTEIN BINDING;

ARTICLE; BACTERIAL CELL; BINDING AFFINITY; BINDING SITE; CELL ASSAY; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN TRANSPORT; RECEPTOR BINDING DOMAIN; CALORIMETRY; ESCHERICHIA COLI; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

ESCHERICHIA COLI;

CALORIMETRY; COLICINS; ESCHERICHIA COLI; LIPOPOLYSACCHARIDES; MAGNETIC RESONANCE SPECTROSCOPY; PORINS; PROTEIN BINDING;

EID: 84899629137     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12568     Document Type: Article

References (55)

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. Baboolal, T.G., Conroy, M.J., Gill, K., Ridley, H., Visudtiphole, V., Bullough, P.A., and Lakey, J.H. (2008) Colicin N binds to the periphery of its receptor and translocator, outer membrane protein F. Structure 16: 371-379.
4. Blume, A., and Garidel, P. (1999) Lipid model membranes and biomembranes. In From Macromolecules to Man. Kemp, R.B. (ed.). Amsterdam: Elsevier, pp. 109-173.
5. Bonev, B.B., Breukink, E., Swiezewska, E., De Kruijff, B., and Watts, A. (2004) Targeting extracellular pyrophosphates underpins the high selectivity of nisin. FASEB J 18: 1862-1869.
6. Bourdineaud, J.P., Boulanger, P., Lazdunski, C., and Letellier, L. (1990a) 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.
7. Bourdineaud, J.P., Fierobe, H.P., Lazdunski, C., and Pages, J.M. (1990b) Involvement of OmpF during reception and translocation steps of colicin N entry. Mol Microbiol 4: 1737-1743.
8. Brandenburg, K., David, A., Howe, J., Koch, M.H., Andra, J., and Garidel, P. (2005) Temperature dependence of the binding of endotoxins to the polycationic peptides polymyxin B and its nonapeptide. Biophys J 88: 1845-1858.
9. 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.
10. Cascales, E., Buchanan, S.K., Duche, D., Kleanthous, C., Lloubes, R., Postle, K., etal. (2007) Colicin biology. Microbiol Mol Biol Rev 71: 158-229.
11. Ciesielski, F., Griffin, D.C., Rittig, M., and Bonev, B.B. (2009) High-resolution J-coupled C-13 MAS NMR spectroscopy of lipid membranes. Chem Phys Lipids 161: 77-85.
12. Ciesielski, F., Griffin, D.C., Rittig, M., Moriyón, I., and Bonev, B.B. (2013) Interactions of lipopolysaccharide with lipid membranes, raft models - a solid state NMR study. Biochim Biophys Acta 1828: 1731-1742.
13. 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.
14. Cowan, S.W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Paupit, R.A., etal. (1992) Crystal structures explain functional properties of two E.coli porins. Nature 358: 727-733.
15. Dertli, E., Colquhoun, I.J., Gunning, A.P., Bongaerts, R.J., Le Gall, G., Bonev, B.B., etal. (2013) Structure and biosynthesis of two exopolysaccharides produced by Lactobacillus johnsonii FI9785. J Biol Chem 288: 31938-31951.
16. Duché, D., Parker, M.W., Gonzaléz-Mañas, J.M., Pattus, F., and Baty, D. (1994) Uncoupled steps of the colicin A pore formation demonstrated by disulfide bond engineering. J Biol Chem 269: 6332-6339.
17. 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.
18. 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.
19. 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.
20. Evans, L.J., 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.
21. 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.
22. 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.
23. Frirdich, E., and Whitfield, C. (2005) Lipopolysaccharide inner core oligosaccharide structure and outer membrane stability in human pathogens belonging to the Enterobacteriaceae. J Endotoxin Res 11: 133-144.
24. Fung, B.M., Khitrin, A.K., and Ermolaev, K. (2000) An improved broadband decoupling sequence for liquid crystals and solids. J Magn Reson 142: 97-101.
25. Garidel, P., Howe, J., and Brandenburg, K. (2008) Thermodynamic analysis of the interaction of lipopolysaccharides with cationic compounds. Eng Life Sci 8: 523-529.
26. Hazes, B., and Dijkstra, B.W. (1988) Model-building of disulfide bonds in proteins with known 3-dimensional structure. Protein Eng 2: 119-125.
27. Heerklotz, H. (2004) The microcalorimetry of lipid membranes. J Phys Condens Matter 16: R441-R467.
28. Holzenburg, A., Engel, A., Kessler, R., Manz, H.J., Lustig, A., and Aebi, U. (1989) Rapid isolation of Ompf porin LPS complexes suitable for structure-function studies. Biochemistry 28: 4187-4193.
29. Housden, N.G., and Kleanthous, C. (2012) Colicin translocation across the Escherichia coli outer membrane. Biochem Soc Trans 40: 1475-1479.
30. 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.
31. Housden, N.G., Wojdyla, J.A., Korczynska, J., Grishkovskaya, I., Kirkpatrick, N., Brzozowski, A.M., and Kleanthous, C. (2010) Directed epitope delivery across the Escherichia coli outer membrane through the porin OmpF. Proc Natl Acad Sci USA 107: 21412-21417.
32. Housden, N.G., Hopper, J.T.S., Lukoyanova, N., Rodriguez-Larrea, D., Wojdyla, J.A., Klein, A., etal. (2013) Intrinsically disordered protein threads through the bacterial outer-membrane porin OmpF. Science 340: 1570-1574.
33. Jakes, K.S., and Cramer, W.A. (2012) Border crossings: colicins and transporters. Annu Rev Genet 46: 209-231.
34. Jakes, K.S., and Finkelstein, A. (2010) The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Mol Microbiol 75: 567-578.
35. Johnson, C.L., Ridley, H., Pengelly, R.J., Salleh, M.Z., and Lakey, J.H. (2013) The unstructured domain of colicin N kills Escherichia coli. Mol Microbiol 89: 84-95.
36. Klein, G., Mueller-Loennies, S., Lindner, B., Kobylak, N., Brade, H., and Raina, S. (2013) Molecular and structural basis of inner core lipopolysaccharide alterations in Escherichia coli: incorporation of glucuronic acid and phosphoethanolamine in the heptose region. J Biol Chem 288: 8111-8127.
37. Kurisu, G., Zakharov, S.D., Zhalnina, M.V., Bano, S., Eroukova, V.Y., Rokitskaya, T.I., etal. (2003) The structure of BtuB with bound colicin E3 R-domain implies a translocon. Nat Struct Biol 10: 948-954.
38. Le Brun, A.P., Clifton, L.A., Halbert, C.E., Lin, B., Meron, M., Holden, P.J., etal. (2013) Structural characterization of a model gram-negative bacterial surface using lipopolysaccharides from rough strains of Escherichia coli. Biomacromolecules 14: 2014-2022.
39. Lindberg, A.A., and Hellerqvist, C.G. (1971) Bacteriophage attachment sites, serological specificity, and chemical composition of the lipopolysaccharides of semirough and rough mutants of Salmonella typhimurium. J Bacteriol 105: 57-64.
40. Mayer, M., and Meyer, B. (1999) Characterization of ligand binding by saturation transfer difference NMR spectroscopy. Angew Chem Int Ed Engl 38: 1784-1788.
41. Molinaro, A., De Castro, C., Lanzetta, R., Evidente, A., Parrilli, M., and Holst, O. (2002) Lipopolysaccharides possessing two L-glycero-D-manno-heptopyranosyl-alpha-(1->5)-3-deoxy-D-manno-oct-2-ulopyranosonic acid moieties in the core region - the structure of the core region of the lipopolysaccharides from Burkholderia caryophylli. J Biol Chem 277: 10058-10063.
42. Muller-Loennies, S., Holst, O., Lindner, B., and Brade, H. (1999) Isolation and structural analysis of phosphorylated oligosaccharides obtained from Escherichia coli J-5 lipopolysaccharide. Eur J Biochem 260: 235-249.
43. Parisot, J.L., Carey, S., Breukink, E., Chan, W.C., Narbad, A., and Bonev, B. (2008) Molecular mechanism of target recognition by subtilin, a class I lanthionine antibiotic. Antimicrob Agents Chemother 52: 612-618.
44. Park, B.S., Song, D.H., Kim, H.M., Choi, B.S., Lee, H., and Lee, J.O. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458: 1191-U1130.
45. Penfold, C.N., Garinot-Schneider, C., Hemmings, A.M., Moore, G.R., Kleanthous, C., and James, R. (2000) A 76-residue polypeptide of colicin E9 confers receptor specificity and inhibits the growth of vitamin B12-dependent Escherichia coli 113/3 cells. Mol Microbiol 38: 639-649.
46. Pilsl, H., Smajs, D., and Braun, V. (1999) Characterization of colicin S4 and its receptor, OmpW, a minor protein of the Escherichia coli outer membrane. J Bacteriol 181: 3578-3581.
47. 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.
48. Qimron, U., Marintcheva, B., Tabor, S., and Richardson, C.C. (2006) Genomewide screens for Escherichia coli genes affecting growth of T7 bacteriophage. Proc Natl Acad Sci USA 103: 19039-19044.
49. Raetz, C.R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635-700.
50. Sanghera, N., Correia, B.E.F.S., Correia, J.R.S., Ludwig, C., Agarwal, S., Nakamura, H.K., etal. (2011) Deciphering the molecular details for the binding of the prion protein to main ganglioside GM1 of neuronal membranes. Chem Biol 18: 1422-1431.
51. 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.
52. 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.
53. Soelaiman, S., Jakes, K., Wu, N., Li, C.M., and Shoham, M. (2001) Crystal structure of colicin E3: implications for cell entry and ribosome inactivation. Mol Cell 8: 1053-1062.
54. 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 38: 389-392.
55. Vetter, I.R., Parker, M.W., Tucker, A.D., Lakey, J.H., Pattus, F., and Tsernoglou, D. (1998) Crystal structure of a colicin N fragment suggests a model for toxicity. Structure 6: 863-874.