Fluoresceination of FepA during colicin B killing: Effects of temperature, toxin and TonB

Molecular Microbiology

Volumn 72, Issue 5, 2009, Pages 1171-1180

  Smallwood, Chuck R ^a   Marco, Amparo Gala ^a   Xiao, Qiaobin ^a   Trinh, Vy ^a   Newton, Salete M C ^a   Klebba, Phillip E ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCIN; BOVINE SERUM ALBUMIN; COLICIN B; FLUORESCEIN DERIVATIVE; OUTER MEMBRANE PROTEIN; PROTEIN FEPA; PROTEIN TONB; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERICIDAL ACTIVITY; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; GENE LOCUS; GENETIC ENGINEERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; STEREOSPECIFICITY; TEMPERATURE DEPENDENCE;

BACTERIAL OUTER MEMBRANE PROTEINS; CARRIER PROTEINS; COLICINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCEINS; FLUORESCENCE; MEMBRANE PROTEINS; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE; TEMPERATURE;

BOVINAE; ESCHERICHIA COLI;

EID: 65949115310     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06715.x     Document Type: Article

References (55)

1. Ames, G.F. (1974) Resolution of bacterial proteins by polyacrylamide electrophoresis on slabs: membrane, soluble and periplasmic fractions. J Biol Chem 249 : 634 644.
2. Annamalai, R., Jin, B., Cao, Z., Newton, S.M. Klebba, P.E. (2004) Recognition of ferric catecholates by FepA. J Bacteriol 186 : 3578 3589. (Pubitemid 38661556)
3. Benedetti, H., Lloubes, R., Lazdunski, C. 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.
4. Bouveret, E., Benedetti, H., Rigal, A., Loret, E. Lazdunski, C. (1999) In vitro characterization of peptidoglycan-associated lipoprotein (PAL)- peptidoglycan and PAL-TolB interactions. J Bacteriol 181 : 6306 6311. (Pubitemid 29512939)
5. Bradbeer, C. (1993) The proton motive force drives the outer membrane transport of cobalamin in Escherichia coli. J Bacteriol 175 : 3146 3150. (Pubitemid 23148752)
6. Buchanan, S.K., Smith, B.S., Venkatramani, L., Xia, D., Esser, L., Palnitkar, M., et al. (1999) Crystal structure of the outer membrane active transporter FepA from Escherichia coli[see comments]. Nat Struct Biol 6 : 56 63. (Pubitemid 29232425)
7. Buchanan, S.K., Lukacik, P., Grizot, S., Ghirlando, R., Ali, M.M., Barnard, T.J., et al. (2007) Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. EMBO J 26 : 2594 2604. (Pubitemid 46788319)
8. Cao, Z. Klebba, P.E. (2002) Mechanisms of colicin binding and transport through outer membrane porins. Biochimie 84 : 399 412. (Pubitemid 35350870)
9. Cao, Z., Qi, Z., Sprencel, C., Newton, S.M. Klebba, P.E. (2000) Aromatic components of two ferric enterobactin binding sites in Escherichia coli fepA. Mol Microbiol 37 : 1306 1317.
10. Cao, Z., Warfel, P., Newton, S.M. Klebba, P.E. (2003) Spectroscopic observations of ferric enterobactin transport. J Biol Chem 278 : 1022 1028. (Pubitemid 36790780)
11. Cascales, E. Lloubes, R. (2004) Deletion analyses of the peptidoglycan-associated lipoprotein Pal reveals three independent binding sequences including a TolA box. Mol Microbiol 51 : 873 885. (Pubitemid 38233951)
12. Cowan, S.W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R.A., et al. (1992) Crystal structures explain functional properties of two E. coli porins. Nature 358 : 727 733.
13. Davies, J.K. Reeves, P. (1975) Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group B. J Bacteriol 123 : 96 101.
14. Devanathan, S. Postle, K. (2007) Studies on colicin B translocation: FepA is gated by TonB. Mol Microbiol 65 : 441 453. (Pubitemid 47052733)
15. Ferguson, A.D., Hofmann, E., Coulton, J.W., Diederichs, K. Welte, W. (1998) Siderophoremediated iron transport: crystal structure of FhuA with bound lipopolysaccharide [see comments]. Science 282 : 2215 2220. (Pubitemid 29004062)
16. Ferguson, A.D., Chakraborty, R., Smith, B.S., Esser, L., van der Helm, D. Deisenhofer, J. (2002) Structural basis of gating by the outer membrane transporter FecA. Science 295 : 1715 1719. (Pubitemid 34202907)
17. Gerding, M.A., Ogata, Y., Pecora, N.D., Niki, H. 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. (Pubitemid 46188263)
18. Goemaere, E.L., Cascales, E. Lloubes, R. (2007) Mutational analyses define helix organization and key residues of a bacterial membrane energy-transducing complex. J Mol Biol 366 : 1424 1436. (Pubitemid 46215605)
19. Gumbart, J.C., Wiener, M.C. Tajkhorshid, E. (2007) Mechanics of force propagation in TonB-dependent outer membrane transport. Biophys J 93 : 496 504. (Pubitemid 47057815)
20. Guterman, S.K. Dann, L. (1973) Excretion of enterochelin by exbA and exbB mutants of Escherichia coli. J Bacteriol 114 : 1225 1230.
21. Gutfreund, H. (1995) Kinetics for the Life Sciences: Receptors, Transmitters and Catalysts. Cambridge : Cambridge University Press.
22. Hashimoto-Gotoh, T., Franklin, F.C., Nordheim, A. Timmis, K.N. (1981) Specific-purpose plasmid cloning vectors. I. Low copy number, temperature-sensitive, mobilization-defective pSC101-derived containment vectors. Gene 16 : 227 235.
23. James, K.J., Hancock, M.A., Moreau, V., Molina, F. Coulton, J.W. (2008) TonB induces conformational changes in surface-exposed loops of FhuA, outer membrane receptor of Escherichia coli. Protein Sci 17 : 1679 1688.
24. Jiang, X., Payne, M.A., Cao, Z., Foster, S.B., Feix, J.B., Newton, S.M. Klebba, P.E. (1997) Ligand specific opening of a gated-porin channel in the outer membrane of living bacteria. Science 276 : 1261 1264. (Pubitemid 27227365)
25. Kadner, R.J. McElhaney, G. (1978) Outer membrane-dependent transport systems in Escherichia coli: turnover of TonB function. J Bacteriol 134 : 1020 1029. (Pubitemid 8360914)
26. Kaserer, W.A., Jiang, X., Xiao, Q., Scott, D.C., Bauler, M., Copeland, D., et al. (2008) Insight from TonB hybrid proteins into the mechanism of iron transport through the outer membrane. J Bacteriol 190 : 4001 4016.
27. Liu, J., Rutz, J. M., Klebba, P.E., Feiz, J.B. (1994) A site-directed spin-labeling study of ligand-induced conformational change in the ferric enterobactin receptor, FepA. Biochemistry 33 : 13274 13283. (Pubitemid 24373242)
28. Locher, K.P., Rees, B., Koebnik, R., Mitschler, A., Moulinier, L., Rosenbusch, J.P. Moras, D. (1998) Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95 : 771 778. (Pubitemid 29014457)
29. Luria, S.E. (1964) On the mechanisms of action of colicins. Ann Institute Pasteur (Paris) 107 (Suppl 67 73.
30. Ma, L., Kaserer, W., Annamalai, R., Scott, D.C., Jin, B., Jiang, X., et al. (2007) Evidence of ball-andchain transport of ferric enterobactin through FepA. J Biol Chem 282 : 397 406. (Pubitemid 47076635)
31. McIntosh, M.A. Earhart, C.F. (1976) Effect of iron of the relative abundance of two large polypeptides of the Escherichia coli outer membrane. Biochem Biophys Res Commun 70 : 315 322.
32. Murphy, C.K., Kalve, V.I. Klebba, P.E. (1990) Surface topology of the Escherichia coli K-12 ferric enterobactin receptor. J Bacteriol 172 : 2736 2746. (Pubitemid 20141432)
33. Newton, S.M., Igo, J.D., Scott, D.C. Klebba, P.E. (1999) Effect of loop deletions on the binding and transport of ferric enterobactin by FepA. Mol Microbiol 32 : 1153 1165. (Pubitemid 29286656)
34. Nikaido, H. Rosenberg, E.Y. (1981) Effect on solute size on diffusion rates through the transmembrane pores of the outer membrane of Escherichia coli. J Gen Physiol 77 : 121 135. (Pubitemid 12192985)
35. Nikaido, H. Vaara, M. (1985) Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49 : 1 32. (Pubitemid 15134118)
36. Novo, D., Perlmutter, N.G., Hunt, R.H. Shapiro, H.M. (1999) Accurate flow cytometric membrane potential measurement in bacteria using diethyloxacarbocyanine and a ratiometric technique. Cytometry 35 : 55 63. (Pubitemid 29031192)
37. Pawelek, P.D., Croteau, N., Ng-Thow-Hing, C., Khursigara, C.M., Moiseeva, N., Allaire, M. Coulton, J.W. (2006) Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312 : 1399 1402. (Pubitemid 43839555)
38. Payne, M.A., Igo, J.D., Cao, Z., Foster, S.B., Newton, S.M. Klebba, P.E. (1997) Biphasic binding kinetics between FepA and its ligands. J Biol Chem 272 : 21950 21955. (Pubitemid 27382815)
39. Pommier, S., Gavioli, M., Cascales, E., Lloubes, R. (2005) Tol-Dependent Macromolecule Import through the Escherichia coli Cell Envelope Requires the Presence of an Exposed TolA Binding Motif. J Bacteriol 187 : 7526 7534. (Pubitemid 41507808)
40. Postle, K. (1993) TonB protein and energy transduction between membranes. J Bioenerg Biomembr 25 : 591 601. (Pubitemid 24012892)
41. Pugsley, A.P. Reeves, P. (1976) Iron uptake in colicin B-resistant mutants of Escherichia coli K-12. J Bacteriol 126 : 1052 1062.
42. Pugsley, A.P. Reeves, P. (1977) Uptake of ferrienterochelin by Escherichia coli: energy dependent stage of uptake. J Bacteriol 130 : 26 36. (Pubitemid 8093425)
43. Rabsch, W., Ma, L., Wiley, G., Najar, F.Z., Kaserer, W., Schuerch, D.W., et al. (2007) FepA- and TonB-dependent bacteriophage H8: receptor binding and genomic sequence. J Bacteriol 189 : 5568 5574. (Pubitemid 47206413)
44. Reynolds, P.R., Mottur, G.P. Bradbeer, C. (1980) Transport of vitamin B12 in Escherichia coli. Some observations on the roles of the gene products of BtuC and TonB. J Biol Chem 255 : 4313 4319. (Pubitemid 10051110)
45. Saier, M.H., Jr (2000) Families of proteins forming transmembrane channels. J Membr Biol 175 : 165 180. (Pubitemid 30421888)
46. Scott, D.C., Newton, S.M. Klebba, P.E. (2002) Surface loop motion in FepA. J Bacteriol 184 : 4906 4911.
47. Shultis, D.D., Purdy, M.D., Banchs, C.N. Wiener, M.C. (2006) Outer membrane active transport: structure of the BtuB: TonB complex. Science 312 : 1396 1399. (Pubitemid 43839554)
48. Sims, P.J., Waggoner, A.S., Wang, C.H. Hoffman, J.F. (1974) Studies on the mechanism by which cyanine dyes measure membrane potential in red blood cells and phosphatidylcholine vesicles. Biochemistry 13 : 3315 3330.
49. Suzuki, H., Wang, Z.Y., Yamakoshi, M., Kobayashi, M. Nozawa, T. (2003) Probing the transmembrane potential of bacterial cells by voltage-sensitive dyes. Anal Sci 19 : 1239 1242.
50. Takeshita, S., Sato, M., Toba, M., Masahashi, W. Hashimoto-Gotoh, T. (1987) High-copynumber and lowcopy-number plasmid vectors for lacZ alpha-complementation and chloramphenicol- or kanamycin-resistance selection. Gene 61 : 63 74. (Pubitemid 18038065)
51. Wang, C.C. Newton, A. (1969) Iron transport in Escherichia coli: roles of energy-dependent uptake and 2,3-dihydroxybenzoylserine. J Bacteriol 98 : 1142 1150.
52. Wang, C.C. Newton, A. (1971) An additional step in the transport of iron defined by the tonB locus of Escherichia coli. J Biol Chem 246 : 2147 2151.
53. Wayne, R., Frick, K. Neilands, J.B. (1976) Siderophore protection against colicins M, B, V, and Ia in Escherichia coli. J Bacteriol 126 : 7 12.
54. Yamashita, E., Zhalnina, M.V., Zakharov, S.D., Sharma, O. Cramer, W.A. (2008) Crystal structures of the OmpF porin: function in a colicin translocon. EMBO J 27 : 2171 2180.
55. Zakharov, S.D., Sharma, O., Zhalnina, M.V. Cramer, W.A. (2008) Primary events in the colicin translocon: FRET analysis of colicin unfolding initiated by binding to BtuB and OmpF. Biochemistry 47 : 12802 12809.