Specific in vivo labeling of cell surface-exposed protein loops: Reactive cysteines in the predicted gating loop mark a ferrichrome binding site and a ligand-induced conformational change of the Escherichia coli FhuA protein

Journal of Bacteriology

Volumn 180, Issue 3, 1998, Pages 605-613

  Bös, Christoph ^a   Lorenzen, Dirk ^b   Braun, Volkmar ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FERRICHROME; OUTER MEMBRANE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ESCHERICHIA COLI; FLOW CYTOMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DETERMINATION;

EID: 0031888244     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.3.605-613.1998     Document Type: Article

References (39)

1. Bardwell, J. C. A., K. McGovern, and J. Beckwith. 1991. Identification of a protein required for disulfide bond formation in vivo. Cell 67:581-589.
2. Bassford, P. J., Jr., R. J. Kadner, and C. A. Schnaitman. 1977. Functional stability of the bfe and tonB gene products in Escherichia coli. J. Bacteriol. 130:750-758.
3. Bayer, E. A., M. Safars, and M. Wilchek. 1987. Selective labeling of sulfhydryls and disulfides on blot transfers using avidin-biotin technology: studies on purified proteins and erythrocyte membranes. Anal. Biochem. 161:262-271.
4. Bayer, E. A., M. G. Zalis, and M. Wilchek. 1985. 3-(N-Maleimido-propionyl) biocytin: a versatile thiol-specific biotinylating reagent. Anal. Biochem. 149: 529-536.
5. Bonhivers, M., A. Ghazi, P. Boulanger, and L. Lettelier. 1996. FhuA, a transporter of the Escherichia coli outer membrane, is converted into a channel upon binding of bacteriophage T5. EMBO J. 15:1850-1856.
6. Bös, C., and V. Braun. 1997. Specific in vivo thiol-labeling of the FhuA outer membrane ferrichrome transport protein of Escherichia coli K-12: evidence for a disulfide bridge in the predicted gating loop. FEMS Microbiol. Lett. 153:311-319.
7. Braun, V. 1996. Energy-coupled transport and signal transduction through the Gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol. Lett. 16:295-307.
8. Braun, V., K. Schaller, and H. Wolff. 1973. A common receptor protein for phage T5 and colicin M in the outer membrane of Escherichia coli. Biochim. Biophys. Acta 323:87-97.
9. Coulton, J. W., P. Mason, D. R. Cameron, G. Carmel, R. Jean, and H. N. Rode. 1986. Protein fusions of β-galactosidase to the ferrichrome-iron receptor of Escherichia coli K-12. J. Bacleriol. 165:181-192.
10. O. Giacomini, A., V. Corich, F. J. Ollero, A. Suqartini, and M. P. Nuti. 1992. Experimental conditions may affect reproducibility of the β-galactosidase assay. FEMS Microbiol. Lett. 100:87-90.
11. Günter, K., and V. Braun. 1990. In vivo evidence for FhuA outer membrane receptor interaction with the TonB inner membrane protein of Escherichia coli. FEBS Lett. 274:85-88.
12. Hantke, K. 1981. Regulation of the ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol. Gen. Genet. 182:288-292.
13. Hoffmann, H., E. Fischer, H. Schwarz, and V. Braun. 1986. Overproduction of the proFhuA outer membrane receptor protein of Escherichia coli K-12: isolation, properties, and immunocytochemical localization at the inner side of the cytoplasmic membrane. Arch. Microbiol. 145:334-341.
14. Jiang, X., M. A. Payne, Z. Cao, S. B. Foster, J. B. Feix, S. M. C. Newton, and P. E. Klebba. 1997. Ligand-specific opening of a gated-porin channel in the outer membrane of living bacteria. Science 276:1261-1264.
15. Kadner, R. J., and K. J. Heller. 1995. Mutual inhibition of cobalamin and siderophore uptake systems suggests their competition for TonB function. J. Bacteriol. 177:4829-4835.
16. Killmann, H., R. Benz, and V. Braun. 1993. Conversion of the FhuA transport protein into a diffusion channel through the outer membrane of Escherichia coli. EMBO J. 12:3007-3016.
17. Killmann, H., R. Benz, and V. Braun. 1996. Properties of the FhuA channel in the Escherichia coli outer membrane after deletion of FhuA portions within and outside the predicted gating loop. J. Bacteriol. 178:6913-6920.
18. Killmann, H., and V. Braun. 1992. An aspartate deletion mutation defines a binding site of the multifunctional FhuA outer membrane receptor of Escherichia coli. J. Bacteriol. 174:3479-3486.
19. Killmann, H., G. Videnov, G. Jung, H. Schwarz, and V. Braun. 1995. Identification of receptor binding sites by competitive peptide mapping: phages T1, T5, and φ80 and colicin M bind to the gating loop. J. Bacteriol. 177: 694-698.
20. Klebba, P. E., J. M. Rutz, J. Liu, and C. L. Murphy. 1993. Mechanisms of TonB-catalyzed iron uptake through the enteric bacterial cell envelope. J. Bioenerg. Biomembr. 25:603-611.
21. Koebnik, R., and V. Braun. 1993. Insertion derivatives containing segments of up to 16 amino acids identify surface-and periplasm-exposed regions of the FhuA outer membrane receptor of Escherichia coli K-12. J. Bacteriol. 175:826-839.
22. Lettelier, L., K. P. Locher, L. Planton, and J. Rosenbusch. 1997. Modeling ligand-gated receptor activity. FhuA-mediated ferrichrome efflux from vesicles triggered by phage T5. J. Biol. Chem. 272:1448-1451, 8836.
23. Liu, J., J. M. Rutz, J. B. Feix, and P. E. Klebba. 1993. Permeability properties of a large gated channel within the ferric enterobactin receptor, FepA. Proc. Natl. Acad. Sci. USA 90:10653-10657.
24. Liu, J., J. M. Rutz, P. E. Klebba, and J. B. Feix. 1995. A site-directed spin-labeling study of ligand-induced conformational changes in the ferric enterobactin receptor, FepA. Biochemistry 33:13274-13283.
25. Locher, K., and J. P. Rosenbusch. 1997. Oligomeric states and siderophore binding of the ligand-gated FhuA protein that forms channels across Escherichia coli outer membranes. Eur. J. Biochem. 247:770-775.
26. Lundrigan, M. D., J. H. Lancaster, and C. F. Earhart. 1983. UC-1, a new bacteriophage that uses the TonA polypeptide as its receptor. J. Virol. 45:700-707.
27. Moeck, G. S., S. F. Bazzaz, M. F. Gras, T. S. Ravi, M. J. H. Ratcliffe, and J. W. Coulton. 1994. Genetic insertion and exposure of a reporter epitope in the ferrichrome-iron receptor of Escherichia coli. J. Bacteriol. 176:4250-4259.
28. Moeck, G. S., M. J. H. Ratcliffe, and J. W. Coulton. 1995. Topological analysis of the Escherichia coli ferrichrome-iron receptor by using monoclonal antibodies. J. Bacteriol. 177:6118-6125.
29. Moeck, G. S., P. Tawa, H. Xiang, A. A. Ismail, J. L. Turnbull, and J. W. Coulton. 1996. Ligand-induced conformational change in the ferrichrome-iron receptor of Escherichia coli K-12. Mol. Microbiol. 22:459-471.
30. Newton, S. M. C., J. S. Allen, Z. Cao, X. Jiang, C. Sprencel, J. D. Igo, S. B. Foster, M. A. Payne, and P. E. Klebba. 1997. Double mutagenesis of a positive charge cluster in the ligand-binding site of the ferric enterobactin receptor, FepA. Proc. Natl. Acad. Sci. USA 94:4560-4565.
31. Plancon, L., M. Chami, and L. Lettelier. 1997. Reconstitution of FhuA, an Escherichia coli outer membrane protein, into liposomes. Binding of phage T5 to FhuA triggers transfer of DNA into the proteoliposomes. J. Biol. Chem. 272:16868-16872.
32. Postle, K. 1993. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25:5591-5601.
33. Qiu, X. Q., K. S. Jakes, A. Finkelstein, and S. L. Slatin. 1994. Site specific biotinylation of colicin A. J. Biol. Chem. 269:7483-7488.
34. Rutz, J. M., T. Abdallah, S. Singh, V. I. Kalve, and P. E. Klebba. 1991. Evolution of the ferric enterobactin receptor in gram-negative bacteria. J. Bacteriol. 173:5964-5974.
35. Rutz, J. M., J. Liu, J. A. Lyons, J. Goranson, S. K. Armstrong, M. A. McIntosh, J. B. Feix, and P. E. Klebba. 1992. Formation of a gated channel by a ligand-specific transport protein in the bacterial outer membrane. Science 258:471-475.
36. Salomon, R. A., and R. N. Farias. 1995. The peptide antibiotic microcin 25 is imported through the TonB pathway and the SbmA protein. J. Bacteriol. 177:3323-3325.
37. Sanger, F., A. R. Coulson, B. G. Barrel, A. J. H. Smith, and B. A. Roe. 1980. Cloning in a single-stranded bacteriophage as an aid of rapid DNA sequencing. J. Mol. Biol. 143:161-178.
38. Schöffler, H., and V. Braun. 1998. Transport across the outer membrane of Escherichia coli K12 via the FhuA receptor is regulated by the TonB protein of the cytoplasmic membrane. Mol. Gen. Genet. 217:378-383.
39. Tabor, S., and C. C. Richardson. 1985. A bacteriophage T7 polymerase/ promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA 182:1074-1078.