Interactions between the outer membrane ferric citrate transporter FecA and TonB: Studies of the FecA TonB box

Journal of Bacteriology

Volumn 185, Issue 6, 2003, Pages 1870-1885

  Ogierman, Monica ^a   Braun, Volkmar ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FECA PROTEIN; FERRIC CITRATE; FERRIC CITRATE TRANSPORTER; RECOMBINANT DNA; TONB PROTEIN; UNCLASSIFIED DRUG;

ACTIVE TRANSPORT; ARTICLE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERIUM MUTANT; CROSS LINKING; ESCHERICHIA COLI; IMMUNOBLOTTING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTON MOTIVE FORCE;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CITRATES; CROSS-LINKING REAGENTS; CYSTEINE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FERRIC COMPOUNDS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MUTATION; PHENOTYPE; PLASMIDS; PROTON-MOTIVE FORCE; RECEPTORS, CELL SURFACE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0037337264     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.6.1870-1885.2003     Document Type: Article

References (65)

1. Ahmer, B. M., M. G. Thomas, R. A. Larsen, and K. Postle. 1995. Characterization of the exbBD operon of Escherichia coli and the role of ExbB and ExbD in TonB functions and stability. J. Bacteriol. 177:4742-4747.
2. Angerer, A., and V. Braun. 1998. Iron regulates transcription of the Escherichia coli ferric citrate transport genes directly and through the transcription initiation proteins. Arch. Microbiol. 169:483-490.
3. 70-type factors that respond to extracytoplasmic stimuli. Mol. Microbiol. 18:163-174.
4. Bell, P. E., C. D. Nau, J. T. Brown, J. Konisky, and R. J. Kadner. 1990. Genetic suppression demonstrates interaction of TonB protein with outer membrane transport proteins in Escherichia coli. J. Bacteriol. 172:3826-3829.
5. Braun, V. 1989. The structurally related exbB and tolQ genes are interchangeable in conferring tonB-dependent colicin, bacteriophage, and albomycin sensitivity. J. Bacteriol. 11:6387-6390.
6. Braun, V. 1995. Energy-coupled transport and signal transduction through the gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol. Rev. 16:295-307.
7. Braun, V., and C. Herrmann. 1993. Evolutionary relationship of uptake systems for biopolymers in Escherichia coli: cross-complementation between the TonB-ExbB-ExbD and the TolA-TolQ-TolR proteins. Mol. Microbiol. 8:261-268.
8. Braun, V., S. Gaisser, C. Herrmann, K., Kampfenkel, H. Killmann, and I. Traub. 1996. Energy-coupled transport across the outer membrane of Escherichia coli: ExbB binds ExbD and TonB in vitro, and leucine 132 in the periplasmic region and aspartate 25 in the transmembrane region are important for ExbD activity. J. Bacteriol. 178:2836-2845.
9. Brinkley, M. 1992. A brief survey of methods for preparing protein conjugates with dyes, haptens, and cross-linking reagents. Bioconjug. Chem. 3:2-13.
10. Buchanan, S. K., B. S. Smith, L. Venkatramani, D. Xia, L. Esser, M. Palnitkar, R. Chakraborty, D. van der Helm, and J. Deisenhofer. 1999. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat. Struct. Biol. 6:56-63.
11. Cadieux, N., and R. J. Kadner. 1999. Site-directed disulfide bonding reveals an interaction site between energy-coupling protein TonB and BtuB, the outer membrane cobalamin transporter. Proc. Natl. Acad. Sci. USA 96: 10673-10678.
12. Coulton, J. W., P. Mason, D. R. Cameron, G. Carmel, R. Jean, and H. N. Rode. 1986. Protein fusions of beta-galactosidase to the ferrichrome-iron receptor of Escherichia coli K-12. J. Bacteriol. 165:181-192.
13. Desai, P. J., E. Garges, and C. A. Genco. 2000. Pathogenic neisseriae can use hemoglobin, transferrin, and lactoferrin independently of the tonB locus. J. Bacteriol. 182:5586-5591.
14. Enz, S., S. Mahren, U. H. Stroeher, and V. Braun. 2000. Surface signaling in ferric citrate transport gene induction: interaction of the FecA, FecR, and FecI regulatory proteins. J. Bacteriol, 182:637-646.
15. Ferguson, A. D., R. Chakraborty, B. S. Smith, L. Esser, D. Van der Helm, and J. Deisenhofer. 2002, Structural basis of gating by the outer membrane transporter FecA. Science 295:1715-1719.
16. Ferguson, A. D., E. Hofmann, J. W. Coulton, K. Diederiens, and W. Welte. 1998. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215-2220,
17. Fischer, E., K. Günter, and V. Braun. 1989. Involvement of ExbB and TonB in transport across the outer membrane of Escherichia coli: phenotypic complementation of exb mutants by overexpressed tonB and physical stabilization of TonB by ExbB. J. Bacteriol. 711:5127-5134.
18. Giacomini, A., B. Corich, F. J. Ollero, A. Squartini, and M. P. Nuti. 1992. Experimental conditions may affect reproducibility of the β-galactosidase assay. FEMS Microbiol. Lett. 100:87-90.
19. BAD promoter. J. Bacteriol. 177:4121-4130.
20. Habeck, M. 1998. Ph.D. thesis. University of Tübingen, Tübingen, Germany.
21. Hantke, K., and V. Braun. 1978. Functional interaction of the TonA/TonB receptor system in Escherichia coli. J. Bacteriol. 135:190-197.
22. Härle, C., I. Kim, A. Angerer, and V. Braun. 1995. Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J. 14:1430-1438.
23. Horton, R. M., H. D. Hunt, S. N. Ho, J. K. Pullen, and L. R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
24. Howard, S. P., C. Herrmann, C. W. Stratilo, and V. Braun. 2001. In vivo synthesis of the periplasmic domain of TonB inhibits transport through the FecA and FhuA iron siderophore transporters of Escherichia coli. J. Bacteriol. 183:5885-5895.
25. Jaskula, J. C., T. E. Letain, S. K. Roof, J. T. Skare, and K. Postle. 1994. Role of the TonB amino terminus in energy transduction between membranes. J. Bacteriol. 176:2326-2338.
26. 12 transport in Escherichia coli: energy coupling between membranes. Mol. Microbiol. 4:2027-2033.
27. Kadner, R. J., and K. J. Heller. 1995. Mutual inhibition of cobalamin and siderophore uptake systems suggest their competition for TonB function. J. Bacteriol. 177:4829-4835.
28. Kim, I., A. Stiefel, S. Plantör, A. Angerer, and V. Braun. 1997. Transcription induction of the ferric citrate transport genes via the N-terminus of the FecA outer membrane protein, the Ton system and the electrochemical potential of the cytoplasmic membrane. Mol. Microbiol. 23:333-344.
29. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Larsen, R. A., D. Foster-Hartnett, M. A. McIntosh, and K. Postle. 1997. Regions of Escherichia coli TonB and FepA proteins essential for in vivo physical interactions. J. Bacteriol. 179:3213-3221.
31. Larsen, R. A., P. S. Myers, J. T. Skare, C. L. Seachord, R. P. Darveau, and K. Postle. 1996. Identification of TonB homologs in the family Enterobacteriaceae and evidence for conservation of TonB-dependent energy transduction complexes. J. Bacteriol. 178:1363-1373.
32. Larsen, R. A., M. G, Thomas, and K. Postle. 1999. Protonmotive force, ExbB and ligand-bound FepA drive conformational changes in TonB. Mol. Microbiol. 31:1809-1824.
33. Larsen, R. A., G. E. Wood, and K. Postle. 1993. The conserved proline-rich motif is not essential for energy transduction by Escherichia coli TonB protein. Mol. Microbiol. 10:943-953.
34. Locher, K. P., B. Rees, R. Koebnik, A. Mitschler, L. Moulinier, J. P. Rosenbusch, and D. Moras. 1998. Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771-778.
35. Lundrigan, M. D., and R. J. Kadner. 1986. Nucleotide sequence of the gene for the ferrienterochelin receptor FepA in Escherichia coli. Homology among outer membrane transporters that interact with TonB. J. Biol. Chem. 261:10797-10801.
36. Martinez, E., B. Bartolome, and F. De la Cruz. 1988. pACY184-derived cloning vectors containing the multiple cloning site and lacZ reporter gene of pUC8/9 and pUC18/19 plasmids. Gene 68:159-162.
37. Means, G. E., and R. E. Feeney. 1971. Chemical modifications of proteins. Holden-Day Publishers, San Francisco, Calif.
38. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
39. Moeck, G. S., and L. Letellier. 2001. Characterization of in vitro interactions between a truncated TonB protein from Escherichia coli and the outer membrane receptors FhuA and FepA. J. Bacteriol. 183:2755-2764.
40. Moeck, G. S., J. W. Coulton, and K. Postle. 1997. Cell envelope signalling in Escherichia coli: ligand binding to the ferrichrome-iron receptor FhuA promotes interaction with the energy-transducing protein TonB. J. Biol. Chem. 272:28391-28397.
41. Occhino, D. A., E. E. Wyckoff, D. P. Henderson, T. W. Wrona, and S. M. Payne. 1998. Vibrio cholerae iron transport: haem transport genes are linked to one of two sets of tonB, exbB, exbD genes. Mol. Microbiol. 29:1493-1507.
42. Ochs, M., A. Angerer, S. Enz, and V. Braun. 1996. Surface signaling in transcriptional regulation of the ferric citrate transport system of Escherichia coli: mutational analysis of the alternative sigma factor FecI supports its essential role in fec transport gene transcription.
43. Ochs, M., S. Veitinger, K. InSook, D. Welz, A. Angerer, and V. Braun. 1995. Regulation of citrate-dependent iron transport of Escherichia coli: FecR is required for transcription activation by FecI. Mol. Microbiol. 15:119-132.
44. Paquelin, A., J. M. Ghigo, S. Bertin, and C. Wandersman. 2001. Characterisation of HasB, a Serratia marcescens TonB-like protein specifically involved in the haemophore-dependent haem acquisition system. Mol. Microbiol. 42:995-1005.
45. Possot, O., L. Letellier, and A. Pugsley. 1997. Energy requirement for pullulanase secretion by the main branch of the general secretory pathway. Mol. Microbiol. 24:457-464.
46. Postle, K. 1993. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25:591-601.
47. Pressler, U., H. Staudenmaier, L. Zimmermann, and V. Braun. 1988. Genetics of the iron dicitrate transport system of Escherichia coli. J. Bacteriol. 170:2716-2724.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Schöffler, H., and V. Braun. 1989. Transport across the outer membrane of Escherichia coli via the FhuA receptor is regulated by the TonB protein of the cytoplasmic membrane. Mol. Gen. Genet. 217:378-383.
50. Seliger, S. S., A. R. Mey, A.-M. Valle, and S. M. Payne. 2001. The two TonB systems of Vibrio cholerae: redundant and specific functions. Mol. Microbiol. 39:801-812.
51. Skare, J. T., B. M Ahmer, C. L. Seachord, R. P. Darveau, and K. Postle. 1993. Energy transduction between membranes. TonB, a cytoplasmic membrane protein, can be chemically cross-linked in vivo to the outer membrane receptor FepA. J. Biol. Chem. 268:16302-16308.
52. Staudenmaier, H., B. van Hove, Z. Yaraghi, and V. Braun. 1989. Nucleotide sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic-binding-dependent transport mechanism for iron(III) dicitrate in Escherichia coli. J. Bacteriol. 171:2626-2633.
53. Stiefel, A., S. Mahren, M. Ochs, P. T. Schindler, S. Enz, and V. Braun. 2001. Control of the ferric citrate transport system of Escherichia coli: mutations in region 2.1 of the FecI extracytoplasmic-function sigma factor suppress mutations in the FecR transmembrane regulatory protein. J. Bacteriol. 183:162-170.
54. Studier, J. T., and B. A. Moffat. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
55. 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 82:1074-1078.
56. Takeshita, S., S. Masahiro, M. Toba, W. Masahashi, and T. Hashimoto-Gotoh. 1987. High-copy-number and low-copy-number plasmid vectors for lacZ α-complementation and chloramphenicol- or kanamycin-resistance selection. Gene 61:63-74.
57. Traub, I., S. Gaisser, and V. Braun. 1993. Activity domains of the TonB protein. Mol. Microbiol. 8:409-423.
58. Valdivia, R. H., and S. Falkow. 1996. Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol. Microbiol. 22:367-378.
59. Van Hove, B., H. Staudenmaier, and V. Braun. 1990. Novel two-component transmembrane transcriptional control: regulation of iron dicitrate transport in Escherichia coli K-12. J. Bacteriol. 172:6749-6758.
60. Visca, P., L. Leoni, M. J. Wilson, and I. L. Lamont. 2002. Iron transport and regulation, cell signaling and genomics: lessons from Escherichia coli and Pseudomonas. Mol. Microbiol. 45:1177-1190.
61. Wagegg, W., and V. Braun. 1981. Ferric citrate transport in Escherichia coli requires outer membrane receptor protein FecA. J. Bacteriol. 145:156-163.
62. Welz, D., and V. Braun. 1998. Ferric citrate transport of Escherichia coli: functional regions of the FccR transmembrane regulatory protein. 180:2387-2394.
63. Young, G. M., and K. Postle. 1994. Repression of tonB transcription during anaerobic growth requires Fur binding at the promoter and a second factor binding upstream. Mol. Microbiol. 11:943-954.
64. Zhao, Q., and K. Poole. 2000. A second tonB gene in Pseudomonas aeruginosa is linked to the exbB and exbD genes. FEMS Microbiol. Lett. 184:127-132.
65. Zimmermann, L., K. Hantke, and V. Braun. 1984. Exogenous induction of the iron dicitrate transport system of Escherichia coli K-12. J. Bacteriol. 159:271-277.