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

Journal of Bacteriology

Volumn 178, Issue 10, 1996, Pages 2836-2845

  Braun, Volkmar ^a,b   Gaisser, Sabine ^b   Herrmann, Christina ^b   Kampfenkel, Karlheinz ^b   Killmann, Helmut ^b   Traub, Irene ^b  

^a Mikrobiologie II   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLICIN; CYANOCOBALAMIN; SIDEROPHORE;

ACTIVE TRANSPORT; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CHANNEL GATING; ESCHERICHIA COLI; NONHUMAN; OUTER MEMBRANE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; CELL MEMBRANE; COLICINS; ENERGY METABOLISM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FERRICHROME; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, CELL SURFACE; SIDEROPHORES; VITAMIN B 12;

ESCHERICHIA COLI;

EID: 0029913411     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.178.10.2836-2845.1996     Document Type: Article

References (57)

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 function and stability. J. Bacteriol. 177:4742-4747.
2. 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.
3. Bitter, W., J. Tommassen, and P. J. Weisbeek. 1993. Identification and characterization of the exbB, exbD, and tonB genes of Pseudomonas putida WCS358: their involvement in ferric pseudobactin transport. Mol. Microbiol. 7:117-130.
4. Bradbeer, C. 1993. The proton motive force drives the outer membrane transport of cobalamin in Escherichia coli. J. Bacteriol. 175:3146-3150.
5. Braun, V. 1989. The structurally related exbB and tolQ genes are interchangeable in conferring tonB-dependent colicin, bacteriophage, and albomycin sensitivity. J. Bacteriol. 171:6387-6390.
6. Braun, V. 1995. Energy-coupled transport and signal transduction through the Gram-negative outer membrane via the 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., H. Pilsl, and P. Groß. 1994. Colicins: structures, modes of action, transfer through membranes, and evolution. Arch. Microbiol. 161:199-206.
9. Eick-Helmerich, K., and V. Braun. 1989. Import of biopolymers into Escherichia coli: nucleotide sequences of the exbB and exbD genes are homologous to those of the tolQ and tolR genes, respectively. J. Bacteriol. 171:5117-5126.
10. 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.
11. Günter, K., and V. Braun. 1990. In vivo evidence for FhuA outer membrane receptor interaction with TonB inner membrane protein of Escherichia coli. FEBS Lett. 274:85-88.
12. Hancock, R. E. W., and V. Braun. 1976. Nature of energy requirement for the irreversible adsorption of bacteriophages T1 and φ80 to Escherichia coli. J. Bacteriol. 125:409-415.
13. Hannavy, K., G. C. Barr, C. J. Dorman, J. Adamson, L. R. Mazengera, M. P. Gallagher, J. S. Evans, B. A. Levine, I. P. Trayer, and C. F. Higgins. 1990. TonB protein of Salmonella typhimurium: a model for signal transduction between membranes. J. Mol. Biol. 216:897-910.
14. Hantke, K., and V. Braun. 1978. Functional interaction of the tonA/tonB receptor system in Escherichia coli. J. Bacteriol. 135:190-197.
15. 12 and ferric iron transport. FEMS Microbiol. Lett. 12:31-35.
16. 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. 15:1430-1438.
17. Heller, K. J., R. J. Kadner, and K. Günter. 1988. Suppression of the btuB451 mutation by mutations in the tonB gene suggests a direct interaction between TonB and TonB-dependent receptor proteins in the outer membrane of Escherichia coli. Gene 64:147-153.
18. Hennesy, E. S., and J. Broome-Smith. 1994. Two related bacterial membrane proteins, ExbD and TolR, have opposite transmembrane charge dipolarity. Mol. Microbiol. 11:417.
19. 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.
20. 12 transport in Escherichia coli: energy coupling between membranes. Mol. Microbiol. 4:2027-2033.
21. Kampfenkel, K., and V. Braun. 1992. Membrane topology of the Escherichia coli ExbD protein. J. Bacteriol. 174:5485-5487.
22. Kampfenkel, K., and V. Braun. 1993. Topology of the ExbB protein in the cytoplasmic membrane of Escherichia coli. J. Biol. Chem. 268:6050-6057.
23. Kampfenkel, K., and V. Braun. 1993. Membrane topologies of the TolQ and TolR proteins of Escherichia coli: inactivation of TolQ by a missense mutation in proposed first transmembrane segment. J. Bacteriol. 175:4485-4491.
24. Karlsson, M., K. Hannavy, and C. F. Higgins. 1993. ExbB acts as a chaperone-like protein to stabilize TonB in the cytoplasm. Mol. Microbiol. 8:389-396.
25. Karlsson, M., K. Hannavy, and C. F. Higgins. 1993. A sequence-specific function for the N-terminal signal-like sequence of the TonB protein. Mol. Microbiol. 8:379-388.
26. 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.
27. Killmann, H., and V. Braun. 1994. Energy-dependent receptor activities of Escherichia coli K-12: mutated TonB proteins alter FhuA receptor activities to phages T5, T1, φ80, and to colicin M. FEMS Microbiol. Lett. 119:71-76.
28. Larsen, R. A., M. G. Thomas, G. E. Wood, and K. Postle. 1994. Partial suppression of an Escherichia coli TonB transmembrane domain mutation (DV17) by a missense mutation in ExbB. Mol. Microbiol. 13:627-640.
29. Lazzaroni, J. C., A. Vianney, J. L. Popot, H. Benedetti, F. Samatey, C. Lazdunski, R. Portalier, and V. Geli. 1995. Transmembrane α-helix interactions required for the functional assembly of the Escherichia coli Tol complex. J. Mol. Biol. 246:1-7.
30. Levengood, S. K., W. F. Beyer, Jr., and R. E. Webster. 1991. TolA: a membrane protein involved in colicin uptake contains an extended helical region. Proc. Natl. Acad. Sci. USA 88:5939-5943.
31. 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.
32. 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.
33. Müller, M. M., A. Vianney, J. C. Lazzaroni, R. E. Portalier, and R. E. Webster. 1993. Membrane topology of the Escherichia coli TolR protein required for cell envelope integrity. J. Bacteriol. 175:6059-6061.
34. Ochs, M., S. Veitinger, I. Kim, D. Welz, A. Angerer, and V. Braun. 1994. Regulation of citrate-dependent iron transport of Escherichia coli. FecR is required for transcription activation by FecI. Mol. Microbiol. 15:119-132.
35. Postle, K. 1993. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25:5591-5601.
36. Postle, K., and R. F. Good. 1983. DNA sequence of the Escherichia coli tonB gene. Proc. Natl. Acad. Sci. USA 80:5235-5239.
37. Postle, K., and J. T. Skare. 1988. Escherichia coli TonB protein is exported from the cytoplasm without protcolytic cleavage of its amino terminus. J. Biol. Chem. 263:11000-11007.
38. 12 in Escherichia coli. Some observations on the roles of the gene products btuC and tonB. J. Biol. Chem. 255:4313-4319.
39. Rohrbach. M. R., S. Paul, and W. Köster. 1995. In vivo reconstitution of an active siderophore transport system by a binding protein derivative lacking a signal sequence. Mol. Gen. Genet. 248:33-42.
40. 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.
41. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
42. Schöffler, H., and V. Braun. 1989. 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.
43. Schwyn, B., and J. B. Neilands. 1987. Universal chemical assay for detection and determination of siderophores. Anal. Biochem. 160:47-56.
44. Skare, J. T., B. M. M. Ahmer, C. L. Seachord, R. P. Darveau, and K. Postle. 1993. Energy transduction between membranes. J. Biol. Chem. 268:16302-16308.
45. Skare, J. T., and K. Postle. 1991. Evidence for a TonB-dependent energy transduction complex in Escherichia coli. Mol. Microbiol. 5:2883-2890.
46. 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.
47. Sun, T. P., and R. E. Webster. 1986. fii, a bacterial locus required for filamentous phage infection and its relation to colicin-tolerant tolA and tolB. J. Bacteriol. 165:107-115.
48. Sun, T. P., and R. E. Webster. 1987. Nucleotide sequence of a gene cluster involved in entry of E colicins and single-stranded DNA of infecting filamentous bacteriophages into Escherichia coli. J. Bacteriol. 169:2667-2874.
49. 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.
50. Traub, I., and V. Braun. 1994. Energy-coupled colicin transport through the outer membrane of Escherichia coli K-12: mutated TonB proteins alter receptor activities and colicin uptake. FEMS Microbiol. Lett. 119:65-75.
51. Traub, I., S. Gaisser, and V. Braun. 1993. Activity domains of the TonB protein. Mol. Microbiol. 8:409-423.
52. Tuckman, M., and M. S. Osburne. 1992. In vivo inhibition of TonB-dependent processes by a TonB box consensus pentapeptide. J. Bacteriol. 174:320-323.
53. Vianney, A., T. M. Levin, W. E. Bayer, J. C. Lazzaroni, R. Portalier, and R. E. Webster. 1994. Membrane topology and mutational analysis of the TolQ protein of Escherichia coli required for the uptake of macromolecules and cell envelope integrity. J. Bacteriol. 176:822-825.
54. von Heijne, G. 1992. Membrane protein structure prediction. Hydrophobicity analysis and the positive inside rule. J. Mol. Biol. 225:487-494.
55. Wang, R. F., and S. R. Kushner. 1991. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
56. Webster, R. E. 1991. The tol gene products and the import of macromolecules into Escherichia coli. Mol. Microbiol. 5:1005-1011.
57. 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.