Interaction of TonB with the outer membrane receptor FpvA of Pseudomonas aeruginosa

Journal of Bacteriology

Volumn 188, Issue 16, 2006, Pages 5752-5761

  Adams, Hendrik ^a,c   Zeder Lutz, Gabrielle ^a   Schalk, Isabelle ^a   Pattus, Franc ^a   Celia, Hervé ^a,b  

^a ESBS   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; DETERGENT; FERRIC PYOVERDINE; GLUTATHIONE TRANSFERASE; HETERODIMER; HEXAHISTIDINE; HISTIDINE DERIVATIVE; IRON; IRON BINDING PROTEIN; IRON DERIVATIVE; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; OUTER MEMBRANE PROTEIN; PROTEIN FPVA; PROTEIN TONB; PROTEIN TONB1; PYOVERDINE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; FPVA PROTEIN, PSEUDOMONAS AERUGINOSA; OLIGOPEPTIDE; TONB PROTEIN, BACTERIA;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; BINDING AFFINITY; BINDING SITE; CELL FRACTIONATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; ENERGY TRANSFER; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; IRON TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TARGETING; PROTON MOTIVE FORCE; PSEUDOMONAS AERUGINOSA; SURFACE PLASMON RESONANCE; GENETICS; METABOLISM;

ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; IRON; MEMBRANE PROTEINS; OLIGOPEPTIDES; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA;

EID: 33748657558     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00435-06     Document Type: Article

References (55)

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. 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.
3. 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.
4. Chang, C., A. Mooser, A. Plückthun, and A. Wlodawer. 2001. Crystal structure of the dimeric C-terminal domain of TonB reveals a novel fold. J. Biol. Chem. 276:27535-27540.
5. Clarke, T. E., L. W. Tari, and H. J. Vogel. 2001. Structural biology of bacterial iron uptake systems. Curr. Top. Med. Chem. 1:7-30.
6. Clement, E., P. J. Mesini, F. Pattus, and I. J. Schalk. 2004. The binding mechanism of pyoverdin with the outer membrane receptor FpvA in Pseudomonas aeruginosa is dependent on its iron-loaded status. Biochemistry 43:7954-7965.
7. Cobessi, D., H. Celia, N. Folschweiller, I. J. Schalk, M. A. Abdallah, and F. Pattus. 2005. The crystal structure of the pyoverdine outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 angstroms resolution. J. Mol. Biol. 347:121-134.
8. Demange, P., A. Bateman, C. Mertz, A. Dell, Y. Piemont, and M. A. Abdallah. 1990. Bacterial siderophores: structures of pyoverdins Pt, siderophores of Pseudomonas tolaasii NCPPB 2192, and pyoverdins Pf, siderophores of Pseudomonas fluorescens CCM 2798. Identification of an unusual natural amino acid. Biochemistry 29:11041-11051.
9. Endriss, F., M. Braun, H. Killmann, and V. Braun. 2003. Mutant analysis of the Escherichia coli FhuA protein reveals sites of FhuA activity. J. Bacteriol. 185:4683-4692.
10. 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.
11. Ferguson, A. D., and J. Deisenhofer. 2002. TonB-dependent receptors-structural perspectives. Biochim. Biophys. Acta 1565:318-332.
12. Ferguson, A. D., E. Hofmann, J. W. Coulton, K. Diederichs, and W. Welte. 1998. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215-2220.
13. Figurski, D. H., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
14. 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. 171:5127-5134.
15. Ghosh, J., and K. Postle. 2005. Disulphide trapping of an in vivo energy-dependent conformation of Escherichia coli TonB protein. Mol. Microbiol. 55:276-288.
16. Hoegy, F., H. Celia, G. L. Mislin, M. Vincent, J. Gallay, and I. J. Schalk. 2005. Binding of iron-free siderophore, a common feature of siderophore outer membrane transporters of Escherichia coli and Pseudomonas aeruginosa. J. Biol. Chem. 280:20222-20230.
17. Holloway, B. W. 1969. Genetics of Pseudomonas. Bacteriol. Rev. 33:419-443.
18. 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.
19. Huang, B., K. Ru, Z. Yuan, C. B. Whitchurch, and J. S. Mattick. 2004. tonB3 is required for normal twitching motility and extracellular assembly of type IV pili. J. Bacteriol. 186:4387-4389.
20. Kadner, R. J. 1990. Vitamin B12 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. Kaniga, K., I. Delor, and G. R. Cornelis. 1991. A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocotilica. Gene. 109:137-141.
23. 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.
24. Khursigara, C. M., G. De Crescenzo, P. D. Pawelek, and J. W. Coulton. 2005. Deletion of the proline-rich region of TonB disrupts formation of a 2:1 complex with FhuA, an outer membrane receptor of Escherichia coli. Protein Sci. 14:1266-1273.
25. Khursigara, C. M., G. De Crescenzo, P. D. Pawelek, and J. W. Coulton. 2004. Enhanced binding of TonB to a ligand-loaded outer membrane receptor: role of the oligomeric state of TonB in formation of a functional FhuA. TonB complex. J. Biol. Chem. 279:7405-7412.
26. Khursigara, C. M., G. De Crescenzo, P. D. Pawelek, and J. W. Coulton. 2005. Kinetic analyses reveal multiple steps in forming TonB-FhuA complexes from Escherichia coli. Biochemistry 44:3441-3453.
27. Ködding, J., P. Howard, L. Kaufmann, P. Polzer, A. Lustig, and W. Welte. 2004. Dimerization of TonB is not essential for its binding to the outer membrane siderophore receptor FhuA of Escherichia coli. J. Biol. Chem. 279:9978-9986.
28. Ködding, J., F. Killig, P. Polzer, S. P. Howard, K. Diederichs, and W. Welte. 2005. Crystal structure of a 92-residue C-terminal fragment of TonB from Escherichia coli reveals significant conformational changes compared to structures of smaller TonB fragments. J. Biol. Chem. 280:3022-3028.
29. Koebnik, R. 2005. TonB-dependent trans-envelope signaling: the exception or the rule? Trends Microbiol. 13:343-347.
30. Larsen, R. A., T. E. Letain, and K. Postle. 2003. In vivo evidence of TonB shuttling between the cytoplasmic and outer membrane in Escherichia coli. Mol. Microbiol. 49:211-218.
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. 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.
34. Moeck, G. S., J. W. Coulton, and K. Postle. 1997. Cell envelope signaling 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.
35. 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.
36. Morales, V. M., A. Backman, and M. Bagdasarian. 1991. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97:39-47.
37. Peacock, S. R., A. M. Weljie, S. Peter Howard, F. D. Price, and H. J. Vogel. 2005. The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J. Mol. Biol. 345:1185-1197.
38. Poole, K., S. Neshat, K. Krebes, and D. E. Heinrichs. 1993. Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J. Bacteriol. 175:4597-4604.
39. Poole, K., Q. Zhao, S. Neshat, D. E. Heinrichs, and C. R. Dean. 1996. The Pseudomonas aeruginosa tonB gene encodes a novel TonB protein. Microbiology 142:1449-1458.
40. Postle, K. 1993. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25:591-601.
41. Postle, K., and R. J. Kadner. 2003. Touch and go: tying TonB to transport. Mol. Microbiol. 49:869-882.
42. Postle, K., and J. T. Skare. 1988. Escherichia coli TonB protein is exported from the cytoplasm without proteolytic cleavage of its amino terminus. J. Biol. Chem. 263:11000-11007.
43. Rich, R. L., and D. G. Myszka. 2000. Advances in surface plasmon resonance biosensor analysis. Curr. Opin. Biotechnol. 11:54-61.
44. Sauter, A., S. P. Howard, and V. Braun. 2003. In vivo evidence for TonB dimerization. J. Bacteriol. 185:5747-5754.
45. Schalk, I. J., C. Hennard, C. Dugave, K. Poole, M. A. Abdallah, and F. Pattus. 2001. Iron-free pyoverdin hinds to its outer membrane receptor FpvA in Pseudomonas aeruginosa: a new mechanism for membrane iron transport. Mol. Microbiol. 39:351-360.
46. Schalk, I. J., P. Kyslik, D. Prome, A. van Dorsselaer, K. Poole, M. A. Abdallah, and F. Pattus. 1999. Copurification of the FpvA ferric pyoverdin receptor of Pseudomonas aeruginosa with its iron-free ligand: implications for siderophore-mediated iron transport. Biochemistry 38:9357-9365.
47. Schalk, I. J., W. W. Yue, and S. K. Buchanan. 2004. Recognition of iron-free siderophores by TonB-dependent iron transporters. Mol. Microbiol. 54:14-22.
48. 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.
49. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Mickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, I. T. Paulsen, J. Reizer, M. H. Saier, R. E. Hancock, S. Lory, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406:959-964.
50. Takase, H., H. Nitanai, K. Hoshino, and T. Otani. 2000. Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect. Immun. 68:4498-4504.
51. Wiener, M. C. 2005. TonB-dependent outer membrane transport: going for Baroque? Curr. Opin. Struct. Biol. 15:394-400.
52. Wilson, R., and R. B. Dowling. 1998. Lung infections. 3. Pseudomonas aeruginosa and other related species. Thorax 53:213-219.
53. Wooldridge, K. G., and P. H. Williams. 1993. Iron uptake mechanisms of pathogenic bacteria. FEMS Microbiol. Rev. 12:325-348.
54. Zhao, Q., and K. Poole. 2002. Mutational analysis of the TonB1 energy coupler of Pseudomonas aeruginosa. J. Bacteriol. 184:1503-1513.
55. 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.