Phage display reveals multiple contact sites between FhuA, an outer membrane receptor of Escherichia coli, and TonB

Journal of Molecular Biology

Volumn 357, Issue 1, 2006, Pages 236-251

  Carter, David M ^a   Gagnon, Jean Nicolas ^a   Damlaj, Moussab ^a   Mandava, Suneeta ^b   Makowski, Lee ^b   Rodi, Diane J ^b   Pawelek, Peter D ^a   Coulton, James W ^a  

^a MCGILL UNIVERSITY   (Canada)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

OM receptor, E. coli; Phage display; Protein protein interactions; TonB, FhuA

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; BACTERIAL PROTEIN; DNA; FERRIC HYDROXAMATE UPTAKE PROTEIN COMPONENT A; MALTOSE BINDING PROTEIN; OLIGONUCLEOTIDE; OUTER MEMBRANE PROTEIN; PEPTIDE LIBRARY; PROTEIN TONB; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CLUSTER ANALYSIS; CONTROLLED STUDY; CYTOPLASM; DNA SEQUENCE; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; GENE CLUSTER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33644787225     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.12.039     Document Type: Article

References (53)

1. C. Wandersman, and P. Delepelaire Bacterial iron sources: from siderophores to hemophores Annu. Rev. Microbiol. 58 2004 611 647
2. K.N. Raymond, and E.D. Dertz Biochemical and physical properties of siderophores J.H. Crosa A.R. Rey S.M. Payne Iron Transport in Bacteria 2004 ASM Press Washington, DC 3 17
3. V. Braun, and M. Braun Iron transport and signaling in Escherichia coli FEBS Letters 529 2002 78 85
4. G.S. Moeck, J.W. Coulton, and K. Postle 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 1997 28391 28397
5. J.T. Skare, B.M. Ahmer, C.L. Seachord, R.P. Darveau, and K. Postle 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 1993 16302 16308
6. V. Braun, K. Hantke, and W. Köster Bacterial iron transport: mechanisms, genetics, and regulation A. Sigel H. Sigel Metal Ions in Biological Systems 1998 Marcel Dekker Inc. New York 68 145
7. A.D. Ferguson, J.W. Coulton, K. Diederichs, and W. Welte The ferric hydroxamate uptake receptor FhuA and related TonB-dependent transporters in the outer membrane of gram-negative bacteria A. Messerschmidt R. Huber T. Poulos K. Wieghardt Handbook of Metalloproteins 2001 John Wiley & Sons Ltd Chichester 834 849
8. G.S. Moeck, and J.W. Coulton TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport Mol. Microbiol. 28 1998 675 681
9. A.D. Ferguson, E. Hofmann, J.W. Coulton, K. Diederichs, and W. Welte Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide Science 282 1998 2215 2220
10. K.P. Locher, B. Rees, R. Koebnik, A. Mitschler, L. Moulinier, J.P. Rosenbusch, and D. Moras Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes Cell 95 1998 771 778
11. S.K. Buchanan, B.S. Smith, L. Venkatramani, D. Xia, L. Esser, and M. Palnitkar Crystal structure of the outer membrane active transporter FepA from Escherichia coli Nature Struct. Biol. 6 1999 56 63
12. A.D. Ferguson, R. Chakraborty, B.S. Smith, L. Esser, D. van der Helm, and J. Deisenhofer Structural basis of gating by the outer membrane transporter FecA Science 295 2002 1715 1719
13. D.P. Chimento, A.K. Mohanty, R.J. Kadner, and M.C. Wiener Substrate-induced transmembrane signaling in the cobalamin transporter BtuB Nature Struct. Biol. 10 2003 394 401
14. D. Cobessi, H. Celia, N. Folschweiller, I.J. Schalk, M.A. Abdallah, and F. Pattus The crystal structure of the pyoverdine outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 angstroms resolution J. Mol. Biol. 347 2005 121 134
15. D. Cobessi, H. Celia, and F. Pattus Crystal structure at high resolution of ferric-pyochelin and its membrane receptor FptA from Pseudomonas aeruginosa J. Mol. Biol. 352 2005 893 904
16. D.P. Chimento, R.J. Kadner, and M.C. Wiener Comparative structural analysis of TonB-dependent outer membrane transporters: implications for the transport cycle Proteins: Struct. Funct. Genet. 59 2005 240 251
17. J.D. Faraldo-Gómez, G.R. Smith, and M.S. Sansom Molecular dynamics simulations of the bacterial outer membrane protein FhuA: a comparative study of the ferrichrome-free and bound states Biophys. J. 85 2003 1406 1420
18. C. Chang, A. Mooser, A. Plückthun, and A. Wlodawer Crystal structure of the dimeric C-terminal domain of TonB reveals a novel fold J. Biol. Chem. 276 2001 27535 27540
19. R.A. Larsen, T.E. Letain, and K. Postle In vivo evidence of TonB shuttling between the cytoplasmic and outer membrane in Escherichia coli Mol. Microbiol. 49 2003 211 218
20. K. Postle, and R.J. Kadner Touch and go: tying TonB to transport Mol. Microbiol. 49 2003 869 882
21. J. Ködding, F. Killig, P. Polzer, S.P. Howard, K. Diederichs, and W. Welte 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 2005 3022 3028
22. S.R. Peacock, A.M. Weljie, S.P. Howard, F.D. Price, and H.J. Vogel The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides J. Mol. Biol. 345 2005 1185 1197
23. C.M. Khursigara, G. De Crescenzo, P.D. Pawelek, and J.W. Coulton 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 2004 7405 7412
24. A. Sauter, S.P. Howard, and V. Braun In vivo evidence for TonB dimerization J. Bacteriol. 185 2003 5747 5754
25. J. Koedding, P. Howard, L. Kaufmann, P. Polzer, A. Lustig, and W. Welte Dimerization of TonB is not essential for its binding to the outer membrane siderophore receptor FhuA of Escherichia coli J. Biol. Chem. 279 2004 9978 9986
26. J. Ghosh, and K. Postle Disulphide trapping of an in vivo energy-dependent conformation of Escherichia coli TonB protein Mol. Microbiol. 55 2005 276 288
27. R.J. Kadner Vitamin B12 transport in Escherichia coli: energy coupling between membranes Mol. Microbiol. 4 1990 2027 2033
28. H. Schoffler, and V. Braun 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 1989 378 383
29. A. Gudmundsdottir, P.E. Bell, M.D. Lundrigan, C. Bradbeer, and R.J. Kadner Point mutations in a conserved region (TonB box) of Escherichia coli outer membrane protein BtuB affect vitamin B12 transport J. Bacteriol. 171 1989 6526 6533
30. N. Cadieux, and R.J. Kadner 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 1999 10673 10678
31. N. Cadieux, C. Bradbeer, and R.J. Kadner Sequence changes in the Ton box region of BtuB affect its transport activities and interaction with TonB protein J. Bacteriol. 182 2000 5954 5961
32. M. Ogierman, and V. Braun Interactions between the outer membrane ferric citrate transporter FecA and TonB: studies of the FecA TonB box J. Bacteriol. 185 2003 1870 1885
33. H.J. Merianos, N. Cadieux, C.H. Lin, R.J. Kadner, and D.S. Cafiso Substrate-induced exposure of an energy-coupling motif of a membrane transporter Nature Struct. Biol. 7 2000 205 209
34. N. Cadieux, P.G. Phan, D.S. Cafiso, and R.J. Kadner Differential substrate-induced signaling through the TonB-dependent transporter BtuB Proc. Natl Acad. Sci. USA 100 2003 10688 10693
35. M. Braun, H. Killmann, and V. Braun The β-barrel domain of FhuAΔ5-160 is sufficient for TonB-dependent FhuA activities of Escherichia coli Mol. Microbiol. 33 1999 1037 1049
36. D.C. Scott, Z. Cao, Z. Qi, M. Bauler, J.D. Igo, S.M. Newton, and P.E. Klebba Exchangeability of N termini in the ligand-gated porins of Escherichia coli J. Biol. Chem. 276 2001 13025 13033
37. S.P. Howard, C. Herrmann, C.W. Stratilo, and V. Braun 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 2001 5885 5895
38. H. Killmann, C. Herrmann, A. Torun, G. Jung, and V. Braun TonB of Escherichia coli activates FhuA through interaction with the β-barrel Microbiology 148 2002 3497 3509
39. H.L. Vakharia, and K. Postle FepA with globular domain deletions lacks activity J. Bacteriol. 184 2002 5508 5512
40. M. Braun, F. Endriss, H. Killmann, and V. Braun In vivo reconstitution of the FhuA transport protein of Escherichia coli K-12 J. Bacteriol. 185 2003 5508 5518
41. J. Ghosh, and K. Postle Evidence for dynamic clustering of carboxy-terminal aromatic amino acids in TonB-dependent energy transduction Mol. Microbiol. 51 2004 203 213
42. C.M. Khursigara, G. De Crescenzo, P.D. Pawelek, and J.W. Coulton 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 2005 1266 1273
43. C.M. Khursigara, G. De Crescenzo, P.D. Pawelek, and J.W. Coulton Kinetic analyses reveal multiple steps in forming TonB-FhuA complexes from Escherichia coli Biochemistry 44 2005 3441 3453
44. S. Mandava, L. Makowski, S. Devarapalli, J. Uzubell, and D.J. Rodi RELIC - a bioinformatics server for combinatorial peptide analysis and identification of protein-ligand interaction sites Proteomics 4 2004 1439 1460
45. L. Makowski, and A. Soares Estimating the diversity of peptide populations from limited sequence data Bioinformatics 19 2003 483 489
46. D.J. Rodi, A.S. Soares, and L. Makowski Quantitative assessment of peptide sequence diversity in M13 combinatorial peptide phage display libraries J. Mol. Biol. 322 2002 1039 1052
47. D.J. Rodi, R.W. Janes, H.J. Sanganee, R.A. Holton, B.A. Wallace, and L. Makowski Screening of a library of phage-displayed peptides identifies human Bcl-2 as a taxol-binding protein J. Mol. Biol. 285 1999 197 203
48. T.J. Barnard, M.E. Watson, and M.A. McIntosh Mutations in the Escherichia coli receptor FepA reveal residues involved in ligand binding and transport Mol. Microbiol. 41 2001 527 536
49. R. Chakraborty, E.A. Lemke, Z. Cao, P.E. Klebba, and D. van der Helm Identification and mutational studies of conserved amino acids in the outer membrane receptor protein. FepA, which affect transport but not binding of ferric-enterobactin in Escherichia coli Biometals 16 2003 507 518
50. M.B. Zwick, L.L. Bonnycastle, K.A. Noren, S. Venturini, E. Leong, and C.F. Barbas The maltose-binding protein as a scaffold for monovalent display of peptides derived from phage libraries Anal. Biochem. 264 1998 87 97
51. G.S. Moeck, and L. Letellier Characterization of in vitro interactions between a truncated TonB protein from Escherichia coli and the outer membrane receptors FhuA and FepA J. Bacteriol. 183 2001 2755 2764
52. G.S. Moeck, P. Tawa, H. Xiang, A.A. Ismail, J.L. Turnbull, and J.W. Coulton Ligand-induced conformational change in the ferrichrome-iron receptor of Escherichia coli K-12 Mol. Microbiol. 22 1996 459 471
53. G.M. Morris, D.S. Goodsell, R.S. Halliday, R. Huey, W.E. Hart, R.K. Belew, and A.J. Olson Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 19 1998 1639 1662