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Science 2 June 2006:
Vol. 312. no. 5778, pp. 1399 - 1402
DOI: 10.1126/science.1128057
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Reports

Structure of TonB in Complex with FhuA, E. coli Outer Membrane Receptor

Peter D. Pawelek,1 Nathalie Croteau,1 Christopher Ng-Thow-Hing,1 Cezar M. Khursigara,1 Natalia Moiseeva,2 Marc Allaire,2 James W. Coulton1*

The cytoplasmic membrane protein TonB spans the periplasm of the Gram-negative bacterial cell envelope, contacts cognate outer membrane receptors, and facilitates siderophore transport. The outer membrane receptor FhuA from Escherichia coli mediates TonB-dependent import of ferrichrome. We report the 3.3 angstrom resolution crystal structure of the TonB carboxyl-terminal domain in complex with FhuA. TonB contacts stabilize FhuA's amino-terminal residues, including those of the consensus Ton box sequence that form an interprotein ß sheet with TonB through strand exchange. The highly conserved TonB residue arginine-166 is oriented to form multiple contacts with the FhuA cork, the globular domain enclosed by the ß barrel.

1 Department of Microbiology and Immunology, McGill University, 3775 University Street, Montreal, Quebec, H3A 2B4, Canada.
2 National Synchrotron Light Source, Brookhaven National Laboratory, Upton, NY 11973–5000, USA.

* To whom correspondence should be addressed. E-mail: james.coulton{at}mcgill.ca

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THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
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S. Eisenbeis, S. Lohmiller, M. Valdebenito, S. Leicht, and V. Braun (2008)
J. Bacteriol. 190, 5230-5238
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TonB-dependent maltose transport by Caulobacter crescentus.
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Insight from TonB Hybrid Proteins into the Mechanism of Iron Transport through the Outer Membrane.
W. A. Kaserer, X. Jiang, Q. Xiao, D. C. Scott, M. Bauler, D. Copeland, S. M. C. Newton, and P. E. Klebba (2008)
J. Bacteriol. 190, 4001-4016
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Predicting the Complex Structure and Functional Motions of the Outer Membrane Transporter and Signal Transducer FecA.
T. Z. Sen, M. Kloster, R. L. Jernigan, A. Kolinski, J. M. Bujnicki, and A. Kloczkowski (2008)
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Dual Roles of the Central Domain of Colicin D tRNase in TonB-mediated Import and in Immunity.
L. Mora, M. Klepsch, R. H. Buckingham, V. Heurgue-Hamard, S. Kervestin, and M. de Zamaroczy (2008)
J. Biol. Chem. 283, 4993-5003
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HasB, the Serratia marcescens TonB Paralog, Is Specific to HasR.
N. Benevides-Matos, C. Wandersman, and F. Biville (2008)
J. Bacteriol. 190, 21-27
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Identification of Novel Surface Proteins of Anaplasma phagocytophilum by Affinity Purification and Proteomics.
Y. Ge and Y. Rikihisa (2007)
J. Bacteriol. 189, 7819-7828
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Siderophore-Based Iron Acquisition and Pathogen Control.
M. Miethke and M. A. Marahiel (2007)
Microbiol. Mol. Biol. Rev. 71, 413-451
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FepA- and TonB-Dependent Bacteriophage H8: Receptor Binding and Genomic Sequence.
W. Rabsch, L. Ma, G. Wiley, F. Z. Najar, W. Kaserer, D. W. Schuerch, J. E. Klebba, B. A. Roe, J. A. L. Gomez, M. Schallmey, et al. (2007)
J. Bacteriol. 189, 5658-5674
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Substrate-dependent transmembrane signaling in TonB-dependent transporters is not conserved.
M. Kim, G. E. Fanucci, and D. S. Cafiso (2007)
PNAS 104, 11975-11980
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Mechanics of Force Propagation in TonB-Dependent Outer Membrane Transport.
J. Gumbart, M. C. Wiener, and E. Tajkhorshid (2007)
Biophys. J. 93, 496-504
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Deletion and Substitution Analysis of the Escherichia coli TonB Q160 Region.
H. Vakharia-Rao, K. A. Kastead, M. I. Savenkova, C. M. Bulathsinghala, and K. Postle (2007)
J. Bacteriol. 189, 4662-4670
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Characterization of the Outer Membrane Receptor ShuA from the Heme Uptake System of Shigella dysenteriae: SUBSTRATE SPECIFICITY AND IDENTIFICATION OF THE HEME PROTEIN LIGANDS.
K. A. Burkhard and A. Wilks (2007)
J. Biol. Chem. 282, 15126-15136
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His20 Provides the Sole Functionally Significant Side Chain in the Essential TonB Transmembrane Domain.
R. A. Larsen, G. E. Deckert, K. A. Kastead, S. Devanathan, K. L. Keller, and K. Postle (2007)
J. Bacteriol. 189, 2825-2833
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Colicin Biology.
E. Cascales, S. K. Buchanan, D. Duche, C. Kleanthous, R. Lloubes, K. Postle, M. Riley, S. Slatin, and D. Cavard (2007)
Microbiol. Mol. Biol. Rev. 71, 158-229
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Identification of amino acid residues required for ferric-anguibactin transport in the outer-membrane receptor FatA of Vibrio anguillarum.
C. S. Lopez, A. F. Alice, R. Chakraborty, and J. H. Crosa (2007)
Microbiology 153, 570-584
   Abstract »    Full Text »    PDF »
Signal transduction pathway of TonB-dependent transporters.
A. D. Ferguson, C. A. Amezcua, N. M. Halabi, Y. Chelliah, M. K. Rosen, R. Ranganathan, and J. Deisenhofer (2007)
PNAS 104, 513-518
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Evidence of Ball-and-chain Transport of Ferric Enterobactin through FepA.
L. Ma, W. Kaserer, R. Annamalai, D. C. Scott, B. Jin, X. Jiang, Q. Xiao, H. Maymani, L. M. Massis, L. C. S. Ferreira, et al. (2007)
J. Biol. Chem. 282, 397-406
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Interactions between TonB from Escherichia coli and the Periplasmic Protein FhuD.
D. M. Carter, I. R. Miousse, J.-N. Gagnon, E. Martinez, A. Clements, J. Lee, M. A. Hancock, H. Gagnon, P. D. Pawelek, and J. W. Coulton (2006)
J. Biol. Chem. 281, 35413-35424
   Abstract »    Full Text »    PDF »
Highlights From The Literature.
(2006)
Physiology 21, 302-306
   Full Text »    PDF »


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Science. ISSN 0036-8075 (print), 1095-9203 (online)