TonB interacts with BtuF, the Escherichia coli periplasmic binding protein for cyanocobalamin

Biochemistry

Volumn 48, Issue 39, 2009, Pages 9212-9220

  James, Karron J ^a   Hancock, Mark A ^a   Gagnon, Jean Nicolas ^a   Coulton, James W ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ISOTHERMS; BINDING MODELS; BINDING PROTEINS; CYTOPLASMIC MEMBRANE; DATA SUPPORT; DIRECT CONTACT; HETERODIMERS; HYDRODYNAMIC RADIUS; INTERACTION KINETICS; INTRINSIC FLUORESCENCE; NUTRIENT UPTAKE; OUTER MEMBRANE; PHAGE DISPLAY; POTENTIAL BINDING; PROTEIN-PROTEIN INTERACTIONS;

ATMOSPHERIC TEMPERATURE; CELL MEMBRANES; ESCHERICHIA COLI; FLUID DYNAMICS; SURFACE PLASMON RESONANCE;

BINDING ENERGY;

BTUF PROTEIN; CYANOCOBALAMIN; HETERODIMER; PERIPLASMIC BINDING PROTEIN; PROTEIN TONB; UNCLASSIFIED DRUG;

ARTICLE; ESCHERICHIA COLI; FLUORESCENCE; HYDRODYNAMICS; KINETICS; LIGHT SCATTERING; NONHUMAN; NUTRIENT; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SURFACE PLASMON RESONANCE;

AMINO ACID SEQUENCE; DIMERIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PERIPLASMIC BINDING PROTEINS; PROTEIN BINDING; RECEPTORS, CELL SURFACE; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; VITAMIN B 12;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 70349629987     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900722p     Document Type: Article

References (38)

1. Braun, V., Killmann, H., and Benz, R. (1994) Energy-coupled transport through the outer membrane of Escherichia coli small deletions in the gating loop convert the FhuA transport protein into a diffusion channel. FEBS Lett. 346, 59-64. (Pubitemid 24183828)
2. Peacock, R. S., Weljie, A. M., Peter, H. S., Price, F. D., and Vogel, H. J. (2005) The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J. Mol. Biol. 345, 1185-1197.
3. Khursigara, C. M., De Crescenzo, G., Pawelek, P. D., and Coulton, J. W. (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.
4. Kaserer, W. A., Jiang, X., Xiao, Q., Scott, D. C., Bauler, M., Copeland, D., Newton, S. M., and Klebba, P. E. (2008) Insight from TonB hybrid proteins into the mechanism of iron transport through the outer membrane. J. Bacteriol. 190, 4001-4016. (Pubitemid 351732880)
5. Ogierman, M., and Braun, V. (2003) Interactions between the outer membrane ferric citrate transporter FecA and TonB: studies of the FecA TonB box. J. Bacteriol. 185, 1870-1885. (Pubitemid 36297887)
6. Cadieux, N., and Kadner, R. J. (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. U.S.A. 96, 10673-10678.
7. Pawelek, P. D., Croteau, N., Ng-Thow-Hing, C., Khursigara, C. M., Moiseeva, N., Allaire, M., and Coulton, J. W. (2006) Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312, 1399-1402.
8. Shultis, D. D., Purdy, M. D., Banchs, C. N., and Wiener, M. C. (2006) Outer membrane active transport: structure of the BtuB:TonB complex. Science 312, 1396-1399. (Pubitemid 43839554)
9. Larsen, R. A., Thomas, M. G., and Postle, K. (1999) Protonmotive force, ExbB and ligand-bound FepA drive conformational changes in TonB. Mol. Microbiol. 31, 1809-1824.
10. Ghosh, J., and Postle, K. (2005) Disulphide trapping of an in vivo energy-dependent conformation of Escherichia coli TonB protein. Mol. Microbiol. 55, 276-288.
11. Braun, V. (2003) Iron uptake by Escherichia coli. Front. Biosci. 8, s1409-s1421.
12. Cadieux, N., Bradbeer, C., Reeger-Schneider, E., Koster, W., Mohanty, A. K., Wiener, M. C., and Kadner, R. J. (2002) Identification of the periplasmic cobalamin-binding protein BtuF of Escherichia coli. J. Bacteriol. 184, 706-717. (Pubitemid 34150217)
13. Hvorup, R. N., Goetz, B. A., Niederer, M., Hollenstein, K., Perozo, E., and Locher, K. P. (2007) Asymmetry in the structure of the ABC transporter-binding protein complex BtuCD-BtuF. Science 317, 1387-1390. (Pubitemid 47417478)
14. Braun, V., and Endriss, F. (2007) Energy-coupled outer membrane transport proteins and regulatory proteins. Biometals 20, 219-231. (Pubitemid 46776586)
15. Borths, E. L., Locher, K. P., Lee, A. T., and Rees, D. C. (2002) The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter. Proc. Natl. Acad. Sci. U.S.A. 99, 16642-16647.
16. Karpowich, N. K., Huang, H. H., Smith, P. C., and Hunt, J. F. (2003) Crystal structures of the BtuF periplasmic-binding protein for vitamin B12 suggest a functionally important reduction in protein mobility upon ligand binding. J. Biol. Chem. 278, 8429-8434.
17. Clarke, T. E., Ku, S. Y., Dougan, D. R., Vogel, H. J., and Tari, L. W. (2000) The structure of the ferric siderophore binding protein FhuD complexed with gallichrome. Nat. Struct. Biol. 7, 287-291.
18. Ho, W. W., Li, H., Eakanunkul, S., Tong, Y., Wilks, A., Guo, M., and Poulos, T. L. (2007) Holo- and apo-bound structures of bacterial periplasmic heme-binding proteins. J. Biol. Chem. 282, 35796-35802.
19. Lawrence, M. C., Pilling, P. A., Epa, V. C., Berry, A. M., Ogunniyi, A. D., and Paton, J. C. (1998) The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure 6, 1553-1561.
20. Lee, Y. H., Deka, R. K., Norgard, M. V., Radolf, J. D., and Hasemann, C. A. (1999) Treponema pallidum TroA is a periplasmic zinc-binding protein with a helical backbone. Nat. Struct. Biol. 6, 628-633.
21. Carter, D. M., Miousse, I. R., Gagnon, J.-N., Martinez, E., Clements, A., Lee, J., Hancock, M. A., Gagnon, H., Pawelek, P. D., and Coulton, J. W. (2006) Interactions between TonB from Escherichia coli and the periplasmic protein FhuD. J. Biol. Chem. 281, 35413-35424.
22. Khursigara, C. M., De Crescenzo, G., Pawelek, P. D., and Coulton, J. W. (2005) Kinetic analyses reveal multiple steps in forming TonB-FhuA complexes from Escherichia coli. Biochemistry 44, 3441-3453. (Pubitemid 40322014)
23. Carter, D. M., Gagnon, J.-N., Damlaj, M., Mandava, S., Makowski, L., Rodi, D. J., Pawelek, P. D., and Coulton, J. W. (2006) Phage display reveals multiple contact sites between FhuA, an outer membrane receptor of Escherichia coli, and TonB. J. Mol. Biol. 357, 236-251.
24. James, K. J., Hancock, M. A., Moreau, V., Molina, F., and Coulton, J. W. (2008) TonB induces conformational changes in surface-exposed loops of FhuA, outer membrane receptor of Escherichia coli. Protein Sci. 17, 1679-1688.
25. Mandava, S., Makowski, L., Devarapalli, S., Uzubell, J., and Rodi, D. J. (2004) RELIC - a bioinformatics server for combinatorial peptide analysis and identification of protein-ligand interaction sites. Proteomics 4, 1439-1460. (Pubitemid 38648034)
26. Endriss, F., Braun, M., Killmann, H., and Braun, V. (2003) Mutant analysis of the Escherichia coli FhuA protein reveals sites of FhuA activity. J. Bacteriol. 185, 4683-4692. (Pubitemid 36962274)
27. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619.
28. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) Computer-aided interpretation of analytical sedimentation data for proteins, in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S., Rowe, A., and Horton, J., Eds.) pp 90-125, Royal Society of Chemistry, London.
29. Blondel, A., and Bedouelle, H. (1990) Export and purification of a cytoplasmic dimeric protein by fusion to the maltose-binding protein of Escherichia coli. Eur. J. Biochem. 193, 325-330.
30. Sangrar, W., Gabel, B. R., Boffa, M. B., Walker, J. B., Hancock, M. A., Marcovina, S. M., Horrevoets, A. J., Nesheim, M. E., and Koschinsky, M. L. (1997) The solution phase interaction between apolipoprotein(a) and plasminogen inhibits the binding of plasminogen to a plasmin-modified fibrinogen surface. Biochemistry 36, 10353-10363. (Pubitemid 27374127)
31. Borths, E. L., Poolman, B., Hvorup, R. N., Locher, K. P., and Rees, D. C. (2005) In vitro functional characterization of BtuCD-F, the Escherichia coli ABC transporter for vitamin B12 uptake. Biochemistry 44, 16301-16309.
32. Brewer, S., Tolley, M., Trayer, I. P., Barr, G. C., Dorman, C. J., Hannavy, K., Higgins, C. F., Evans, J. S., Levine, B. A., and Wormald, M. R. (1990) Structure and function of X-Pro dipeptide repeats in the TonB proteins of Salmonella typhimurium and Escherichia coli. J. Mol. Biol. 216, 883-895.
33. Kodding, J., Killig, F., Polzer, P., Howard, S. P., Diederichs, K., and Welte, W. (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.
34. Koedding, J., Howard, P., Kaufmann, L., Polzer, P., Lustig, A., and Welte, W. (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.
35. Chang, C., Mooser, A., Pluckthun, A., and Wlodawer, A. (2001) Crystal structure of the dimeric C-terminal domain of TonB reveals a novel fold. J. Biol. Chem. 276, 27535-27540.
36. Kandt, C., Xu, Z., and Tieleman, D. P. (2006) Opening and closing motions in the periplasmic vitamin B12 binding protein BtuF. Biochemistry 45, 13284-13292. (Pubitemid 44707688)
37. Kadner, R. J., and McElhaney, G. (1978) Outer membrane-dependent transport systems in Escherichia coli: turnover of TonB function. J. Bacteriol. 134, 1020-1029.
38. Richarme, G., and Caldas, T. D. (1997) Chaperone properties of the bacterial periplasmic substrate-binding proteins. J. Biol. Chem. 272, 15607-15612.