Structural evidence for iron-free citrate and ferric citrate binding to the TonB-dependent outer membrane transporter FecA

Journal of Molecular Biology

Volumn 332, Issue 2, 2003, Pages 353-368

  Yue, Wyatt W ^a,b   Grizot, Sylvestre ^a   Buchanan, Susan K ^a,b  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Active transport; FecA; Ferric citrate; Outer membrane protein; TonB

Indexed keywords

CITRIC ACID; FECABCDE PROTEIN; FERRIC CITRATE; OUTER MEMBRANE PROTEIN; PROTEIN; PROTEIN FECA; SIDEROPHORE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONFORMATION; CYTOPLASM; LIGAND BINDING; MEMBRANE TRANSPORT; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN STRUCTURE;

ESCHERICHIA COLI;

EID: 0042508859     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00855-6     Document Type: Article

References (60)

1. Raymond K.N., Carrano C.J. Coordination chemistry and microbial iron transport. Accts Chem. Res. 12:1979;183-190.
2. Aisen P., Leibman A., Zweier J. Stoichiometric and site characteristics of the binding of iron to human transferrin. J. Biol. Chem. 253:1978;1930-1937.
3. 3+. Clin. Chem. 33:1987;405-407.
4. Kretchmar S.A., Reyes Z.E., Raymond K.N. The spectroelectrochemical determination of the reduction potential of diferric serum transferrin. Biochim. Biophys. Acta. 956:1988;85-94.
5. Guerinot M.L. Microbial iron transport. Annu. Rev. Microbiol. 48:1994;743-772.
6. Bos C., Lorenzen D., Braun V. Specific in vivo labeling of cell surface-exposed protein loops: reactive cysteines in the predicted gating loop mark a ferrichrome binding site and a ligand-induced conformational change of the Escherichia coli FhuA protein. J. Bacteriol. 180:1998;605-613.
7. Neilands J.B. Siderophores: structure and function of microbial iron transport compounds. J. Biol. Chem. 270:1995;26723-26726.
8. Moeck G.S., Coulton J.W. TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol. Microbiol. 28:1998;675-681.
9. Skare J.T., Ahmer B.M., Seachord C.L., Darveau R.P., Postle K. 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.
10. Torres A.G., Redford P., Welch R.A., Payne S.M. TonB-dependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect. Immun. 69:2001;6179-6185.
11. Law D., Kelly J. Use of heme and hemoglobin by Escherichia coli O157 and other Shiga-like-toxin-producing E. coli serogroups. Infect. Immun. 63:1995;700-702.
12. Jacoboni I., Martelli P.L., Fariselli P., De Pinto V., Casadio R. Prediction of the transmembrane regions of beta-barrel membrane proteins with a neural network-based predictor. Protein Sci. 10:2001;779-787.
13. Wimley W.C. Toward genomic identification of beta-barrel membrane proteins: composition and architecture of known structures. Protein Sci. 11:2002;301-312.
14. Molloy M.P., Herbert B.R., Slade M.B., Rabilloud T., Nouwens A.S., Williams K.L., Gooley A.A. Proteomic analysis of the Escherichia coli outer membrane. Eur. J. Biochem. 267:2000;2871-2881.
15. Buchanan S.K., Smith B.S., Venkatramani L., Xia D., Esser L., Palnitkar M., et al. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nature Struct. Biol. 6:1999;56-63.
16. Ferguson A.D., Hofmann E., Coulton J.W., Diederichs K., Welte W. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science. 282:1998;2215-2220.
17. Locher K.P., Rees B., Koebnik R., Mitschler A., Moulinier L., Rosenbusch J.P., Moras D. Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell. 95:1998;771-778.
18. Braun V., Braun M. Iron transport and signaling in Escherichia coli. FEBS Letters. 529:2002;78.
19. Hussein S., Hantke K., Braun V. Citrate-dependent iron transport system in Escherichia coli K-12. Eur. J. Biochem. 117:1981;431-437.
20. Loomis L.D., Raymond K.N. Solution equilibria of enterobactin and metal-enterobactin complexes. Inorg. Chem. 30:1991;906-911.
21. Pierre J.L., Gautier-Luneau I. Iron and citric acid: a fuzzy chemistry of ubiquitous biological relevance. Biometals. 13:2000;91-96.
22. Pressler U., Staudenmaier H., Zimmermann L., Braun V. Genetics of the iron dicitrate transport system of Escherichia coli. J. Bacteriol. 170:1988;2716-2724.
23. Staudenmaier H., Van Hove B., Yaraghi Z., Braun V. Nucleotide sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic-binding-protein-dependent transport mechanism for iron(III) dicitrate in Escherichia coli. J. Bacteriol. 171:1989;2626-2633.
24. Harle C., Kim I., Angerer A., Braun V. Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J. 14:1995;1430-1438.
25. Kim I., Stiefel A., Plantor S., Angerer A., Braun V. Transcription induction of the ferric citrate transport genes via the N-terminus of the FecA outer membrane protein, the Ton system and the electrochemical potential of the cytoplasmic membrane. Mol. Microbiol. 23:1997;333-344.
26. Zimmermann L., Hantke K., Braun V. Exogenous induction of the iron dicitrate transport system of Escherichia coli K-12. J. Bacteriol. 159:1984;271-277.
27. Ogierman M., Braun V. Interactions between the outer membrane ferric citrate transporter FecA and TonB: studies of the FecA TonB box. J. Bacteriol. 185:2003;1870-1885.
28. Enz S., Mahren S., Stroeher U.H., Braun V. Surface signaling in ferric citrate transport gene induction: interaction of the FecA, FecR, and FecI regulatory proteins. J. Bacteriol. 182:2000;637-646.
29. Stiefel A., Mahren S., Ochs M., Schindler P.T., Enz S., Braun V. Control of the ferric citrate transport system of Escherichia coli: mutations in region 2.1 of the FecI extracytoplasmic-function sigma factor suppress mutations in the FecR transmembrane regulatory protein. J. Bacteriol. 183:2001;162-170.
30. Mahren S.V.B. The FecI extracytoplasmic-function sigma factor of Escherichia coli interacts with the B′ subunit of RNA polymerase. J. Bacteriol. 185:2003;1796-1802.
31. Newton S.M., Igo J.D., Scott D.C., Klebba P.E. Effect of loop deletions on the binding and transport of ferric enterobactin by FepA. Mol. Microbiol. 32:1999;1153-1165.
32. Locher K.P., Rosenbusch J.P. Oligomeric states and siderophore binding of the ligand-gated FhuA protein that forms channels across Escherichia coli outer membranes. Eur. J. Biochem. 247:1997;770-775.
33. 3+. J. Inorg. Biochem. 28:1986;181-187.
34. Wagegg W., Braun V. Ferric citrate transport in Escherichia coli requires outer membrane receptor protein FecA. J. Bacteriol. 145:1981;156-163.
35. Stintzi A., Barnes C., Xu J., Raymond K.N. Microbial iron transport via a siderophore shuttle: a membrane ion transport paradigm. Proc. Natl Acad. Sci. USA. 97:2000;10691-10696.
36. Schalk I.J., Hennard C., Dugave C., Poole K., Abdallah M.A., Pattus F. Iron-free pyoverdin binds to its outer membrane receptor FpvA in Pseudomonas aeruginosa: a new mechanism for membrane iron transport. Mol. Microbiol. 39:2001;351-360.
37. Ferguson A.D., Chakraborty R., Smith B.S., Esser L., van_der_Helm D., Deisenhofer J. Structural basis of gating by the outer membrane transporter FecA. Science. 295:2002;1715-1719.
38. Lin J., Hogan J.S., Smith K.L. Antigenic homology of the inducible ferric citrate receptor (FecA) of coliform bacteria isolated from herds with naturally occurring bovine intramammary infections. Clin. Diag. Lab. Immunol. 6:1999;966-969.
39. Braun V. Surface signaling: novel transcription initiation mechanism starting from the cell surface. Arch. Microbiol. 167:1997;325-331.
40. Shweky I., Bino A., Goldberg D.P., Lippard S.J. Syntheses, structures, and magnetic properties of two dinuclear iron(III) citrate complexes. Inorg. Chem. 33:1994;5161-5162.
41. Chimento D.P., Mohanty A.K., Kadner R.J., Wiener M.C. Substrate-induced transmembrane signaling in the cobalamin trnasporter BtuB. Nature Struct. Biol. 10:2003;394-401.
42. Lundrigan M.D., Kadner R.J. Nucleotide sequence of the gene for the ferrienterochelin receptor FepA in Escherichia coli. Homology among outer membrane receptors that interact with TonB. J. Biol. Chem. 261:1986;10797-10801.
43. Schalk I.J., Kyslik P., Prome D., van Dorsselaer A., Poole K., Abdallah M.A., Pattus F. Copurification of the FpvA ferric pyoverdin receptor of Pseudomonas aeruginosa with its iron-free ligand: implications for siderophore-mediated iron transport. Biochemistry. 38:1999;9357-9365.
44. Schalk I.J., Abdallah M.A., Pattus F. Recycling of pyoverdin on the FpvA receptor after ferric pyoverdin uptake and dissociation in Pseudomonas aeruginosa. Biochemistry. 41:2002;1663-1671.
45. Frost G.E., Rosenberg H. The inducible citrate-dependent iron transport system in Escherichia coli K12. Biochim. Biophys. Acta. 330:1973;90-101.
46. Hancock R.E.W., Hantke K., Braun V. Iron transport in Escherichia coli K-12: involvement of the colicin B receptor and of a citrate-inducible protein. J. Bacteriol. 127:1976;1370-1375.
47. Woodrow G.C., Langman L., Young I.G., Gibson F. Mutations affecting the citrate-dependent iron uptake system in Escherichia coli. J. Bacteriol. 13:1978;1524-1526.
48. Visca P., Leoni L., Wilson M.J., Lamont I.L. Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol. Microbiol. 45:2002;1177-1190.
49. Beare P.A., For R.J., Martin L.W., Lamont I.L. Siderophore-mediated cell signalling in Pseudomonas aeruginosa: divergent pathways regulate virulence factor prodcution and siderophore receptor synthesis. Mol. Microbiol. 47:2003;195-207.
50. Zhou X.H., van der Helm D. A novel purification of ferric citrate receptor (FecA) from Escherichia coli UT5600 and further characterization of its binding activity. Biometals. 6:1993;37-44.
51. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Acta Crystallog. sect. D. 276:1997;307-326.
52. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallog. 30:1997;1022-1025.
53. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
54. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
55. 2O. J. Am. Chem. Soc. 120:1998;13266-13267.
56. Kleywegt G.J. Experimental assessment of differences between related protein crystal structures. Acta Crystallog. sect. D. 55:1999;1878-1884.
57. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
58. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. Procheck-a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
59. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
60. Merritt E.A., Bacon D.J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.