Modulation by Substrates of the Interaction between the HasR Outer Membrane Receptor and Its Specific TonB-like Protein, HasB

Journal of Molecular Biology

Volumn 378, Issue 4, 2008, Pages 840-851

  Lefèvre, Julien ^a   Delepelaire, Philippe ^a   Delepierre, Muriel ^a   Izadi Pruneyre, Nadia ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

HasB; heme transport; signal transduction; TonB

Indexed keywords

HEME; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; PROTEIN HASB; PROTEIN HASR; PROTEIN TONB; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; ENTHALPY; ENTROPY; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STOICHIOMETRY;

NEGIBACTERIA; SERRATIA MARCESCENS;

EID: 41949109350     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.03.044     Document Type: Article

References (51)

1. Kadner R.J. Vitamin B12 transport in Escherichia coli: energy coupling between membranes. Mol. Microbiol. 4 (1990) 2027-2033
2. Postle K. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25 (1993) 591-601
3. Larsen R.A., Myers P.S., Skare J.T., Seachord C.L., Darveau R.P., and Postle K. Identification of TonB homologs in the family Enterobacteriaceae and evidence for conservation of TonB-dependent energy transduction complexes. J. Bacteriol. 178 (1996) 1363-1373
4. Ferguson A.D., Hofmann E., Coulton J.W., Diederichs K., and Welte W. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282 (1998) 2215-2220
5. 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. Nat. Struct. Biol. 6 (1999) 56-63
6. Ferguson A.D., Chakraborty R., Smith B.S., Esser L., van der Helm D., and Deisenhofer J. Structural basis of gating by the outer membrane transporter FecA. Science 295 (2002) 1715-1719
7. Chimento D.P., Mohanty A.K., Kadner R.J., and Wiener M.C. Substrate-induced transmembrane signaling in the cobalamin transporter BtuB. Nat. Struct. Biol. 10 (2003) 394-401
8. Cobessi D., Celia H., and Pattus F. Crystal structure at high resolution of ferric-pyochelin and its membrane receptor FptA from Pseudomonas aeruginosa. J. Mol. Biol. 352 (2005) 893-904
9. Cobessi D., Celia H., Folschweiller N., Schalk I.J., Abdallah M.A., and Pattus F. 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
10. Braun V., and Endriss F. Energy-coupled outer membrane transport proteins and regulatory proteins. Biometals 20 (2007) 219-231
11. Gunter K., and Braun V. In vivo evidence for FhuA outer membrane receptor interaction with the TonB inner membrane protein of Escherichia coli. FEBS Lett. 274 (1990) 85-88
12. Cadieux N., and Kadner R.J. 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
13. Chang C., Mooser A., Pluckthun A., and Wlodawer A. Crystal structure of the dimeric C-terminal domain of TonB reveals a novel fold. J. Biol. Chem. 276 (2001) 27535-27540
14. Kodding J., Killig F., Polzer P., Howard S.P., Diederichs K., and Welte W. 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
15. Sauter A., Howard S.P., and Braun V. In vivo evidence for TonB dimerization. J. Bacteriol. 185 (2003) 5747-5754
16. Ghosh J., and Postle K. Disulphide trapping of an in vivo energy-dependent conformation of Escherichia coli TonB protein. Mol. Microbiol. 55 (2005) 276-288
17. Shultis D.D., Purdy M.D., Banchs C.N., and Wiener M.C. Outer membrane active transport: structure of the BtuB:TonB complex. Science 312 (2006) 1396-1399
18. Pawelek P.D., Croteau N., Ng-Thow-Hing C., Khursigara C.M., Moiseeva N., Allaire M., and Coulton J.W. Structure of TonB in complex with FhuA. E. coli outer membrane receptor. Science 312 (2006) 1399-1402
19. Krewulak, K. D. & Vogel, H. J. (2007). Structural biology of bacterial iron uptake. Biochim. Biophys. Acta, Biomembr., in press. doi:10.1016/j.bbamem.2007.07.026.
20. Eisenhauer H.A., Shames S., Pawelek P.D., and Coulton J.W. Siderophore transport through Escherichia coli outer membrane receptor FhuA with disulfide-tethered cork and barrel domains. J. Biol. Chem. 280 (2005) 30574-30580
21. Ma L., Kaserer W., Annamalai R., Scott D.C., Jin B., Jiang X., et al. Evidence of ball-and-chain transport of ferric enterobactin through FepA. J. Biol. Chem. 282 (2007) 397-406
22. Gumbart J., Wiener M.C., and Tajkhorshid E. Mechanics of force propagation in TonB-dependent outer membrane transport. Biophys. J. 93 (2007) 496-504
23. Kadner R.J., and Heller K.J. Mutual inhibition of cobalamin and siderophore uptake systems suggests their competition for TonB function. J. Bacteriol. 177 (1995) 4829-4835
24. Postle K., and Larsen R.A. TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20 (2007) 453-465
25. Paquelin A., Ghigo J.M., Bertin S., and Wandersman C. Characterization of HasB, a Serratia marcescens TonB-like protein specifically involved in the haemophore-dependent haem acquisition system. Mol. Microbiol. 42 (2001) 995-1005
26. Létoffé S., Ghigo J.M., and Wandersman C. Secretion of the Serratia marcescens HasA protein by an ABC transporter. J. Bacteriol. 176 (1994) 5372-5377
27. Ghigo J.M., Létoffé S., and Wandersman C. A new type of hemophore-dependent heme acquisition system of Serratia marcescens reconstituted in Escherichia coli. J. Bacteriol. 179 (1997) 3572-3579
28. Deniau C., Gilli R., Izadi-Pruneyre N., Létoffé S., Delepierre M., Wandersman C., et al. Thermodynamics of heme binding to the HasA(SM) hemophore: effect of mutations at three key residues for heme uptake. Biochemistry 42 (2003) 10627-10633
29. Izadi-Pruneyre N., Huche F., Lukat-Rodgers G.S., Lecroisey A., Gilli R., Rodgers K.R., et al. The heme transfer from the soluble HasA hemophore to its membrane-bound receptor HasR is driven by protein-protein interaction from a high to a lower affinity binding site. J. Biol. Chem. 281 (2006) 25541-25550
30. Létoffé S., Delepelaire P., and Wandersman C. Free and hemophore-bound heme acquisitions through the outer membrane receptor HasR have different requirements for the TonB-ExbB-ExbD complex. J. Bacteriol. 186 (2004) 4067-4074
31. Khursigara C.M., De Crescenzo G., Pawelek P.D., and Coulton J.W. 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
32. Moeck G.S., and Letellier L. 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
33. Benevides-Matos N., Wandersman C., and Biville F. HasB, the Serratia marcescens TonB paralog, is specific to HasR. J. Bacteriol. 190 (2007) 21-27
34. Koedding J., Howard P., Kaufmann L., Polzer P., Lustig A., and Welte W. 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
35. Larsen R.A., Deckert G.E., Kastead K.A., Devanathan S., Keller K.L., and Postle K. His(20) provides the sole functionally significant side chain in the essential TonB transmembrane domain. J. Bacteriol. 189 (2007) 2825-2833
36. Adams H., Zeder-Lutz G., Schalk I., Pattus F., and Celia H. Interaction of TonB with the outer membrane receptor FpvA of Pseudomonas aeruginosa. J. Bacteriol. 188 (2006) 5752-5761
37. Khursigara C.M., De Crescenzo G., Pawelek P.D., and Coulton J.W. 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
38. Dyson H.J., and Wright P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6 (2005) 197-208
39. Wandersman C., and Delepelaire P. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 58 (2004) 611-647
40. Cwerman H., Wandersman C., and Biville F. Heme and a five-amino-acid hemophore region form the bipartite stimulus triggering the has signaling cascade. J. Bacteriol. 188 (2006) 3357-3364
41. Rossi M.S., Paquelin A., Ghigo J.M., and Wandersman C. Haemophore-mediated signal transduction across the bacterial cell envelope in Serratia marcescens: the inducer and the transported substrate are different molecules. Mol. Microbiol. 48 (2003) 1467-1480
42. Devanathan S., and Postle K. Studies on colicin B translocation: FepA is gated by TonB. Mol. Microbiol. 65 (2007) 441-453
43. Brillet K., Journet L., Célia H., Paulus L., Stahl A., Pattus F., and Cobessi D. A β strand lock exchange for signal transduction in TonB-dependent transducers on the basis of a common structural motif. Structure 15 (2007) 1383-1391
44. Chu B.C., Peacock R.S., and Vogel H.J. Bioinformatic analysis of the TonB protein family. Biometals 20 (2007) 467-483
45. Sean Peacock R., Weljie A.M., Peter Howard S., Price F.D., and Vogel H.J. The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J. Mol. Biol. 345 (2005) 1185-1197
46. Lefèvre J., Simenel C., Delepelaire P., Delepierre M., and Izadi-Pruneyre N. 1H, 13C and 15N resonance assignments of the C-terminal domain of HasB, a specific TonB like protein from Serratia marcescens. Biomol. NMR Assignments 1 (2007) 197-199
47. Izadi-Pruneyre N., Wolff N., Castagné C., Czisch M., Wandersman C., Delepierre M., and Lecroisey A. Backbone NMR assignment and secondary structure of the 19 kDa hemophore HasA. J. Biomol. NMR 14 (1999) 193-194
48. Izadi N., Henry Y., Haladjian J., Goldberg M.E., Wandersman C., Delepierre M., and Lecroisey A. Purification and characterization of an extracellular heme-binding protein, HasA, involved in heme iron acquisition. Biochemistry 36 (1997) 7050-7057
49. Moeck G.S., Tawa P., Xiang H., Ismail A.A., Turnbull J.L., and Coulton J.W. Ligand-induces conformational change in the ferrichrome-iron receptor of E. coli K-12. Mol. Microbiol. 22 (1996) 459-471
50. Létoffé S., Deniau C., Wolff N., Dassa E., Delepelaire P., Lecroisey A., and Wandersman C. Haemophore-mediated bacterial haem transport: evidence for a common or overlapping site for haem-free and haem-loaded haemophore on its specific outer membrane receptor. Mol. Microbiol. 41 (2001) 439-450
51. Létoffé S., Debarbieux L., Izadi N., Delepelaire P., and Wandersman C. Ligand delivery by haem carrier proteins: the binding of Serratia marcescens haemophore to its outer membrane receptor is mediated by two distinct peptide regions. Mol. Microbiol. 50 (2003) 77-88