The Crystal Structure of the Secreted Dimeric Form of the Hemophore HasA Reveals a Domain Swapping with an Exchanged Heme Ligand

Journal of Molecular Biology

Volumn 365, Issue 4, 2007, Pages 1176-1186

  Czjzek, Mirjam ^b   Létoffé, Sylvie ^a   Wandersman, Cécile ^a   Delepierre, Muriel ^a   Lecroisey, Anne ^a   Izadi Pruneyre, Nadia ^a  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

domain swapped; HasA; hemophore; S. marcescens

Indexed keywords

HEME; LIGAND; POLYPEPTIDE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; IRON DEFICIENCY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; SERRATIA MARCESCENS; X RAY ANALYSIS;

NEGIBACTERIA; SERRATIA MARCESCENS;

EID: 33845892486     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.063     Document Type: Article

References (34)

1. Létoffé S., Ghigo J.M., and Wandersman C. Iron acquisition from heme and hemoglobin by a Serratia marcescens extracellular protein. Proc. Natl Acad. Sci. USA 91 (1994) 9876-9880
2. 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
3. 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
4. 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. 1281 (2006) 25541-25550
5. 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
6. Arnoux P., Haser R., Izadi N., Lecroisey A., Delepierre M., Wandersman C., and Czjzek M. The crystal structure of HasA, a hemophore secreted by Serratia marcescens. Nature Struct Biol. 6 (1999) 516-520
7. Bennett M.J., Choe S., and Eisenberg D. Refined structure of monomeric diphteria toxin at 2.3 A resolution. Protein Sci. 3 (1994) 1464-1475
8. Yang S., Cho S.S., Levy Y., Levine H., Wolynes P.G., and Onuchic J.N. Domain swapping is a consequence of minimal frustration. Proc. Natl Acad. Sci. USA 101 (2004) 13786-13791
9. Liu Y., and Eisenberg D. 3D domain swapping: as domains continue to swap. Protein Sci. 11 (2002) 1285-1299
10. Izadi-Pruneyre N., Wolff N., Redeker V., Wandersman C., Delepierre M., and Lecroisey A. NMR studies of the C-terminal secretion signal of the haem-binding protein, HasA. Eur. J. Biochem. 261 (1999) 562-568
11. Arnoux P., Haser R., Izadi-Pruneyre N., Lecroisey A., and Czjzek M. Functional aspects of the heme bound hemophore HasA by structural analysis of various crystal forms. Proteins: Struct. Funct. Genet. 41 (2000) 202-210
12. 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
13. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 33 (1968) 491-497
14. Caillet-Saguy C., Delepierre M., Lecroisey A., Bertini I., Piccioli M., and Turano P. Direct-detected 13C NMR to investigate the iron(III) hemophore HasA. J. Am. Chem. Soc. 128 (2006) 150-158
15. 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
16. Létoffé S., Nato F., Goldberg M.E., and Wandersman C. Interactions of HasA, a bacterial haemophore, with haemoglobin and with its outer membrane receptor HasR. Mol. Microbiol. 33 (1999) 546-555
17. Wolff N., Sapriel G., Bodenreider C., Chaffotte A., and Delepelaire P. Antifolding activity of the SecB chaperone is essential for secretion of HasA, a quickly folding ABC pathway substrate. J. Biol. Chem. 278 (2003) 38247-38253
18. Rousseau F., Schymkowitz J.W., Wilkinson H.R., and Itzhaki L.S. Three-dimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues. Proc. Natl Acad. Sci. USA 98 (2001) 5596-5601
19. Rousseau F., Schymkowitz J.W., and Itzhaki L.S. The unfolding story of three-dimensional domain swapping. Review. Structure 11 (2003) 243-245
20. Delepelaire P., and Wandersman C. The SecB chaperone is involved in the secretion of the Serratia marcescens HasA protein through an ABC transporter. EMBO J. 17 (1998) 936-944
21. Debarbieux L., and Wandersman C. Folded HasA inhibits its own secretion through its ABC exporter. EMBO J. 20 (2001) 4657-4663
22. Saint-Jean A.P., Phillips K.R., Creighton D.J., and Stone M.J. Active monomeric and dimeric forms of Pseudomonas putida Glyoxalase I : evidence for 3D domain swapping. Biochemistry 37 (1998) 10345-10353
23. Vitagliano L., Adinolfi S., Sica F., Merlino A., Zagari A., and Mazzarella L. A potential allosteric subsite generated by domain swapping in bovine seminal ribonuclease. J. Mol. Biol. 293 (1999) 569-577
24. Barrientos L.G., and Gronenborn A.M. The highly specific carbohydrate-binding protein cyanovirin-N: structure, anti-HIV/Ebola activity and possibilities for therapy. Mini. Rev. Med. Chem. 5 (2005) 21-31
25. 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
26. Gattoni M., Boffi A., Sarti P., and Chiancone E. Stability of the heme-globin linkage in alphabeta dimers and isolated chains of human hemoglobin. A study of the heme transfer reaction from the immobilized proteins to albumin. J. Biol. Chem. 271 (1996) 10130-10136
27. Dawson R.M.C., Elliott D.C., Elliott W.H., and Jones K.M. Porphyrins and related compounds. In Data for Biochemical Research (1986), Oxford University Press, Oxford, England 230-231
28. Sigurskjold B.W. Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal. Biochem. 277 (2000) 260-266
29. Kay L.E., Keifer E.P., and Saarinen T. Pure absorption gradient enhanced heteronuclear single quantum correlation with improved sensitivity. J. Am. Chem. Soc. 114 (1992) 10663-10665
30. Leslie A.G.W. Mosflm. In Crystallographic Computing (1990), Oxford University Press 50-61
31. CCP4. The CCP4 Suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
32. Navaza J. AmoRe: an automated package for molecular replacement. Acta Crystallog. sect. A 50 (1994) 157-163
33. Perrakis A., Sixma T.K., Wilson K.S., and Lamzin V.S. wARP: improvement and extension of crystallographic phases by weighted averaging of multiple-refined dummy atomic models. Acta Crystallog. sect. D 53 (1997) 448-455
34. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291