Comparative Analysis of Structural and Dynamic Properties of the Loaded and Unloaded Hemophore HasA: Functional Implications

Journal of Molecular Biology

Volumn 376, Issue 2, 2008, Pages 517-525

  Wolff, Nicolas ^a   Izadi Pruneyre, Nadia ^a   Couprie, Joël ^a   Habeck, Michael ^b   Linge, Jens ^b   Rieping, Wolfgang ^b   Wandersman, Cécile ^a   Nilges, Michael ^b   Delepierre, Muriel ^a   Lecroisey, Anne ^a  

^a CNRS   (France)

^b Unité de Bioinformatique Structurale   (France)

Author keywords

dynamics; hemophore; NMR; Serratia marcescens; structure

Indexed keywords

BACTERIAL PROTEIN; IRON; PROTEIN HAS A; PROTEIN HAS R; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GRAM NEGATIVE ANAEROBIC BACTERIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; SERRATIA MARCESCENS; THREE DIMENSIONAL IMAGING;

NEGIBACTERIA; SERRATIA MARCESCENS;

EID: 38349194082     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.11.072     Document Type: Article

References (42)

1. Wandersman C., and Delepelaire P. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 58 (2004) 611-647
2. Ghigo J.M., Letoffe 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
3. Letoffe 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
4. Deniau C., Gilli R., Izadi-Pruneyre N., Letoffe 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
5. 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. Nat. Struct. Biol. 6 (1999) 516-520
6. Wolff N., Deniau C., Letoffe S., Simenel C., Kumar V., Stojiljkovic I., et al. Histidine pK(a) shifts and changes of tautomeric states induced by the binding of gallium-protoporphyrin IX in the hemophore HasA(SM). Protein Sci. 11 (2002) 757-765
7. 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
8. Letoffe 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
9. Letoffe 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
10. Deniau C., Couprie J., Simenel C., Kumar V., Stojiljkovic I., Wandersman C., et al. 1H, 15N and 13C resonance assignments for the gallium protoporphyrin IX-HasA(sm) hemophore complex. J. Biomol. NMR 21 (2001) 189-190
11. Lipari G.S., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104 (1982) 4559-4570
12. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104 (1982) 4546-4559
13. Clore G.M., Szabo A., Bax A., Kay L.E., Driscoll P.C., and Gronenborn A.M. Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 112 (1990) 4989-4991
14. Lee L.K., Rance M., Chazin W.J., and Palmer III A.G. Rotational diffusion anisotropy of proteins from simultaneous analysis of 15N and 13C alpha nuclear spin relaxation. J. Biomol. NMR 9 (1997) 287-298
15. Brüschweiler R., Morikis D., and Wright P.E. Hydration of the partially folded peptide RN-24 studied by multidimensional NMR. J. Biomol. NMR 5 (1995) 353-356
16. Mispelter J., Izadi-Pruneyre N., Quiniou E., and Adjadj E. Simple and accurate determination of global tau(R) in proteins using (13)C or (15)N relaxation data. J. Magn. Reson. 143 (2000) 229-232
17. Baker H.M., Anderson B.F., and Baker E.N. Dealing with iron: common structural principles in proteins that transport iron and heme. Proc. Natl Acad. Sci. USA 100 (2003) 3579-3583
18. Clarke T.E., Tari L.W., and Vogel H.J. Structural biology of bacterial iron uptake systems. Curr. Top. Med. Chem. 1 (2001) 7-30
19. Schneider S., Sharp K.H., Barker P.D., and Paoli M. An induced fit conformational change underlies the binding mechanism of the heme transport proteobacteria-protein HemS. J. Biol. Chem. 281 (2006) 32606-32610
20. Gunasekaran K., Ma B., and Nussinov R. Triggering loops and enzyme function: identification of loops that trigger and modulate movements. J. Mol. Biol. 332 (2003) 143-159
21. Gunasekaran K., and Nussinov R. Modulating functional loop movements: the role of highly conserved residues in the correlated loop motions. ChemBioChem 5 (2004) 224-230
22. Flores S., Echols N., Milburn D., Hespenheide B., Keating K., Lu J., et al. The Database of Macromolecular Motions: new features added at the decade mark. Nucleic Acids Res. 34 (2006) D296-D301
23. Grunberg R., Nilges M., and Leckner J. Flexibility and conformational entropy in protein-protein binding. Structure 14 (2006) 683-693
24. Aparicio R., Ferreira S.T., and Polikarpov I. Closed conformation of the active site loop of rabbit muscle triosephosphate isomerase in the absence of substrate: evidence of conformational heterogeneity. J. Mol. Biol. 334 (2003) 1023-1041
25. Koshland D.E. Application of a theory of enzyme specificity to protein synthesis. Proc. Natl Acad. Sci. USA 44 (1958) 98-104
26. 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
27. Izadi-Pruneyre N., Wolff N., Castagne 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
28. 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
29. 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
30. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
31. Bartels C., Xia T.-H., Billeter M., Güntert P., and Wüthrich K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR 6 (1995) 1-10
32. Wishart D.S., Bigam C.G., Yao J., Abildgaard F., Dyson H.J., Oldfield E., et al. 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6 (1995) 135-140
33. α coupling constants as a probe for protein backbone conformation. J. Biomol. NMR 3 (1993) 67-80
34. α J couplings in calcium-free calmodulin using new 2D and 3D water-flip-back methods. J. Biomol. NMR 4 (1994)
35. Habeck M., Rieping W., Linge J.P., and Nilges M. NOE assignment with ARIA 2.0: the nuts and bolts. Methods Mol. Biol. 278 (2004) 379-402
36. Rieping W., Habeck M., Bardiaux B., Bernard A., Malliavin T.E., and Nilges M. ARIA2: automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 23 (2007) 381-382
37. 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 Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
38. Nilges M., Macias M.J., O'Donoghue S.I., and Oschkinat H. Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from beta-spectrin. J. Mol. Biol. 269 (1997) 408-422
39. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., and Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8 (1996) 477-486
40. Vriend, G. (1990). WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8, 52-56, 29.
41. Palmer III A.G., Rance M., and Wright P.E. Intramolecular motions of a zinc finger DNA-binding domain from Xfin characterized by proton-detected natural abundance carbon-13 heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113 (1991) 4371-4380
42. Mandel A.M., Akke M., and Palmer III A.G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246 (1995) 144-163