Structural basis for iron piracy by pathogenic Neisseria

Nature

Volumn 483, Issue 7387, 2012, Pages 53-61

  Noinaj, Nicholas ^a   Easley, Nicole C ^a   Oke, Muse ^a   Mizuno, Naoko ^b   Gumbart, James ^c   Boura, Evzen ^a   Steere, Ashley N ^d   Zak, Olga ^e   Aisen, Philip ^e   Tajkhorshid, Emad ^f   Evans, Robert W ^g   Gorringe, Andrew R ^h   Mason, Anne B ^d   Steven, Alasdair C ^b   Buchanan, Susan K ^a  

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

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^g BRUNEL UNIVERSITY   (United Kingdom)

^h PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; TRANSFERRIN; TRANSFERRIN BINDING PROTEIN A; TRANSFERRIN BINDING PROTEIN B;

BACTERIUM; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; IRON; MEMBRANE; PATHOGENICITY; PROTEIN; SURVIVAL; VACCINE; X-RAY;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; IRON TRANSPORT; NEISSERIA; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

ANIMALS; APOPROTEINS; BACTERIAL PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; CATTLE; CRYSTALLOGRAPHY, X-RAY; HUMANS; IRON; MICE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; NEISSERIA; PROTEIN CONFORMATION; SCATTERING, SMALL ANGLE; SPECIES SPECIFICITY; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFERRIN; TRANSFERRIN-BINDING PROTEIN A; TRANSFERRIN-BINDING PROTEIN B; X-RAY DIFFRACTION;

BACTERIA (MICROORGANISMS); NEISSERIA;

EID: 84857783784     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10823     Document Type: Article

References (52)

1. Deasy, A. & Read, R. C. Challenges for development of meningococcal vaccines in infants and children. Expert Rev. Vaccines 10, 335-343 (2011).
2. Centers for Disease Control and Prevention. Cephalosporin susceptibility among Neisseria gonorrhoeae isolates-United States, 2000-2010. Morbid. Mortal. Weekly Rep. 60, 873-877 (2011).
3. Grifantini, R. et al. Identification of iron-activated and-repressed Fur-dependent genes by transcriptome analysis of Neisseria meningitidis group B. Proc. Natl Acad. Sci. USA 100, 9542-9547 (2003). (Pubitemid 37033964)
4. Noinaj, N., Guillier, M., Barnard, T. J. & Buchanan, S. K. TonB-dependent transporters: regulation, structure, and function. Annu. Rev. Microbiol. 64, 43-60 (2010).
5. Boulton, I. C. et al. Transferrin-binding protein B isolated from Neisseria meningitidis discriminates between apo and diferric human transferrin. Biochem. J. 334, 269-273 (1998).
6. Krell, T. et al. Insight into the structure and functionofthe transferrin receptor from Neisseria meningitidis using microcalorimetric techniques. J. Biol. Chem. 278, 14712-14722 (2003). (Pubitemid 36799794)
7. Anderson, J. E., Sparling, P. F. & Cornelissen, C. N. Gonococcal transferrin-binding protein 2 facilitates but is not essential for transferrin utilization. J. Bacteriol. 176, 3162-3170 (1994). (Pubitemid 24166705)
8. Irwin, S. W., Averil, N., Cheng, C. Y. & Schryvers, A. B. Preparation and analysis of isogenic mutants in the transferrin receptor protein genes, tbpA and tbpB, from Neisseria meningitidis. Mol. Microbiol. 8, 1125-1133 (1993). (Pubitemid 23187031)
9. Rokbi, B. et al. Evaluation of recombinant transferrin-binding protein B variants from Neisseria meningitidis for their ability to induce cross-reactive and bactericidal antibodies against a genetically diverse collection of serogroup B strains. Infect. Immun. 65, 55-63 (1997). (Pubitemid 27008903)
10. Weynants, V. E. et al. Additive and synergistic bactericidal activity of antibodies directed against minor outer membrane proteins of Neisseria meningitidis. Infect. Immun. 75, 5434-5442 (2007). (Pubitemid 350033632)
11. Price, G. A., Masri, H. P., Hollander, A. M., Russell, M. W. & Cornelissen, C. N. Gonococcal transferrin binding protein chimeras induce bactericidal and growth inhibitory antibodies in mice. Vaccine 25, 7247-7260 (2007). (Pubitemid 47464665)
12. Yost-Daljev, M. K. & Cornelissen, C. N. Determination of surface-exposed, functional domainsof gonococcal transferrin-binding proteinA. Infect. Immun. 72, 1775-1785 (2004). (Pubitemid 38263803)
13. Noto, J. M. & Cornelissen, C. N. Identification of TbpA residues required for transferrin-iron utilization by Neisseria gonorrhoeae. Infect. Immun. 76, 1960-1969 (2008). (Pubitemid 351656128)
14. Wally, J. et al. The crystal structure of iron-free human serum transferrin provides insight into inter-lobe communication and receptor binding. J. Biol. Chem. 281, 24934-24944 (2006). (Pubitemid 44274264)
15. Cornelissen, C. N., Biswas, G. D. & Sparling, P. F. Expression of gonococcal transferrin-binding protein 1 causes Escherichia coli to bind human transferrin. J. Bacteriol. 175, 2448-2450 (1993). (Pubitemid 23123522)
16. Schryvers, A. B. & Morris, L. J. Identification and characterization of the transferrin receptor from Neisseria meningitidis. Mol. Microbiol. 2, 281-288 (1988).
17. Stokes, R. H., Oakhill, J. S., Joannou, C. L., Gorringe, A. R. & Evans, R. W. Meningococcal transferrin-binding proteins A and B show cooperation in their binding kinetics for human transferrin. Infect. Immun. 73, 944-952 (2005). (Pubitemid 40165753)
18. Schryvers, A. B. & Gonzalez, G. C. Comparison of the abilities of different protein sources of iron to enhance Neisseria meningitidis infection in mice. Infect. Immun. 57, 2425-2429 (1989). (Pubitemid 19183852)
19. Calmettes, C. et al. Structural variations within the transferrin binding site on transferrin-binding protein B, TbpB. J. Biol. Chem. 286, 12683-12692 (2011).
20. Moraes, T. F., Yu, R. H., Strynadka, N. C. & Schryvers, A. B. Insights into the bacterial transferrin receptor: the structure of transferrin-binding protein B from Actinobacillus pleuropneumoniae. Mol. Cell 35, 523-533 (2009).
21. Cornelissen, C. N., Anderson, J. E. & Sparling, P. F. Characterization of the diversity and the transferrin-binding domain of gonococcal transferrin-binding protein 2. Infect. Immun. 65, 822-828 (1997). (Pubitemid 27053260)
22. Silva, L. P. et al. Conserved interaction between transferrin and transferrin-binding proteins from porcine pathogens. J. Biol. Chem. 286, 21353-21360 (2011).
23. Mason, A. B. et al. Expression, purification, and characterization of authentic monoferric and apo-human serum transferrins. Protein Expr. Purif. 36, 318-326 (2004). (Pubitemid 38893170)
24. Svergun, D. I., Petoukhov, M. V. & Koch, M. H. Determinationofdomain structure of proteins from X-ray solution scattering. Biophys. J. 80, 2946-2953 (2001). (Pubitemid 32521666)
25. Halbrooks, P. J. et al. Investigationofthe mechanismofiron release from the C-lobe of human serum transferrin: mutational analysis of the role of a pH sensitive triad. Biochemistry 42, 3701-3707 (2003). (Pubitemid 36402662)
26. Steere, A. N., Byrne, S. L., Chasteen, N. D. & Mason, A. B. Kinetics ofiron release from transferrin bound to the transferrin receptor at endosomal pH. Biochim. Biophys. Acta http://dx.doi.org/10.1016/j.bbagen.2011.06.003 (2011).
27. Cheng, Y., Zak, O., Aisen, P., Harrison, S. C. & Walz, T. Structure of the human transferrin receptor-transferrin complex. Cell 116, 565-576 (2004). (Pubitemid 38264433)
28. Eckenroth, B. E., Steere, A. N., Chasteen, N. D., Everse, S. J. & Mason, A. B. How the binding of human transferrin primes the transferrin receptor potentiating iron release at endosomal pH. Proc. Natl Acad. Sci. USA 108, 13089-13094 (2011).
29. Hobbs, M. M. et al. Experimental gonococcal infection in male volunteers: cumulative experience with Neisseria gonorrhoeae strains FA1090 andMS11mkC. Front. Microbiol. 2, 123 (2011).
30. Scarselli, M. et al. Rational design of a meningococcal antigen inducing broad protective immunity. Sci. Transl. Med. 3, 91ra62 (2011).
31. Zak, O. & Aisen, P. A new method for obtaining human transferrin C-lobe in the native conformation: preparation and properties. Biochemistry 41, 1647-1653 (2002). (Pubitemid 34112755)
32. Steere, A. N. et al. Properties of a homogeneous C-lobe preparedbyintroduction of a TEV cleavage site between the lobes of human transferrin. Protein Expr. Purif. 72, 32-41 (2010).
33. Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005). (Pubitemid 43078511)
34. Otwinowski, Z. & Minor, W. Processing of X-ray data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
35. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658-674 (2007). (Pubitemid 47080256)
36. Adams, P. D. et al. Phenix: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002). (Pubitemid 35337293)
37. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004). (Pubitemid 41742764)
38. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D 60, 2210-2221 (2004). (Pubitemid 41742773)
39. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODELworkspace:aweb-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (2006). (Pubitemid 43205406)
40. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
41. Petoukhov, M. V. & Svergun, D. I. Analysis of X-ray and neutron scattering from biomacromolecular solutions. Curr. Opin. Struct. Biol. 17, 562-571 (2007). (Pubitemid 350041656)
42. Svergun, O. & Genkina, O. A. The dependenceofthe dynamicsofthe extinctionofa temporary connectionon the recognizabilityofa reinforcing stimulus in Russian. Zh. Vyssh. Nerv. Deiat. Im. I P Pavlova 41, 700-707 (1991).
43. Volkov, V. V. & Svergun, D. I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Cryst. 36, 860-864 (2003).
44. Shaikh, T. R. et al. SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nature Protocols 3, 1941-1974 (2008).
45. Ludtke, S. J. 3-D structures of macromolecules using single-particle analysis in EMAN. Methods Mol. Biol. 673, 157-173 (2010).
46. Heymann, J. B. & Belnap, D. M. Bsoft: image processing and molecular modeling for electron microscopy. J. Struct. Biol. 157, 3-18 (2007). (Pubitemid 44880789)
47. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996). (Pubitemid 26152973)
48. Gumbart, J., Wiener, M. C. & Tajkhorshid, E. Coupling of calcium and substrate binding through loop alignment in the outer-membrane transporter BtuB. J. Mol. Biol. 393, 1129-1142 (2009).
49. Sotomayor, M. & Schulten, K. Single-molecule experiments in vitro and in silico. Science 316, 1144-1148 (2007). (Pubitemid 46877468)
50. Gumbart, J., Wiener, M. C. & Tajkhorshid, E. Mechanics of force propagation in TonB-dependent outer membrane transport. Biophys. J. 93, 496-504 (2007). (Pubitemid 47057815)
51. Gille, C. & Frommel, C. STRAP: editor for STRuctural Alignments of Proteins. Bioinformatics 17, 377-378 (2001). (Pubitemid 32421936)
52. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M. & Barton, G. J. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 (2009).