Steric and allosteric factors prevent simultaneous binding of transferrin-binding proteins A and B to transferrin

Biochemical Journal

Volumn 444, Issue 2, 2012, Pages 189-197

  Silva, Leslie P ^a   Yu, Rong Hua ^b   Calmettes, Charles ^c   Yang, Xue ^b   Moraes, Trevor F ^c   Schriemer, David C ^a   Schryvers, Anthony B ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Iron transport; Lipoprotein; Outer membrane; TonB dependent receptor; Transferrin; Transferrin binding protein

Indexed keywords

TERNARY COMPLEX FACTOR; TRANSFERRIN; TRANSFERRIN BINDING PROTEIN A; TRANSFERRIN BINDING PROTEIN B;

ACTINOBACILLUS PLEUROPNEUMONIAE; ARTICLE; BINDING SITE; COMPLEX FORMATION; DEUTERIUM HYDROGEN EXCHANGE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE; RECEPTOR BINDING; SWINE;

ACTINOBACILLUS PLEUROPNEUMONIAE; ALLOSTERIC REGULATION; ANIMALS; PICHIA; PROTEIN BINDING; PROTEIN TRANSPORT; STEREOISOMERISM; SWINE; TRANSFERRIN-BINDING PROTEIN A; TRANSFERRIN-BINDING PROTEIN B;

ACTINOBACILLUS PLEUROPNEUMONIAE; BACTERIA (MICROORGANISMS); MORAXELLACEAE; NEISSERIACEAE; PASTEURELLACEAE; SUS;

EID: 84860870450     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20112133     Document Type: Article

References (42)

1. Gray-Owen, S. D. and Schryvers, A. B. (1993) The interaction of primate transferrins with receptors on bacteria pathogenic to humans. Microb. Path. 14, 389-398
2. Schryvers, A. B. and Gonzalez, G. C. (1990) Receptors for transferrin in pathogenic bacteria are specific for the host's protein. Can. J. Microbiol. 36, 145-147 (Pubitemid 20144330)
3. Gray-Owen, S. D. and Schryvers, A. B. (1996) Bacterial transferrin and lactoferrin receptors. Trends Microbiol. 4, 185-191 (Pubitemid 26162132)
4. Alcantara, J., Yu, R.-H. and Schryvers, A. B. (1993) The region of human transferrin involved in binding to bacterial transferrin receptors is localized in the C-lobe. Mol. Microbiol. 8, 1135-1143 (Pubitemid 23187032)
5. Stojiljkovic, I. and Srinivasan, N. (1997) Neisseria meningitidis tonB, exbB, and exbD genes: Ton-dependent utilization of protein-bound iron in Neisseriae. J. Bacteriol. 179, 805-812 (Pubitemid 27051836)
6. Anderson, J. A., Sparling, P. F. and Cornelissen, C. N. (1994) Gonococcal transferrin-binding protein 2 facilitates but is not essential for transferrin utilization. J. Bacteriol. 176, 3162-3170 (Pubitemid 24166705)
7. Gray-Owen, S. D., Loosmore, S. and Schryvers, A. B. (1995) Identification and characterization of genes encoding the human transferrin binding proteins from Haemophilus influenzae. Infect. Immun. 63, 1201-1210
8. Luke, N. R. and Campagnari, A. A. (1999) Construction and characterization of Moraxella catarrhalis mutants defective in expression of transferrin receptors. Infect. Immun. 67, 5815-5819 (Pubitemid 29508104)
9. Renauld-Mongenie, G., Poncet, D., Mignon, M., Fraysse, S., Chabanel, C., Danve, B., Krell, T. and Quentin-Millet, M.-J. (2004) Role of transferrin receptor from a Neisseria meningitidis tbpB isotype II strain in human transferrin binding and virulence. Infect. Immun. 72, 3461-3470 (Pubitemid 38697772)
10. Irwin, S. W., Averill, N., Cheng, C. Y. and Schryvers, A. B. (1993) Preparation and analysis of isogenic mutants in the transferrin receptor protein genes, tbp1 and tbp2, from Neisseria meningitidis. Mol. Microbiol. 8, 1125-1133 (Pubitemid 23187031)
11. Baltes, N., Hennig-Pauka, I. and Gerlach, G. F. (2002) Both transferrin binding proteins are virulence factors in Actinobacillus pleuropneumoniae serotype 7 infection. FEMS Microbiol. Lett. 209, 283-287 (Pubitemid 34465605)
12. Retzer, M. D., Yu, R.-H., Zhang, Y., Gonzalez, G. C. and Schryvers, A. B. (1998) Discrimination between apo and iron-loaded forms of transferrin by transferrin binding protein B and its N-terminal subfragment. Microb. Path. 25, 175-180 (Pubitemid 28523765)
13. Yu, R.-H. and Schryvers, A. B. (1993) The interaction between human transferrin and transferrin binding protein 2 from Moraxella (Branhamella) catarrhalis differs from that of other human pathogens. Microb. Path. 15, 443-445
14. Moraes, T. F., Yu, R.-H., Strynadka, N. C. and Schryvers, A. B. (2009) Insights into the bacterial transferrin receptor: the structure of transferrin binding protein B from Actinobacillus pleuropneumoniae. Mol. Cell 35, 523-533
15. DeRocco, A. J., Yost-Daljev, M. K., Kenney, C. D. and Cornelissen, C. N. (2009) Kinetic analysis of ligand interaction with the gonococcal transferrin-iron acquisition system. Biometals 22, 439-451
16. Calmettes, C., Yu, R.-H., Silva, L. P., Curran, D., Schriemer, D. C., Schryvers, A. B. and Moraes, T. F. (2011) Structural variations within the transferrin binding site on transferrin binding protein, TbpB. J. Biol. Chem. 286, 12683-12692
17. Silva, L. P., Yu, R., Calmettes, C., Yang, X., Moraes, T. F., Schryvers, A. B. and Schriemer, D. C. (2011) Conserved interaction between transferrin and transferrin-binding proteins from porcine pathogens. J. Biol. Chem. 286, 21353-21360
18. Ling, J. M., Shima, C. H., Schriemer, D. C. and Schryvers, A. B. (2010) Delineating the regions of human transferrin involved in interactions with transferrin binding protein B from Neisseria meningitidis. Mol. Microbiol. 77, 1301-1314
19. Oakhill, J. S., Sutton, B. J., Gorringe, A. R. and Evans, R. W. (2005) Homology modelling of transferrin-binding protein A from Neisseria meningitidis. Protein Eng., Des. Sel. 18, 221-228 (Pubitemid 40863426)
20. MacGillivray, R. T. A., Moore, S. A., Chen, J., Anderson, B. F., Baker, H., Luo, Y. G., Bewley, M., Smith, C. A., Murphy, M. E. P., Wang, Y. et al. (1998) Two high-resolution crystal structures of the recombinant N-lobe of human transferrin reveal a structural change implicated in iron release. Biochemistry 37, 7919-7928 (Pubitemid 28307052)
21. Wong, H. and Schryvers, A. B. (2003) Bacterial lactoferrin binding protein A binds to both domains of the human lactoferrin C-lobe. Microbiology 149, 1729-1737 (Pubitemid 36874319)
22. Schryvers, A. B. and Stojiljkovic, I. (1999) Iron acquisition systems in the pathogenic Neisseria . Mol. Microbiol. 32, 1117-1123 (Pubitemid 29286652)
23. Silburt, C., Roulhac, P., Weaver, K., Noto, J., Mietzner, T., Cornelissen, C., Fitzgerald, M. and Crumbliss, A. (2009) Hijacking transferrin bound iron: protein-receptor interactions involved in iron transport in N. gonorrhoeae. Metallomics 1, 249-255
24. Masri, H. P. and Cornelissen, C. N. (2002) Specific ligand binding attributable to individual epitopes of gonococcal transferrin binding protein A. Infect. Immun. 70, 732-740 (Pubitemid 34083835)
25. Yost-Daljev, M. K. and Cornelissen, C. N. (2004) Determination of surface-exposed, functional domains of gonococcal transferrin-binding protein A. Infect. Immun. 72, 1775-1785 (Pubitemid 38263803)
26. Powell, N. B. L., Bishop, K., Palmer, H. M., Ala'Aldeen, D. A., Gorringe, A. R. and Borriello, S. P. (1998) Differential binding of apo and holo human transferrin to meningococci and co-localisation of the transferrin-binding proteins (TbpA and TbpB). J. Med. Microbiol. 47, 257-264 (Pubitemid 28090055)
27. Cornelissen, C. N. and Sparling, P. F. (1996) Binding and surface exposure characteristics of the gonococcal transferrin receptor are dependent on both transferrin binding proteins. J. Bacteriol. 178, 1437-1444 (Pubitemid 26073402)
28. Cornelissen, C. N., Anderson, J. E. and Sparling, P. F. (1997) Energy-dependent changes in the gonococcal transferrin receptor. Mol. Microbiol. 26, 25-35 (Pubitemid 27438235)
29. Rey, M., Mrazek, H., Pompach, P., Novak, P., Pelosi, L., Brandolin, G., Forest, E., Havlicek, V. and Man, P. (2010) Effective removal of nonionic detergents in protein mass spectrometry, hydrogen/deuterium exchange, and proteomics. Anal. Chem. 82, 5107-5116
30. Padda, J. S. and Schryvers, A. B. (1990) N-linked oligosaccharides of human transferrin are not required for binding to bacterial transferrin receptors. Infect. Immun. 58, 2972-2976 (Pubitemid 20267690)
31. Miroux, B. and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (Pubitemid 26254109)
32. DeWinter, L. M. and Schryvers, A. B. (2002) Methods for manipulation of transferrin-binding proteins. In Meningococcal Vaccines: Methods and Protocols (Pollard, A. J. and Maiden, M. C., eds), pp. 109-120, Humana Press, Totowa, NJ
33. Slysz, G. W., Baker, C. A., Bozsa, B. M., Dang, A., Percy, A. J., Bennett, M. and Schriemer, D. C. (2009) Hydra: software for tailored processing of H/D exchange data from MS or tandem MS analyses. BMC Bioinformatics 10, 162
34. Bennett, M. J., Chik, J. K., Slysz, G. W., Luchko, T., Tuszynski, J., Sackett, D. L. and Schriemer, D. C. (2009) Structural mass spectrometry of the α/β-tubulin dimer supports a revised model of microtubule assembly. Biochemistry 48, 4858-4870
35. Calmettes, C., Alcantara, J., Schryvers, A. B. and Moraes, T. F. (2012) The structural basis of transferrin iron sequestration by transferrin binding protein B. Nat. Struc. Mol. Biol. 19, 358-360
36. Wally, J., Halbrooks, P. J., Vonrhein, C., Rould, M. A., Everse, S. J., Mason, A. B. and Buchanan, S. K. (2006) The crystal structure of iron-free human serum transferrin provides insight into inter-lobe communication and receptor binding. J. Biol. Chem. 281, 24934-24944 (Pubitemid 44274264)
37. Yang, X., Yu, R. H., Calmettes, C., Moraes, T. F. and Schryvers, A. B. (2011) The anchor peptide of transferrin binding protein B is required for interaction with transferrin binding protein A. J. Biol. Chem. 286, 45165-45173
38. Schryvers, A. B. and Morris, L. J. (1988) Identification and characterization of the human lactoferrin-binding protein from Neisseria meningitidis. Infect. Immun. 56, 1144-1149
39. Schryvers, A. B. and Morris, L. J. (1988) Identification and characterization of the transferrin receptor from Neisseria meningitidis. Mol. Microbiol. 2, 281-288
40. Cornelissen, C. N., Kelley, M., Hobbs, M. M., Anderson, J. E., Cannon, J. G., Cohen, M. S. and Sparling, P. F. (1998) The transferrin receptor expressed by gonococcal strain FA1090 is required for the experimental infection of human male volunteers. Mol. Microbiol. 27, 611-616 (Pubitemid 28045742)
41. Anderson, J. E., Hobbs, M. M., Biswas, G. D. and Sparling, P. F. (2003) Opposing selective forces for expression of the gonococcal lactoferrin receptor. Mol. Microbiol. 48, 1325-1337 (Pubitemid 36718226)
42. Gray-Owen, S. D. and Schryvers, A. B. (1995) Characterization of transferrin binding proteins 1 and 2 in invasive type b and nontypable strains of Haemophilus influenzae. Infect. Immun. 63, 3809-3815