Structural analysis of haemoglobin binding by HpuA from the Neisseriaceae family

Nature Communications

Volumn 6, Issue , 2015, Pages

  Wong, Chi T ^a   Xu, Yingqi ^a   Gupta, Akshari ^a,b   Garnett, James A ^a,c   Matthews, Steve J ^a   Hare, Stephen A ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HEMOGLOBIN; HPUA PROTEIN; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; HPUA PROTEIN, NEISSERIA; PROTEIN BINDING;

BACTERIUM; BIOCHEMISTRY; CHEMICAL ANALYSIS; CRYSTAL STRUCTURE; HEMOGLOBIN; IRON;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; KINGELLA; KINGELLA DENITRIFICANS; NEISSERIA GONORRHOEAE; NEISSERIACEAE; NONHUMAN; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS); KINGELLA DENITRIFICANS; NEISSERIA GONORRHOEAE; NEISSERIACEAE;

BACTERIAL PROTEINS; CRYSTALLIZATION; HEMOGLOBINS; HUMANS; KINGELLA; NEISSERIA GONORRHOEAE; NEISSERIACEAE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE;

EID: 84950267595     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10172     Document Type: Article

References (69)

1. Bullen, J. J., Rogers, H. J. & Griffiths, E. Role of iron in bacterial infection. Curr. Top. Microbiol. Immunol. 80, 1-35 (1978).
2. Shim, B. S., Lee, T. H. & Kang, Y. S. Immunological and biochemical investigations of human serum haptoglobin: composition of haptoglobinhaemoglobin intermediate, haemoglobin-binding sites and presence of additional alleles for beta-chain. Nature 207, 1264-1267 (1965).
3. Wada, T., Oara, H., Watanabe, K., Kinoshita, H. & Yachi, A. Autoradiographic study on the site of uptake of the haptoglobin-hemoglobin complex. J. Reticuloendothel. Soc. 8, 185-193 (1970).
4. Lim, S. K. et al. Increased susceptibility in Hp knockout mice during acute hemolysis. Blood 92, 1870-1877 (1998).
5. Kristiansen, M. et al. Identification of the haemoglobin scavenger receptor. Nature 409, 198-201 (2001).
6. Lewis, L. A. & Dyer, D. W. Identification of an iron-regulated outer membrane protein of Neisseria meningitidis involved in the utilization of hemoglobin complexed to haptoglobin. J. Bacteriol. 177, 1299-1306 (1995).
7. Lewis, L. A., Gray, E., Wang, Y. P., Roe, B. A. & Dyer, D. W. Molecular characterization of hpuAB, the haemoglobin-haptoglobin-utilization operon of Neisseria meningitidis. Mol. Microbiol. 23, 737-749 (1997).
8. Stephens, D. S., Greenwood, B. & Brandtzaeg, P. Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 369, 2196-2210 (2007).
9. Ohnishi, M. et al. Is Neisseria gonorrhoeae initiating a future era of untreatable gonorrhea Detailed characterization of the first strain with high-level resistance to ceftriaxone. Antimicrob. Agents Chemother. 55, 3538-3545 (2011).
10. Unemo, M. & Shafer, W. M. Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin. Microbiol. Rev. 27, 587-613 (2014).
11. Chen, C. K. & Wilson, M. E. Eikenella corrodens in human oral and non-oral infections: a review. J. Periodontol. 63, 941-953 (1992).
12. Yagupsky, P., Dagan, R., Prajgrod, F. & Merires, M. Respiratory carriage of Kingella kingae among healthy children. Pediatr. Infect. Dis. J. 14, 673-678 (1995).
13. Yagupsky, P. Kingella kingae: from medical rarity to an emerging paediatric pathogen. Lancet Infect. Dis. 4, 358-367 (2004).
14. Goldstein, E. J. Bite wounds and infection. Clin. Infect. Dis. 14, 633-638 (1992).
15. Chambers, S. T. et al. HACEK infective endocarditis: characteristics and outcomes from a large, multi-national cohort. PLoS ONE 8, e63181 (2013).
16. Stojiljkovic, I. et al. The Neisseria meningitidis haemoglobin receptor: its role in iron utilization and virulence. Mol. Microbiol. 15, 531-541 (1995).
17. Stojiljkovic, I., Larson, J., Hwa, V., Anic, S. & So, M. HmbR outer membrane receptors of pathogenic Neisseria spp.: iron-regulated, hemoglobin-binding proteins with a high level of primary structure conservation. J. Bacteriol. 178, 4670-4678 (1996).
18. Lewis, L. A., Sung, M. H., Gipson, M., Hartman, K. & Dyer, D. W. Transport of intact porphyrin by HpuAB, the hemoglobin-haptoglobin utilization system of Neisseria meningitidis. J. Bacteriol. 180, 6043-6047 (1998).
19. Tauseef, I. et al. Influence of the combination and phase variation status of the haemoglobin receptors HmbR and HpuAB on meningococcal virulence. Microbiology 157, 1446-1456 (2011).
20. Chen, C. J., Elkins, C. & Sparling, P. F. Phase variation of hemoglobin utilization in Neisseria gonorrhoeae. Infect. Immun. 66, 987-993 (1998).
21. Anderson, J. E. et al. Selection for expression of the gonococcal hemoglobin receptor during menses. J. Infect. Dis. 184, 1621-1623 (2001).
22. Lucidarme, J. et al. The distribution and 'in vivo' phase variation status of haemoglobin receptors in invasive meningococcal serogroup B disease: genotypic and phenotypic analysis. PLoS ONE 8, e76932 (2013).
23. Rohde, K. H. & Dyer, D. W. Analysis of haptoglobin and hemoglobinhaptoglobin interactions with the Neisseria meningitidis TonB-dependent receptor HpuAB by flow cytometry. Infect. Immun. 72, 2494-2506 (2004).
24. Rohde, K. H., Gillaspy, A. F., Hatfield, M. D., Lewis, L. A. & Dyer, D. W. Interactions of haemoglobin with the Neisseria meningitidis receptor HpuAB: the role of TonB and an intact proton motive force. Mol. Microbiol. 43, 335-354 (2002).
25. Harrison, O. B., Bennett, J. S., Derrick, J. P., Maiden, M. C. & Bayliss, C. D. Distribution and diversity of the haemoglobin-haptoglobin iron-acquisition systems in pathogenic and non-pathogenic Neisseria. Microbiology 159, 1920-1930 (2013).
26. Anderson, J. E., Sparling, P. F. & Cornelissen, C. N. Gonococcal transferrinbinding protein 2 facilitates but is not essential for transferrin utilization. J. Bacteriol. 176, 3162-3170 (1994).
27. 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).
28. Calmettes, C., Alcantara, J., Yu, R. H., Schryvers, A. B. & Moraes, T. F. The structural basis of transferrin sequestration by transferrin-binding protein B. Nat. Struct. Mol. Biol. 19, 358-360 (2012).
29. Noinaj, N. et al. Structural basis for iron piracy by pathogenic Neisseria. Nature 483, 53-58 (2012).
30. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845-858 (2015).
31. Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549 (2010).
32. Schneider, M. C. et al. Neisseria meningitidis recruits factor H using protein mimicry of host carbohydrates. Nature 458, 890-893 (2009).
33. Esposito, V. et al. Structure of the C-terminal domain of Neisseria heparin binding antigen (NHBA), one of the main antigens of a novel vaccine against Neisseria meningitidis. J. Biol. Chem. 286, 41767-41775 (2011).
34. Xu, D., Tsai, C. J. & Nussinov, R. Hydrogen bonds and salt bridges across protein-protein interfaces. Protein Eng. 10, 999-1012 (1997).
35. Bahadur, R. P. & Zacharias, M. The interface of protein-protein complexes: analysis of contacts and prediction of interactions. Cell Mol. Life Sci. 65, 1059-1072 (2008).
36. Andersen, C. B. et al. Structure of the haptoglobin-haemoglobin complex. Nature 489, 456-459 (2012).
37. Silva, M. M., Rogers, P. H. & Arnone, A. A third quaternary structure of human hemoglobin A at 1.7-A resolution. J. Biol. Chem. 267, 17248-17256 (1992).
38. Park, S. Y., Yokoyama, T., Shibayama, N., Shiro, Y. & Tame, J. R. 1.25A resolution crystal structures of human haemoglobin in the oxy, deoxy and carbonmonoxy forms. J. Mol. Biol. 360, 690-701 (2006).
39. Lane-Serff, H., MacGregor, P., Lowe, E. D., Carrington, M. & Higgins, M. K. Structural basis for ligand and innate immunity factor uptake by the trypanosome haptoglobin-haemoglobin receptor. Elife 3, e05553 (2014).
40. Lukin, J. A. et al. Quaternary structure of hemoglobin in solution. Proc. Natl Acad. Sci. USA 100, 517-520 (2003).
41. Jia, Y., Buehler, P. W., Boykins, R. A., Venable, R. M. & Alayash, A. I. Structural basis of peroxide-mediated changes in human hemoglobin: a novel oxidative pathway. J. Biol. Chem. 282, 4894-4907 (2007).
42. Hamilton, H. L. & Dillard, J. P. Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol. Microbiol. 59, 376-385 (2006).
43. Adamiak, P., Calmettes, C., Moraes, T. F. & Schryvers, A. B. Patterns of structural and sequence variation within isotype lineages of the Neisseria meningitidis transferrin receptor system. Microbiologyopen 4, 491-504 (2015).
44. Cornelissen, C. N. & Sparling, P. F. Binding and surface exposure characteristics of the gonococcal transferrin receptor are dependent on both transferrin-binding proteins. J. Bacteriol. 178, 1437-1444 (1996).
45. Newton, S. M., Igo, J. D., Scott, D. C. & Klebba, P. E. Effect of loop deletions on the binding and transport of ferric enterobactin by FepA. Mol. Microbiol. 32, 1153-1165 (1999).
46. Scott, D. C. et al. Exchangeability of N termini in the ligand-gated porins of Escherichia coli. J. Biol. Chem. 276, 13025-13033 (2001).
47. Na, N., Ouyang, J., Taes, Y. E. & Delanghe, J. R. Serum free hemoglobin concentrations in healthy individuals are related to haptoglobin type. Clin. Chem. 51, 1754-1755 (2005).
48. Henriksen, S. D. & Bovre, K. Moraxella kingii sp.nov., a haemolytic, saccharolytic species of the genus Moraxella. J. Gen. Microbiol. 51, 377-385 (1968).
49. Matsunaga, T. et al. Genomic recombination through plasmid-encoded recombinase enhances hemolytic activity and adherence to epithelial cells in the periodontopathogenic bacterium Eikenella corrodens. Biosci. Biotechnol. Biochem. 75, 748-751 (2011).
50. Paul, K. & Patel, S. S. Eikenella corrodens infections in children and adolescents: case reports and review of the literature. Clin. Infect. Dis. 33, 54-61 (2001).
51. Sobel, J. D., Carrizosa, J., Ziobrowski, T. F. & Gluckman, S. J. Polymicrobial endocarditis involving Eikenella corrodens. Am. J. Med. Sci. 282, 41-44 (1981).
52. Huebers, H. A. et al. Plasma iron and transferrin iron-binding capacity evaluated by colorimetric and immunoprecipitation methods. Clin. Chem. 33, 273-277 (1987).
53. Cherepanov, P. LEDGF/p75 interacts with divergent lentiviral integrases and modulates their enzymatic activity in vitro. Nucleic Acids Res. 35, 113-124 (2007).
54. Perutz, M. F. Preparation of haemoglobin crystals. J. Cryst. Growth 2, 54-56 (1968).
55. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
56. Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82 (2006).
57. Leslie, A. G. W. & Powell, H. R in Evolving Methods for Macromolecular Crystallography (eds Read R. J., Sussman J. L.) 41-51 (Springer, Netherlands, 2007).
58. Bricogne, G., Vonrhein, C., Flensburg, C., Schiltz, M. & Paciorek, W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D Biol. Crystallogr. 59, 2023-2030 (2003).
59. Schneider, T. R. & Sheldrick, G. M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (2002).
60. Vonrhein, C., Blanc, E., Roversi, P. & Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230 (2007).
61. Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011 (2006).
62. Perrakis, A., Morris, R. & Lamzin, V. S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6, 458-463 (1999).
63. Vagin, A. & Teplyakov, A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025 (1997).
64. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
65. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
66. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
67. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
68. Heinig, M. & Frishman, D. STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins. Nucleic Acids Res. 32, W500-W502 (2004).
69. Landau, M. et al. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299-W302 (2005).