Identification of amino acid residues involved in heme binding and hemoprotein utilization in the Porphyromonas gingivalis heme receptor HmuR

Infection and Immunity

Volumn 74, Issue 2, 2006, Pages 1222-1232

  Liu, Xinyan ^a   Olczak, Teresa ^b   Guo, Hwai Chen ^a   Dixon, Dabney W ^c   Genco, Caroline Attardo ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WROC AW   (Poland)

^c GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; ARGININE; ASPARAGINE; ASPARTIC ACID; HEME; HEMIN; HEMOGLOBIN; HEMOPROTEIN; HISTIDINE; HUMAN SERUM ALBUMIN; LEUCINE; PROLINE; PROTEIN HMUR; RECEPTOR; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIUM MUTANT; NONHUMAN; POINT MUTATION; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ESCHERICHIA COLI; HEMEPROTEINS; HEMIN; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; POINT MUTATION; PORPHYROMONAS GINGIVALIS; RECEPTORS, CELL SURFACE;

EID: 31844433620     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.2.1222-1232.2006     Document Type: Article

References (57)

1. Amano, A., M. Kuboniwa, K. Kataoka, K. Tazaki, E. Inoshita, H. Nagata, H. Tamagawa, and S. Shizukuishi. 1995. Binding of hemoglobin by Porphyromonas gingivalis. FEMS Microbiol. Lett. 134:63-67.
2. Andrews, S. C., A. K. Robinson, and F. Rodriguez-Quinones. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215-237.
3. Bracken, C. S., M. T. Baer, A. Abdur-Rashid, W. Helms, and I. Stojiljkovic. 1999. Use of heme-protein complexes by the Yersinia enterocolitica HemR receptor: histidine residues are essential for receptor function. J. Bacteriol. 181:6063-6072.
4. Bramanti, T. E., and S. C. Holt. 1993. Hemin uptake in Porphyromonas gingivalis: Omp26 is a hemin-binding surface protein. J. Bacteriol. 175:7413-7420.
5. Bramanti, T. E., and S. C. Holt. 1991. Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50. J. Bacteriol. 173:7330-7339.
6. Brochu, V., D. Grenier, K. Nakayama, and D. Mayrand. 2001. Acquisition of iron from human transferrin by Porphyromonas gingivalis: a role for Arg- and Lys-gingipain activities. Oral Microbiol. Immunol. 16:79-87.
7. Buchanan, S. K., B. S. Smith, L. Venkatramani, D. Xia, L. Esser, M. Palnitkar, R. Chakraborty, D. van der Helm, and J. Deisenhofer. 1999. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat. Struct. Biol. 6:56-63.
8. Camejo, G., C. Halberg, A. Manschik-Lundin, E. Hurt-Camejo, B. Rosengren, H. Olsson, G. I. Hansson, G. B. Forsberg, and B. Ylhen. 1998. Hemin binding and oxidation of lipoproteins in serum: mechanisms and effect on the interaction of LDL with human macrophages. J. Lipid Res. 39:755-766.
9. Chakraborti, A. S. 2003. Interaction of porphyrins with heme proteins - a brief review. Mol. Cell. Biochem. 253:49-54.
10. Chimento, D. P., R. J. Kadner, and M. C. Wiener. 2003. The Escherichia coli outer membrane cobalamin transporter BtuB: structural analysis of calcium and substrate binding, and identification of orthologous transporters by sequence/structure conservation. J. Mol. Biol. 332:999-1014.
11. Curtis, M. A., H. K. Kuramitsu, M. Lantz, F. L. Macrina, K. Nakayama, J. Potempa, E. C. Reynolds, and J. Aduse-Opoku. 1999. Molecular genetics and nomenclature of proteases of Porphyromonas gingivalis. J. Periodont. Res. 34:464-472.
12. Curtis, M. A., J. A. Sterne, S. J. Price, G. S. Griffiths, S. K. Coulthurst, J. M. Wilton, and N. W. Johnson. 1990. The protein composition of gingival crevicular fluid sampled from male adolescents with no destructive periodontitis: baseline data of a longitudinal study. J. Periodont. Res. 25:6-16.
13. Dashper, S. G., A. Hendtlass, N. Slakeski, C. Jackson, K. J. Cross, L. Brownfield, R. Hamilton, I. Barr, and E. C. Reynolds. 2000. Characterization of a novel outer membrane hemin-binding protein of Porphyromonas gingivalis. J. Bacteriol. 182:6456-6462.
14. DeCarlo, A. A., M. Paramaesvaran, P. L. Yun, C. Collyer, and N. Hunter. 1999. Porphyrin-mediated binding to hemoglobin by the HA2 domain of cysteine proteinases (gingipains) and hemagglutinins from the periodontal pathogen Porphyromonas gingivalis. J. Bacteriol. 181:3784-3791.
15. Evans, R. W., J. B. Crawley, C. Joannou, and N. Sharma. 1999. Iron proteins, p. 27-86. In J. J. Bullen and E. Griffiths (ed.), Iron and infection. John Wiley & Sons, Chichester, England.
16. Ferguson, A. D., R. Chakraborty, B. S. Smith, L. Esser, D. van der Helm, and J. Deisenhofer. 2002. Structural basis of gating by the outer membrane transporter FecA. Science 295:1715-1719.
17. Ferguson, A. D., E. Hofmann, J. W. Coulton, K. Diederichs, and W. Welte. 1998. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215-2220.
18. Fujimura, S., Y. Shibata, K. Hirai, and T. Nakamura. 1996. Binding of hemoglobin to the envelope of Porphyromonas gingivalis and isolation of the hemoglobin-binding protein. Infect. Immun. 64:2339-2342.
19. Genco, C. A., and D. W. Dixon. 2001. Emerging strategies in microbial haeme capture. Mol. Microbiol. 39:1-11.
20. Genco, C. A., B. M. Odusanya, and G. Brown. 1994. Binding and accumulation of hemin in Porphyromonas gingivalis are induced by hemin. Infect. Immun. 62:2885-2892.
21. Ghigo, J. M., S. Letoffe, and C. Wandersman. 1997. A new type of hemophore-dependent heme acquisition system of Serratia marcescens reconstituted in Escherichia coli. J. Bacteriol. 179:3572-3579.
22. Grinberg, L. N., P. J. O'Brien, and Z. Hrkal. 1999. The effects of heme-binding proteins on the peroxidative and catalytic activities of hemin. Free Radic. Biol. Med. 27:214-219.
23. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723.
24. Holt, S. C., L. Kesavalu, S. Walker, and C. A. Genco. 1999. Virulence factors of Porphyromonas gingivalis. Periodontol. 2000 20:168-238.
25. Jones, T. A. 1978. A graphics model building and refinement system for macromolecules. J. Appl. Crystallogr. 11:268-272.
26. Karunakaran, T., T. Madden, and H. Kuramitsu. 1997. Isolation and characterization of a hemin-regulated gene, hemR, from Porphyromonas gingivalis. J. Bacteriol. 179:1898-1908.
27. Kihara, D., and J. Skolnick. 2003. The PDB is a covering set of small protein structures. J. Mol. Biol. 334:793-802.
28. Kongshaug, M. 1992. Distribution of tetrapyrrole photosensitizers among human plasma proteins. Int. J. Biochem. 24:1239-1265.
29. Kuboniwa, M., A. Amano, and S. Shizukuishi. 1998. Hemoglobin-binding protein purified from Porphyromonas gingivalis is identical to lysine-specific cysteine proteinase (Lys-gingipain). Biochem. Biophys. Res. Commun. 249:38-43.
30. Kuramitsu, H. K. 1999. Proteases of Porphyromonas gingivalis: what don't they do? Oral Microbiol. Immunol. 13:263-270.
31. Kusaba, A., T. Ansai, S. Akifusa, K. Nakahigashi, S. Taketani, H. Inokuchi, and T. Takehara. 2002. Cloning and expression of a Porphyromonas gingivalis gene for protoporphyrinogen oxidase by complementation of a hemG mutant of Escherichia coli. Oral Microbiol. Immunol. 17:290-295.
32. Letoffe, S., F. Nato, M. E. Goldberg, and C. Wandersman. 1999. Interactions of HasA, a bacterial haemophore, with haemoglobin and with its outer membrane receptor HasR. Mol. Microbiol. 33:546-555.
33. Lewis, J. P., J. A. Dawson, J. C. Hannis, D. Muddiman, and F. L. Macrina. 1999. Hemoglobinase activity of the lysine gingipain protease (Kgp) of Porphyromonas gingivalis W83. J. Bacteriol. 181:4905-4913.
34. Liu, M., and B. Lei. 2005. Heme transfer from streptococcal cell surface protein Shp to HtsA of transporter HtsABC. Infect. Immun. 73:5086-5092.
35. Liu, X., A. Sroka, J. Potempa, and C. A. Genco. 2004. Coordinate expression of the Porphyromonas gingivalis lysine-specific gingipain proteinase, Kgp, arginine-specific gingipain proteinase, RgpA, and the heme/hemoglobin receptor, HmuR. Biol. Chem. 385:1049-1057.
36. Loomis, L. D., and K. N. Raymond. 1991. Solution equilibria of enterobactin and metal enterobactin complexes. Inorg. Chem. 30:906-911.
37. Marti-Renom, M. A., A. C. Stuart, A. Fiser, R. Sanchez, F. Melo, and A. Sali. 2000. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29:291-325.
38. Miller, Y. I., and N. Shaklai. 1999. Kinetics of hemin distribution in plasma reveals its role in lipoprotein oxidation. Biochim. Biophys. Acta 1454:153-164.
39. Nelson, K. E., R. D. Fleischmann, R. T. DeBoy, I. T. Paulsen, D. E. Fouts, J. A. Eisen, S. C. Daugherty, R. J. Dodson, A. S. Durkin, M. Gwinn, D. H. Haft, J. F. Kolonay, W. C. Nelson, T. Mason, L. Tallon, J. Gray, D. Granger, H. Tettelin, H. Dong, J. L. Galvin, M. J. Duncan, F. E. Dewhirst, and C. M. Fraser. 2003. Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J. Bacteriol. 185:5591-5601.
40. Okamoto, K., K. Nakayama, T. Kadowaki, N. Abe, D. B. Ratnayake, and K. Yamamoto. 1998. Involvement of a lysine-specific cysteine proteinase in hemoglobin adsorption and heme accumulation by Porphyromonas gingivalis. J. Biol. Chem. 273:21225-21231.
41. Olczak, T., D. W. Dixon, and C. A. Genco. 2001. Binding specificity of the Porphyromonas gingivalis heme and hemoglobin receptor HmuR, gingipain K, and gingipain R1 for heme, porphyrins, and metalloporphyrins. J. Bacteriol. 183:5599-5608.
42. Paoli, M., B. F. Anderson, H. M. Baker, W. T. Morgan, A. Smith, and E. N. Baker. 1999. Crystal structure of hemopexin reveals a novel high-affinity heme site formed between two beta-propeller domains. Nat. Struct. Biol. 6:926-931.
43. Perkins-Balding, D., M. T. Baer, and I. Stojiljkovic. 2003. Identification of functionally important regions of a haemoglobin receptor from Neisseria meningitidis. Microbiology 149:3423-3435.
44. Poulos, T. L. 1996. Ligands and electrons and haem proteins. Nat. Struct. Biol. 3:401-403.
45. Raymond, K. N., and E. A. Dertz. 2004. Biochemical and physical properties of siderophores, p. 3-17. In J. H. Crosa, A. R. Mey and S. M. Payne (ed.), Iron transport in bacteria. American Society for Microbiology, Washington, D.C.
46. Rossi, M. S., J. D. Fetherston, S. Letoffe, E. Carniel, R. D. Perry, and J. M. Ghigo. 2001. Identification and characterization of the hemophore-dependent heme acquisition system of Yersinia pestis. Infect. Immun. 69:6707-6717.
47. Rouault, T. A. 2004. Pathogenic bacteria prefer heme. Science 305:1577-1578.
48. Shi, Y., D. B. Ratnayake, K. Okamoto, N. Abe, K. Yamamoto, and K. Nakayama. 1999. Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis. Construction of mutants with a combination of rgpA, rgpB, kgp, and hagA. J. Biol. Chem. 274:17955-17960.
49. Simpson, W., T. Olczak, and C. A. Genco. 2000. Characterization and expression of HmuR, a TonB-dependent hemoglobin receptor of Porphyromonas gingivalis. J. Bacteriol. 182:5737-5748.
50. Simpson, W., T. Olczak, and C. A. Genco. 2004. Lysine-specific gingipain K and heme/hemoglobin receptor HmuR are involved in heme utilization in Porphyromonas gingivalis. Acta Biochim. Pol. 51:253-262.
51. Skaar, E. P., M. Humayun, T. Bae, K. L. DeBord, and O. Schneewind. 2004. Iron-source preference of Staphylococcus aureus infections. Science 305:1626-1628.
52. Slakeski, N., S. G. Dashper, P. Cook, C. Poon, C. Moore, and E. C. Reynolds. 2000. A Porphyromonas gingivalis genetic locus encoding a heme transport system. Oral Microbiol. Immunol. 15:388-392.
53. Sroka, A., M. Sztukowska, J. Potempa, J. Travis, and C. A. Genco. 2001. Degradation of host heme proteins by lysine- and arginine-specific cysteine proteinases (gingipains) of Porphyromonas gingivalis. J. Bacteriol. 183:5609-5616.
54. Wandersman, C., and P. Delepelaire. 2004. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 58:611-647.
55. Wandersman, C., and I. Stojiljkovic. 2000. Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr. Opin. Microbiol. 3:215-220.
56. Yamamoto, S., N. Okujo, T. Yoshida, S. Matsuura, and S. Shinoda. 1994. Structure and iron transport activity of vibrioferrin, a new siderophore of Vibrio parahaemolyticus. J. Biochem. (Tokyo) 115:868-874.
57. Yost-Daljev, M. K., and C. N. Cornelissen. 2004. Determination of surface-exposed, functional domains of gonococcal transferrin-binding protein A. Infect. Immun. 72:1775-1785.