Haemoglobin receptor protein is intragenically encoded by the cysteine proteinase-encoding genes and the haemagglutinin-encoding gene of Porphyromonas gingivalis

Molecular Microbiology

Volumn 27, Issue 1, 1998, Pages 51-61

  Nakayama, Koji ^a   Ratnayake, Dinath B ^a   Tsukuba, Takayuki ^a   Kadowaki, Tomoko ^a   Yamamoto, Kenji ^a   Fujimura, Setsuo ^b  

^a KYUSHU UNIVERSITY   (Japan)

^b MATSUMOTO DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; HEMAGGLUTININ; HEMOGLOBIN; RECEPTOR PROTEIN;

AMINO ACID SEQUENCE; ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL VIRULENCE; CELL CULTURE; ESCHERICHIA COLI; GENE OVEREXPRESSION; GENETIC ANALYSIS; IN VITRO STUDY; PH; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN ISOLATION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BASE SEQUENCE; BLOTTING, WESTERN; CHROMATOGRAPHY, AGAROSE; CYSTEINE ENDOPEPTIDASES; DNA, BACTERIAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; HEMAGGLUTININS; HEMOGLOBINS; MOLECULAR SEQUENCE DATA; PLASMIDS; POLYMERASE CHAIN REACTION; PORPHYROMONAS GINGIVALIS; RECEPTORS, CELL SURFACE; SEQUENCE ANALYSIS, DNA;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; PORPHYROMONAS GINGIVALIS; PROKARYOTA;

EID: 0031962568     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.00656.x     Document Type: Article

References (47)

1. Aduse-Opoku, J., Muir, J., Slaney, J.M., Rangarajan, M., and Curtis, M.A. (1995) Characterization, genetic analysis, and expression of a protease antigen. (PrpR1) of Porphyromonas gingivalis W50. Infect Immun 63: 4744-4754.
2. Amano, A., Kuboniwa, M., Kataoka, K., Tazaki, K., Inoshita, E., Nagata, H., Tamagawa, H., and Shizukuishi, S. (1995) Binding of hemoglobin by Porphyromonas gingivalis. FEMS Microbiol Lett 134: 63-67.
3. Bagg, A., and Neilands, J.B. (1987) Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol Rev 51: 509-518.
4. Barkocy-Gallagher, G.A., Han, N., Patti, J.M., Whitlock, J., Progulske-Fox, A., and Lantz, M. (1996) Analysis of the prtP gene encoding porphypain, a cysteine proteinase of Porphyromonas gingivalis. J Bacteriol 178: 2734-2741.
5. Bramanti, T.E., and Holt, S.C. (1991) Roles of porphyrins and host iron transport proteins in regulation of growth in Porphyromonas gingivalis W50. J Bacteriol 173: 7330-7339.
6. Chu, L., Bramanti, T.E., Ebersole, J.L., and Holt, S.C. (1991) Hemolytic activity in the periodontopathogen, Porphyromonas gingivalis: kinetics of enzyme formation and localization. Infect Immun 59: 1932-40.
7. 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.
8. Cornelissen, C., Biswas, G.D., Tsai, J., Paruchuri, D.K., Thompson, S.A., and Sparling, P.F. (1992) Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors. J Bacteriol 174: 5788-5797.
9. Curtis, M.A., Ramakrishnan, M., and Slaney, J.M. (1993) Characterization of the trypsin-like enzymes of Porphymmonas gingivalis W83 using a radiolabelled active-site-directed inhibitor. J Gen Microbiol 139: 949-955.
10. Curtis, M.A., Aduse-Opoku, J., Slaney, J.M., Rangarajan, M., Booth, V., Cridland, J., and Shepherd, P. (1996) Characterization of an adherence and antigenic determinant of the ArgI protease of Porphyromonas gingivalis which is present on multiple gene products. Infect Immun 64: 2532-2539.
11. Daskaleros, P.A., Stoebner, J.A., and Payne, S.M. (1991) Iron uptake in Plesiomonas shigelloides: cloning of the genes for the heme-iron uptake system. Infect Immun 59: 2706-2711.
12. Decarlo, A.A., and Harber, G.J. (1997) Hemagglutinin activity and heterogeneity of related Porphyromonas gingivalis proteinases. Oral Microbiol Immunol 12: 47-56.
13. Elkins, C., Chen, C.-J., and Thomas, C.E. (1995) Characterization of the hgbA locus encoding a hemoglobin receptor from Haemophilus ducreyi. Infect Immun 63: 2194-2200.
14. Fletcher, H.M., Schenkein, H.A., and Macrina, F.L. (1994) Cloning and characterization of a new protease gene (prtH) from Porphyromonas gingivalis. Infect Immun 62: 4279-4286.
15. Fujimura, S., Shibata, Y., Hirai, K., and Nakamura, T. (1995) Some binding properties of the envelope of Porphyromonas gingivalis to hemoglobin. FEMS Immunol Med Microbiol 10: 109-114.
16. Fujimura, S., Shibata, Y., Hirai, K., and Nakamura, T. (1996) Binding of hemoglobin to the envelope of Porphyromonas gingivalis and isolation of the hemoglobin-binding protein. Infect Immun 64: 2339-2342.
17. Gibbons, R.J., and MacDonald, J.B. (1960) Hemin and vitamin K compounds as required for the cultivation of certain strains of Bacteroides melaninogenicus. J Bacteriol 80: 164-170.
18. Han, N., Whitlock, J., and Progulske-Fox, A. (1996) The hemagglutinin gene A (hagA) of Porphyromonas gingivalis 381 contains four large, continuous, direct repeats. Infect Immun 64: 4000-4007.
19. Hanson, M.S., Pelzel, S.E., Latimer, J., Muller-Eberhard, U., and Hansen, E.J. (1992) Identification of a genetic locus of Haemophilus influenzae type b necessary for the binding and utilization of heme bound to human hemopexin. Proc Natl Acad Sci USA 89: 1973-77.
20. Hayashi, H., Nagata, A., Hinode, D., Sato, M., and Nakamura, R. (1992) Survey of a receptor protein in human erythrocytes for hemagglutinin of Porphyromonas gingivalis. Oral Microbiol Immunol 7: 204-211.
21. Henderson, D.P., and Payne, S.M. (1993) Cloning and characterization of the Vibrio cholerae genes encoding the utilization of iron from haemin and haemoglobin. Mol Microbiol 7: 461-469.
22. Inoshita, E., Amano, A., Hanioka, T., Tamagawa, H., Shizukuishi, S., and Tsunemitsu, A. (1986) Isolation and some properties of exohemagglutinin from culture medium of Bacteroides gingivalis 381. Infect Immun 52: 421-427.
23. Kirszbaum, L., Sotiropoulos, C., Jackson, C., Cleal, S., Slakeski, N., and Reynolds, E.C. (1995) Complete nucleotide sequence of a gene prtR of Porphyromonas gingivalis W50 encoding a 132kDa protein that contains an arginine-specific thiol endopeptidase domain and a haemagglutinin domain. Biochem Biophys Res Commun 207: 424-431.
24. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
25. Lewis, L.A., Gray, E., Wang, Y.-P., Roe, B.A., and Dyer, D.W. (1997) Molecular characterization of hpuAB, the haemoglobin-haptoglobin-utilization operon of Neisseria meningitidis. Mol Microbiol 23: 737-749.
26. McKee, A.S., McDermid, A.S., Wait, R., Baskerville, A., and Marsh, P.D. (1988) Isolation of colonial variants of Bacteroides gingivalis W50 with a reduced virulence. J Med Microbiol 27: 59-64.
27. Nakayama, K. (1997) Domain-specific rearrangement between the two Arg-gingipain-encoding genes in Porphyromonas gingivalis: possible involvement of non-reciprocal recombination. Microbiol Immunol 41: 185-196.
28. Nakayama, K., Kadowaki, T., Okamoto, K., and Yamamoto, K. (1995) Construction and characterization of arginine-specific cysteine proteinase (Arg-gingipain)-deficient mutants of Porphyromonas gingivalis: evidence for significant contribution of Arg-gingipain to virulence. J Biol Chem 270: 23619-23626.
29. Neilands, J.B. (1992) Mechanism and regulation of synthesis of aerobactin in Escherichia coli K12 (pColV-K30). Can J Microbiol 38: 728-733.
30. Nishikata, M., and Yoshimura, F. (1991) Characterization of Porphyromonas (Bacteroides) gingivalis hemagglutinin as a protease. Biochem Biophys Res Communication 178: 336-342.
31. Nishikata, M., Yoshimura, F., and Nodasaka, Y. (1989) Possibility of Bacteroides gingivalis hemagglutinin possessing protease activity revealed by inhibition studies. Microbiol Immunol 33: 75-80.
32. Okamoto, K., Kadowaki, T., Nakayama, K., and Yamamoto, K. (1996) Cloning and sequencing of the gene encoding a novel lysine-specific cysteine proteinase (Lys-gingipain) in Porphyromonas gingivalis: structural relationship with the arginine-specific cysteine proteinase (Arg-gingipain). J Biochem 120: 398-406.
33. Okuda, K., Yamamoto, A., Naito, Y., Takazoe, I., Slot, J., and Genco, R.J. (1986) Purification and properties of hemagglutinin from culture supernatant of Bacteroides gingivalis. Infect Immun 54: 659-665.
34. Pavloff, N., Potempa, J., Pike, R.N., Prochazka, V., Kiefer, M.C., Travis, J., and Barr, P.J. (1995) Molecular cloning and structural characterization of the Arg-gingipain proteinase of Porphyromonas gingivalis. J Biol Chem 270: 1007-1010.
35. Pavloff, N., Pemberton, P.A., Potempa, J., Chen, W.-C., A., Pike, R.N., Prochazka, V., Kiefer, M.C., Travis, J., and Barr, P.J. (1997) Molecular cloning and characterization of Porphyromonas gingivalis Lysine-specific gingipain: new member of an emerging family of pathogenic bacterial cysteine proteinase. J Biol Chem 272: 1595-1600.
36. Pike, R.N., McGraw, W.T., Potempa, J., and Travis, J. (1994) Lysine- and arginine-specific proteinases from Porphyromonas gingivalis: isolation, characterization, and evidence for the existence of complexes with hemagglutinins. J Biol Chem 269: 406-411.
37. Pike, R.N., Potempa, J., McGraw, W., Coetzer, T.H., and Travis, J. (1996) Characterization of the binding activities of proteinase-adhesin complexes from Porphyromonas gingivalis. J Bacteriol 178: 2876-2882.
38. Potempa, J., Pavloff, N., and Travis, J. (1995) Porphyromonas gingivalis: a proteinase/gene accounting audit. Trends Microbiol 3: 430-434.
39. Shah, H.N., and Gharbia, S.E. (1989) Lysis of erythrocytes by the secreted cysteine proteinase of Porphyromonas gingivalis W83. FEMS Microbiol Lett 61: 213-218.
40. Shah, H.N., Bonnett, R., Mateen, B., and Williams, R.A.D. (1979) The porphyrin pigmentation of subspecies of Bacteroides melaninogenicus. Biochem J 180: 45-50.
41. Shah, H.N., Seddon, S.V., and Gharbia, S.E. (1989) Studies on the virulence properties and metabolism of peiotropic mutants of Porphyromonas gingivalis (Bacteroides gingivalis) W50. Oral Microbiol Immunol 4: 19-23.
42. Stojiljkovic, I., Hwa, V., Martin, L.d.S., O'Gaora, P., Nassif, X., Heffron, F., and So, M. (1995) The Neisseria meningitidis haemoglobin receptor: its role in iron utilization and virulence. Mol Microbiol 15: 531-541.
43. Stojiljkovic, I., Larson, J., Hwa, V., Anic, S., and So, M. (1996) HmbR membrane receptors of pathogenic Neisseria spp.: iron-regulated, hemoglobin-binding proteins with a high level of primary structure conservation. J Bacteriol 178: 4670-4678.
44. Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185: 60-89.
45. Torres, A.G., and Payne, S.M. (1997) Haem iron-transport system in enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 23: 825-833.
46. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
47. Zambon, J.J., Grossi, S., Dunford, R., Haraszthy, V.I., Preus, H., and Genco, R.J. (1994) Epidemiology of subgingival bacterial pathogens in periodontal disease. In Molecular Pathogenesis of Periodontal Disease. Genco, R., Hamada, S., Lehner, T., McGhee, J., and Mergenhagen, S. (eds). Washington, D.C: American Society for Microbiology Press, pp. 3-12.