The Tla protein of Porphyromonas gingivalis W50: A homolog of the RI protease precursor (PrpRI) is an outer membrane receptor required for growth on low levels of hemin

Journal of Bacteriology

Volumn 179, Issue 15, 1997, Pages 4778-4788

  Aduse Opoku, Joseph ^a,b   Slaney, Jennifer M ^a   Rangarajan, Minnie ^a   Muir, Justine ^a   Young, K Anne ^a   Curtis, Michael A ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b ST BARTHOLOMEW S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BACTERIAL DNA; BACTERIAL ENZYME; BACTERIAL PROTEIN; HEMIN; LYSINE; MEMBRANE RECEPTOR; PROTEINASE;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; NONHUMAN; PORPHYROMONAS; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS;

EID: 0030792046     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.15.4778-4788.1997     Document Type: Article

References (59)

1. Aduse-Opoku, J., J. Muir, J. M. Slaney, M. Rangarajan, and M. A. Curtis. 1995. Characterisation, genetic analysis and expression studies of a protease antigen (PrpRI) of Porphyromonas gingivalis. Infect. Immun. 63:4744-4754.
2. Barkocy-Gallagher, G. A., N. Han, J. M. Patti, J. Whitlock, A. Progulske-Fox, and M. S. Lantz. 1996. Analysis of the prtP gene encoding porphypain, a cysteine proteinase of Porphvromonas gingivalis. J. Bacteriol. 178:2734-2741.
3. Bell, P. M., C. D. Nau, J. T. Brown, J. Konisky, and R. J. Kadner. 1990. Genetic suppression demonstrates interaction of TonB protein with outer membrane transport proteins in Escherichia coli. J. Bacteriol. 172:3826-3829.
4. Biswas, G. D., and P. F. Sparling. 1995. Characterisation of lbpA, the structural gene for a lactoferrin receptor in Neisseria gonorrhoeae. Infect. Immun. 63:2958-2967.
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. Bramanti, T. E., and S. C. Holt. 1990. Iron-regulated outer membrane proteins in the periodontopathic bacterium, Bacteroides gingivalis. Biochem. Biophys. Res. Commun. 166:1146-1154.
7. Braun, V. 1995. Energy-coupled transport and signal transduction through the Gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol. Rev. 16:295-307.
8. Carman, R. J., M. D. Kamakrishnan, F. H. Harper. 1990. Hemin levels in culture medium of Porphyromonas gingivalis regulate both hemin binding and trypsin-like protease production. Infect. Immun. 58:4016-4019.
9. Cornelissen, C. N., G. D. Biswas, J. Tsai, D. K. Paruchuri, S. A. Thompson, and P. F. Sparling. 1992. Gonococcal transferrin-binding protein 1 is required tor transferrin utilisation and is homologous to TonB-dependent outer membrane receptors. J. Bacteriol. 174:5788-5797.
10. Cornelissen, C. N., and P. F. Sparling. 1994. Iron piracy: acquisition of transferrin-bound iron by bacterial pathogens. Mol. Microbiol. 14:843-850.
11. Cridland, J. C., V. Booth, F. P. Ashley, M. A. Curtis, R. F. Wilson, and P. Shepherd. 1994. Preliminary characterisation of antigens recognised by monoclonal antibodies raised to Porphyromonas gingivalis and by sera of patients with periodontitis. J. Periodontal. Res. 29:339-347.
12. Curtis, M. A., J. Aduse-Opoku, J. M. Slaney, M. Rangarajan, V. Booth, J. Cridland, and P. Shepherd. 1996. Characterization of an adherence and antigenic determinant of the RI protease of Porphyromonas gingivalis which is present on multiple gene products. Infect. Immun. 64:2532-2539.
13. Dame, J. B., J. L. William, T. F. McCutchan, J. L. Weber, R. A. Wirtz, W. T. Hockmeyer, W. L. Maloy, J. D. Haynes, I. Schneider, D. Roberts, G. S. Sanders, E. P. Reddy, C. L. Diggs, and L. H. Miller. 1984. Structure of the gene encoding the immunodominant surface-antigen on the sporozoite of the human malarial parasite Plasmodium falciparum. Science 225:593-599.
14. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acid. Res. 12:387-395.
15. Ebersole, J. L., M. A. Taubman, D. J. Smith, and D. E. Frey. 1986. Human immune responses to microorganisms: patterns of systemic antibody levels to Bacteroides spp. Infect. Immun. 51:507-513.
16. Fletcher, H. M., H. A. Schenkein, R. M. Morgan, K. A. Bailey, C. R. Berry, and F. L. Macrina. 1995. Virulence of Porphyromonas gingivalis W83 mutant defective in the prtH gene. Infect. Immun. 63:1521-1528.
17. Goldberg, M. B., S. A. Boyko, J. R. Butterton, J. A. Stoebner, S. M. Payne, and S. B. Calderwood. 1992. Characterisation of a Vibrio cholerae virulence factor homologous to the family of TonB-dependent proteins. Mol. Microbiol. 6:2407-2418.
18. Han, N., J. Whitlock, and A. Progulske-Fox. 1996. The hemagglutinin gene (hagA) of Porphyromonas gingivalis 381 contains four large, contiguous, direct repeats. Infect. Immun. 64:4000-4007.
19. Härle, C., I.-S. Kim, A. Angerer, and V. Braun. 1995. Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J. 14:1430-1438.
20. Izard, J. W., and A. A. Kendall. 1994. Signal peptides: exquisitely designed transport promoters. Mol. Microbiol. 13:765-773.
21. Jarosik, G. P., J. D. Sanders, L. D. Cope, U. Muller-Eberhard, and E. J. Hansen. 1994. A functional tonB gene is required for both utilisation of heme and virulence expression by Haemophilus influenza? type b. Infect. Immun. 62:2470-2477.
22. Kadowaki, T., M. Yoneda, K. Okamoto, K. Maeda, and K. Yamamoto. 1994. Purification and characterization of a novel arginine-specific cysteine proteinase (argingipain) involved in the pathogenesis of periodontal-disease from the culture supernatant of Porphyromonas gingivalis. J. Biol. Chem. 269:21371-21378.
23. Kelly, C. G., V. Booth, H. Kendal, J. Aduse-Opoku, J. Slaney, M. A. Curtis, and T. Lehner. Colonization and haemagglutination inhibiting epitopes of Porphyromonas gingivalis. Clin. Exp. Immunol., in press.
24. Kirszbaum, L., C. Sotiropoulos, C. Jackson, S. Cleal, N. Slakeski, and E. Reynolds. 1995. Complete nucleotide sequence of a gene prtR of Porphyromonas gingivalis W50 encoding a 132 kDa protein that contains an arginine-specific thiol endopeptidase domain and a haemagglutinin domain. Biochem. Biophys. Res. Commun. 207:424-431.
25. Koster, M., W. van Klompenburg, W. Bitter, J. Leong, and P. Weisbeek. 1994. Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope. EMBO J. 13:2805-2813.
26. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
27. Legrain, M., V. Marzarin, S. W. Irwin, B. Bouchon, M.-R. Quentin-Millet, E. Jacobs, and A. B. Schryvers. 1993. Cloning and characterisation of Neisseria meningitidis genes encoding the transferrin-binding proteins Thp1 and Thp2. Gene 130:81-90.
28. Maley, J., and I. S. Roberts. 1994. Characterisation of IS1126 from Porphyromonas gingivalis W83: a new member of the IS4 family of insertion sequence elements. FEMS Microbiol. Lett. 123:239-224.
29. Markham, P. F., M. D. Glew, K. G. Whithear, and I. D. Walker. 1993. Molecular cloning of a member of the gene family that encodes pMGA, a hemagglutinin of Mycoplasma gallisepticum. Infect. Immun. 61:903-909.
30. Marsh, P. D., A. S. McDermid, A. S. McKee, and A. Baskerville. 1994. The effect of growth rate and haemin on the virulence and proteolytic activity of Porphyromonas gingivalis W50. Microbiology 140:861-865.
31. Marsh, P. D., A. S. McKee, and A. S. McDermid. 1988. Effect of haemin on enzyme activity and cytotoxin production by Bacteroides gingivalis W50. FEMS Microbiol. Lett. 55:87-92.
32. McKee, A. S., A. S. McDermid, A. Baskerville, A. B. Dowsett, D. C. Ellwood, and P. D. Marsh. 1986. Effect of hemin on the physiology and virulence of Bacteroides gingivalis W50. Infect. Immun. 52:349-355.
33. Millar, D. J., E. E. Scott, J. M. Slaney, S. U, P. Benjamin, and M. A. Curtis. 1993. Production and characterisation of monoclonal antibodies to the principle sonicate antigens of Porphyromonas gingivalis W50. FEMS Immunol. Med. Microhiol. 7:211-222.
34. Moncla, B. J., P. Braham, L. K. Rabe, and S. L. Hillier. 1991. Rapid presumptive identification of black-pigmented gram-negative anaerobic bacteria by using 4-methylumbelliferone derivatives. J. Clin. Microbiol. 29:1955-1958.
35. Nakayama, K., T. Kadowaki, K. Okamoto, and K. Yamamoto. 1995. Construction and characterization of arginine-specific cysteine proteinase (Arggingipain)-deficient mutants of Porphyromonas gingivalis. J. Biol. Chem. 270: 23619-23626.
36. Nishikata, M., and F. Yoshimura. 1991. Characterization of Porphyromonas (Bacteroides) gingivalis hemagglutinin as a protease. Bioch. Biophys. Res. Commun. 178:336-342.
37. Okamoto, K., T. Kadowaki, K. Nakayama, and K. Yamamoto. 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.
38. Okamoto, K., Y. Misumi, T. Kadowaki, M. Yoneda, K. Yamamoto, and Y. Ikehara. 1995. Structural characterisation of argingipain, a novel arginine-specific cysteine proteinase as a major periodontal pathogenic factor from Porphyromonas gingivalis. Arch. Biochem. Biophys. 316:917-925.
39. Oppenheim, D. S., and C. Yanofsky. 1980. Translational coupling during expression of the tryptophan operon of Escherichia coli. Genetics 95:785-795.
40. Pavloff, N., J. Potempa, R. N. Pike, V. Prochazka, M. C. Kiefer, J. Travis, and P. J. Barr. 1995. Molecular cloning and structural characterisation of the Arg-gingipain proteinase of Porphyromonas gingivalis. Biosynthesis as a proteinase-adhesin polyprotein. J. Biol. Chem. 270:1007-1010.
41. Pike, R., W. McGraw, J. Potempa, and J. Travis. 1994. Lysine-specific and arginine-specific proteinases from Porphyromonas gingivalis: isolation, characterization and evidence for the existence of complexes with hemagglutinins. J. Biol. Chem. 269:406-411.
42. Pike, R. N., J. Potempa, W. McGraw, T. H. Coetzev, and J. Travis. 1996. Characterisation of the binding activities of proteinase-adhesin complexes from Porphyromonas gingivalis. J. Bacteriol. 178:2876-2892.
43. Postle, K. 1990. TonB and the Gram-negative dilemma. Mol. Microbiol. 4:2019-2025.
44. Potempa, J., R. Pike, and J. Travis. 1995. The multiple forms of trypsin-like activity present in various strains of Porphyromonas gingivalis are due to the presence of either Arg-gingipain or Lys-gingipain. Infect. Immun. 63:1176-1182.
45. Rangarajan, M., J. Aduse-Opoku, J. M. Slaney, K. A. Young, and M. A. Curtis. 1997. The prpR1 and prR2 arginine-specific protease genes of Porphyromonas gingivalis W50 produce five biochemically distinct enzymes. Mol. Microbiol. 23:955-965.
46. Rangarajan, M., S. J. M. Smith, S. U, and M. A. Curtis. 1997. Biochemical characterisation of the arginine-specific proteases of Porphyromonas gingivalis W50 suggests a common precursor. Biochem. J. 323:701-709.
47. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Harbor Laboratory Press, Cold Spring Harbor, N.Y.
48. Scott, C. F., E. J. Whitaker, B. F. Hammond, and R. W. Colman. 1993. Purification and characterization of a potent 70-kDa thiol lysyl-proleinase (Lys-gingivain) from Porphyromonas gingivalis that cleaves kininogens and fibrinogen. J. Biol. Cehm. 268:7935-7942.
49. Shine, J., and L. Dalgarno. 1974. The 3 prime-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosomal binding sites. Proc. Natl. Acad. Sci. USA 71:1342-1346.
50. Slots, J., L. Bragd, M. Wikstrom, and G. Dahlén. 1986. The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults. J. Periodontol. 13: 576-577.
51. Smalley, J. W., A. J. Birss, A. S. McKee, and P. D. Marsh. 1993. Haemin-binding proteins of Porphyromonas gingivalis W50 grown in a chemostat under haemin-limitation. J. Gen. Microbiol. 139:2145-2150.
52. Stojiljkovic, I., and K. Hantke. 1992. Hemin uptake system of Yersinia enterocolitica: similarities with other TonB-dependent systems in Gram-negative bacteria. EMBO J. 11:4359-1367.
53. Stojiljkovic, I., V. Hwa, L. D-S. Martin, P. O'Goara, X. Nassif, F. Heffron, and M. So. 1995. The Neisseria meningitidis haemoglobin receptor: its role in the iron utilisation and virulence. Mol. Microbiol. 15:531-541.
54. Tomkinson, A. E., N. F. Totty, M. Ginsburg, and T. Lindahl. 1991. Location of the active site for enzyme-adenylate formation in DNA ligases. Proc. Natl. Acad. Sci. USA 88:400-404.
55. von Heijne, G. 1985. Structural and thermodynamic aspects of the transfer of proteins into and across membranes. Curr. Top. Membr. Transp. 24:151-179.
56. Westerlund, B., and T. K. Korhonen. 1993. Bacterial proteins binding to mammalian extracellular matrix. Mol. Microbiol. 9:687-694.
57. Williamson, M. P. 1994. The structure and function of proline-rich regions in proteins. Biochem. J. 297:249-260.
58. Wingrove, J. A., R. G. DiScipio, Z. Chen, J. Potempa, J. Travis, and T. E. Hugli. 1992. Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J. Biol. Chem. 267:18902-18907.
59. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.