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. 1997 Mar;65(3):1101–1104. doi: 10.1128/iai.65.3.1101-1104.1997

Inducible expression of a Porphyromonas gingivalis W83 membrane-associated protease.

Y Park 1, B Lu 1, C Mazur 1, B C McBride 1
PMCID: PMC175095  PMID: 9038323

Abstract

The Tpr protease of Porphyromonas gingivalis W83 is a membrane-associated enzyme capable of hydrolyzing a chromogenic bacterial collagenase substrate. An isogenic mutant lacking a functional tpr gene had a greatly reduced ability to hydrolyze the collagenase substrate. Activity was restored to the tpr mutant by introducing a shuttle plasmid containing the tpr gene. Expression of the gene is induced by nutrient limitation, as shown by enzymatic and Northern analyses.

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Selected References

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  1. Arnott M. A., Rigg G., Shah H., Williams D., Wallace A., Roberts I. S. Cloning and expression of a Porphyromonas (Bacteroides) gingivalis protease gene in Escherichia coli. Arch Oral Biol. 1990;35 (Suppl):97S–99S. doi: 10.1016/0003-9969(90)90137-y. [DOI] [PubMed] [Google Scholar]
  2. Bedi G. S., Williams T. Purification and characterization of a collagen-degrading protease from Porphyromonas gingivalis. J Biol Chem. 1994 Jan 7;269(1):599–606. [PubMed] [Google Scholar]
  3. Birkedal-Hansen H., Taylor R. E., Zambon J. J., Barwa P. K., Neiders M. E. Characterization of collagenolytic activity from strains of Bacteroides gingivalis. J Periodontal Res. 1988 Jul;23(4):258–264. doi: 10.1111/j.1600-0765.1988.tb01369.x. [DOI] [PubMed] [Google Scholar]
  4. Bourgeau G., Lapointe H., Péloquin P., Mayrand D. Cloning, expression, and sequencing of a protease gene (tpr) from Porphyromonas gingivalis W83 in Escherichia coli. Infect Immun. 1992 Aug;60(8):3186–3192. doi: 10.1128/iai.60.8.3186-3192.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carman R. J., Ramakrishnan M. D., Harper F. H. Hemin levels in culture medium of Porphyromonas (Bacteroides) gingivalis regulate both hemin binding and trypsinlike protease production. Infect Immun. 1990 Dec;58(12):4016–4019. doi: 10.1128/iai.58.12.4016-4019.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ellen R. P., Song M., Buivids I. A. Inhibition of Actinomyces viscosus--Porphyromonas gingivalis coadhesion by trypsin and other proteins. Oral Microbiol Immunol. 1992 Aug;7(4):198–203. doi: 10.1111/j.1399-302x.1992.tb00025.x. [DOI] [PubMed] [Google Scholar]
  7. Fletcher H. M., Schenkein H. A., Macrina F. L. Cloning and characterization of a new protease gene (prtH) from Porphyromonas gingivalis. Infect Immun. 1994 Oct;62(10):4279–4286. doi: 10.1128/iai.62.10.4279-4286.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gharbia S. E., Williams J. C., Andrews D. M., Shah H. N. Genomic clusters and codon usage in relation to gene expression in oral Gram-negative anaerobes. Anaerobe. 1995 Oct;1(5):239–262. doi: 10.1006/anae.1995.1024. [DOI] [PubMed] [Google Scholar]
  9. Grenier D., Mayrand D., McBride B. C. Further studies on the degradation of immunoglobulins by black-pigmented Bacteroides. Oral Microbiol Immunol. 1989 Mar;4(1):12–18. doi: 10.1111/j.1399-302x.1989.tb00400.x. [DOI] [PubMed] [Google Scholar]
  10. Hino M., Nakano G., Harada M., Nagatsu T. Distribution of PZ-peptidase and glycylprolyl beta-naphthylamidase activities in oral tissues. Arch Oral Biol. 1975 Jan;20(1):19–22. doi: 10.1016/0003-9969(75)90147-8. [DOI] [PubMed] [Google Scholar]
  11. Jun K. C., Barua P. K., Zambon J. J., Neiders M. E. Proteolytic activity in black-pigmented bacteroides species. J Endod. 1989 Oct;15(10):463–467. doi: 10.1016/s0099-2399(89)80025-1. [DOI] [PubMed] [Google Scholar]
  12. Kilian M. Degradation of immunoglobulins A2, A2, and G by suspected principal periodontal pathogens. Infect Immun. 1981 Dec;34(3):757–765. doi: 10.1128/iai.34.3.757-765.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. Lantz M. S., Allen R. D., Vail T. A., Switalski L. M., Hook M. Specific cell components of Bacteroides gingivalis mediate binding and degradation of human fibrinogen. J Bacteriol. 1991 Jan;173(2):495–504. doi: 10.1128/jb.173.2.495-504.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lawson D. A., Meyer T. F. Biochemical characterization of Porphyromonas (Bacteroides) gingivalis collagenase. Infect Immun. 1992 Apr;60(4):1524–1529. doi: 10.1128/iai.60.4.1524-1529.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Li J., Ellen R. P., Hoover C. I., Felton J. R. Association of proteases of Porphyromonas (Bacteroides) gingivalis with its adhesion to Actinomyces viscosus. J Dent Res. 1991 Feb;70(2):82–86. doi: 10.1177/00220345910700021501. [DOI] [PubMed] [Google Scholar]
  17. Lu B., McBride B. C. Stress response of Porphyromonas gingivalis. Oral Microbiol Immunol. 1994 Jun;9(3):166–173. doi: 10.1111/j.1399-302x.1994.tb00054.x. [DOI] [PubMed] [Google Scholar]
  18. Madden T. E., Thompson T. M., Clark V. L. Expression of Porphyromonas gingivalis proteolytic activity in Escherichia coli. Oral Microbiol Immunol. 1992 Dec;7(6):349–356. doi: 10.1111/j.1399-302x.1992.tb00635.x. [DOI] [PubMed] [Google Scholar]
  19. Maley J., Shoemaker N. B., Roberts I. S. The introduction of colonic-Bacteroides shuttle plasmids into Porphyromonas gingivalis: identification of a putative P. gingivalis insertion-sequence element. FEMS Microbiol Lett. 1992 May 15;72(1):75–81. doi: 10.1016/0378-1097(92)90492-7. [DOI] [PubMed] [Google Scholar]
  20. McDermid A. S., McKee A. S., Marsh P. D. Effect of environmental pH on enzyme activity and growth of Bacteroides gingivalis W50. Infect Immun. 1988 May;56(5):1096–1100. doi: 10.1128/iai.56.5.1096-1100.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nakamura S., Takeuchi A., Masamoto Y., Abiko Y., Hayakawa M., Takiguchi H. Cloning of the gene encoding a glycylprolyl aminopeptidase from Porphyromonas gingivalis. Arch Oral Biol. 1992 Oct;37(10):807–812. doi: 10.1016/0003-9969(92)90114-n. [DOI] [PubMed] [Google Scholar]
  22. Nishikata M., Yoshimura F. Characterization of Porphyromonas (bacteroides) gingivalis hemagglutinin as a protease. Biochem Biophys Res Commun. 1991 Jul 15;178(1):336–342. doi: 10.1016/0006-291x(91)91819-x. [DOI] [PubMed] [Google Scholar]
  23. Nishikata M., Yoshimura F., Nodasaka Y. Possibility of Bacteroides gingivalis hemagglutinin possessing protease activity revealed by inhibition studies. Microbiol Immunol. 1989;33(1):75–80. doi: 10.1111/j.1348-0421.1989.tb01499.x. [DOI] [PubMed] [Google Scholar]
  24. Otogoto J., Kuramitsu H. K. Isolation and characterization of the Porphyromonas gingivalis prtT gene, coding for protease activity. Infect Immun. 1993 Jan;61(1):117–123. doi: 10.1128/iai.61.1.117-123.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Park Y., McBride B. C. Characterization of the tpr gene product and isolation of a specific protease-deficient mutant of Porphyromonas gingivalis W83. Infect Immun. 1993 Oct;61(10):4139–4146. doi: 10.1128/iai.61.10.4139-4146.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Park Y., McBride B. C. Cloning of a Porphyromonas (Bacteroides) gingivalis protease gene and characterization of its product. FEMS Microbiol Lett. 1992 May 1;71(3):273–278. doi: 10.1016/0378-1097(92)90721-y. [DOI] [PubMed] [Google Scholar]
  27. Potempa J., Pike R., Travis J. 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. 1995 Apr;63(4):1176–1182. doi: 10.1128/iai.63.4.1176-1182.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Robertson P. B., Lantz M., Marucha P. T., Kornman K. S., Trummel C. L., Holt S. C. Collagenolytic activity associated with Bacteroides species and Actinobacillus actinomycetemcomitans. J Periodontal Res. 1982 May;17(3):275–283. doi: 10.1111/j.1600-0765.1982.tb01154.x. [DOI] [PubMed] [Google Scholar]
  29. Schenkein H. A. Complement factor D-like activity of Porphyromonas gingivalis W83. Oral Microbiol Immunol. 1991 Aug;6(4):216–220. doi: 10.1111/j.1399-302x.1991.tb00480.x. [DOI] [PubMed] [Google Scholar]
  30. Schenkein H. A. The effect of periodontal proteolytic Bacteroides species on proteins of the human complement system. J Periodontal Res. 1988 May;23(3):187–192. doi: 10.1111/j.1600-0765.1988.tb01356.x. [DOI] [PubMed] [Google Scholar]
  31. Smalley J. W., Birss A. J., Shuttleworth C. A. The degradation of type I collagen and human plasma fibronectin by the trypsin-like enzyme and extracellular membrane vesicles of Bacteroides gingivalis W50. Arch Oral Biol. 1988;33(5):323–329. doi: 10.1016/0003-9969(88)90065-9. [DOI] [PubMed] [Google Scholar]
  32. Smalley J. W., Shuttleworth C. A., Birss A. J. Collagenolytic activity of the extracellular vesicles of Bacteroides gingivalis W50 and an avirulent variant W50/BE1. Arch Oral Biol. 1989;34(7):579–583. doi: 10.1016/0003-9969(89)90098-8. [DOI] [PubMed] [Google Scholar]
  33. Sojar H. T., Lee J. Y., Bedi G. S., Genco R. J. Purification and characterization of a protease from Porphyromonas gingivalis capable of degrading salt-solubilized collagen. Infect Immun. 1993 Jun;61(6):2369–2376. doi: 10.1128/iai.61.6.2369-2376.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sorsa T., Uitto V. J., Suomalainen K., Turto H., Lindy S. A trypsin-like protease from Bacteroides gingivalis: partial purification and characterization. J Periodontal Res. 1987 Sep;22(5):375–380. doi: 10.1111/j.1600-0765.1987.tb01602.x. [DOI] [PubMed] [Google Scholar]
  35. Sundqvist G. K., Carlsson J., Herrmann B. F., Höfling J. F., Vätäinen A. Degradation in vivo of the C3 protein of guinea-pig complement by a pathogenic strain of Bacteroides gingivalis. Scand J Dent Res. 1984 Feb;92(1):14–24. doi: 10.1111/j.1600-0722.1984.tb00854.x. [DOI] [PubMed] [Google Scholar]
  36. Sundqvist G., Carlsson J., Herrmann B., Tärnvik A. Degradation of human immunoglobulins G and M and complement factors C3 and C5 by black-pigmented Bacteroides. J Med Microbiol. 1985 Feb;19(1):85–94. doi: 10.1099/00222615-19-1-85. [DOI] [PubMed] [Google Scholar]
  37. Sundqvist G., Carlsson J., Hänström L. Collagenolytic activity of black-pigmented Bacteroides species. J Periodontal Res. 1987 Jul;22(4):300–306. doi: 10.1111/j.1600-0765.1987.tb01589.x. [DOI] [PubMed] [Google Scholar]
  38. Takahashi N., Kato T., Kuramitsu H. K. Isolation and preliminary characterization of the Porphyromonas gingivalis prtC gene expressing collagenase activity. FEMS Microbiol Lett. 1991 Nov 15;68(2):135–138. doi: 10.1016/0378-1097(91)90116-r. [DOI] [PubMed] [Google Scholar]
  39. Toda K., Otsuka M., Ishikawa Y., Sato M., Yamamoto Y., Nakamura R. Thiol-dependent collagenolytic activity in culture media of Bacteroides gingivalis. J Periodontal Res. 1984 Jul;19(4):372–381. doi: 10.1111/j.1600-0765.1984.tb01010.x. [DOI] [PubMed] [Google Scholar]
  40. Uitto V. J., Larjava H., Heino J., Sorsa T. A protease of Bacteroides gingivalis degrades cell surface and matrix glycoproteins of cultured gingival fibroblasts and induces secretion of collagenase and plasminogen activator. Infect Immun. 1989 Jan;57(1):213–218. doi: 10.1128/iai.57.1.213-218.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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