Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase

Infection and Immunity

Volumn 67, Issue 7, 1999, Pages 3248-3256

  McGraw, Walker T ^a   Potempa, Jan ^c   Farley, David ^b   Travis, James ^a,d  

^a UNIVERSITY OF GEORGIA   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; ARGININE; BRADYKININ; CITRULLINE; DNA; PROTEIN ARGININE DEIMINASE; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ARTICLE; DNA SEQUENCE; ENZYME ANALYSIS; ENZYME PURIFICATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOELECTRIC POINT; MASS SPECTROMETRY; NONHUMAN; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN DEGRADATION;

PORPHYROMONAS GINGIVALIS;

EID: 0033004481     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.7.3248-3256.1999     Document Type: Article

References (47)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Bjellqvist, B., G. J. Hughes, C. Pasquali, N. Paquet, F. Ravier, J. C. Sanchez, S. Frutiger, and D. Hochstrasser. 1993. The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14:1023-1031.
4. Boyde, T. R., and M. Rahmatullah. 1980. Optimization of conditions for the colorimetric determination of citrulline, using diacetyl monoxime. Anal. Biochem. 107:424-431.
5. Carlsson, J., J. F. Hofling, and G. K. Sundqvist. 1984. Degradation of albumin, haemopexin, haptoglobin and transferrin, by black-pigmented Bacteroides species. J. Med. Microbiol. 18:39-46.
6. Casiano-Colon, A., and R. E. Marquis. 1988. Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl. Environ. Microbiol. 54:1318-1324.
7. Chen, Z., J. Potempa, A. Polanowski, M. Wikstrom, and J. Travis. 1992. Purification and characterization of a 50-kDa cysteine proteinase (gingipain) from Porphyromonas gingivalis. J. Biol. Chem. 267:18895-18901.
8. Eley, B. M., and S. W. Cox. 1996. Correlation between gingivain/gingipain and bacterial dipeptidyl peptidase activity in gingival crevicular fluid and periodontal attachment loss in chronic periodontitis patients. A 2-year longitudinal study. J. Periodontol. 67:703-716.
9. Enwonwu, C. O., F. Ilupeju, and R. C. Warren. 1994. Arginine metabolism in the salivary glands of protein-deficient rats and its potential association with the oral microflora. Caries Res. 28:99-105.
10. Gazi, M. I., S. W. Cox, D. T. Clark, and B. M. Eley, 1996. A comparison of cysteine and serine proteinases in human gingival crevicular fluid with tissue, saliva and bacterial enzymes by analytical isoelectric focusing. Arch. Oral. Biol. 41:393-400.
11. Grenier, D., and D. Mayrand. 1987. Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect. Immun. 55:111-117.
12. Grenier, D., and D. Mayrand. 1987. Selected characteristics of pathogenic and nonpathogenic strains of Bacteroides gingivalis. J. Clin. Microbiol. 25: 738-740.
13. Hanneken, A., P. A. Maher, and A. Baird. 1995. High affinity immunoreactive FGF receptors in the extracellular matrix of vascular endothelial cells - implications for the modulation of FGF-2. J. Cell Biol. 128:1221-1228.
14. Hayashi, H., M. Morioka, S. Ichimiya, K. Yamato, D. Hinode, A. Nagata, and R. Nakamura. 1993. Participation of an arginyl residue of insulin chain B in the inhibition of hemagglutination by Porphyromonas gingivalis. Oral Microbiol. Immunol. 8:386-389.
15. Henskens, Y. M., U. van der Velden, E. C. Veerman, and A. V. Nieuw Amerongen. 1993. Protein, albumin and cystatin concentrations in saliva of healthy subjects and of patients with gingivitis or periodontitis. J. Periodontal Res. 28:43-48.
16. Holt, S. C., J. Ebersole, J. Felton, M. Brunsvold, and K. S. Kornman. 1988. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 239:55-57.
17. Imamura, T., R. N. Pike, J. Potempa, and J. Travis. 1994. Pathogenesis of periodontitis: a major arginine-specific cysteine proteinase from Porphyromonas gingivalis induces vascular permeability enhancement through activation of the kallikrein/kinin pathway. J. Clin. Investig. 94:361-367.
18. Imamura, T., J. Potempa, R. N. Pike, and J. Travis. 1995. Dependence of vascular permeability enhancement on cysteine proteinases in vesicles of Porphyromonas gingivalis. Infect. Immun. 63:1999-2003.
19. Imamura, T., T. Yamamoto, and T. Kambara. 1984. Guinea pig plasma kallikrein as a vascular permeability enhancement factor. Its dependence on kinin generation and regulation mechanisms in vivo. Am. J. Pathol. 115:92-101.
20. Kanapka, J. A., and I. Kleinberg. 1983. Catabolism of arginine by the mixed bacteria in human salivary sediment under conditions of low and high glucose concentration. Arch. Oral Biol. 28:1007-1015.
21. Kilian, M. 1981. Degradation of immunoglobulins A1, A2, and G by suspected principal periodontal pathogens. Infect. Immun. 34:757-765.
22. Lehrer, R. I., A. K. Lichtenstein, and T. Ganz. 1993. Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu. Rev. Immunol. 11:105-128.
23. Marquis, R. E., G. R. Bender, D. R. Murray, and A. Wong. 1987. Arginine deiminase system and bacterial adaptation to acid environments. Appl. Environ. Microbiol. 53:198-200.
24. Marsh, P. D., A. S. McKee, A. S. McDermid, and A. B. Dowsett. 1989. Ultrastructure and enzyme activities of a virulent and an avirulent variant of Bacteroides gingivalis W50. FEMS Microbiol. Lett. 50:181-185.
25. Matsudaira, P. 1987. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 262: 10035-10038.
26. Mayrand, D., and S. C. Holt. 1988. Biology of asaccharolytic black-pigmented Bacteroides species. Microbiol. Rev. 52:134-152.
27. Miller, J. W., D. W. Turner, and E. D. Pedersen. 1991. Trypsin, T. denticola and P. gingivalis levels as diagnostic markers for periodontitis. Northwest Dent. Res. 3:12-14.
28. Miller, K., and M. E. Neville. 1976. Evaluation of alternate coupling reagents to replace alpha-naphthyl amine for the detection of nitrate reduction. Microbios 17:207-212.
29. Narayanan, K., L. Spack, K. McMillan, R. G. Kilbourn, M. A. Hayward, B. S. Masters, and O. W. Griffith. 1995. S-alkyl-L-thiocitrullines. Potent stereoselective inhibitors of nitric oxide synthase with strong presser activity in vivo. J. Biol. Chem. 270:11103-11110.
30. Niederman, R., B. Brunkhorst, S. Smith, R. N. Weinreb, and M. I. Ryder. 1990. Ammonia as a potential mediator of adult human periodontal infection: inhibition of neutrophil function. Arch. Oral Biol. 35(Suppl.):205S-209S.
31. Nishikata, M., and F. Yoshimura. 1991. Characterization of Porphyromonas (Bacteroides) gingivalis hemagglutinin as a protease. Biochem. Biophys. Res. Commun. 178:336-342.
32. Pike, R., W. McGraw, J. Potempa, and J. Travis. 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.
33. Porphyromonas gingivalis Genome Sequencing Project. 10 November 1997, posting date. [Online.] http://www.forsyth.org/pggp. [20 January 1999, last date accessed.]
34. 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.
35. Potempa, J., R. Pike, and J. Travis. 1997. Titration and mapping of the active site of cysteine proteinases from Porphyromonas gingivalis (gingipains) using peptidyl chloromethanes. Biol. Chem. 378:223-230.
36. Potempa, J., and J. Travis. 1996. Porphyromonas gingivalis proteinases in periodontitis, a review. Acta Biochim. Pol. 43:455-465.
37. Schagger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
38. Schenkein, H. A., and C. R. Berry. 1988. Production of chemotactic factors for neutrophils following the interaction of Bacteroides gingivalis with purified C5. J. Periodontal Res. 23:308-312.
39. Slots, J. 1977. Microflora in the healthy gingival sulcus in man. Scand. J. Dent. Res. 85:247-254.
40. Slots, J. 1977. The predominant cultivable microflora of advanced periodontitis. Scand. J. Dent. Res. 85:114-121.
41. Stuehr, D. J., and M. A. Marletta. 1985. Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proc. Natl. Acad. Sci. USA 82:7738-7742.
42. Travis, J., R. Pike, T. Imamura, and J. Potempa. 1997. Porphyromonas gingivalis proteinases as virulence factors in the development of periodontitis. J. Periodontal Res. 32:120-125.
43. Uitto, V. J., H. Larjava, J. Heino, and T. Sorsa. 1989. 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. 57:213-218.
44. Weickmann, J. L., M. E. Himmel, D. W. Smith, and D. E. Fahrney. 1978. Arginine deiminase: demonstration of two active sites and possible half-of-the-sites reactivity. Biochem. Biophys. Res. Commun. 83:107-113.
45. Weickmann, J. L., M. E. Himmel, P. G. Squire, and D. E. Fahrney. 1978. Arginine deiminase from Mycoplasma arthritidis. Properties of the enzyme from log phase cultures. J. Biol. Chem. 253:6010-6015.
46. 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.
47. Zhang, J., and T. L. Madden. 1997. PowerBLAST: a new network BLAST application for interactive or automated sequence analysis and annotation. Genome Res. 7:649-656.