The role of gingipains in the pathogenesis of periodontal disease

Journal of Periodontology

Volumn 74, Issue 1, 2003, Pages 111-118

  Imamura, Takahisa ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Cysteine proteinase; Gingipains; Peridontitis therapy; Periodontitis microbiology; Porphyromonas gingivalis

Indexed keywords

2 [4 [(1 ACETIMIDOYL 3 PYRROLIDINYL)OXY]PHENYL] 3 (7 AMIDINO 2 NAPHTHYL)PROPIONIC ACID; AMINO ACID; ANTIBIOTIC AGENT; ARGININE; BACTERIAL ENZYME; BLOOD CLOTTING FACTOR; BLOOD CLOTTING FACTOR 10A INHIBITOR; CD14 ANTIGEN; CYSTEINE PROTEINASE; CYSTEINE PROTEINASE INHIBITOR; FIBRIN; FIBRINOGEN; GAMMA INTERFERON; GENE PRODUCT; GINGIPAIN; HEMAGGLUTININ; INTERLEUKIN 6; INTERLEUKIN 8; KALLIKREIN; KININ; LIPOPOLYSACCHARIDE; LYSINE; PHOSPHOLIPID; PROTEIN SUBUNIT; TETRACYCLINE; TETRACYCLINE DERIVATIVE; TRYPTASE; TRYPTASE INHIBITOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIRULENCE FACTOR;

ACTIVE IMMUNIZATION; ALVEOLAR BONE; AMINO ACID SEQUENCE; AMINO ACID TRANSPORT; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL INFECTION; BINDING AFFINITY; BLEEDING TENDENCY; BLOOD CLOTTING; BLOOD VESSEL PERMEABILITY; COMPLEX FORMATION; DISEASE COURSE; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME INHIBITION; FIMBRIA; GINGIVA DISEASE; GRAM NEGATIVE INFECTION; HUMAN; INHIBITION KINETICS; LEUKOCYTE ACTIVATION; MOUSE; NONHUMAN; OSTEOLYSIS; PATHOGENESIS; PERIODONTAL DISEASE; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INDUCTION; REVIEW; STRUCTURAL HOMOLOGY;

ADHESINS, BACTERIAL; ADULT; ALVEOLAR BONE LOSS; ANIMALS; ANTIGENS, CD14; BACTEROIDACEAE INFECTIONS; BLOOD COAGULATION; CAPILLARY PERMEABILITY; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; DISEASE PROGRESSION; FIBRIN FIBRINOGEN DEGRADATION PRODUCTS; GINGIVAL CREVICULAR FLUID; GINGIVAL HEMORRHAGE; HEMAGGLUTININS; HUMANS; MICE; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; TRYPSIN; VIRULENCE FACTORS;

EID: 0037261991     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2003.74.1.111     Document Type: Review

References (62)

1. Slots J. Importance of black-pigmented Bacteroides in human periodontal disease. In: Genco, RJ, Mergenhagen SE, eds. Host-Parasite Interactions in Periodontal Diseases. Washington DC: American Society of Microbiology; 1982:27-45.
2. Holt SC, Ebersole J, Fenton J, Brunsvold M, Kornman KS. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 1987;239:55-57.
3. Zambon JJ. Microbiology of periodontal disease. In: Genco RJ, Goldman HM, Cohen DW, eds. Contemporary Periodontics. St. Louis: CV Mosby Company; 1990:147-160.
4. Grenier D, Mayrand D. Selected characteristics of pathogenic and nonpathogenic strains of Bacteroides gingivalis. J Clin Microbiol 1987;25:738-740.
5. Smalley JW, Birss AJ, Kay HM, McKee AS, Marsh PD. The distribution of trypsin-like enzyme activity in the cultures of a virulent and an avirulent strain of Bacteroides gingivalis W50. Oral Microbiol Immunol 1989;4: 178-181.
6. Kesavalu L, Holt SC, Ebersole JL. Trypsin-like protease activity of Porphyromonas gingivalis as a potential virulence factor in a murine lesion model. Microb Pathog 1996;20:1-10.
7. Potempa J, Pike R, Travis J. Titration and mapping of the active site of cysteine proteinases from Porphyromonas gingivalis (gingipains) using peptidyl chloromethanes. Biol Chem 1997;378:223-230.
8. 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;63: 1176-1182.
9. Potempa J, Pavloff N, Travis J. Porphyromonas gingivalis: A proteinase/gene accounting audit. Trend Microbiol 1995;3:430-434.
10. Curtis MA, Kuramitsu HK, Lanz M, et al. Molecular genetics and nomenclature of proteinases of Porphyromonas gingivalis. J Periodont Res 1999;34:464-472.
11. Potempa J, Banbula A, Travis J. Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontol 2000 2000;24:153-192.
12. Rangarajan M, Aduse-Opoku J, Slanet JM, Young KA, Curtis MA. The prpR1 and the prpR2 arginine-specific protease genes of Porphyromonas gingivalis W50 produce five biochemically distinct enzymes. Mol Microbiol 1997;23:855-865.
13. Curtis MA, Thickett A, Slaney JM, Rangarajan M, et al. Variable carbohydrate modification to the catalytic chains of the rgpA and rgpB proteases of Porphyromonas gingivalis W50. Infect Immun 1999;67:3816-3823.
14. Pavloff N, Potempa J, Pike RN, et al. Molecular cloning and structural characterization of the Arg-gingipain proteinase of Porphyromonas gingivalis. J Biol Chem 1995; 270:1007-1010.
15. Mikolajczyk-Pawlinska J, Kordula T, Pavloff N, et al. Genetic variations of Porphyromonas gingivalis genes encoding gingipains, cysteine proteinases with arginine or lysine specificity. Biol Chem 1998;379:205-211.
16. Potempa J, Mikolajczyk-Pawlinska J, Brassell D, et al. Comparative properties of two cysteine proteinases (gingipain Rs), the products of two related but individual genes of Porphyromonas gingivalis. J Biol Chem 1998;273:21648-21657.
17. Pavloff N, Pemberton PA, Potempa J, et al. Molecular cloning and characterization of Porphyromonas gingivalis Lys-gingipain. A new member of an emerging family of pathogenic bacterial proteinase. J Biol Chem 1997; 272:1595-1600.
18. Chen JM, Rawlings ND, Stevens RA, Barett JA. Identification of the active site of legumain links it to caspase, clostripain and gingipains in a new clan of cysteine endopeptidases. FEBS Lett 1998;441:361-365.
19. Eichinger A, Beisel H-G, Jacob U, et al. Crystal structure of gingipain R: An Arg-specific bacterial cysteine protease with a caspase-like fold. EMBO J 1999;18: 5453-5462.
20. Hinode D, Nagata A, Ichimiya S, Hayashi H, Morioka M, Nakamura R. Generation of plasma kinin by three types of protease isolated from Porphyromonas gingivalis 381. Arch Oral Biol 1992;37:859-868.
21. Kaminishi H, Cho T, Itoh T, et al. Vascular permeability enhancing activity of Porphyromonas gingivalis protease in guinea pig. FEMS Microbiol Lett 1993;114:109-114.
22. Imamura T, Pike RN, Potempa J, Travis J. 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 Invest 1994;94: 361-367.
23. Imamura T, Pike RN, Potempa J, Travis J. Dependence of vascular permeability enhancement on cysteine proteinases in vesicles of Porphyromonas gingivalis. Infect Immun 1995;63:1999-2003.
24. Imamura T, Potempa J, Travis J. Comparison of pathogenic properties between two types of arginine-specific cysteine proteinases (gingipains-R) from Porphyromonas gingivalis. Microb Pathog 2000;29:155-163.
25. Ransjo M, Marklund M, Persson M, Lerner UH. Synergistic interactions of bradykinin, thrombin, interleukin-1 and tumor necrosis factor on prostanoid biosynthesis in human periodontal ligament cells. Arch Oral Biol 1998;43:253-260.
26. 2 and interleukin-6 in human osteoblast-like cells. Biochim Biophys Acta 1992;1135:97-102.
27. Lerner UH. Regulation of bone metabolism by the kallikrein-kinin system, the coagulation cascade, and the acute-phase reactants. Oral Surg Oral Med Oral Pathol 1994;78:481-493.
28. DeMichele MAA, Moon DG, Fenton JW II, Minnear FL. Thrombin's enzymatic activity increases permeability of endothelial cell monolayers. J Appl Physiol 1990;69: 1599-1606.
29. Bizios R, Lai L, Fenton JW II, Malik AB. Thrombin-induced chemotaxis and aggregation of neutrophils. J Cell Physiol 1986;128:485-490.
30. Bar-Shavit R, Kahn A, Fenton JW II, Wilner GD. Monocyte chemotaxis: Stimulation by specific exosite region in thrombin. Science 1983;220:728-730.
31. Partridge NC, Hillyard CJ, Nolan RD, Martin TJ. Regulation of prostaglandin production by osteoblast-rich calvarial cells. Prostaglandins 1985;30:527-539.
32. Jones A, Geczy CL. Thrombin and factor Xa enhance the production of interleukin-1. Immunology 1990;71: 236-241.
33. 2 level as a predictor of periodontal attachment loss. J Periodont Res 1986;21: 101-112.
34. Masada MP, Persson R, Kenney JS, Lee SW, Page RC, Allison AC. Measurement of interleukin-1α and -1β in gingival crevicular fluid: Implications for the pathogenesis of periodontal disease. J Periodont Res 1990;25:156-163.
35. Hoffmann O, Klaushofer K, Koller K, Peterlik M, Mavreas T, Stern P. Indomethacin inhibits thrombin, but not throxin-stimulated resorption, of fetal rat limb bones. Prostaglandins 1986;31:601-608.
36. Imamura T, Potempa J, Tanase S, Travis J. Activation of blood coagulation factor X by arginine-specific cysteine proteases (gingipain-Rs) from Porphyromonas gingivalis. J Biol Chem 1997;272:16062-16067.
37. Imamura T, Tanase S, Hamamoto T, Potempa J, Travis, J. Activation of blood coagulation factor IX by gingipains R, arginine-specific cysteine proteases from Porphyromonas gingivalis. Biochem J 2001;353:325-331.
38. Imamura T, Banbula A, Pereira PJB, Travis J, Potempa J. Activation of human prothrombin by arginine-specific cysteine proteases (gingipains R) from Porphyromonas gingivalis. J Biol Chem 2001;276:18984-18991.
39. Hosotaki K, Imamura T, Potempa J, Kitamura N, Travis J. Activation of protein C by arginine-specific cysteine proteinases (gingipains-R) from Porphyromonas gingivalis. Biol Chem 1999;380:75-80.
40. Albandar JM, Olsen I, Gjermo P. Association between six DNA probe-detected periodontal bacteria and alveolar bone loss and other clinical signs of periodontitis. Acta Odontol Scand 1990;48:415-423.
41. Pike RN, Potempa J, McGraw W, Coetzer THT, Travis J. Characterization of the binding activities of protease-adhesin complexes from Porphyromonas gingivalis. J Bacteriol 1996; 178:2876-2882.
42. Imamura T, Potempa J, Pike RN, Moore JN, Barton MH, Travis J. Effect of free and vesicle-bound cysteine proteases of Porphyromonas gingivalis on plasma clot formation: Implications for bleeding tendency at periodontitis sites. Infect Immun 1995;63:4877-4882.
43. 2-macroglobulin in the control of cysteine proteinases (gingipains) from Porphyromonas gingivalis. J Periodont Res 1997;32:61-68.
44. Schenkein, HA. Complement factor D-like activity of Porphyromonas gingivalis W83. Oral Microbiol Immunol 1991;6:216-220.
45. Wingrove JA, DiScipio RG, Chen Z, Potempa J, Travis J, Hugli TE. Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J Biol Chem 1992;267:18902-18907.
46. Kadowaki T, Yoneda M, Okamoto K, Maeda K, Yamamoto K. 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 1994;269:21371-21378.
47. Jagels MA, Travis J, Potempa J, Pike R, Hugli TE. Proteolytic inactivation of the leukocyte C5a receptor by proteinases derived from Porphyromonas gingivalis. Infect Immun 1996;64:1984-1991.
48. Sugawara S, Nemoto E, Tada H, Miyake K, Imamura T, Takada H. Proteolysis of human monocyte CD14 by cysteine proteinases (gingipains) from Porphyromonas gingivalis leading to lipopolysaccharide hyporesponsiveness. J Immunol 2000; 165:411-418.
49. Mikolajczyk-Pawlinska J, Travis J, Potempa J. Modulation of interleukin-8 activity by gingipains from Porphyromonas gingivalis: Implications for pathogenicity of periodontal disease. FEBS Lett 1998;440:282-286.
50. Banbula A, Bugno M, Kuster, A, Heinrich PC, Travis J, Potempa J. Rapid and efficient inactivation of IL-6 by lysine and arginine specific proteinases (gingipains) from Porphyromonas gingivalis. Biochem Biophys Res Commun 1999;261:598-602.
51. McGee JM, Tucci MA, Edmundson TP, Serio CL, Johnson RB. The relationship between concentrations of proinflammatory cytokines within gingiva and the adjacent sulcular depth. J Periodontol 1998;69:865-871.
52. Fletcher J, Nair S, Poole S, Henderson B, Wilson M. Cytokine degradation by biofilms of Porphyromonas gingivalis. Curr Microbiol 1998;36:216-219.
53. Calkins CC, Platt K, Potempa J, Travis J. Inactivation of tumor necrosis factor by proteinases (gingipains) from the periodontal pathogen, Porphyromonas gingivalis. Implications for immune evasion. J Biol Chem 1998; 273:6611-6614.
54. Yun PL, DeCarlo AA, Hunter N. Modulation of major histocompatibility complex protein expression by human γ interferon mediated by cysteine proteinase-adhesin polyproteins of Porphyromonas gingivalis. Infect Immun 1999;67:2986-2995.
55. DeCarlo AA, Grenett HE, Harber GJ, et al. Induction of matrix metalloproteinases and a collagen-degrading phenotype in fibroblasts and epithelial cells by secreted Porphyromonas gingivalis proteinase. J Periodont: Res 1998;33:408-420.
56. DeCarlo AA, Windsor LJ, Bodden MK, Harber GJ, Birkedal-Hansen B, Birkedal-Hansen H. Activation and novel processing of matrix metalloproteinases and a thiol-proteinase from the oral anaerobe Porphyromonas gingivalis. J Dent Res 1997;76:1260-1270.
57. Moritz AJ, Cappelli D, Lantz MS, Holt SC, Ebersole JL. Immunization with Porphyromonas gingivalis cysteine proteinase: Effect on experimental gingivitis and ligature-induced periodontitis in Macaca fascicularis. J Periodontol 1998;69:686-697.
58. Genco CA, Odusanya BM, Mikolajczyk-Pawlinska J, Potempa J, Travis J. A peptide domain on gingipain R which confers immunity against Porphyromonas gingivalis infection in mice. Infect Immun 1998;66:4108-4114.
59. Matsushita K, Imamura T, Tomikawa M, et al. Selective inhibition of P. gingivalis growth by a factor Xa-specific inhibitor, DX-9065a. J Dent Res; in press.
60. Ciancio SG. Clinical experiences with tetracyclines in the treatment of periodontal diseases. Ann NY Acad Sci 1994;732:132-139.
61. Feres M, Haffajee AD, Goncalves C, et al. Systemic doxycycline administration in the treatment of periodontal infections. (I). Effect on the subgingival microbiota. J Clin Periodontol 1999;26:775-783.
62. Imamura T, Matsushita K, Travis J, Potempa J. Inhibition of trypsin-like cysteine proteinases (gingipains) from Porphyromonas gingivalis by tetracycline and the analogues. Antimicrob Agents Chemother 2001;45:2871-2876.