4,134
Views
46
CrossRef citations to date
0
Altmetric
Review Articles

Strategies for the inhibition of gingipains for the potential treatment of periodontitis and associated systemic diseases

&
Article: 24800 | Received 29 Apr 2014, Accepted 15 Jul 2014, Published online: 18 Aug 2014

References

  • Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999; 4: 1–6. [PubMed Abstract].
  • Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998; 25: 134–44. [PubMed Abstract].
  • Guo Y, Nguyen K-A, Potempa J. Dichotomy of gingipains action as virulence factors: from cleaning substrates with the precision of a surgeon's knife to a meat chopper-like brutal degradation of proteins. Periodontol 2000. 2010; 54: 15–44. [PubMed Abstract] [PubMed CentralFull Text].
  • Fitzpatrick RE, Wijeyewickrema LC, Pike RN. The gingipains: scissors and glue of the periodontal pathogen, Porphyromonas gingivalis. Future Microbiol. 2009; 4: 471–87. [PubMed Abstract].
  • Sztukowska M, Veillard F, Potempa B, Bogyo M, Enghild JJ, Thogersen IB, etal. Disruption of gingipain oligomerization into non-covalent cell-surface attached complexes. Biol Chem. 2012; 393: 971–7. [PubMed Abstract] [PubMed CentralFull Text].
  • Pathirana RD, O'Brien-Simpson NM, Brammar GC, Slakeski N, Reynolds EC. Kgp and RgpB, but not RgpA, are important for Porphyromonas gingivalis virulence in the murine periodontitis model. Infect Immun. 2007; 75: 1436–42. [PubMed Abstract] [PubMed CentralFull Text].
  • Wilensky A, Polak D, Houri-Haddad Y, Shapira L. The role of RgpA in the pathogenicity of Porphyromonas gingivalis in the murine periodontitis model. J Clin Periodontol. 2013; 40: 924–32. [PubMed Abstract].
  • Yongqing T, Potempa J, Pike RN, Wijeyewickrema LC. The lysine-specific gingipain of Porphyromonas gingivalis: importance to pathogenicity and potential strategies for inhibition. Adv Exp Med Biol. 2011; 712: 15–29. [PubMed Abstract].
  • Grenier D, La VD. Proteases of Porphyromonas gingivalis as important virulence factors in periodontal disease and potential targets for plant-derived compounds: a review article. Curr Drug Targets. 2011; 12: 322–31. [PubMed Abstract].
  • Veillard F, Sztukowska M, Mizgalska D, Ksiazek M, Houston J, Potempa B, etal. Inhibition of gingipains by their profragments as the mechanism protecting Porphyromonas gingivalis against premature activation of secreted proteases. Biochim Biophys Acta. 2013; 1830: 4218–28. [PubMed Abstract] [PubMed CentralFull Text].
  • Huq NL, Seers CA, Toh EC, Dashper SG, Slakeski N, Zhang L, etal. Propeptide-mediated inhibition of cognate gingipain proteinases. PLoS One. 2013; 8: e65447. [PubMed Abstract] [PubMed CentralFull Text].
  • de Diego I, Veillard FT, Guevara T, Potempa B, Sztukowska M, Potempa J, etal. Porphyromonas gingivalis virulence factor gingipain RgpB shows a unique zymogenic mechanism for cysteine peptidases. J Biol Chem. 2013; 288: 14287–96. [PubMed Abstract] [PubMed CentralFull Text].
  • Veillard F, Potempa B, Poreba M, Drag M, Potempa J. Gingipain aminopeptidase activities in Porphyromonas gingivalis. Biol Chem. 2012; 393: 1471–6. [PubMed Abstract].
  • Curtis MA, Slaney JM, Carman RJ, Pemberton PA. Interaction of a trypsin-like enzyme of Porphyromonas gingivalis W83 with antithrombin III. FEMS Microbiol Lett. 1993; 108: 169–74. [PubMed Abstract].
  • Grøn H, Pike R, Potempa J, Travis J, Thøgersen IB, Enghild JJ, etal. The potential role of alpha 2-macroglobulin in the control of cysteine proteinases (gingipains) from Porphyromonas gingivalis. J Periodontal Res. 1997; 32: 61–8.
  • Blankenvoorde MF, Henskens YM, van't Hof W, Veerman EC, Nieuw Amerongen AV. Inhibition of the growth and cysteine proteinase activity of Porphyromonas gingivalis by human salivary cystatin S and chicken cystatin. Biol Chem. 1996; 377: 847–50. [PubMed Abstract].
  • Blankenvoorde MF, van't Hof W, Walgreen-Weterings E, van Steenbergen TJ, Brand HS, Veerman EC, etal. Cystatin and cystatin-derived peptides have antibacterial activity against the pathogen Porphyromonas gingivalis. Biol Chem. 1998; 379: 1371–5. [PubMed Abstract].
  • Umemoto T, Naito Y, Li M, Suzuki I, Namikawa I. Growth inhibition of a human oral bacterium Porphyromonas gingivalis by rat cysteine proteinase inhibitor cystatin S. Lett Appl Microbiol. 1996; 23: 151–3. [PubMed Abstract].
  • Bania J, Kubiak A, Wojtachnio K, Polanowski A. Pancreatic secretory trypsin inhibitor acts as an effective inhibitor of cysteine proteases gingipains from Porphyromonas gingivalis. J Periodontal Res. 2008; 43: 232–6. [PubMed Abstract].
  • Snipas SJ, Stennicke HR, Riedl S, Potempa J, Travis J. Inhibition of distant caspase homologues by natural caspase inhibitors. Biochem J. 2001; 357: 575–80. [PubMed Abstract] [PubMed CentralFull Text].
  • Barrett AJ, Rawlings ND. Evolutionary lines of cysteine peptidases. Biol Chem. 2001; 382: 727–33. [PubMed Abstract].
  • Taiyoji M, Shitomi Y, Taniguchi M, Saitoh E, Ohtsubo S. Identification of proteinaceous inhibitors of a cysteine proteinase (an Arg-specific gingipain) from Porphyromonas gingivalis in rice grain, using targeted-proteomics approaches. J Proteome Res. 2009; 8: 5165–74. [PubMed Abstract].
  • Taiyoji M, Yamanaka T, Tsuno T, Ohtsubo S. Potential value of a rice protein extract containing proteinaceous inhibitors against cysteine proteinases from Porphyromonas gingivalis, for managing periodontal diseases. Biosci Biotechnol Biochem. 2013; 77: 80–6. [PubMed Abstract].
  • Daspher SG, Pan Y, Veith PD, Chen Y-Y, Toh ECY, Liu SW, etal. Lactoferrin inhibits Porphyromonas gingivalis proteinases and has sustained biofilm inhibitory activity. Antimicrob Agents Chemother. 2012; 56: 1548–56.
  • Gusman H, Grogan J, Kagan HM, Troxler RF, Oppenheim FG. Salivary histatin 5 is a potent competitive inhibitor of the cysteine proteinase clostripain. FEBS Lett. 2001; 489: 97–100. [PubMed Abstract].
  • Toh ECY, Daspher SG, Huq NL, Attard TJ, O'Brien-Simpson NM, Chen Y-Y, etal. Porphyromonas gingivalis cysteine proteinase inhibition by κ-casein peptides. Antimicrob Agents Chemother. 2011; 55: 1155–61. [PubMed Abstract] [PubMed CentralFull Text].
  • Ekici ÖD, Götz MG, James KE, Li ZZ, Rukamp BJ, Asgian JL, etal. Aza-peptide Michael acceptors: a new class of inhibitors specific for caspases and other clan CD cysteine proteases. J Med Chem. 2004; 47: 1889–92. [PubMed Abstract].
  • Curtis MA, Opoku JA, Rangarajan M, Gallagher A, Sterne JAC, Reid CR, etal. Attenuation of the virulence of Porphyromonas gingivalis by using a specific synthetic Kgp protease inhibitor. Infect Immun. 2002; 70: 6968–75. [PubMed Abstract] [PubMed CentralFull Text].
  • Kadowaki T, Baba A, Abe N, Takii R, Hashimoto M, Tsukuba T, etal. Suppression of pathogenicity of Porphyromonas gingivalis by newly developed gingipain inhibitors. Mol Pharmacol. 2004; 66: 1599–606. [PubMed Abstract].
  • Kataoka S, Baba A, Suda Y, Takii R, Hashimoto M, Kawakubo T. A novel, potent dual inhibitor of Arg-gingipains and Lys-gingipain as a promising agent for periodontal disease therapy. FASEB J. 2014; 28: 3564–78. doi: 10.1096/fj.14-252130
  • Nagahara T, Yokoyama Y, Inamura K, Katakura S, Komoriya S, Yamaguchi H, etal. Dibasic (amidinoaryl) propanoic acid derivatives as novel blood coagulation factor Xa inhibitors. J Med Chem. 1994; 37: 1200–7. [PubMed Abstract].
  • Matsushita K, Imamura T, Tancharoen S, Tatsuyama S, Tomikawa M, Travis J, etal. Selective inhibition of Porphyromonas gingivalis growth by a factor Xa inhibitor, DX-9065a. J Periodontal Res. 2006; 41: 171–6. [PubMed Abstract].
  • 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: 223–30. [PubMed Abstract].
  • Bialas A, Grembecka J, Krowarsch D, Otlewski J, Potempa J, Mucha A. Exploring the Sn binding pockets in gingipains by newly developed inhibitors: structure-based design, chemistry and activity. J Med Chem. 2006; 49: 1744–53. [PubMed Abstract].
  • Kadowaki T, Kitano S, Baba A, Takii R, Hashimoto M, Katunuma N, etal. Isolation and characterization of a novel and potent inhibitor of Arg-gingipain from Streptomyces sp. strain FA-70. Biol Chem. 2003; 384: 911–20. [PubMed Abstract].
  • Travis J, Potempa J. Bacterial proteinases as targets for the development of second-generation antibiotics. Biochim Biophys Acta. 2000; 1477: 35–50. [PubMed Abstract].
  • Krauser JA, Potempa J, Travis J, Powers JC. Inhibition of arginine gingipains (RgpB and HRgpA) with benzamidine inhibitors: zinc increases inhibitory potency. Biol Chem. 2002; 383: 1193–8. [PubMed Abstract].
  • Eick S, Pfister W, Stürzebecher U, Jarema S, Stürzebecher J. Inhibitors of benzamidine type influence the virulence properties of Porphyromonas gingivalis strains. Acta Biochim Pol. 2003; 50: 725–34. [PubMed Abstract].
  • Fröhlich E, Kantyka T, Plaza K, Schmidt K-H, Pfister W, Potempa J, etal. Benzamidine derivatives inhibit the virulence of Porphyromonas gingivalis. Mol Oral Microbiol. 2013; 28: 192–203.
  • Imamura T, Matsushita K, Travis J, Potempa J. Inhibition of trypsin-like cysteine proteinases (gingipains) from Porphyromonas gingivalis by tetracycline and its analogues. Antimicrob Agents Chemother. 2001; 45: 2871–6. [PubMed Abstract] [PubMed CentralFull Text].
  • Grenier D, Plamondon P, Sorsa T, Lee H-M, McNamara T, Ramamurthy NS, etal. Inhibition of proteolytic, serpinolytic, and progelatinase-b activation activities of periodontopathogens by doxycycline and the non-antimicrobial chemically modified tetracycline derivatives. J Periodontol. 2002; 73: 79–85. [PubMed Abstract].
  • Genco CA, Odusanya BM, Potempa J, Mikolajczyk-Pawlinska J, Travis J. A peptide domain on gingipain R which confers immunity against Porphyromonas gingivalis. Infect Immun. 1998; 66: 4108–14. [PubMed Abstract] [PubMed CentralFull Text].
  • Sela MN, Babitski E, Steinberg D, Kohavi D, Rosen G. Degradation of collagen-guided tissue regeneration membranes by proteolytic enzymes of Porphyromonas gingivalis and its inhibition by antibacterial agents. Clin Oral Impl Res. 2009; 20: 496–502.
  • Li L, Li Z, Chen D, Lu X, Feng X, Wright EC, etal. Inactivation of microbial arginine deiminases by L-canavanine. J Am Chem Soc. 2008; 130: 1918–31. [PubMed Abstract].
  • Nakatsuka Y, Nagasawa T, Yumoto Y, Nakazawa F, Furuichy Y. Inhibitory effects of sword bean extract on alveolar bone resorption induced in rats by Porphyromonas gingivalis infection. J Periodontal Res. 2014; 49
  • Koziel J, Mydel P, Potempa J. The link between periodontal disease and rheumatoid arthritis: an updated review. Curr Rheumatol Rep. 2014; 16: 408. [PubMed Abstract] [PubMed CentralFull Text].
  • Bodet C, Piché M, Chandad F, Grenier D. Inhibition of periodontopathogen-derived proteolytic enzymes by a high-molecular-weight fraction isolated from cranberry. J Antimicrob Chemother. 2006; 57: 685–90. [PubMed Abstract].
  • Yamanaka A, Kouchi T, Kasai K, Kato T, Ishihara K, Okuda K. Inhibitory effect of cranberry polyphenol on biofilm formation and cysteine proteases of Porphyromonas gingivalis. J Periodontal Res. 2007; 42: 589–92. [PubMed Abstract].
  • La VD, Howell AB, Grenier D. Anti-Porphyromonas gingivalis and anti-inflammatory activities of A-type cranberry proanthocyanidins. Antimicrob Agents Chemother. 2010; 54: 1778–84. [PubMed Abstract] [PubMed CentralFull Text].
  • Polak D, Naddaf R, Shapira L, Weiss EI, Houri-Haddad Y. Protective potential of non-dialyzable material fraction of cranberry juice on the virulence of P. gingivalis and F. nucleatum mixed infection. J Periodontol. 2013; 84: 1019–25. [PubMed Abstract].
  • Hirasawa M, Takada K, Makimura M, Otake S. Improvement of periodontal status by green tea catechin using a local delivery system: a clinical pilot study. J Periodontal Res. 2002; 37: 433–8. [PubMed Abstract].
  • Gadagi JS, Chava VK, Reddy VR. Green tea extract as a local drug therapy on periodontitis patients with diabetes mellitus: a randomized case-control study. J Indian Soc Periodontol. 2013; 17: 198–203. [PubMed Abstract] [PubMed CentralFull Text].
  • Hattarki SA, Pushpa SP, Bhat K. Evaluation of the efficacy of green tea catechins as an adjunct to scaling and root planing in the management of chronic periodontitis using PCR analysis: a clinical and microbiological study. J Indian Soc Periodontol. 2013; 17: 204–9. [PubMed Abstract] [PubMed CentralFull Text].
  • Chava VK, Vedula BD. Thermo-reversible green tea catechin gel for local application in chronic periodontitis: a 4-week clinical trial. J Periodontol. 2013; 84: 1290–6. [PubMed Abstract].
  • Kudva P, Tabasum ST, Shekhawat NK. Effect of green tea catechin, a local drug delivery system as an adjunct to scaling and root planing in chronic periodontitis patients: a clinicomicrobiological study. J Indian Soc Periodontol. 2011; 15: 39–45. [PubMed Abstract] [PubMed CentralFull Text].
  • Zhao L, La VD, Grenier D. Antibacterial, antiadherence, antiprotease, and anti-inflammatory activities of various tea extracts: potential benefits for periodontal diseases. J Med Food. 2013; 16: 428–36. [PubMed Abstract].
  • Makimura M, Hirasawa M, Kobayashi K, Indo J, Sakanaka S, Taguchi T, etal. Inhibitory effect of tea catechins on collagenase activity. J Periodontol. 1993; 64: 630–6. [PubMed Abstract].
  • Hosokawa Y, Hosokawa I, Shindo S, Ozaki K, Matsuo T. (-)-Epigallocatechin-3-gallate inhibits CC chemokine ligand 11 production in human gingival fibroblasts. Cell Physiol Biochem. 2013; 31: 960–7. [PubMed Abstract].
  • Okamoto M, Sugimoto A, Leung KP, Nakayama K, Kamaguchi A, Maeda N. Inhibitory effect of green tea catechins on cysteine proteinases in Porphyromonas gingivalis. Oral Microbiol Immunol. 2004; 19: 118–200. [PubMed Abstract].
  • Cai Y, Kurita-Ochiai T, Hashizume T, Yamamoto M. Green tea epigallocatechin-3-gallate attenuates Porphyromonas gingivalis-induced atherosclerosis. Pathog Dis. 2013; 67: 76–83. [PubMed Abstract].
  • Löhr G, Beikler T, Podbielski A, Standar K, Redanz S, Hensel A. Polyphenols from Myrothamnus flabellifolia Welv. inhibit in vitro adhesion of Porphyromonas gingivalis and exert antiinflammatory cytoprotective effects in KB cells. J Clin Periodontol. 2011; 38: 457–69.
  • Devenyi AG, Plaut AG, Grundy FJ, Wright A. Post-infectious human serum antibodies inhibit IgA1 proteinases by interaction with the cleavage site specificity determinant. Mol Immunol. 1993; 30: 1243–8. [PubMed Abstract].
  • Frandsen EV, Kjeldsen M, Kilian M. Inhibition of Prevotella and Capnocytophaga immunoglobulin A1 proteases by human serum. Clin Diagn Lab Immunol. 1997; 4: 458–64. [PubMed Abstract] [PubMed CentralFull Text].
  • Kirkeby L, Rasmussen TT, Reinholdt J, Kilian M. Immunoglobulins in nasal secretions of healthy humans: structural integrity of secretory immunoglobulin A1 (IgA1) and occurrence of neutralizing antibodies to IgA1 proteases of nasal bacteria. Clin Diagn Lab Immunol. 2000; 7: 31–9. [PubMed Abstract] [PubMed CentralFull Text].
  • Mistry D, Stockley RA. IgA1 protease. Int J Biochem Cell Biol. 2006; 38: 1244–8. [PubMed Abstract].
  • Yokoyama K, Sugano N, Rahman AK, Oshikawa M, Ito K. Activity of anti-Porphyromonas gingivalis egg yolk antibody against gingipains in vitro. Oral Microbiol Immunol. 2007; 22: 352–5. [PubMed Abstract].
  • Yokoyama K, Sugano N, Shimada T, Shofigur RA, Ibrahim el-SM, Isoda R, etal. Effects of egg yolk antibody against Porphyromonas gingivalis gingipains in periodontitis patients. J Oral Sci. 2007; 49: 201–6. [PubMed Abstract].
  • Gibson FC III, Genco CA. Prevention of Porphyromonas gingivalis-induced oral bone loss following immunization with gingipain R1. Infect Immun. 2001; 69: 7959–63. [PubMed Abstract] [PubMed CentralFull Text].
  • Yonezawa H, Ishihara K, Okuda K. Arg-gingipain a DNA vaccine induces protective immunity against infection by Porphyromonas gingivalis in a murine model. Infect Immun. 2001; 69: 2858–64. [PubMed Abstract] [PubMed CentralFull Text].
  • Miyachi K, Ishihara K, Kimizuka R, Okuda K. Arg-gingipain A DNA vaccine prevents alveolar bone loss in mice. J Dent Res. 2007; 86: 446–50. [PubMed Abstract].
  • Nakagawa T, Saito A, Hosaka Y, Ishihara K. Gingipains as candidate antigens for Porphyromonas gingivalis vaccine. Keio J Med. 2003; 52: 158–62. [PubMed Abstract].
  • O'Brien-Simpson NM, Paolini RA, Reynolds EC. Rgp-Kgp peptide-based immunogens provide protection against Porphyromonas gingivalis challenge in a murine lesion model. Infect Immun. 2000; 68: 4055–63. [PubMed Abstract] [PubMed CentralFull Text].
  • Kuboniwa M, Amano A, Shizukuishi S, Nakagawa I, Hamada S. Specific antibodies to Porphyromonas gingivalis lys-gingipain by DNA vaccination inhibit bacterial binding to hemoglobin and protect mice from infection. Infect Immun. 2001; 69: 2972–9. [PubMed Abstract] [PubMed CentralFull Text].
  • Rajapakse PS, O'Brien-Simpson NM, Slakeski N, Hoffmann B, Reynolds EC. Immunization with RgpA-Kgp proteinase-adhesion complexes of Porphyromonas gingivalis protects against periodontal bone loss in the rat periodontitis model. Infect Immun. 2002; 70: 2480–6. [PubMed Abstract] [PubMed CentralFull Text].
  • Sharma D, Prasad S, Karthikeyan BV. Vaccination against periodontitis: the saga continues. Expert Rev Vaccines. 2007; 6: 579–90. [PubMed Abstract].
  • Inagaki S, Ishihara K, Yasaki Y, Yamada S, Okuda K. Antibody responses of periodontitis patients to gingipains of Porphyromonas gingivalis. J Periodontol. 2003; 74: 1432–9. [PubMed Abstract].
  • Nakayama K. Molecular genetics of Porphyromonas gingivalis: gingipains and other virulence factors. Curr Protein Pept Sci. 2003; 4: 389–95. [PubMed Abstract].
  • Booth V, Ashley FP, Lehner T. Passive immunization with monoclonal antibodies against Porphyromonas gingivalis in patients with periodontitis. Infect Immun. 1996; 64: 422–7. [PubMed Abstract] [PubMed CentralFull Text].
  • Kelly CG, Booth V, Kendal H, Slaney JM, Curtis MA, Lehner T. The relationship between colonization and haemagglutination inhibiting and B cell epitopes of Porphyromonas gingivalis. Clin Exp Immunol. 1997; 110: 285–91. [PubMed Abstract] [PubMed CentralFull Text].
  • O'Brien-Simpson NM, Pathirana RD, Paolini RA, Chen YY, Veith PD, Tam V, etal. An immune response directed to proteinase and adhesin functional epitopes protects against Porphyromonas gingivalis-induced periodontal bone loss. J Immunol. 2005; 175: 3980–9. [PubMed Abstract].
  • Muramatsu K, Kokubu E, Shibahara T, Okuda K, Ishihara K. HGP44 induces protection against Porphyromonas gingivalis-induced alveolar bone loss in mice. Clin Vaccine Immunol. 2011; 18: 888–91. [PubMed Abstract] [PubMed CentralFull Text].
  • Yasaki-Inagaki Y, Inagaki S, Yamada S, Okudo K, Ishihara K. Production of protective antibodies against Porphyromonas gingivalis strains by immunization with recombinant gingipain domains. FEMS Immunol Med Microbiol. 2006; 47: 287–95. [PubMed Abstract].
  • Yonezawa H, Kato T, Kuramitsu HK, Okuda K, Ishihara K. Immunization by Arg-gingipain A DNA vaccine protects mice against an invasive Porphyromonas gingivalis infection through regulation of interferon-γ production. Oral Microbiol Immunol. 2005; 20: 259–66. [PubMed Abstract].
  • Tenorio EL, Klein BA, Cheung WS, Hu LT. Identification of interspecies interactions affecting Porphyromonas gingivalis virulence phenotypes. J Oral Microbiol. 2011; 3: 8396.