Inhibition of gingipains and Porphyromonas gingivalis growth and biofilm formation by prenyl flavonoids

Journal of Periodontal Research

Volumn 52, Issue 1, 2017, Pages 89-96

  Kariu, T ^a   Nakao, R ^b   Ikeda, T ^c   Nakashima, K ^c   Potempa, J ^d,e   Imamura, T ^f  

^a Kumamoto University   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c SOJO UNIVERSITY   (Japan)

^d JAGIELLONIAN UNIVERSITY   (Poland)

^e UNIVERSITY OF LOUISVILLE   (United States)

^f KUMAMOTO UNIVERSITY   (Japan)

Author keywords

biofilm; gingipains; Porphyromonas gingivalis growth; prenylated flavonoids

Indexed keywords

ADHESIN; ARGINGIPAIN, PORPHYROMONAS GINGIVALIS; CYSTEINE PROTEINASE; FLAVONOID;

BIOFILM; DRUG EFFECT; EPIMEDIUM; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; PORPHYROMONAS GINGIVALIS; PRENYLATION;

ADHESINS, BACTERIAL; BIOFILMS; CYSTEINE ENDOPEPTIDASES; EPIMEDIUM; FLAVONOIDS; PORPHYROMONAS GINGIVALIS; PRENYLATION;

EID: 84960192734     PISSN: 00223484     EISSN: 16000765     Source Type: Journal    
DOI: 10.1111/jre.12372     Document Type: Article

References (34)

1. Slots J. Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in periodontal disease: introduction. Periodontol 2000 1999;20:7–13.
2. Oliver RC, Brown LJ. Periodontal diseases and tooth loss. Periodontol 2000 1993;2:117–127.
3. Imamura T. The role of gingipains in the pathogenesis of periodontal disease. J Periodontol 2003;74:111–118.
4. Ob-S NM, Veith PD, Dashper SG, Reynolds EC. Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Protein Pept Sci 2003;4:409–426.
5. Potempa J, Sroka A, Imamura T, Travis J. Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes. Curr Protein Pept Sci 2003;4:397–407.
6. Lourbakos A, Yuan YP, Jenkins AL et al. Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: a new trait in microbial pathogenicity. Blood 2001;97:3790–3797.
7. Kim J, Amar S. Periodontal disease and systemic conditions: a bidirectional relationship. Odontology 2006;94:10–21.
8. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol 1995;49:711–745.
9. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999;284:1318–1322.
10. Bodet C, Piche M, Chandad F, Grenier D. Inhibition of periodontopathogen-derived proteolytic enzymes by a high-molecular-weight fraction isolated from cranberry. J Antimicrob Chemother 2006;57:685–690.
11. La VD, Howell AB, Grenier D. Anti-Porphyromonas gingivalis and anti-inflammatory activities of A-type cranberry proanthocyanidins. Antimicrob Agents Chemother 2010;54:1778–1784.
12. 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;42:589–592.
13. Asahi Y, Noiri Y, Miura J et al. Effects of the tea catechin epigallocatechin gallate on Porphyromonas gingivalis biofilms. J Appl Microbiol 2014;116:1164–1171.
14. 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;19:118–120.
15. Mukai R, Fujikura Y, Murota K et al. Prenylation enhances quercetin uptake and reduces efflux in Caco-2 cells and enhances tissue accumulation in mice fed long-term. J Nutr 2013;143:1558–1564.
16. Botta B, Vitali A, Menendez P, Misiti D, Monache GD. Prenylated flavonoids: pharmacology and biotechnology. Curr Med Chem 2005;12:713–739.
17. Zhao HY, Sun JH, Fan MX et al. Analysis of phenolic compounds in Epimedium plants using liquid chromatography coupled with electrospray ionization mass spectrometry. J Chromatogr A 2008;1190:157–181.
18. 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;45:2871–2876.
19. Nakao R, Senpuku H, Watanabe H. Porphyromonas gingivalis galE is involved in lipopolysaccharide O-antigen synthesis and biofilm formation. Infect Immun 2006;74:6145–6153.
20. Davey ME, Costerton JW. Molecular genetics analyses of biofilm formation in oral isolates. Periodontol 2000 2006;42:13–26.
21. Marsh PD. Microbiological aspects of the chemical control of plaque and gingivitis. J Dent Res 1992;71:1431–1438.
22. Lamont RJ, Jenkinson HF. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 1998;62:1244–1263.
23. Kadowaki T, Nakayama K, Yoshimura F, Okamoto K, Abe N, Yamamoto K. Arg-gingipain acts as a major processing enzyme for various cell surface proteins in Porphyromonas gingivalis. J Biol Chem 1998;273:29072–29076.
24. Tahara S, Ibrahim RK. Prenylated isoflavonoids: an update. Phytochemistry 1995;38:1073–1094.
25. Barron D, Ibrahim RK. Isoprenylated flavonoids – survey. Phytochemistry 1996;43:921–982.
26. Ming LG, Lv X, Ma XN et al. The prenyl group contributes to activities of phytoestrogen 8-prenynaringenin in enhancing bone formation and inhibiting bone resorption in vitro. Endocrinology 2013;154:1202–1214.
27. Xiao J, Muzashvili TS, Georgiev MI. Advances in the biotechnological glycosylation of valuable flavonoids. Biotechnol Adv 2014;32:1145-1156.
28. Shi Y, Ratnayake DB, Okamoto K, Abe N, Yamamoto K, Nakayama K. Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis. Construction of mutants with a combination of rgpA, rgpB, kgp, and hagA. J Biol Chem 1999;274:17955–17960.
29. Kataoka S, Baba A, Suda Y et al. A novel, potent dual inhibitor of Arg-gingipains and Lys-gingipain as a promising agent for periodontal disease therapy. FASEB J 2014;28:3564–3578.
30. 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;77:80–86.
31. Gharbia SE, Shah HN. Hydrolytic enzymes liberated by black-pigmented gram-negative anaerobes. FEMS Immunol Med Microbiol 1993;6:139–145.
32. Blankenvoorde MF, van't Hof W, Walgreen-Weterings E et al. Cystatin and cystatin-derived peptides have antibacterial activity against the pathogen Porphyromonas gingivalis. Biol Chem 1998;379:1371–1375.
33. Dashper SG, Pan Y, Veith PD et al. Lactoferrin inhibits Porphyromonas gingivalis proteinases and has sustained biofilm inhibitory activity. Antimicrob Agents Chemother 2012;56:1548–1556.
34. Kuboniwa M, Amano A, Hashino E et al. Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by Porphyromonas gingivalis. BMC Microbiol 2009;9:105.