Portal de Periódicos da CAPES

Bacterial adhesins to host components in periodontitis

2009; Wiley; Volume: 52; Issue: 1 Linguagem: Inglês

10.1111/j.1600-0757.2009.00307.x

1600-0757

Atsuo Amano,

Oral Health Pathology and Treatment

Periodontology 2000Volume 52, Issue 1 p. 12-37 Bacterial adhesins to host components in periodontitis Atsuo Amano, Atsuo AmanoSearch for more papers by this author Atsuo Amano, Atsuo AmanoSearch for more papers by this author First published: 11 December 2009 https://doi.org/10.1111/j.1600-0757.2009.00307.xCitations: 77Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat References 1 Abdallah AM, Gey van Pittius NC, Champion PA, Cox J, Luirink J, Vandenbroucke-Grauls CM, Appelmelk BJ, Bitter W. Type VII secretion-mycobacteria show the way. Nat Rev Microbiol 2007: 5: 883–891. 2 Abe N, Baba A, Takii R, Nakayama K, Kamaguchi A, Shibata Y, Abiko Y, Okamoto K, Kadowaki T, Yamamoto K. Roles of Arg- and Lys-gingipains in coaggregation of Porphyromonas gingivalis: identification of its responsible molecules in translation products of rgpA, kgp, and hagA genes. Biol Chem 2004: 385: 1041–1047. 3 Amano A. Disruption of epithelial barrier and impairment of cellular function by Porphyromonas gingivalis. Front Biosci 2007: 12: 3965–3974. 4 Amano A. Molecular interaction of Porphyromonas gingivalis with host cells: implication for the microbial pathogenesis of periodontal disease. J Periodontol 2003: 74: 90–96. 5 Amano A, Kuboniwa M, Horie H, Kataoka K, Nagata H, Shizukuishi S. Effects of temperature stress on adhesive abilities and antigenicity of Porphyromonas gingivalis. J Jpn Soc Periodontol 1997: 39: 86–92. (in Japanese). 6 Amano A, Kuboniwa M, Kataoka K, Tazaki K, Inoshita E, Nagata H, Tamagawa H, Shizukuishi S. Binding of hemoglobin by Porphyromonas gingivalis. FEMS Microbiol Lett 1995: 134: 63–67. 7 Amano A, Kuboniwa M, Nakagawa I, Akiyama S, Morisaki I, Hamada S. Prevalence of specific genotypes of Porphyromonas gingivalis fimA and periodontal health status. J Dent Res 2000: 79: 1664–1668. 8 Amano A, Nakagawa I, Kataoka K, Morisaki I, Hamada S. Distribution of Porphyromonas gingivalis strains with fimA genotypes in periodontitis patients. J Clin Microbiol 1999: 37: 1426–1430. 9 Amano A, Nakagawa I, Okahashi N, Hamada N. Variations of Porphyromonas gingivalis fimbriae in relation to microbial pathogenesis. J Periodontal Res 2004: 39: 136–142. 10 Amano A, Nakamura T, Kimura S, Morisaki I, Nakagawa I, Kawabata S, Hamada S. Molecular interactions of Porphyromonas gingivalis fimbriae with host proteins: kinetic analyses based on surface plasmon resonance. Infect Immun 1999: 67: 2399–2405. 11 Amano A, Sharma A, Sojar HT, Kuramitsu HK, Genco RJ. Effects of temperature stress on expression of fimbriae and superoxide dismutase by Porphyromonas gingivalis. Infect Immun 1994: 62: 4682–4685. 12 Amano A, Sharma A, Lee JY, Sojar HT, Raj PA, Genco RJ. Structural domains of Porphyromonas gingivalis recombinant fimbrillin that mediate binding to salivary proline-rich protein and statherin. Infect Immun 1996: 64: 1631–1637. 13 Asai Y, Ohyama Y, Gen K, Ogawa T. Bacterial fimbriae and their peptides activate human gingival epithelial cells through Toll-like receptor 2. Infect Immun 2001: 69: 7387–7395. 14 Asakawa R, Komatsuzawa H, Kawai T, Yamada S, Goncalves RB, Izumi S, Fujiwara T, Nakano Y, Suzuki N, Uchida Y, Ouhara K, Shiba H, Taubman MA, Kurihara H, Sugai M. Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 2003: 50: 1125–1139. 15 Bahrani-Mougeot FK, Buckles EL, Lockatell CV, Hebel JR, Johnson DE, Tang CM, Donnenberg MS. Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract. Mol Microbiol 2002: 45: 1079–1093. 16 Barnhart MM, Chapman MR. Curli biogenesis and function. Annu Rev Microbiol 2006: 60: 131–147. 17 Bamford CV, Fenno JC, Jenkinson HF, Dymock D. The chymotrypsin-like protease complex of Treponema denticola ATCC 35405 mediates fibrinogen adherence and degradation. Infect Immun 2007: 75: 4364–4372. 18 Burrows LL. Weapons of mass retraction. Mol Microbiol 2005: 57: 878–888. 19 Campellone KG, Leong JM. Tails of two Tirs: actin pedestal formation by enteropathogenic E. coli and enterohemorrhagic E. coli O157:H7. Curr Opin Microbiol 2003: 6: 82–90. 20 Capitani G, Eidam O, Glockshuber R, Grütter MG. Structural and functional insights into the assembly of type 1 pili from Escherichia coli. Microbes Infect 2006: 8: 2284–2290. 21 Capone R, Wang HT, Ning Y, Sweier DG, Lopatin DE, Fenno JC. Human serum antibodies recognize Treponema denticola Msp and PrtP protease complex proteins. Oral Microbiol Immunol 2008: 23: 165–169. 22 Cascales E. The type VI secretion tool kit. EMBO Rep 2008: 9: 735–741. 23 Cascales E, Christie PJ. The versatile bacterial type IV secretion systems. Nat Rev Microbiol 2003: 1: 137–1149. 24 Chen P, Cisar JO, Hess S, Ho JT, Leung KP. Amended description of the genes for synthesis of Actinomyces naeslundii T14V type 1 fimbriae and associated adhesin. Infect Immun 2007: 75: 4181–4185. 25 Chen T, Nakayama K, Belliveau LL, Duncan MJ. Porphyromonas gingivalis gingipains and adhesion to epithelial cells. Infect Immun 2001: 69: 3048–3056. 26 Cisar JO, Takahashi Y, Ruhl S, Donkersloot JA, Sandberg AL. Specific inhibitors of bacterial adhesion: observations from the study of gram-positive bacteria that initiate biofilm formation on the tooth surface. Adv Dent Res 1997: 11: 168–175. 27 Cole W, Chan D, Hickey A, Wilcken D. Collagen composition of normal and myxomatous human mitral heart valves. Biochem J 1984: 219: 451–460. 28 Cox EA, Sastry SK, Huttenlocher A. Integrin-mediated adhesion regulates cell polarity and membrane protrusion through the Rho family of GTPases. Mol Biol Cell 2001: 12: 265–277. 29 Craig L, Pique ME, Tainer JA. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2004: 2: 363–378. 30 Darveau RP, Tanner A, Page RC. The microbial challenge in periodontitis. Periodontol 2000 1997: 14: 12–32. 31 Davey M, Liu X, Ukai T, Jain V, Gudino C, Gibson FC III, Golenbock D, Visintin A, Genco CA. Bacterial fimbriae stimulate proinflammatory activation in the endothelium through distinct TLRs. J Immunol 2008: 180: 2187–2195. 32 De Vries FP, Cole R, Dankert J, Frosch M, Van Putten JP. Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 1998: 27: 1203–1212. 33 Dickinson DP, Kubiniec MA, Yoshimura F, Genco RJ. Molecular cloning and sequencing of the gene encoding the fimbrial subunit protein of Bacteroides gingivalis. J Bacteriol 1988: 170: 1658–1665. 34 Donkersloot JA, Cisar JO, Wax ME, Harr RJ, Chassy BM. Expression of Actinomyces viscosus antigens in Escherichia coli: cloning of a structural gene (fimA) for type 2 fimbriae. J Bacteriol 1985: 162: 1075–1078. 35 Dorn BR, Leung KL, Progulske-Fox A. Invasion of human oral epithelial cells by Prevotella intermedia. Infect Immun 1998: 66: 6054–6057. 36 Drobni M, Hallberg K, Ohman U, Birve A, Persson K, Johansson I, Strömberg N. Sequence analyses of fimbriae subunit FimA proteins on Actinomyces naeslundii genospecies 1 and 2 and Actinomyces odontolyticus with variant carbohydrate binding specificities. BMC Microbiol 2006: 6: 43. 37 Duncan MJ, Mann EL, Cohen MS, Ofek I, Sharon N, Abraham SN. The distinct binding specificities exhibited by enterobacterial type 1 fimbriae are determined by their fimbrial shafts. J Biol Chem 2005: 280: 37707–37716. 38 Edwards AM, Dymock D, Jenkinson HF. From tooth to hoof: treponemes in tissue-destructive diseases. J Appl Microbiol 2003: 94: 767–780. 39 Edwards AM, Jenkinson HF, Woodward MJ, Dymock D. Binding properties and adhesion-mediating regions of the major sheath protein of Treponema denticola ATCC 35405. Infect Immun 2005: 73: 2891–2898. 40 Eick S, Rodel J, Einax JW, Pfister W. Interaction of Porphyromonas gingivalis with KB cells: comparison of different clinical isolates. Oral Microbiol Immunol 2002: 17: 201–208. 41 Ellen RP, Buivids IA, Simardone JR. Actinomyces viscosus fibril antigens detected by immunogold electron microscopy. Infect Immun 1989: 57: 1327–1331. 42 Ellen PP, Ko KS, Lo CM, Grove DD, Ishihara K. Insertional inactivation of the prtP gene of Treponema denticola confirms dentilisin's disruption of epithelial junctions. J Mol Microbiol Biotechnol 2000: 2: 581–586. 43 Eto DS, Jones TA, Sundsbak JL, Mulvey MA. Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog 2007: 3: e100. 44 Fenno JC, Muller KH, McBride BC. Sequence analysis, expression, and binding activity of recombinant major outer sheath protein (Msp) of Treponema denticola. J Bacteriol 1996: 178: 2489–2497. 45 Fenno JC, Tamura M, Hannam PM, Wong GW, Chana RA, McBride BC. Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect Immun 2000: 68: 1884–1892. 46 Figdor D, Davis J. Cell surface structures of Actinomyces israelli. Aust Dent J 1997: 42: 125–128. 47 Fine DH, Furgang D, Schreiner HC, Goncharoff P, Charlesworth J, Ghazwan G, Fitzgerald-Bocarsly P, Figurski DH. Phenotypic variation in Actinobacillus actinomycetemcomitans during laboratory growth: implications for virulence. Microbiology 1999: 145: 1335–1347. 48 Fine DH, Velliyagounder K, Furgang D, Kaplan JB. The Actinobacillus actinomycetemcomitans autotransporter adhesin Aae exhibits specificity for buccal epithelial cells from humans and old world primates. Infect Immun 2005: 73: 1947–1953. 49 Fujise O, Miura M, Hamachi T, Maeda K. Involvement of Porphyromonas gingivalis fimA genotype in treatment outcome following nonsurgical periodontal therapy. J Periodontol 2005: 76: 1661–1666. 50 Fujise O, Wang Y, Chen W, Chen C. Adherence of Aggregatibacter actinomycetemcomitans via serotype-specific polysaccharide antigens in lipopolysaccharides. Oral Microbiol Immunol 2008: 23: 226–233. 51 Fujiwara T, Morishima S, Takahashi I, Hamada S. Molecular cloning and sequencing of the fimbrilin gene of Porphyromonas gingivalis strains and characterization of recombinant proteins. Biochem Biophys Res Commun 1993: 197: 241–247. 52 Gerlach RG, Hensel M. Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 2007: 297: 401–415. 53 Gibbons RJ, Hay DI, Cisar JO, Clark WB. Adsorbed salivary proline-rich protein 1 and statherin: receptors for type 1 fimbriae of Actinomyces viscosus T14V-J1 on apatitic surfaces. Infect Immun 1988: 56: 2990–2993. 54 Gibson FC, Hong C III, Chou HH, Yumoto H, Chen J, Lien E, Wong J, Genco CA. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 2004: 109: 2801–2806. 55 Goulbourne PA, Ellen RP. Evidence that Porphyromonas (Bacteroides) gingivalis fimbriae function in adhesion to Actinomyces viscosus. J Bacteriol 1991: 173: 5266–5274. 56 Hajishengallis G, Martin M, Sojar HT, Sharma A, Schifferle RE, DeNardin E, Russell MW, Genco RJ. Dependence of bacterial protein adhesins on Toll-like receptors for proinflammatory cytokine induction. Clin Diagn Lab Immunol 2002: 9: 403–411. 57 Hajishengallis G, Shakhatreh MA, Wang M, Liang S. Complement receptor 3 blockade promotes IL-12-mediated clearance of Porphyromonas gingivalis and negates its virulence in vivo. J Immunol 2007: 179: 2359–2367. 58 Hajishengallis G, Tapping RI, Harokopakis E, Nishiyama S, Ratti P, Schifferle RE, Lyle EA, Triantafilou M, Triantafilou K, Yoshimura F. Differential interactions of fimbriae and lipopolysaccharide from Porphyromonas gingivalis with the Toll-like receptor 2-centred pattern recognition apparatus. Cell Microbiol 2006: 8: 1557–1570. 59 Hajishengallis G, Wang M, Liang S, Triantafilou M, Triantafilou K. Pathogen induction of CXCR4/TLR2 cross-talk impairs host defense function. Proc Natl Acad Sci U S A 2008: 105: 13532–13537. 60 Hallberg K, Holm C, Ohman U, Strömberg N. Actinomyces naeslundii displays variant fimP and fimA fimbrial subunit genes corresponding to different types of acidic proline-rich protein and beta-linked galactosamine binding specificity. Infect Immun 1998: 66: 4403–4410. 61 Hamada N, Sojar HT, Cho MI, Genco RJ. Isolation and characterization of a minor fimbria from Porphyromonas gingivalis. Infect Immun 1996: 64: 4788–4794. 62 Hamada N, Watanabe K, Arai M, Hiramine H, Umemoto T. Cytokine production induced by a 67-kDa fimbrial protein from Porphyromonas gingivalis. Oral Microbiol Immunol 2002: 17: 197–200. 63 Hamada S, Amano A, Kimura S, Nakagawa I, Kawabata S, Morisaki I. The importance of fimbriae in the virulence and ecology of some oral bacteria. Oral Microbiol Immunol 1998: 13: 129–138. 64 Hamada S, Fujiwara T, Morishima S, Takahashi I, Nakagawa I, Kimura S, Ogawa T. Molecular and immunological characterization of the fimbriae of Porphyromonas gingivalis. Microbiol Immunol 1994: 38: 921–930. 65 Han YW, Ikegami A, Rajanna C, Kawsar HI, Zhou Y, Li M, Sojar HT, Genco RJ, Kuramitsu HK, Deng CX. Identification and characterization of a novel adhesin unique to oral Fusobacteria. J Bacteriol 2005: 187: 5330–5340. 66 Han YW, Shi W, Huang GT, Kinder Haake S, Park NH, Kuramitsu H, Genco RJ. Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells. Infect Immun 2000: 68: 3140–3146. 67 Han YW, Redline RW, Li M, Yin L, Hill GB, McCormick TS. Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect Immun 2004: 72: 2272–2279. 68 Harokopakis E, Albzreh MH, Martin MH, Hajishengallis G. TLR2 transmodulates monocyte adhesion and transmigration via Rac1- and PI3K-mediated inside-out signaling in response to Porphyromonas gingivalis fimbriae. J Immunol 2006: 176: 7645–7656. 69 Hashimoto M, Ogawa S, Asai Y, Takai Y, Ogawa T. Binding of Porphyromonas gingivalis fimbriae to Treponema denticola dentilisin. FEMS Microbiol Lett 2003: 226: 267–271. 70 Hauck CR, Agerer F, Muenzner P, Schmitter T. Cellular adhesion molecules as targets for bacterial infection. Eur J Cell Biol 2006: 85: 235–242. 71 Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala'Aldeen D. Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 2004: 68: 692–744. 72 Hiramine H, Watanabe K, Hamada N, Umemoto T. Porphyromonas gingivalis 67-kDa fimbriae induced cytokine production and osteoclast differentiation utilizing TLR2. FEMS Microbiol Lett 2003: 229: 49–55. 73 Hiratsuka K, Hayakawa M, Kiyama-Kishikawa M, Sasaki Y, Hirai T, Abiko Y. Role of the hemin-binding protein 35 (HBP35) of Porphyromonas gingivalis in coaggregation. Microb Pathog 2008: 44: 320–328. 74 Holden N, Totsika M, Dixon L, Catherwood K, Gally DL. Regulation of P-fimbrial phase variation frequencies in Escherichia coli CFT073. Infect Immun 2007: 75: 3325–3334. 75 Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the 'red complex', a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 2005: 38: 72–122. 76 Hung CS, Bouckaert J, Hung D, Pinkner J, Widberg C, DeFusco A, Auguste CG, Strouse R, Langermann S, Waksman G, Hultgren SJ. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol Microbiol 2002: 44: 903–915. 77 Ikegami A, Honma K, Sharma A, Kuramitsu HK. Multiple functions of the leucine-rich repeat protein LrrA of Treponema denticola. Infect Immun 2004: 72: 4619–4627. 78 Inagaki S, Onishi S, Kuramitsu HK, Sharma A. Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by "Tannerella forsythia". Infect Immun 2006: 74: 5023–5028. 79 Inoue T, Ohta H, Kokeguchi S, Fukui K, Kato K. Colonial variation and fimbriation of Actinobacillus actinomycetemcomitans. FEMS Microbiol Lett 1990: 57: 13–17. 80 Inoue T, Tanimoto I, Ohta H, Kato K, Murayama Y, Fukui K. Molecular characterization of low-molecular-weight component protein, Flp, in Actinobacillus actinomycetemcomitans fimbriae. Microbiol Immunol 1998: 42: 253–258. 81 Isberg RR, Leong JM. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 1990: 60: 861–871. 82 Izano EA, Sadovskaya I, Wang H, Vinogradov E, Ragunath C, Ramasubbu N, Jabbouri S, Perry MB, Kaplan JB. Poly-N-acetylglucosamine mediates biofilm formation and detergent resistance in Aggregatibacter actinomycetemcomitans. Microb Pathog 2008: 44: 52–60. 83 Johnson R, Brown JJ, Maslow JN. Clonal distribution of the three alleles of the Gal(α1-4)Gal-specific adhesin gene papG among Escherichia coli strains from patients with bacteremia. J Infect Dis 1998: 177: 651–661. 84 Kachlany SC, Planet PJ, Desalle R, Fine DH, Figurski DH, Kaplan JB. flp-1, the first representative of a new pilin gene subfamily, is required for nonspecific adherence of Actinobacillus actinomycetemcomitans. Mol Microbiol 2001: 40: 542–554. 85 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. 86 Kaplan CW, Lux R, Haake SK, Shi W. The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Mol Microbiol 2008: 71: 35–47. 87 Kaplan JB, Velliyagounder K, Ragunath C, Rohde H, Mack D, Knobloch JK, Ramasubbu N. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J Bacteriol 2004: 186: 8213–8220. 88 Kato T, Kawai S, Nakano K, Inaba H, Kuboniwa M, Nakagawa I, Tsuda K, Omori H, Ooshima T, Yoshimori T, Amano A. Virulence of Porphyromonas gingivalis is altered by substitution of fimbria gene with different genotype. Cell Microbiol 2007: 9: 753–765. 89 Katoh M, Saito S, Takiguchi H, Abiko Y. Bactericidal activity of a monoclonal antibody against a recombinant 40-kDa outer membrane protein of Porphyromonas gingivalis. J Periodontol 2000: 71: 368–375. 90 Kaufman J, DiRienzo JM. Isolation of a corncob (coaggregation) receptor polypeptide from Fusobacterium nucleatum. Infect Immun 1989: 57: 331–337. 91 Kinder SA, Holt SC. Localization of the Fusobacterium nucleatum T18 adhesin activity mediating coaggregation with Porphyromonas gingivalis T22. J Bacteriol 1993: 175: 840–850. 92 Kirn TJ, Jude BA, Taylor RK. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 2005: 438: 863–866. 93 Kobe B, Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 1994: 19: 415–421. 94 Kobe B, Kajava AV. The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 2001: 11: 725–732. 95 Kolenbrander PE. Surface recognition among oral bacteria: multigeneric coaggregations and their mediators. Crit Rev Microbiol 1989: 17: 137–159. 96 Kolenbrander PE, Celesk RA. Coaggregation of human oral Cytophaga species and Actinomyces israelii. Infect Immun 1983: 40: 1178–1185. 97 Komatsuzawa H, Asakawa R, Kawai T, Ochiai K, Fujiwara T, Taubman MA, Ohara M, Kurihara H, Sugai M. Identification of six major outer membrane proteins from Actinobacillus actinomycetemcomitans. Gene 2002: 288: 195–201. 98 Kontani M, Kimura S, Nakagawa I, Hamada S. Adherence of Porphyromonas gingivalis to matrix proteins via a fimbrial cryptic receptor exposed by its own arginine-specific protease. Mol Microbiol 1997: 24: 1179–1187. 99 Kozarov E, Whitlock J, Dong H, Carrasco E, Progulske-Fox A. The number of direct repeats in hagA is variable among Porphyromonas gingivalis strains. Infect Immun 1998: 66: 4721–4725. 100 Kuboniwa M, Amano A, Hashino E, Yamamoto Y, Inaba H, Hamada N, Nakayama K, Tribble GD, Lamont RJ, Shizukuishi S. Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by Porphyromonas gingivalis. BMC Microbiol 2009: 9: 105. 101 Kuboniwa M, Amano A, Shizukuishi S. Hemoglobin-binding protein purified from Porphyromonas gingivalis is identical to lysine-specific cysteine proteinase (Lys-gingipain). Biochem Biophys Res Commun 1998: 249: 38–43. 102 Lakio L, Paju S, Alfthan G, Tiirola T, Asikainen S, Pussinen PJ. Actinobacillus actinomycetemcomitans serotype d-specific antigen contains the O antigen of lipopolysaccharide. Infect Immun 2003: 71: 5005–5011. 103 Lamont RJ, Jenkinson HF. Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol Immunol 2000: 15: 341–349. 104 Lamont RJ, Yilmaz O. In or out: the invasiveness of oral bacteria. Periodontol 2000 2002: 30: 61–69. 105 Lane MC, Mobley HL. Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int 2007: 72: 19–25. 106 Latasa C, Solano C, Penadés JR, Lasa I. Biofilm-associated proteins. C R Biol 2006: 329: 849–857. 107 Le Bouguénec C, Servin AL. Diffusely adherent Escherichia coli strains expressing Afa/Dr adhesins (Afa/Dr DAEC): hitherto unrecognized pathogens. FEMS Microbiol Lett 2006: 256: 185–194. 108 Lee JY, Sojar HT, Bedi GS, Genco RJ. Porphyromonas (Bacteroides) gingivalis fimbrillin: size, amino-terminal sequence, and antigenic heterogeneity. Infect Immun 1991: 59: 383–389. 109 Lee KK, Sheth HB, Wong WY, Sherburne R, Paranchych W, Hodges RS, Lingwood CA, Krivan H, Irvin RT. The binding of Pseudomonas aeruginosa pili to glycosphingolipids is a tip-associated event involving the C-terminal region of the structural pilin subunit. Mol Microbiol 1994: 11: 705–713. 110 Lee SF, Andrian E, Rowland E, Marquez IC. Immune response and alveolar bone resorption in a mouse model of Treponema denticola infection. Infect Immun 2009: 77: 694–698. 111 Lee SW, Sabet M, Um HS, Yang L, Kim HC, Zhu W. Identification and characterization of the genes encoding a unique surface (S-) layer of Tannerella forsythia. Gene 2006: 371: 102–111. 112 Lee SY, Bian XL, Wong GW, Hannam PM, McBride BC, Fenno JC. Cleavage of Treponema denticola PrcA polypeptide to yield protease complex-associated proteins Prca1 and Prca2 is dependent on PrtP. J Bacteriol 2002: 184: 3864–3870. 113 Leung K, Nesbitt WE, Okamoto M, Fukushima H. Identification of a fimbriae-associated haemagglutinin from Prevotella intermedia. Microb Pathog 1999: 26: 139–148. 114 Leung KP, Fukushima H, Nesbitt WE, Clark WB. Prevotella intermedia fimbriae mediate hemagglutination. Oral Microbiol Immunol 1996: 11: 42–50. 115 Leung KP, Fukushima H, Sagawa H, Walker CB, Clark WB. Surface appendages, hemagglutination, and adherence to human epithelial cells of Bacteroides intermedius. Oral Microbiol Immunol 1989: 4: 204–210. 116 Leung KP, Nesbitt WE, Fischlschweiger W, Hay DI, Clark WB. Binding of colloidal gold-labeled salivary proline-rich proteins to Actinomyces viscosus type 1 fimbriae. Infect Immun 1990: 58: 1986–1991. 117 Leung WK, Haapasalo M, Uitto VJ, Hannam PM, McBride BC. The surface proteinase of Treponema denticola may mediate attachment of the bacteria to epithelial cells. Anaerobe 1996: 2: 39–46. 118 Li L, Matevski D, Aspiras M, Ellen RP, Lépine G. Two epithelial cell invasion-related loci of the oral pathogen Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 2004: 19: 16–25. 119 Liu H, Redline RW, Han YW. Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J Immunol 2007: 179: 2501–2508. 120 Li T, Khah MK, Slavnic S, Johansson I, Strömberg N. Different type 1 fimbrial genes and tropisms of commensal and potentially pathogenic Actinomyces spp. with different salivary acidic proline-rich protein and statherin ligand specificities. Infect Immun 2001: 69: 7224–7233. 121 London J, Hand AR, Weiss EI, Allen J. Bacteroides loeshei PK1295 cells express two distinct adhesins simultaneously. Infect Immun 1989: 57: 3940–3944. 122 Maeda K, Nagata H, Yamamoto Y, Tanaka M, Tanaka J, Minamino N, Shizukuishi S. Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus oralis functions as a coadhesin for Porphyromonas gingivalis major fimbriae. Infect Immun 2004: 72: 1341–1348. 123 Malek R, Fisher JG, Caleca A, Stinson M, Van Oss CJ, Lee JY, Cho MI, Genco RJ, Evans RT, Dyer DW. Inactivation of Porphyromonas gingivalis fimA gene blocks periodontal damage in gnotobiotic rats. J Bacteriol 1994: 176: 1052–1059. 124 Manch-Citron JN, Allen J, Moos M Jr, London J. The gene encoding a Prevotella loescheii lectin-like adhesin contains an interrupted sequence which causes a frameshift. J Bacteriol 1992: 174: 7328–7336. 125 Manch-Citron JN, London J. Expression of the Prevotella loescheii adhesin gene (plaA) is mediated by a programmed frameshifting hop. J Bacteriol 1994: 176: 1944–1948. 126 Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 2000: 19: 2803–2812. 127 Mathers DA, Leung WK, Fenno JC, Hong Y, McBride BC. The major surface protein complex of Treponema denticola depolarizes and induces ion channels in HeLa cell membranes. Infect Immun 1996: 64: 2904–2910. 128 Matsushita K, Nagaoka S, Arakaki R, Kawabata Y, Iki K, Kawagoe M, Takada H. Immunobiological activities of a 55-kilodalton cell surface protein of Prevotella intermedia ATCC 25611. Infect Immun 1994: 62: 2459–2469. 129 McKee AS, McDermid AS, Baskerville A, Dowsett AB, Ellwood DC, Marsh PD. Effect of hemin on the physiology and virulence of Bacteroides gingivalis W50. Infect Immun 1986: 52: 349–355. 130 Metzger Z, Blasbalg J, Dotan M, Weiss EI. Enhanced attachment of Porphyromonas gingivalis to human fibroblasts mediated by Fusobacterium nucleatum. J Endod 2009: 35: 82–85. 131 Mintz KP. Identification of an extracellular matrix protein adhesin, EmaA, which mediates the adhesion of Actinobacillus actinomycetemcomitans to collagen. Microbiology 2004: 150: 2677–2688. 132 Missailidis CG, Umeda JE, Ota-Tsuzuki C, Anzai D, Mayer MP. Distribution of fimA genotypes of Porphyromonas gingivalis in subjects with various periodontal conditions. Oral Microbiol Immunol 2004: 19: 224–229.