Chapter 9 : the Role of Surface Structures in Virulence and Biofilm Development

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Studies have shown that surface structures play an important role in the life cycle of the oral anaerobe. In particular, cysteine proteases, fimbriae, membrane vesicles (MVs), and surface polysaccharides have been of primary interest. is a gram-negative obligate anaerobe that persists in the subgingival crevice of the oral cavity. The chapter provides a review of molecular genetic studies on cysteine proteases, fimbriae, MVs, and surface polysaccharides. It discusses the use of genome sequence information in deciphering the role of surface structures in biofilm development and pathogenicity. The high proteolytic activity of and its role in nutrient acquisition and virulence are discussed. Surface polysaccharides are key virulence factors of , as well as of many other gram-negative pathogens. The switch from being a benign member of the oral biofilm to being a proliferating virulent pathogen is central to the pathogenicity of this anaerobe, and changes in expression of surface structures play an important role in this switch. Expression of these surface structures modulates cell-cell and cell-host interactions and thus biofilm development; hence, MVs, gingipains, fimbriae, and surface polysaccharides play a central role in both virulence and biofilm growth.

Citation: Davey M, Boisvert H, Arndt A. 2011. the Role of Surface Structures in Virulence and Biofilm Development, p 119-134. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch9

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Outer Membrane Proteins
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Electron micrograph of strain 381, showing MV formation. Magnification, ×180,000.

Citation: Davey M, Boisvert H, Arndt A. 2011. the Role of Surface Structures in Virulence and Biofilm Development, p 119-134. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch9
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Image of FIGURE 2

Electron micrograph of strain 381, showing numerous fimbriae on the surface of the cell. Magnification, ×100,000.

Citation: Davey M, Boisvert H, Arndt A. 2011. the Role of Surface Structures in Virulence and Biofilm Development, p 119-134. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch9
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1. Abaibou, H.,, Z. Chen,, G. J. Olango,, Y. Liu,, J. Edwards, and, H. M. Fletcher. 2001. vimA gene downstream of recA is involved in virulence modulation in Porphyromonas gingivalis W83. Infect. Immun. 69:325335.
2. Abaibou, H.,, Q. Ma,, G. J. Olango,, J. Potempa,, J. Travis, and, H. M. Fletcher. 2000. Unaltered expression of the major protease genes in a non-virulent recA-defective mutant of Porphyromonas gingivalis W83. Oral Microbiol. Immunol. 15:4047.
3. Abe, N.,, A. Baba,, R. Takii,, K. Nakayama,, A. Kamaguchi,, Y. Shibata,, Y. Abiko,, K. Okamoto,, T. Kadowaki, and, K. Yamamoto. 2004. 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. 385:10411047.
4. Abe, N.,, T. Kadowaki,, K. Okamoto,, K. Nakayama,, M. Ohishi, and, K. Yamamoto. 1998. Biochemical and functional properties of lysine-specific cysteine proteinase (Lys-gingipain) as a virulence factor of Porphyromonas gingivalis in periodontal disease. J. Biochem. 123:305312.
5. Aduse-Opoku, J.,, J. M. Slaney,, A. Hashim,, A. Gallagher,, R. P. Gallagher,, M. Rangarajan,, K. Boutaga,, M. L. Laine,, A. J. Van Winkelhoff, and, M. A. Curtis. 2006. Identification and characterization of the capsular polysaccharide (K-antigen) locus of Porphyromonas gingivalis. Infect. Immun. 74:449460.
6. Alberti-Segui, C.,, A. Arndt,, C. Cugini,, R. Priyadarshini, and, M. E. Davey. 2010. HU protein affects transcription of surface polysaccha-ride synthesis genes in Porphyromonas gingivalis. J. Bacteriol. 192:62176229.
7. Amano, A.,, A. Sharma,, H. T. Sojar,, H. K. Kuramitsu, and, R. J. Genco. 1994. Effects of temperature stress on expression of fimbriae and superoxide dismutase by Porphyromonas gingivalis. Infect. Immun. 62:46824685.
8. Barua, P. K.,, D. W. Dyer, and, M. E. Neiders. 1990. Effect of iron limitation on Bacteroides gingivalis. Oral Microbiol. Immunol. 5:263268.
9. Beveridge, T. J. 1999. Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181:47254733.
10. Bhogal, P. S.,, N. Slakeski, and, E. C. Reynolds. 1997. A cell-associated protein complex of Porphyromonas gingivalis W50 composed of Argand Lys-specific cysteine proteinases and adhesins. Microbiology 143:24852495.
11. Boisvert, H.,, and M. J. Duncan. 2008. Clathrin-dependent entry of a gingipain adhesin peptide and Porphyromonas gingivalis into host cells. Cell. Microbiol. 10:25382552.
12. Chen, T.,, K. Abbey,, W. J. Deng, and, M. C. Cheng. 2005. The bioinformatics resource for oral pathogens. Nucleic Acids Res. 33(Web Server issue):W734W740.
13. Chen, T.,, and M. J. Duncan. 2004. Gingipain adhesin domains mediate Porphyromonas gingivalis adherence to epithelial cells. Microb. Pathog. 36:205209.
14. Chen, T.,, K. Nakayama,, L. Belliveau, and, M. J. Duncan. 2001. Porphyromonas gingivalis gingipains and adhesion to epithelial cells. Infect. Immun. 69:30483056.
15. Choi, J. I.,, T. Nakagawa,, S. Yamada,, I. Takazoe, and, K. Okuda. 1990. Clinical, microbiological and immunological studies on recurrent periodontal disease. J. Clin. Periodontol. 17:426434.
16. Chun, Y. H.,, K. R. Chun,, D. Olguin, and, H. L. Wang. 2005. Biological foundation for periodontitis as a potential risk factor for atherosclerosis. J. Periodontal Res. 40:8795.
17. Comstock, L. E.,, and D. L. Kasper. 2006. Bacterial glycans: key mediators of diverse host immune responses. Cell 126:847850.
18. Curtis, M. A.,, J. Aduse-Opoku, and, M. Rangarajan. 2001. Cysteine proteases of Porphyromonas gingivalis. Crit. Rev. Oral Biol. Med. 12:192216.
19. Curtis, M. A.,, J. Aduse-Opoku,, J. M. Slaney,, M. Rangarajan,, V. Booth,, J. Cridland, and, P. Shepherd. 1996. Characterization of an adherence and antigenic determinant of the ArgI protease of Porphyromonas gingivalis which is present on multiple gene products. Infect. Immun. 64:25322539.
20. Curtis, M. A.,, H. K. Kuramitsu,, M. Lantz,, F. L. Macrina,, K. Nakayama,, J. Potempa,, E. C. Reynolds, and, J. Aduse-Opoku. 1999. Molecular genetics and nomenclature of proteases of Porphyromonas gingivalis. J. Periodontal Res. 34:464472.
21. Curtis, M. A.,, A. Thickett,, J. M. Slaney,, M. Rangarajan,, J. Aduse-Opoku,, P. Shepherd,, N. Paramonov, and, E. F. Hounsell. 1999. Variable carbohydrate modifications to the catalytic chains of the RgpA and RgpB proteases of Porphyromonas gingivalis W50. Infect. Immun. 67:38163823.
22. Davey, M. E.,, and M. J. Duncan. 2006. Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis. J. Bacteriol. 188:55105523.
23. Demuth, D. R.,, D. C. Irvine,, J. W. Costerton,, G. S. Cook, and, R. J. Lamont. 2001. Discrete protein determinant directs the species-specific adherence of Porphyromonas gingivalis to oral streptococci. Infect. Immun. 69:57365741.
24. Dickinson, D. P.,, M. A. Kubiniec,, F. Yoshimura, and, R. J. Genco. 1988. Molecular cloning and sequencing of the gene encoding the fimbrial subunit protein of Bacteroides gingivalis. J. Bacteriol. 170:16581665.
25. Dierickx, K.,, M. Pauwels,, M. L. Laine,, J. Van Eldere,, J. J. Cassiman,, A. J. van Winkelhoff,, D. van Steenberghe, and, M. Quirynen. 2003. Adhesion of Porphyromonas gingivalis serotypes to pocket epithelium. J. Periodontol. 74:844848.
26. Dorn, B. R.,, J. N. Burks,, K. N. Seifert, and, A. Progulske-Fox. 2000. Invasion of endothelial and epithelial cells by strains of Porphyromonas gingivalis. FEMS Microbiol. Lett. 187:139144.
27. Dorn, B. R.,, L. J. Harris,, C. T. Wujick,, F. J. Vertucci, and, A. Progulske-Fox. 2002. Invasion of vascular cells in vitro by Porphyromonas endodontalis. Int. Endod. J. 35:366371.
28. Dzink, J. L.,, S. S. Socransky, and, A. D. Haffajee. 1988. The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J. Clin. Periodontol. 15:316323.
29. Ellen, R. P.,, and D. A. Grove. 1989. Bacteroides gingivalis vesicles bind to and aggregate Actinomyces viscosus. Infect. Immun. 57:16181620.
30. Falkow, S. 2006. Is persistent bacterial infection good for your health? Cell 124:699702.
31. Farquharson, S. I.,, G. R. Germaine, and, G. R. Gray. 2000. Isolation and characterization of the cell-surface polysaccharides of Porphyromonas gingivalis ATCC 53978. Oral Microbiol. Immunol. 15:151157.
32. Fiocca, R.,, V. Necchi,, P. Sommi,, V. Ricci,, J. Telford,, T. L. Cover, and, E. Solcia. 1999. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J. Pathol. 188:220226.
33. Fujiwara, T.,, S. Morishima,, I. Takahashi, and, S. Hamada. 1993. Molecular cloning and sequencing of the fimbrilin gene of Porphyromonas gingivalis strains and characterization of recombinant proteins. Biochem. Biophys. Res. Commun. 197:241247.
34. Genco, C. A.,, and D. W. Dixon. 2001. Emerging strategies in microbial haem capture. Mol. Microbiol. 39:111.
35. Gorby, Y.,, J. McLean,, A. Korenevsky,, K. Rosso,, M. Y. El-Naggar, and, T. J. Beveridge. 2008. Redox-reactive membrane vesicles produced by Shewanella. Geobiology 6:232241.
36. Goulbourne, P. A.,, and R. P. Ellen. 1991. Evidence that Porphyromonas (Bacteroides) gingivalis fimbriae function in adhesion to Actinomyces viscosus. J. Bacteriol. 173:52665274.
37. Grenier, D. 1992. Demonstration of a bimodal coaggregation reaction between Porphyromonas gingivalis and Treponema denticola. Oral Microbiol. Immunol. 7:280284.
38. Grenier, D. 1992. Further evidence for a possible role of trypsin-like activity in the adherence of Porphyromonas gingivalis. Can. J. Microbiol. 38:11891192.
39. Grenier, D.,, J. Bertrand, and, D. Mayrand. 1995. Porphyromonas gingivalis outer membrane vesicles promote bacterial resistance to chlorhexidine. Oral Microbiol. Immunol. 10:319320.
40. Grossi, S. G.,, J. J. Zambon,, A. W. Ho,, G. Koch,, R. G. Dunford,, E. E. Machtei,, O. M. Norderyd, and, R. J. Genco. 1994. Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J. Periodontol. 65:260267.
41. Hamada, N.,, K. Watanabe,, C. Sasakawa,, M. Yoshikawa,, F. Yoshimura, and, T. Umemoto. 1994. Construction and characterization of a fimA mutant of Porphyromonas gingivalis. Infect. Immun. 62:16961704.
42. Hasegawa, Y.,, S. Nishiyama,, K. Nishikawa,, T. Kadowaki,, K. Yamamoto,, T. Noguchi, and, F. Yoshimura. 2003. A novel type of two-component regulatory system affecting gingipains in Porphyromonas gingivalis. Microbiol. Immunol. 47:849858.
43. Horstman, A. L.,, and M. J. Kuehn. 2002. Bacterial surface association of heat-labile enterotoxin through lipopolysaccharide after secretion via the general secretory pathway. J. Biol. Chem. 277:3253832545.
44. Horstman, A. L.,, and M. J. Kuehn. 2000. Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J. Biol. Chem. 275:1248912496.
45. Jandik, K. A.,, M. Belanger,, S. L. Low,, B. R. Dorn,, M. C. Yang, and, A. Progulske-Fox. 2008. Invasive differences among Porphyromonas gingivalis strains from healthy and diseased periodontal sites. J. Periodontal Res. 43:524530.
46. Kadowaki, T.,, K. Nakayama,, F. Yoshimura,, K. Okamoto,, N. Abe, and, K. Yamamoto. 1998. Arg-gingipain acts as a major processing enzyme for various cell surface proteins in Porphyromonas gingivalis. J. Biol. Chem. 273:2907229076.
47. Kadowaki, T.,, M. Yoneda,, K. Okamoto,, K. Maeda, and, K. Yamamoto. 1994. 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. 269:2137121378.
48. Kadurugamuwa, J. L.,, and T. J. Beveridge. 1996. Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J. Bacteriol. 178:27672774.
49. Kadurugamuwa, J. L.,, and T. J. Beveridge. 1995. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J. Bacteriol. 177:39984008.
50. Kamaguch, A.,, K. Nakayama,, T. Ohyama,, T. Watanabe,, M. Okamoto, and, H. Baba. 2001. Coaggregation of Porphyromonas gingivalis and Prevotella intermedia. Microbiol. Immunol. 45:649656.
51. Kamaguchi, A.,, K. Nakayama,, S. Ichiyama,, R. Nakamura,, T. Watanabe,, M. Ohta,, H. Baba, and, T. Ohyama. 2003. Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms. Curr. Microbiol. 47:485491.
52. Kamaguchi, A.,, T. Ohyama,, E. Sakai,, R. Nakamura,, T. Watanabe,, H. Baba, and, K. Nakayama. 2003. Adhesins encoded by the gingipain genes of Porphyromonas gingivalis are responsible for co-aggregation with Prevotella intermedia. Microbiology 149:12571264.
53. Kantarci, A.,, and T. E. Van Dyke. 2002. Neutrophil-mediated host response to Porphyromonas gingivalis. J. Int. Acad. Periodontol. 4:119125.
54. Kato, T.,, T. Tsuda,, H. Omori,, T. Kato,, T. Yoshimori, and, A. Amano. 2007. Maturation of fimbria precursor protein by exogenous gingipains in Porphyromonas gingivalis gingipain-null mutant. FEMS Microbiol. Lett. 273:96102.
55. Kesty, N. C.,, K. M. Mason,, M. Reedy,, S. E. Miller, and, M. J. Kuehn. 2004. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23:45384549.
56. Kinder, S. A.,, and S. C. Holt. 1989. Characterization of coaggregation between Bacteroides gingivalis T22 and Fusobacterium nucleatum T18. Infect. Immun. 57:34253433.
57. Kolenbrander, P. E.,, and R. A. Anderson. 1989. Inhibition of coaggregation between Fusobacterium nucleatum and Porphyromonas (Bacteroides) gingivalis by lactose and related sugars. Infect. Immun. 57:32043209.
58. Kozarov, E. V.,, B. R. Dorn,, C. E. Shelburne,, W. A. Dunn, Jr., and, A. Progulske-Fox. 2005. Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler. Thromb. Vasc. Biol. 25:e17e18.
59. Kuehn, M. J.,, and N. C. Kesty. 2005. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 19:26452655.
60. Kuramitsu, H.,, M. Tokuda,, M. Yoneda,, M. Duncan, and, M. I. Cho. 1997. Multiple colonization defects in a cysteine protease mutant of Porphyromonas gingivalis. J. Periodontal Res. 32:140142.
61. Kuramitsu, H. K. 2003. Molecular genetic analysis of the virulence of oral bacterial pathogens: an historical perspective. Crit. Rev. Oral Biol. Med. 14:331344.
62. Laine, M. L.,, B. J. Appelmelk, and, A. J. van Winkelhoff. 1997. Prevalence and distribution of six capsular serotypes of Porphyromonas gingivalis in periodontitis patients. J. Dent. Res. 76:18401844.
63. Laine, M. L.,, and A. J. van Winkelhoff. 1998. Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model. Oral Microbiol. Immunol. 13:322325.
64. Lamont, R. J.,, A. El-Sabaeny,, Y. Park,, G. S. Cook,, J. W. Costerton, and, D. R. Demuth. 2002. Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology 148:16271636.
65. Lamont, R. J.,, and H. F. Jenkinson. 2000. Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol. Immunol. 15:341349.
66. Leduc, A.,, D. Grenier, and, D. Mayrand. 1995. Outer membrane-associated deoxyribonuclease activity of Porphyromonas gingivalis. Anaerobe 1:129134.
67. Lee, J. Y.,, H. T. Sojar,, G. S. Bedi, and, R. J. Genco. 1991. Porphyromonas (Bacteroides) gingivalis fimbrillin: size, amino-terminal sequence, and antigenic heterogeneity. Infect. Immun. 59:383389.
68. Lepine, G.,, R. P. Ellen, and, A. Progulske-Fox. 1996. Construction and preliminary characterization of three hemagglutinin mutants of Porphyromonas gingivalis. Infect. Immun. 64:14671472.
69. Lin, X.,, J. Wu, and, H. Xie. 2006. Porphyromonas gingivalis minor fimbriae are required for cell-cell interactions. Infect. Immun. 74:60116015.
70. Liu, X.,, A. Sroka,, J. Potempa, and, C. A. Genco. 2004. Coordinate expression of the Porphyromonas gingivalis lysine-specific gingipain proteinase, Kgp, arginine-specific gingipain proteinase, RgpA, and the heme/hemoglobin receptor, HmuR. Biol. Chem. 385:10491057.
71. Maeda, K.,, G. D. Tribble,, C. M. Tucker,, C. Anaya,, S. Shizukuishi,, J. P. Lewis,, D. R. Demuth, and, R. J. Lamont. 2008. A Porphyromonas gingivalis tyrosine phosphatase is a multifunctional regulator of virulence attributes. Mol. Microbiol. 69:11531164.
72. Marsh, P. D.,, A. S. McDermid,, A. S. McKee, and, A. Baskerville. 1994. The effect of growth rate and haemin on the virulence and proteolytic activity of Porphyromonas gingivalis W50. Microbiology 140:861865.
73. Mashburn, L. M.,, and M. Whiteley. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422425.
74. Mashburn-Warren, L. M.,, and M. Whiteley. 2006. Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 61:839846.
75. McBroom, A. J.,, and M. J. Kuehn. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 63:545558.
76. McKee, A. S.,, A. S. McDermid,, A. Baskerville,, A. B. Dowsett,, D. C. Ellwood, and, P. D. Marsh. 1986. Effect of hemin on the physiology and virulence of Bacteroides gingivalis W50. Infect. Immun. 52:349355.
77. Minhas, T.,, and J. Greenman. 1989. Production of cell-bound and vesicle-associated trypsin-like protease, alkaline phosphatase and N-acetyl-beta-glucosaminidase by Bacteroides gingivalis strain W50. J. Gen. Microbiol. 135:557564.
78. Moore, W. E.,, L. H. Moore,, R. R. Ranney,, R. M. Smibert,, J. A. Burmeister, and, H. A. Schenkein. 1991. The microflora of periodontal sites showing active destructive progression. J. Clin. Periodontol. 18:729739.
79. Nagata, H.,, A. Amano,, M. Ojima,, M. Tanaka,, K. Kataoka, and, S. Shizukuishi. 1994. Effect of binding of fibrinogen to each bacterium on coaggregation between Porphyromonas gingivalis and Streptococcus oralis. Oral Microbiol. Immunol. 9:359363.
80. Nagata, H.,, Y. Murakami,, E. Inoshita,, S. Shizukuishi, and, A. Tsunemitsu. 1990. Inhibitory effect of human plasma and saliva on co-aggregation between Bacteroides gingivalis and Streptococcus mitis. J. Dent. Res. 69:14761479.
81. Naito, M.,, H. Hirakawa,, A. Yamashita,, N. Ohara,, M. Shoji,, H. Yukitake,, K. Nakayama,, H. Toh,, F. Yoshimura,, S. Kuhara,, M. Hattori,, T. Hayashi, and, K. Nakayama. 2008. Determination of the genome sequence of Porphyromonas gingivalis strain ATCC 33277 and genomic comparison with strain W83 revealed extensive genome rearrangements in P. gingivalis. DNA Res. 15:215225.
82. Nakagawa, I.,, A. Amano,, R. K. Kimura,, T. Nakamura,, S. Kawabata, and, S. Hamada. 2000. Distribution and molecular characterization of Porphyromonas gingivalis carrying a new type of fimA gene. J. Clin. Microbiol. 38:19091914.
83. Nakayama, K.,, T. Kadowaki,, K. Okamoto, and, K. Yamamoto. 1995. Construction and characterization of arginine-specific cysteine proteinase (Arg-gingipain)-deficient mutants of Porphyromonas gingivalis. J. Biol. Chem. 270:2361923626.
84. Nakayama, K.,, D. B. Ratnayake,, T. Tsukuba,, T. Kadowaki,, K. Yamamoto, and, S. Fujimura. 1998. Haemoglobin receptor protein is intragenically encoded by the cysteine proteinase-encoding genes and the haemagglutinin-encoding gene of Porphyromonas gingivalis. Mol. Microbiol. 27:5161.
85. Nakayama, K.,, F. Yoshimura,, T. Kadowaki, and, K. Yamamoto. 1996. Involvement of arginine-specific cysteine proteinase (Arggingipain) in fimbriation of Porphyromonas gingivalis. J. Bacteriol. 178:28182824.
86. Nelson, K. E.,, R. D. Fleischmann,, R. T. DeBoy,, I. T. Paulsen,, D. E. Fouts,, J. A. Eisen,, S. C. Daugherty,, R. J. Dodson,, A. S. Durkin,, M. Gwinn,, D. H. Haft,, J. F. Kolonay,, W. C. Nelson,, T. Mason,, L. Tallon,, J. Gray,, D. Granger,, H. Tettelin,, H. Dong,, J. L. Galvin,, M. J. Duncan,, F. E. Dewhirst, and, C. M. Fraser. 2003. Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J. Bacteriol. 185:55915601.
87. Nguyen, K. A.,, J. Zylicz,, P. Szczesny,, A. Sroka,, N. Hunter, and, J. Potempa. 2009. Verification of a topology model of PorT as an integral outer-membrane protein in Porphyromonas gingivalis. Microbiology 155:328337.
88. Nishikawa, K.,, F. Yoshimura, and, M. J. Duncan. 2004. A regulation cascade controls expression of Porphyromonas gingivalis fimbriae via the FimR response regulator. Mol. Microbiol. 54:546560.
89. Ogawa, T.,, Y. Asai,, Y. Makimura, and, R. Tamai. 2007. Chemical structure and immunobiological activity of Porphyromonas gingivalis lipid A. Front. Biosci. 12:37953812.
90. Okamoto, K.,, T. Kadowaki,, K. Nakayama, and, K. Yamamoto. 1996. Cloning and sequencing of the gene encoding a novel lysinespecific cysteine proteinase (Lys-gingipain) in Porphyromonas gingivalis: structural relationship with the arginine-specific cysteine proteinase (Arg-gingipain). J. Biochem. 120:398406.
91. Okamoto, K.,, K. Nakayama,, T. Kadowaki,, N. Abe,, D. B. Ratnayake, and, K. Yamamoto. 1998. Involvement of a lysine-specific cysteine proteinase in hemoglobin adsorption and heme accumulation by Porphyromonas gingivalis. J. Biol. Chem. 273:2122521231.
92. Olczak, T.,, W. Simpson,, X. Liu, and, C. A. Genco. 2005. Iron and heme utilization in Porphyromonas gingivalis. FEMS Microbiol. Rev. 29:119144.
93. Paramonov, N.,, M. Rangarajan,, A. Hashim,, A. Gallagher,, J. Aduse-Opoku,, J. M. Slaney,, E. Hounsell, and, M. A. Curtis. 2005. Structural analysis of a novel anionic polysaccharide from Porphyromonas gingivalis strain W50 related to Arg-gingipain glycans. Mol. Microbiol. 58:847863.
94. Pathirana, R. D.,, N. M. O’Brien-Simpson,, K. Visvanathan,, J. A. Hamilton, and, E. C. Reynolds. 2007. Flow cytometric analysis of adherence of Porphyromonas gingivalis to oral epithelial cells. Infect. Immun. 75:24842492.
95. Pham, K.,, D. Feik,, B. F. Hammond,, T. E. Rams, and, E. J. Whitaker. 2002. Aggregation of human platelets by gingipain-R from Porphyromonas gingivalis cells and membrane vesicles. Platelets 13:2130.
96. 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. 63:11761182.
97. Qi, M.,, H. Miyakawa, and, H. K. Kuramitsu. 2003. Porphyromonas gingivalis induces murine macrophage foam cell formation. Microb. Pathog. 35:259267.
98. Rangarajan, M.,, J. Aduse-Opoku,, N. Paramonov,, A. Hashim,, N. Bostanci,, O. P. Fraser,, E. Tarelli, and, M. A. Curtis. 2008. Identification of a second lipopolysaccharide in Porphyromonas gingivalis W50. J. Bacteriol. 190:29202932.
99. Rangarajan, M.,, J. Aduse-Opoku,, J. M. Slaney,, K. A. Young, and, M. A. Curtis. 1997. The prpR1 and prR2 arginine-specific protease genes of Porphyromonas gingivalis W50 produce five biochemically distinct enzymes. Mol. Microbiol. 23:955965.
100. Roberts, I. S. 1996. The biochemistry and genetics of capsular polysaccharide production in bacteria. Annu. Rev. Microbiol. 50:285315.
101. Rosen, G.,, and M. N. Sela. 2006. Coaggregation of Porphyromonas gingivalis and Fusobacterium nucleatum PK 1594 is mediated by capsular polysaccharide and lipopolysaccharide. FEMS Microbiol. Lett. 256:304310.
102. Schifferle, R. E.,, S. A. Shostad,, M. T. Bayers-Thering,, D. W. Dyer, and, M. E. Neiders. 1996. Effect of protoporphyrin IX limitation on Porphyromonas gingivalis. J. Endod. 22:352355.
103. Schooling, S. R.,, and T. J. Beveridge. 2006. Membrane vesicles: an overlooked component of the matrices of biofilms. J. Bacteriol. 188:59455957.
104. Shi, Y.,, D. B. Ratnayake,, K. Okamoto,, N. Abe,, K. Yamamoto, and, K. Nakayama. 1999. 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. 274:1795517960.
105. Shoji, M.,, D. B. Ratnayake,, Y. Shi,, T. Kadowaki,, K. Yamamoto,, F. Yoshimura,, A. Akamine,, M. A. Curtis, and, K. Nakayama. 2002. Construction and characterization of a nonpigmented mutant of Porphyromonas gingivalis: cell surface polysaccharide as an anchorage for gingipains. Microbiology 148:11831191.
106. Simionato, M. R.,, C. M. Tucker,, M. Kuboniwa,, G. Lamont,, D. R. Demuth,, G. D. Tribble, and, R. J. Lamont. 2006. Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect. Immun. 74:64196428.
107. Sims, T. J.,, R. E. Schifferle,, R. W. Ali,, N. Skaug, and, R. C. Page. 2001. Immunoglobulin G response of periodontitis patients to Porphyromonas gingivalis capsular carbohydrate and lipopolysaccharide antigens. Oral Microbiol. Immunol. 16:193201.
108. Singh, U.,, D. Grenier, and, B. C. McBride. 1989. Bacteroides gingivalis vesicles mediate attachment of streptococci to serum-coated hydroxyapatite. Oral Microbiol. Immunol. 4:199203.
109. Slaney, J. M.,, and M. A. Curtis. 2008. Mechanisms of evasion of complement by Porphyromonas gingivalis. Front. Biosci. 13:188196.
110. Slaney, J. M.,, A. Gallagher,, J. Aduse-Opoku,, K. Pell, and, M. A. Curtis. 2006. Mechanisms of resistance of Porphyromonas gingivalis to killing by serum complement. Infect. Immun. 74:53525361.
111. Sojar, H. T.,, Y. Han,, N. Hamada,, A. Sharma, and, R. J. Genco. 1999. Role of the amino-terminal region of Porphyromonas gingivalis fimbriae in adherence to epithelial cells. Infect. Immun. 67:61736176.
112. Takii, R.,, T. Kadowaki,, A. Baba,, T. Tsukuba, and, K. Yamamoto. 2005. A functional virulence complex composed of gingipains, adhesins, and lipopolysaccharide shows high affinity to host cells and matrix proteins and escapes recognition by host immune systems. Infect. Immun. 73:883893.
113. Tokuda, M.,, M. Duncan,, M. I. Cho, and, H. K. Kuramitsu. 1996. Role of Porphyromonas gingivalis protease activity in colonization of oral surfaces. Infect. Immun. 64:40674073.
114. Troy, F. A.,, F. E. Frerman, and, E. C. Heath. 1971. The biosynthesis of capsular polysaccharide in Aerobacter aerogenes. J. Biol. Chem. 246:118133.
115. Umemoto, T.,, F. Yoshimura,, H. Kureshiro,, J. Hayashi,, T. Noguchi, and, T. Ogawa. 1999. Fimbria-mediated coaggregation between human oral anaerobes Treponema medium and Porphyromonas gingivalis. Microbiol. Immunol. 43:837845.
116. van Winkelhoff, A. J.,, B. J. Appelmelk,, N. Kippuw, and, J. de Graaff. 1993. K-antigens in Porphyromonas gingivalis are associated with virulence. Oral Microbiol. Immunol. 8:259265.
117. Veith, P. D.,, G. H. Talbo,, N. Slakeski,, S. G. Dashper,, C. Moore,, R. A. Paolini, and, E. C. Reynolds. 2002. Major outer membrane proteins and proteolytic processing of RgpA and Kgp of Porphyromonas gingivalis W50. Biochem. J. 363:105115.
118. Wai, S. N.,, B. Lindmark,, T. Soderblom,, A. Takade,, M. Westermark,, J. Oscarsson,, J. Jass,, A. Richter-Dahlfors,, Y. Mizunoe, and, B. E. Uhlin. 2003. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115:2535.
119. Whitchurch, C. B.,, T. Tolker-Nielsen,, P. C. Ragas, and, J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487.
120. Whitfield, C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75:3968.
121. Whitfield, C.,, and M. A. Valvano. 1993. Biosynthesis and expression of cell-surface polysaccharides in Gram-negative bacteria. Adv. Microb. Physiol. 35:135246.
122. Xie, H.,, S. Cai, and, R. J. Lamont. 1997. Environmental regulation of fimbrial gene expression in Porphyromonas gingivalis. Infect. Immun. 65:22652271.
123. Yamaguchi, T.,, K. Kasamo,, M. Chuman,, M. Machigashira,, M. Inoue, and, T. Sueda. 1998. Preparation and characterization of an Actinomyces naeslundii aggregation factor that mediates coaggregation with Porphyromonas gingivalis. J. Periodontal Res. 33:460468.
124. Yao, E. S.,, R. J. Lamont,, S. P. Leu, and, A. Weinberg. 1996. Interbacterial binding among strains of pathogenic and commensal oral bacterial species. Oral Microbiol. Immunol. 11:3541.
125. Yilmaz, O. 2008. The chronicles of Porphyromonas gingivalis: the microbium, the human oral epithelium and their interplay. Microbiology 154:28972903.
126. Zhou, L.,, R. Srisatjaluk,, D. E. Justus, and, R. J. Doyle. 1998. On the origin of membrane vesicles in Gram-negative bacteria. FEMS Microbiol. Lett. 163:223228.

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