Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the ‘red complex’, a prototype polybacterial pathogenic consortium in periodontitis

Periodontology 2000Volume 38, Issue 1 p. 72-122 Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the ‘red complex’, a prototype polybacterial pathogenic consortium in periodontitis Stanley C. Holt, Stanley C. HoltSearch for more papers by this authorJeffrey L. Ebersole, Jeffrey L. EbersoleSearch for more papers by this author Stanley C. Holt, Stanley C. HoltSearch for more papers by this authorJeffrey L. Ebersole, Jeffrey L. EbersoleSearch for more papers by this author First published: 21 April 2005 https://doi.org/10.1111/j.1600-0757.2005.00113.xCitations: 631Read 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 Aaron L, Saadoun D, Calatroni I, Launay O, Memain N, Vincent V, Marchal G, Dupont B, Bouchaud O, Valeyre D, Lortholary O. Tuberculosis in HIV-infected patients: a comprehensive review. Clin Microbiol Infect 2004: 10: 388–398. 2 Abbas AK. Die and let live: eliminating dangerous lymphocytes. Cell 1996: 84: 655–657. 3 Abdul-Tehrani H, Hudson AJ, Chang YS. Ferritin mutants of Escherichia coli are iron deficient and growth impaired, and fur mutants are iron deficient. J Bacteriol 1999: 181: 1415–1428. 4 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. 5 Abiko Y, Ogura N, Matsuda U, Yanagi K, Takiguchi H. A human monoclonal antibody which inhibits the coaggregation activity of Porphyromonas gingivalis. Infect Immun 1997: 65: 3966–3969. 6 Aduse-Opoku J, Slaney JM, Rangarajan M, Muir J, Young KA, Curtis MA. The Tla protein of Porphyromonas gingivalis W50: a homolog of the RI protease precursor (PrpRI) is an outer membrane receptor required for growth on low levels of hemin. J Bacteriol 1997: 179: 4778–4788. 7 Agnani G, Tricot-Doleux SL, Bonnaure-Mallet M. Adherence of Porphyromonas gingivalis to gingival epithelial cell: modulation of bacterial protein expression. Oral Microbiol Immunol 2000: 15: 48–52. 8 Albander 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. 9 Ali RW, Martin L, Haffajee AD, Socransky SS. Detection of identical ribotypes of Porphyromonas gingivalis in patients residing in the United States, Sudan, Romania, and Norway. Oral Microbiol Immunol 1997: 12: 106–111. 10 Ally N, Whisstock JC, Sieprawska Lupa M, Potempa J, Le Bonniec BF, Travis J, Pike RN. Characterization of the specificity of arginine-specific gingipains from Porphyromonas gingivalis reveals active site differences between different forms of the enzymes. Biochemistry 2003: 42: 11693–11700. 11 Amano A. Molecular interaction of Porphyromonas gingivalis with host cells: implication for the microbial pathogenesis of periodontal disease. J Periodontol 2003: 74: 90–96. 12 Amano A, Fujiwara T, Nagata H, Kuboniwa M, Sharma A, Sojar HT, Genco RJ, Hamada S, Shizukuishi S. Porphyromonas gingivalis fimbriae mediate coaggregation with Streptococcus oralis through specific domains. J Dent Res 1997: 76: 852–857. 13 Amano A, Kuboniwa M, Kataoka K. Binding of hemoglobin by Porphyromonas gingivalis. FEMS Microbiol Lett 1995: 134: 63–67. 14 Amano A, Sharma A, Lee J-Y, Sojar HT, Raj PA, Genco RJ. Structural domains of Porphyromonas gingivalis recombinant fimbrillin that mediates binding to salivary proline-rich protein and statherin. Infect Immun 1996: 64: 1631–1637. 15 Amano A, Sojar HT, Lee J-Y, Sharma A, Levine MJ, Genco RJ. Salivary receptors to recombinant fimbrillin of Porphyromonas gingivalis. Infect Immun 1994: 62: 3372–3380. 16 Amin M, Ho AC, Lin JY, Batista da Silva AP, Glogauer M, Ellen RP. Induction of de novo subcortical actin filament assembly by Treponema denticola major outer sheath protein. Infect Immun 2004: 72: 3650–3654. 17 Andreou, V, D'Addario, M, Zohar, R, Sukhu B, Casper RF, Ellen RP, Tenenbaum HC. Inhibition of osteogenesis in vitro by cigarette smoke-associated hydrocarbon combined with Porphyromonas gingivalis lipopolysaccharide: reversal by resvaratrol. J Periodontol 2004: 75: 939–948. 18 Andrews SC. Iron storage in bacteria. Adv Microb Physiol 1998: 40: 281–351. 19 Andrews SC, Grogan JM, Quail MA, Bishop R, Guest JR. Iron regulation and storage in Escherichia coli. Society of Experimental Medicine, Annual Meeting, April 1997: 7–11 (Abstr C2.23). 20 Andrian E, Grenier D, Rouabhia M. In vitro models of tissue penetration and destruction by Porphyromonas gingivalis. Infect Immun 2004: 72: 4689–4698. 21 Arakawa S, Nakajima T, Ishikura H, Ichinose S, Ishikawa I, Tsuchida N. Novel apoptosis-inducing activity in Bacteroides forsythus: a comparative study with three serotypes of Actinobacillus actinomycetemcomitans. Infect Immun 2000: 68: 4611–4615. 22 Armitage GC, Dickinson WR, Jenderseck RS, Levine SM, Chambers DW. Relationship between the percentage of subgingival spirochetes and the severity of periodontal disease. J Periodontol 1982: 53: 550–556. 23 Asai Y, Jinno T, Ogawa T. Oral treponemes and their outer membrane extracts activate human gingival epithelial cells through toll-like receptor 2. Infect Immun 2003: 71: 717–725. 24 Asai Y, Ohyama Y, General K, Ogawa T. Bacterial fimbriae and their peptides activate human gingival epithelial cells through Toll-like receptor 2. Infect Immun 2001: 69: 7387–7395. 25 Awano S, Ansai T, Mochizuki H, Yu W, Tanzawa K, Turner AJ. Sequencing, expression and biochemical characterization of the Porphyromonas gingivalis pepO gene encoding a protein homologous to human endothelin-converting enzyme. FEBS Lett 1999: 460: 139–144. 26 Baba A, Abe N, Kadowaki T, Nakanishi H, Ohishi M, Asao T, Yamamoto K. Arg-gingipain is responsible for the degradation of cell adhesion molecules of human gingival fibroblasts and their death induced by Porphyromonas gingivalis. Biol Chem 2001: 382: 817–824. 27 Baehni P, Song M, McCulloch CAG, Ellen RP. Treponema denticola induces actin rearrangement and detachment of human gingival fibroblasts. Infect Immun 1992: 60: 3360–3368. 28 Banbula A, Mak P, Bugno M, Silberring J, Dubin A, Nelson D, Travis J, Potempa J. Prolyl tripeptidyl peptidase from Porphyromonas gingivalis. A novel enzyme with possible pathological implications for the development of periodontitis. J Biol Chem 1999: 274: 9246–9252. 29 Banbula A, Yen J, Olesky A, Mak P, Bugno M, Travis J, Potempa J. Porphyromonas gingivalis DPP-7 represents a novel type of dipeptidylpeptidase. J Biol Chem 2001: 276: 6299–6305. 30 Barrow WW. Processing of mycobacterial lipids and effects on host responsiveness. Front Biosci 1997: 15: 387–400. 31 Bar-Shavit R, Kahn A, Fenton JW II, Wilner GD. Monocyte chemotaxis: stimulation by specific exosite region in thrombin. Science 1983: 220: 728–730. 32 Bartold PM. Proteoglycans of the periodontium: structure, role and function. J Periodontal Res 1987: 22: 431–444. 33 Bartold PM, Weibkin OW, Thohard JC. Proteoglycans in human gingival: molecular size distribution in epithelium and in connective tissue. Arch Oral Biol 1982: 27: 1–7. 34 Barua PK, Dyer DW, Meiders ME. Effect of iron limitation on Bacteroides gingivalis. Oral Microbiol Immunol 1990: 5: 263–268. 35 Batista da Silva AP, Lee W, Bajenova E, McCulloch CA, Ellen RP. The major outer sheath protein of Treponema denticola inhibits the binding step of collagen phagocytosis in fibroblasts. Cell Microbiol 2004: 6: 485–498. 36 Baumeister W, Engelhardt H. Three-dimensional structure of bacterial surface layers. In: JR Harris, RW Horne, editors. Electron Microscopy of Proteins: Membranous Structures. London: Academic Press, 1987: 121–126. 37 Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S. Periodontal disease and cardiovascular disease. J Periodontol 1996: 67: 1123–1137. 38 Beighton D, Radford JR, Naylor MN. Glycosidase activities in gingival crevicular fluid in subjects with adult periodontitis or gingivitis. Arch Oral Biol 1992: 37: 343–348. 39 Berry AM, Paton JC, Glare EM, Hansman D, Catcheside DEA. Cloning and expression of the pneumococcal neuraminidase gene in Escherichia coli. Gene 1988: 71: 299–305. 40 Beveridge TJ. Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 1999: 181: 4725–4733. 41 Beveridge TJ, Pouwels PH, Sara M, Kotiranta A, Lounatmaa K, Kari K, Kerosuo E, Haapasalo M, Egelseer EM, Schocher I, Sleytr UB, Morelli L, Callegari ML, Nomellini JF, Bingle WH, Smit J, Leibovitz E, Lemaire M, Miras I, Salamitou S, Beguin P, Ohayon H, Gounon P, Matuschek M, Koval SF. Function of S-Iayers. FEMS Microbiol Rev 1997: 20: 99–149. 42 Birkedal-Hansen H. Role of matrix metalloproteinases in human periodontal diseases. J Periodontol 1993: 64: 474–484. 43 Bizios R, Lai L, Fenton JW II, Malik AB. Thrombin-induced chemotaxis and aggregation of neutrophils. J Cell Physiol 1986: 128: 485–490. 44 Boehringer HE, Taichman NS, Shenker BJ. Suppression of fibroblast proliferation by oral spirochetes. Infect Immun 1984: 45: 155–159. 45 Boreal-Hansen H. Role of matrix metalloproteinases in human periodontal diseases. J Periodontol 1993: 64: 474–484. 46 Borinski R, Holt SC. Surface characteristics of Wolinella recta ATCC 3238 and human clinical isolates: correlation of structure with function. Infect Immun 1990: 58: 2770–2776. 47 Bourgeau G, Lapointe H, Peloquin P, Mayrand D. Cloning, expression and sequencing of a protease gene (tpr) from Porphyromonas gingivalis strain W83 in Escherichia coli. Infect Immun 1992: 60: 3186–3192. 48 Bradshaw DJ, Marsh PD, Watson GK, Allison C. Role of Fusobacterium nucleatum and coaggregation in anaerobe survival in planktonic and biofilm oral microbial communities during aeration. Infect Immun 1998: 66: 4729–4732. 49 Bramanti TE, Holt SC. Iron-regulated outer membrane proteins in the periodontopathic bacterium, Bacteroides gingivalis. J Biochem Biophys Res Commun 1990: 166: 1146–1154. 50 Bramanti TE, Holt SC. Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50. J Bacteriol 1991: 173: 7330–7339. 51 Bramanti TE, Holt SC. Localization of a 26 kilodalton heat-modifiable hemin-regulated outer membrane protein in Porphyromonas gingivalis. J Bacteriol 1992: 174: 5827–5839. 52 Brandtzaeg P. Local formation and transport of immunoglobulins related to the oral cavity. In: MacPhee Host resistant to commensal bacteria. London: Churchill Livingstone, 1972: 116–156. 53 Briselden AM, Moncla BJ, Stevens CE, Hillier SL. Sialidases (neuraminidases) in bacterial vaginosis and bacterial vaginosis-associated microflora. J Clin Microbiol 1992: 30: 663–666. 54 Brissette CA, Lukehart SA. Treponema denticola is resistant to human beta-defensins. Infect Immun 2002: 70: 3982–3984. 55 Brissette CA, Simonson LG, Lukehart SA. Resistance to human beta-defensins is common among oral treponemes. Oral Microbiol Immunol 2004: 19: 403–407. 56 Brochu V, Grenier D, Nakayama K, Mayrand D. Acquisition of iron from human transferrin by Porphyromonas gingivalis: a role for Arg- and Lys-gingipain activities. Oral Microbiol Immunol 2001: 16: 79–87. 57 Brook I. Aerobic and anaerobic microbiology of bacterial tracheitis in children. Pediatr Emerg Care 1997: 13: 16–18. 58 Brook I. Anaerobic bacteria in upper respiratory tract and other head and neck infections. Ann Otol Rhinol Laryngol 2002: 111: 430–440. 59 Brook I. Cutaneous and subcutaneous infections in newborns due to anaerobic bacteria. J Perinat Medical 2002: 30: 197–208. 60 Brook I. Microbiology of polymicrobial abscesses and implications for therapy. J Antimicrob Chemother 2002: 50: 805–810. 61 Brook I. Microbiology of infected hemangiomas in children. Ped Dermatol 2004: 21: 113–116. 62 Budu CE, Luengpailin J, Reyes G. Virulence factors of Porphyromonas gingivalis are modified by polyphenol oxidase and asparaginase. Oral Microbiol Immunol 2003: 18: 313–317. 63 Carlsson J, Höfling JF, Sundqvist GK, Degradation of albumin, haemopexin, haptoglobin and transferrin by black-pigmented Bacteroides species. J Med Microbiol 1984: 18: 39–46. 64 Carman R, Ramakrishnan MD, Harper FH, Haemin levels in culture medium of Porphyromonas (Bacteroides) gingivalis regulate both hemin binding and trypsin like protease production. Infect Immun 1990: 58: 4106–4109. 65 Casadevall A, Pirofski L. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun 1999: 67: 3703–3713. 66 Chen CC, Chang JF, Huang JS, Tsai CC. Correlation of interleukin-1 beta, interleukin-6, and periodontitis. Kaohsiung J Med Sci 1997: 13: 609–617. 67 Chen T, Duncan M. Gingipain adhesin domains mediate Porphyromonas gingivalis adherence to epithelial cells. Microb Pathog 2004: 36: 205–209. 68 Chi B, Qi M, Kuramitsu HK. Role of dentilisin in Treponema denticola epithelial cell layer penetration. Res Microbiol 2003: 154: 637–43. 69 Chiang CY, Fu E, Shen EC. The role of interleukin-1β in Porphyromonas gingivalis lipopolysaccharide-induced bone resorption. Zhonghua Yi Xue Za Zhi (Taipei) 2002: 65: 225–230. 70 Childers BJ, Potyondy LD, Nachreiner R, Rogers FR, Childers ER, Oberg KC, Hendricks DL, Hardesty RA. Necrotizing fasciitis: a fourteen-year retrospective study of 163 consecutive patients. Am Surg 2002: 68: 109–116. 71 Choi BK, Lee HJ, Kang JH, Jeong GJ, Min CK, Yoo YJ. Induction of osteoclastogenesis and matrix metalloproteinase expression by the lipooligosaccharide of Treponema denticola. Infect Immun 2003: 71: 226–233. 72 Choi SH, Lee SO, Kim TH, Chung JW, Choo EJ, Kwak YG, Kim MN, Kim YS, Woo JH, Ryu J, Kim NJ. Clinical features and outcomes of bacteremia caused by Enterococcus casseliflavus and Enterococcus gallinarum: analysis of 56 cases. Clin Infect Dis 2004: 38: 53–61. 73 Chu L, Bramanti TE, Ebersole JL, Holt SC. Hemolytic activity in the periodontopathogen Porphyromonas gingivalis: Kinetics of enzyme release and localization. Infect Immun 1991: 59: 1932–1940. 74 Chu L, Dong Z, Xu Z, Cochran DL, Ebersole JL. Role of glutathione metabolism of Treponema denticola in bacterial growth and virulence expression. Infect Immun 2002: 70: 1113–1120. 75 Chu L, Ebersole JL. Glutathione utilization and hydrogen sulfide production by Treponema denticola and other oral bacteria. J Dent Res 2003: 82: Abstr. 1741. 76 Chu L, Ebersole JL, Holt SC. Hemoxidation and binding of the 46 kDa cystalysin of Treponema denticola leads to a cysteine-dependent hemolysis of human erythrocytes. Oral Microbiol Immunol 1999: 14: 293–303. 77 Chu L, Ebersole JL, Kurzban GP, Holt SC. Cystalysin, a 46-kilodalton cysteine desulfhydrase from Treponema denticola, with hemolytic and hemoxidative activities. Infect Immun 1997: 65: 3232–3238. 78 Chu L, Ebersole JL, Kurzban GP, Holt SC. Cystalysin, a 46 kDa 1-cysteine desulfhydrase from Treponema denticola: biochemical and biophysical characterization. Clin Infect Dis 1999: 28: 442–450. 79 Chu L, Holt SC, Ebersole JL. H2S producing system of Treponema denticola. J Dent Res 2000: 79: 308: Abstr. 1316. 80 Chu L, Xu X, Dong Z, Cappelli D, Ebersole JL. Role for recombinant gamma-glutamyltransferase from Treponema denticola in glutathione metabolism. Infect Immun 2003: 71: 335–342. 81 Cimasoni G, McBride BC. Adherence of Treponema denticola to modified hydroxyapatite. J Dent Res 1987: 66: 1727–1729. 82 Cunha BA. Antibiotic selection for diabetic foot infections: a review. J Foot Ankle Surg 2000: 39: 253–257. 83 Cunningham CO, Selwyn PA. Mastitis due to Mycobacterium avium complex in an HIV-infected woman taking highly active antiretroviral therapy. AIDS Patient Care STDS 2003: 17: 547–550. 84 Curtis MA, Kuramitsu HK, Lantz M, Macrina FL, Nakayama K, Potempa J, Raynolds EC, Aduse-Opoku J. Molecular genetics and nomenclature of proteases of Porphyromonas gingivalis. J Periodontal Res 1999: 34: 464–472. 85 Curtis MA, Sterne JAC, Price SJ, Griffiths GS, Coulthurst SK, Wilton JM, Johnson NW. The protein composition of gingival crevicular fluid sampled from male adolescents with no destructive periodontitis: baseline data of a longitudinal study. J Periodontal Res 1990: 25: 6–16. 86 Curtis MA, Thickett A, Slaney JM, Rangarajan M, Aduse-Opoku J, Shepherd P, Paramonov N, Hounsell EF. Variable carbohydrate modifications to the catalytic chains of the rgpA and rgpB proteases of Porphyromonas gingivalis W50. Infect Immun 1999: 67: 3816–3823. 87 Cutler CW, Eke PI, Genco CA, Van Dyke TE, Arnold RR. Hemin-induced modifications of the antigenicity and hemin-binding capacity of Porphyromonas gingivalis lipopolysaccharide. Infect Immun 1996: 64: 2282–2287. 88 Cutler CW, Kalmar JR, Genco CA, Pathogenic strategies of the oral anaerobe, Porphyromonas gingivalis. Trends Microbiol 1995: 3: 45–50. 89 Darveau RP, Tanner A, Page RC. The microbial challenge in periodontitis. Periodontol 2000 1997: 14: 12–32. 90 Dashper SG, Cross KJ, Slakeski N, Lissel P, Aulakh P, Moore C, Reynolds EC. Hemoglobin hydrolysis and heme acquisition by Porphyromonas gingivalis. Oral Microbiol Immunol 2004: 19: 50–56. 91 DeCarlo AA, Paramaesvaran M, Yun PL, Collyer C, Hunter N. Porphyrin-mediated binding to hemoglobin by the HA2 domain of cysteine proteinases (gingipains) and hemagglutinins from the periodontal pathogen Porphyromonas gingivalis. J Bacteriol 1999: 181: 3784–3791. 92 DeFillipo AB, Ellen RP, McCulloch CAG. Induction of cytoskeletal rearrangements and loss of volume regulation in epithelial cells by Treponema denticola. Arch Oral Biol 1995: 40: 199–207. 93 De Jong BC, Israelski DM, Corbett EL, Small PM. Clinical management of tuberculosis in the context of HIV infection. Ann Rev Med 2004: 55: 283–301. 94 Del Portillo HA, Fernandez-Becerra C, Bowman S, Oliver K, Preuss M, Sanchez CP, Schneider NK, Villalobos JM, Rajandream MA, Harris D, Pereira da Silva LH, Barrell B, Lanzer M. A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature 2001: 410: 839–842. 95 Deng QD, Han Y, Xia X, Kuramitsu HK. Effects of the oral spirochete Treponema denticola on interleukin-8 expression from epithelial cells. Oral Microbiol Immunol 2001: 16: 185–187. 96 Deslauriers M, Eidhin D, Lamonde L, Moutin C. SDS-PAGE analysis of protein and LPS of extracellular vesicles and sarcosyl-insoluble membranes from Bacteroides gingivalis. Oral Microbiol Immunol 1990: 5: 1–7. 97 DiRita VJ, Mekalanos J. Genetic regulation of bacterial virulence. Ann Rev Genet 1989: 23: 455–482. 98 Doring G. Cystic fibrosis respiratory infections: interactions between bacteria and host defense. Monaldi Arch Chest Dis 1997: 52: 363–6. 99 Dorn BR, Burks JN, Seifert KN, Progulske-Fox A. Invasion of endothelial and epithelial cells by strains of Porphyromonas gingivalis. FEMS Microbiol Lett 2000: 187: 139–144. 100 Duncan M. Oral microbiology and genomics. Periodontol 2000 2005: 38: 63–71. 101 Dyer D, West EP, Sparkling PF. Effects of serum carrier proteins on the growth of pathogenic neisseriae with heme-bound iron. Infect Immun 1987: 55: 2171–2175. 102 Dzink JL, Socransky SS, Haffajee AD. The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol 1988: 15: 316–323. 103 Dzink JL, Tanner ACR, Haffajee AD, Socransky SS. Gram negative species associated with active destructive periodontal lesions. J Clin Periodontol 1985: 12: 648–659. 104 Ebersole JL, Kesavalu L, Schneider SL, Machen RL, Holt SC. Comparative virulence of periodontopathogens in a mouse abscess model. Oral Dis 1995: 1: 115–128. 105 Edwards AM, Dymock D, Jenkinson HF. From tooth to hoof: treponemes in tissue-destructive diseases. J Appl Microbiol 2003: 94: 767–780. 106 Egli C, Leung WK, Muller KH, Hancock RE, McBride BC. Pore-forming properties of the major 53 kDa surface antigen from the outer sheath of Treponema denticola. Infect Immun 1993: 61: 1694–1699. 107 Ellen RP, Ko KS, Lo CM, Grove DA, 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. 108 Evans RT, Klausan B, Sojar HT, Bedi GS, Sfintescu C, Ramamurthy NS, Golub LM, Genco RJ. Immunization with Porphyromonas (Bacteroides) gingivalis fimbriae protects against periodontal destruction. Infect Immun 1992: 60: 2926–2935. 109 Falkow S. Bacterial entry into eukaryotic cells. Cell 1991: 65: 1099–1102. 110 Fenno JC, Hannam PM, Leung WK, Tamura M, Uitto VJ, McBride BC. Cytopathic effect of the major surface protein and the chymotrypsinlike protease of Treponema denticola. Infect Immun 1998: 66: 1869–1877. 111 Fenno JC, McBride BC. Virulence factors of oral treponemes. Anaerobe 1998: 4: 1–17. 112 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. 113 Fenno JC, Wong GW, Hannam PM, McBride BC. Mutagenesis of outer membrane virulence determinants of the oral spirochete Treponema denticola. FEMS Microbiol Lett 1998: 163: 209–215. 114 Fenno JC, Tamura M, Hannam PM, Wong GW, Chan 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. 115 Fries BC, Goldman DL, Casadevall A. Phenotypic switching in Cryptococcus neoformans. Microbes Infect 2002: 4: 1345–1352. 116 Froberg MK. Review: CMV escapes!. Ann Clin Lab Sci 2004: 34: 123–130. 117 Fujimura S, Shibata Y, Hirai K, Nakayama T, Binding of hemoglobin to the envelope of P. gingivalis and isolation of the hemoglobin-binding protein. Infect Immun 1996: 64: 2339–2342. 118 Garcia RI, Henshaw MM, Krall EA. Relationship between periodontal disease and systemic health. Periodontol 2000 2001: 254: 21–36. 119 Garduno RA, Moore AR, Olivier G, Lazama AL, Garduno E, Kay WW. Host cell invasion and intracellular residence by Aeromonas salmonicida: role of the S-layer. Can J Microbiol 2000: 46: 660–668. 120 Geatch DR, Harris JI, Heasman PA, Taylor JJ. In vitro studies of lymphocyte apoptosis induced by the periodontal pathogen Porphyromonas gingivalis. J Periodontal Res 1999: 34: 70–78. 121 Geatch DR, Ross DA, Heasman PA, Taylor JJ. Expression of T-cell receptor Vbeta2, 6 and 8 gene families in chronic adult periodontal disease. Eur J Oral Sci 1997: 105: 397–404. 122 Genco CA. Regulation of hemin and iron transport in Porphyromonas gingivalis. Adv Dent Res 1995: 9: 41–47. 123 Genco CA, Cutler CW, Kapczynski D, Maloney K, Arnold RR. A novel mouse model to study the virulence of and host response to Porphyromonas (Bacteroides) gingivalis. Infect Immun 1991: 59: 1255–1263. 124 Genco CA, Dixon DW, Emerging strategies in microbial haem capture. Mol Microbiol 2001: 39: 1–11. 125 Genco CA, Odusanya BM, Potempa J, Mikolajczyk-Pawlinska J, Travis J. A peptide domain on gingipain R which confers immunity against Porphyromonas gingivalis infection in mice. Infect Immun 1998: 66: 4108–4114. 126 Genco CA, Simpson W, Forng RY, Egal M, Odusanya BM. Characterization of a Tn4351-generated hemin uptake mutant of Porphyromonas gingivalis: Evidence for the coordinate regulation of virulence factors by hemin. Infect Immun 1995: 63: 2459–2466. 127 Ghayoumi N, Chen C, Slots J. Dialister pneumosintes, a new putative periodontal pathogen. J Periodontal Res 2002: 37: 75–78. 128 Giambartolomei GH, Dennis VA, Lasater BL, Phillipp MT. Induction of pro- and anti-inflammatory cytokines by Borrelia burgdorferi lipoproteins in monocytes is mediated by CD14. Infect Immun 1999: 67: 40–147. 129 Gibbons RJ, Hay DI. Adsorbed salivary proline-rich proteins as bacterial receptors on apatitic surfaces. In: LM Switalski, M Hook, E Beachey, editors. Molecular Mechanisms of Oral Adhesion. New York: Springer-Verlag, 1988: 143–169. 130 Gibbons RJ, Hay DI, Childs WC III, Davis G. Role of cryptic receptors (cryptotopes) in bacterial adhesion to oral surfaces. Arch Oral Biol 1990: 35 (Suppl.): 107S–114S. 131 Gmür R, Strub JR, Guggenheim B. Prevalence of Bacteroides forsythus and Bacteroides gingivalis in subgingival plaque of prosthodontically treated patients on short recall. J Peridontal Res 1989: 24: 113–120. 132 Goerke C, Wolz C. Regulatory and genomic plasticity of Staphylococcus aureus during persistent colonization and infection. Int J Med Microbiol 2004: 294: 195–202. 133 Gomez DE, Alonso DF, Yoshiji H, Thorgeirsson UP. Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol 1997: 74: 111–122. 134 Gonzalez-Pedraza-Aviles A, Ortiz-Zaragoza MC, Irigoyen-Coria A. Bacterial vaginosis: a ‘broad overview’. Rev Latinoam Microbiol 1999: 41: 25–34. 135 Gopalsami C, Yotis W, Corrigan K, Schade S, Keene J, Simonson L. Effect of outer membrane of Treponema denticola on bone resorption. Oral Microbiol Immunol 1993: 8: 121–124. 136 Goulbourne PA, Ellen RP. Evidence that Porphyromonas (Bacteroides) gingivalis fimbriae function in adhesion to Actinomyces viscosus. J Bacteriol 1991: 173: 5266–5274. 137 Greene SR, Stamm LV. Molecular characterization of the gyrB region of the oral spirochete, Treponema denticola. Gene 2000: 253: 259–269. 138 Grenier D. Characterization of hemolytic and hemagglutinating activities of Treponema denticola. Oral Microbiol Immunol 1991: 6: 246–249. 139 Grenier D. Demonstration of a bimodal coaggregation reaction between Porphyromonas gingivalis and Treponema denticola. Oral Microbiol Immunol 1992: 7: 280–284. 140 Grenier D. Characterization of the trypsin-like activity of Bacteroides forsythus. Microbiology 1995: 141: 921–926. 141 Grenier D, Goulet V, Mayrand D. The capacity of Porphyromonas gingivalis to multiply under iron-limiting conditions correlates with its pathogenicity in an animal model. J Dent Res 2001: 80: 1678–1682. 142 Grenier D, Mayrand D. Selected characteristics of pathogenic and nonpathogenic stains of Bacteroides gingivalis. J Clin Microbiol 1987: 25: 738–740. 143 Grenier D, Mayrand D. Functional characterization of extracellular vesicles produced by Bacteroid