Treponema denticola interactions with host proteins

Journal of Oral Microbiology

Volumn 4, Issue 2012, 2012, Pages

  Fenno, J Christopher ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Periodontal disease; Spirochetes; Virulence factors

Indexed keywords

COLLAGEN; DENTILISIN; FIBRINOGEN; FIBRONECTIN; HYALURONIC ACID; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LAMININ; LIPOPROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; SCLEROPROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BINDING AFFINITY; CHEMOTAXIS; CYTOKINE PRODUCTION; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; PATHOGENESIS; PERIODONTAL DISEASE; PERIODONTITIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECRETION; TREPONEMA DENTICOLA; TREPONEMA PALLIDUM;

EID: 84864812761     PISSN: None     EISSN: 20002297     Source Type: Journal    
DOI: 10.3402/jom.v4i0.9929     Document Type: Article

References (145)

1. Loesche WJ, Grossman NS. Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin Microbiol Rev 2001; 14: 727-52.
2. Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol 1992; 63: 322-31.
3. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA, et al. Bacterial diversity in human subgingival plaque. J Bacteriol 2001; 183: 3770-83.
4. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL. Microbial complexes in subgingival plaque. J Clin Periodontol 1998; 25: 134-44.
5. Moore WE, Moore LH, Ranney RR, Smibert RM, Burmeister JA, Schenkein HA. The microflora of periodontal sites showing active destructive progression. J Clin Periodontol 1991; 18: 729-39.
6. Loesche WJ, Syed SA, Schmidt E, Morrison EC. Bacterial profiles of subgingival plaques in periodontitis. J Periodontol 1985; 56: 447-56.
7. Loesche WJ, Syed SA, Laughon BE, Stoll J. The bacteriology of acute necrotizing ulcerative gingivitis. J Periodontol 1982; 53: 223-30.
8. Choi BK, Paster BJ, Dewhirst FE, Gobel UB. Diversity of cultivable and uncultivable oral spirochetes from a patient with severe destructive periodontitis. Infect Immun 1994; 62: 1889-95.
9. Ellen RP, Galimanas VB. Spirochetes at the forefront of periodontal infections. Periodontol 2005; 38: 13-32.
10. Frank RM. Bacterial penetration in the apical pocket wall of advanced human periodontitis. J Periodontal Res 1980; 15: 563-73.
11. Saglie R, Newman MG, Carranza FA, Jr, Pattison GL. Bacterial invasion of gingiva in advanced periodontitis in humans. J Periodontol 1982; 53: 217-22.
12. Uitto V-J, Pan YM, Leung WK, Larjava H, Ellen RP, Finlay BB, et al. Cytopathic effects of Treponema denticola chymotrypsin-like proteinase on migrating and stratified epithelial cells. Infect Immun 1995; 63: 3401-10.
13. Chi B, Qi M, Kuramitsu HK. Role of dentilisin in Treponema denticola epithelial cell layer penetration. Res Microbiol 2003; 154: 637-43.
14. Peters SR, Valdez M, Riviere G, Thomas DD. Adherence to and penetration through endothelial cells by oral treponemes. Oral Microbiol Immunol 1999; 14: 379-83.
15. Salyers AA, Whitt DD. Bacterial pathogenesis: a molecular approach. Washington, DC: American Society for Microbiology; 1994. p. 30.
16. Hoepelman AI, Tuomanen EI. Consequences of microbial attachment: directing host cell functions with adhesins. Infect Immun 1992; 60: 1729-33.
17. Fenno JC, McBride BC. Virulence factors of oral treponemes. Anaerobe 1998; 4: 1-17.
18. Listgarten MA, Levin S. Positive correlation between the proportions of subgingival spirochetes and motile bacteria and susceptibility of human subjects to periodontal deterioration. J Clin Periodontol 1981; 8: 122-38.
19. Holt SC. Anatomy and chemistry of spirochetes. Microbiol Rev 1978; 42: 114-60.
20. Charon NW, Greenberg EP, Koopman MB, Limberger RJ. Spirochete chemotaxis, motility, and the structure of the spirochetal periplasmic flagella. Res Microbiol 1992; 143: 597-603.
21. Kent C, Gee P, Lee SY, Bian X, Fenno JC. A CDP-choline pathway for phosphatidylcholine biosynthesis in Treponema denticola. Mol Microbiol 2004; 51: 471-81.
22. Haapasalo M, Müller K-H, Uitto V-J, Leung WK, McBride BC. Characterization, cloning, and binding properties of the major 53-kilodalton Treponema denticola surface antigen. Infect Immun 1992; 60: 2058-65.
23. Uitto V-J, Grenier D, Chan EC, McBride BC. Isolation of a chymotrypsin-like enzyme from Treponema denticola. Infect Immun 1988; 56: 2717-22.
24. Kolenbrander PE. Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol 2000; 54: 413-37.
25. Seshadri R, Myers GS, Tettelin H, Eisen JA, Heidelberg JF, Dodson RJ, et al. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci U S A 2004; 101: 5646-51.
26. Brown JR. Ancient horizontal gene transfer. Nat Rev Genet 2003; 4: 121-32.
27. Duncan MJ. Oral microbiology and genomics. Periodontol 2000 2005; 38: 63-71.
28. Chen T, Abbey K, Deng WJ, Cheng MC. The bioinformatics resource for oral pathogens. Nucleic Acids Res 2005; 33: W734-W40.
29. Dewhirst FE, Chen T, Izard T, Paster BJ, Tanner AC, Yu WH, et al. The human oral microbiome. J Bacteriol 2010; 192: 5002-17.
30. Li H, Ruby J, Charon N, Kuramitsu H. Gene inactivation in the oral spirochete Treponema denticola: construction of an flgE mutant. J Bacteriol 1996; 178: 3664-7.
31. Slivienski-Gebhardt LL, Izard J, Samsonoff WA, Limberger RJ. Development of a novel chloramphenicol resistance expression plasmid used for genetic complementation of a fliG deletion mutant in Treponema denticola. Infect Immun 2004; 72: 5493-7.
32. Chi B, Chauhan S, Kuramitsu HK. Development of a system for expressing heterologous genes in the oral spirochete Treponema denticola and its use in expression of the Treponema pallidum flaA gene. Infect Immun 1999; 67: 3653-6.
33. Boehringer H, Taichman NS, Shenker BJ. Suppression of fibroblast proliferation by oral spirochetes. Infect Immun 1984; 45: 155-9.
34. Reijntjens FM, Mikx FH, Wolters-Lutgerhorst JM, Maltha JC. Adherence of oral treponemes and their effect on morphological damage and detachment of epithelial cells in vitro. Infect Immun 1986; 51: 642-7.
35. Baehni PC, Song M, McCulloch M, Ellen RP. Treponema denticola induces actin rearrangement and detachment of human gingival fibroblasts. Infect Immun 1992; 60: 3360-8.
36. Ellen RP, Song M, McCulloch CA. Degradation of endogenous plasma membrane fibronectin concomitant with Treponema denticola 35405 adhesion to gingival fibroblasts. Infect Immun 1994; 62: 3033-7.
37. De Filippo AB, Ellen RP, McCulloch CA. Induction of cytoskeletal rearrangements and loss of volume regulation in epithelial cells by Treponema denticola. Arch Oral Biol 1995; 40: 199-207.
38. Lee W, Pankoski L, Zekavat A, Shenker BJ. Treponema denticola immunoinhibitory protein induces irreversible G1 arrest in activated human lymphocytes. Oral Microbiol Immunol 2004; 19: 144-9.
39. Shenker BJ, Listgarten MA, Taichman NS. Suppression of human lymphocyte responses by oral spirochetes: a monocytedependent phenomenon. J Immunol 1984; 132: 2039-45.
40. Fenno JC, Hannam PM, Leung WK, Tamura M, Uitto V-J, McBride BC. Cytopathic effects of the major surface protein (Msp) and the chymotrypsin-like protease (CTLP) of Treponema denticola. Infect Immun 1998; 66: 1869-77.
41. Egli C, Leung WK, Müller KH, Hancock RE, McBride BC. Pore-forming properties of the major 53-kilodalton surface antigen from the outer sheath of Treponema denticola. Infect Immun 1993; 61: 1694-9.
42. Mathers DA, Leung WK, Fenno JC, Hong Y, McBride BC. Major surface protein complex of Treponema denticola depolarizes and induces ion channels in HeLa cell membranes. Infect. Immun 1996; 64: 2904-10.
43. Ulmer JB, Burke CJ, Shi C, Friedman A, Donnelly JJ, Liu MA. Pore formation and mitogenicity in blood cells by the class 2 protein of Neisseria meningitidis. J Biol Chem 1992; 267: 19266-71.
44. Massari P, King CA, MacLeod H, Wetzler LM. Improved purification of native meningococcal porin PorB and studies on its structure/function. Protein Expr Purif 2005; 44: 136-46.
45. Yang PF, Song M, Grove M, Ellen RP. Filamentous actin disruption and diminished inositol phosphate response in gingival fibroblasts caused by Treponema denticola. Infect Immun 1998; 66: 696-702.
46. 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: 3650-4.
47. 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: 485-98.
48. Amin M, Grove DA, Kapus A, Glogauer M, Ellen RP. An actin-stabilizing peptide conjugate deduced from the major outer sheath protein of the bacterium Treponema denticola. Cell Motil Cytoskeleton 2007; 64: 662-74.
49. Amin M, Magnusson KE, Kapus A, Glogauer M, Ellen RP. Treponema denticola Msp-deduced peptide conjugate, P34BSA, promotes RhoA-dependent actin stress fiber formation independent of its internalization by fibroblasts. Cell Motil Cytoskeleton 2008; 65: 406-21.
50. Wang Q, Ko KS, Kapus A, McCulloch CA, Ellen RP. A spirochete surface protein uncouples store-operated calcium channels in fibroblasts: a novel cytotoxic mechanism. J Biol Chem 2001; 276: 23056-64.
51. Hirschfeld M, Kirschning CJ, Schwandner R, Wesche H, Weis JH, Wooten RM, et al. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol 1999; 163: 2382-6.
52. Ellen RP, Ko KS, Lo KS, 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: 581-6.
53. 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: 717-25.
54. 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: 185-7.
55. Nixon CS, Steffen MJ, Ebersole JL. Cytokine responses to Treponema pectinovorum and Treponema denticola in human gingival fibroblasts. Infect Immun 2000; 68: 5284-92.
56. Rosen G, Sela MN, Naor R, Halabi A, Barak V, Shapira L. Activation of murine macrophages by lipoprotein and lipooligosaccharide of Treponema denticola. Infect Immun 1999; 67: 1180-6.
57. Mao Y, Schwarzbauer JE. Fibronectin fibrillogenesis, a cellmediated matrix assembly process. Matrix Biol 2005; 24: 389-99.
58. Kuusela P. Fibronectin binds to Staphylococcus aureus. Nature (London) 1978; 276: 718-20.
59. Henderson B, Nair S, Pallas J, Williams MA. Fibronectin: a multidomain host adhesin targeted by bacterial fibronectinbinding proteins. FEMS Microbiol Rev 2011; 35: 147-200.
60. Ellen RP, Dawson JR, Yang PF. Treponema denticola as a model for polar adhesion and cytopathogenicity of spirochetes. Trends Microbiol 1994; 2: 114-9.
61. Dawson JR, Ellen RP. Clustering of fibronectin adhesins toward Treponema denticola tips upon contact with immobilized fibronectin. Infect Immun 1994; 62: 2214-21.
62. Dawson JR, Ellen RP. Tip-oriented adherence of Treponema denticola to fibronectin. Infect Immun 1990; 58: 3924-8.
63. Weinberg A, Holt Sc. Interaction of Treponema denticola TD-4, GM-1, and MS25 with human gingival fibroblasts. Infect Immun 1990; 58: 1720-9.
64. Ellen RP. Perturbation and exploitation of host cell cytoskeleton by periodontal pathogens. Microbes Infect 1999; 1: 621-32.
65. Ko KS-C, Glogauer M, McCulloch CAG, Ellen RP. Treponema denticola outer membrane inhibits calcium flux in gingival fibroblasts. Infect Immun 1998; 66: 703-9.
66. 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: 2891-8.
67. Fenno JC, Müller K-H, McBride BC. Sequence analysis, expression and binding activity of recombinant major outer sheath protein (Msp) of Treponema denticola. J Bacteriol 1996; 178: 2489-97.
68. Fenno JC, Tamura M, Hannam PM, Wong GWK, Chan RA, McBride BC. Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect Immun 2000; 68: 1884-92.
69. Cameron CE, Brown EL, Kuroiwa JM, Schnapp LM, Brouwer NL. Treponema pallidum fibronectin-binding proteins. J Bacteriol 2004; 186: 7019-22.
70. Bamford CV, Francescutti T, Cameron CE, Jenkinson HF, Dymock D. Characterization of a novel family of fibronectinbinding proteins with M23 peptidase domains from Treponema denticola. Mol Oral Microbiol 2010; 25: 369-83.
71. Miao D, Fenno JC, Timm JC, Joo NE, Kapila YL. Treponema denticola chymotrypsin-like protease (dentilisin) induces MMP-2-dependent fibronectin fragmentation in periodontal ligament cells. Infect Immun 2011; 79: 806-11.
72. Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol 2010; 48: 504-11.
73. Dai R, Iwama A, Wang S, Kapila YL. Disease-associated fibronectin matrix fragments trigger anoikis of human primary ligament cells: p53 and c-myc are suppressed. Apoptosis 2005; 10: 503-12.
74. Kapila YL, Kapila S, Johnson PW. Fibronectin and fibronectin fragments modulate the expression of proteinases and proteinase inhibitors in human periodontal ligament cells. Matrix Biol 1996; 15: 251-61.
75. Grenier D, Uitto V-J, McBride BC. Cellular location of a Treponema denticola chymotrypsin-like protease and importance of the protease in migration through the basement membrane. Infect Immun 1990; 58: 347-51.
76. Haapasalo M, Singh U, McBride BC, Uitto V-J. Sulfhydryldependent attachment of Treponema denticola to laminin and other proteins. Infect Immun 1991; 59: 4230-7.
77. Umemoto T, Namikawa I. Binding of host-associated treponeme proteins to collagens and laminin: a possible mechanism of spirochetal adherence to host tissues. Microbiol Immunol 1994; 38: 655-63.
78. Sorsa T, Ingman T, Suomalainen K, Haapasalo M, Konttinen YT, Lindy O, et al. Identification of proteases from periodontopathogenic bacteria as activators of latent human neutrophil and fibroblast-type interstitial collagenases. Infect Immun 1992; 60: 4491-5.
79. Haapasalo M, Hannam P, McBride BC, Uitto V-J. Hyaluronan, a possible ligand mediating Treponema denticola binding to periodontal tissue. Oral Microbiol Immunol 1996; 11: 156-60.
80. Girish KS, Kemparaju K. The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sci 2007; 80: 1921-43.
81. Jiang D, Liang J, Noble PW. Hyaluronan as an immune regulator in human diseases. Physiol Rev 2011; 91: 221-64.
82. Kreil G. Hyaluronidases-a group of neglected enzymes. Protein Sci 1995; 4: 1666-9.
83. Scott D, Siboo R, Chan EC, Siboo R. An extracellular enzyme with hyaluronidase and chondroitinase activities from some oral anaerobic spirochaetes. Microbiology 1996; 142: 2567-76.
84. Fenno JC. Laboratory maintenance of Treponema denticola. Curr Protoc Microbiol 2005; 12B.1.1-1.21.
85. Wyss C. Fatty acids synthesized by oral treponemes in chemically defined media. FEMS Microbiol Lett 2007; 269: 70-6.
86. Wyss C, Choi BK, Schupbach P, Guggenheim B, Gobel UB. Treponema maltophilum sp. nov., a small oral spirochete isolated from human periodontal lesions. Int J Syst Bacteriol 1996; 46: 745-52.
87. Van Horn KG, Smibert RM. Albumin requirement of Treponema denticola and Treponema vincentii. Can J Microbiol 1983; 29: 1141-8.
88. Ruby JD, Lux R, Shi W, Charon NW, Dasanayake A. Effect of glucose on Treponema denticola cell behavior. Oral Microbiol Immunol 2008; 23: 234-8.
89. Hespell RB, Canale-Parola E. Amino acid and glucose fermentation by Treponema denticola. Arch Mikrobiol 1971; 78: 234-51.
90. Persson S, Edlund MB, Claesson R, Carlsson J. The formation of hydrogen sulfide and methyl mercaptan by oral bacteria. Oral Microbiol Immunol 1990; 5: 195-201.
91. Gleissner C, Springborn I, Willershausen B. Evaluation of sulcular sulphide level monitoring using a portable sensor system. Eur J Med Res 2002; 7: 491-501.
92. Chu L, Dong Z, Xu X, Cochran DL, Ebersole JL. Role of glutathione metabolism of Treponema denticola in bacterial growth and virulence expression. Infect Immun 2002; 70: 1113-20.
93. Murata T, Yaegaki K, Qian W, Herai M, Calenic B, Imai T, et al. Hydrogen sulfide induces apoptosis in epithelial cells derived from human gingiva. J Breath Res 2008; 2: 017007.
94. Zhang JH, Dong Z, Chu L. Hydrogen sulfide induces apoptosis in human periodontium cells. J Periodontal Res 2010; 45: 71-8.
95. 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: 3231-8.
96. Moreillon P, Entenza JM, Francioli P, McDevitt D, Foster TJ, Francois P, et al. Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun 1995; 63: 4738-43.
97. Mosesson MW. Fibrinogen and fibrin structure and functions. J Thromb Haemost 2005; 3: 1894-904.
98. Mäkinen PL, Mäkinen KK, Syed SA. Role of the chymotrypsin-like membrane-associated proteinase from Treponema denticola ATCC 35405 in inactivation of bioactive peptides. Infect Immun 1995; 63: 3567-75.
99. Rosen G, Naor R, Kutner S, Sela MN. Characterization of fibrinolytic activities of Treponema denticola. Infect Immun 1994; 62: 1749-54.
100. Bamford CV, Fenno JC, Jenkinson HF, Dymock D. The chymotrypsin-like protease (CTLP) complex of Treponema denticola ATCC 35405 mediates fibrinogen adherence and degradation. Infect Immun 2007; 75: 4364-72.
101. Sim JH, Shi W, Lux R. Protein-protein interactions in the chemotaxis signalling pathway of Treponema denticola. Microbiology 2005; 151: 1801-7.
102. Lux R, Sim JH, Tsai JP, Shi W. Construction and characterization of a cheA mutant of Treponema denticola. J Bacteriol 2002; 184: 3130-4.
103. Lux R, Miller JN, Park NH, ShiW. Motility and chemotaxis in tissue penetration of oral epithelial cell layers by Treponema denticola. Infect Immun 2001; 69: 6276-83.
104. Frederick JR, Rogers EA, Marconi RT. Analysis of a growthphase-regulated two-component regulatory system in the periodontal pathogen Treponema denticola. J Bacteriol 2008; 190: 6162-9.
105. Frederick JR, Sarkar J, McDowell JV, Marconi RT. Molecular signaling mechanisms of the periopathogen, Treponema denticola. J Dent Res 2011; 90: 1155-63.
106. Gonzalez CF, Stonestrom AJ, Lorca GL, Saier MH, Jr. Biochemical characterization of phosphoryl transfer involving HPr of the phosphoenolpyruvate-dependent phosphotransferase system in Treponema denticola, an organism that lacks PTS permeases. Biochem 2005; 44: 598-608.
107. Henderson B, Poole S, Wilson M. Bacterial modulins: a novel class of virulence factors which cause host tissue pathology by inducing cytokine synthesis. Microbiol Rev 1996; 60: 316-41.
108. Ebersole JL. Systemic humoral immune responses in periodontal disease. Crit Rev Oral Biol Med 1990; 1: 283-331.
109. Lee SH, Kim KK, Choi BK. Upregulation of intercellular adhesion molecule 1 and proinflammatory cytokines by the major surface proteins of Treponema maltophilum and Treponema lecithinolyticum, the phylogenetic group IV oral spirochetes associated with periodontitis and endodontic infections. Infect Immun 2005; 73: 268-76.
110. Jun HK, Kang YM, Lee HR, Lee SH, Choi BK. Highly conserved surface proteins of oral spirochetes as adhesins and potent inducers of proinflammatory and osteoclastogenic factors. Infect Immun 2008; 76: 2428-38.
111. Coutte L, Willery E, Antoine R, Drobecq H, Locht C, Jacob-Dubuisson F. Surface anchoring of bacterial subtilisin important for maturation function. Mol Microbiol 2003; 49: 529-39.
112. Correia FF, Plummer AR, Ellen RP, Wyss C, Boches SK, Galvin JL, et al. Two paralogous families of a two-gene subtilisin operon are widely distributed in oral treponemes. J Bacteriol 2003; 185: 6860-9.
113. Heuner K, Bergmann I, Heckenbach K, Gobel UB. Proteolytic activity among various oral Treponema species and cloning of a prtP-like gene of Treponema socranskii subsp. socranskii(1). FEMS Microbiol Lett 2001; 201: 169-76.
114. Klein EA, Dewhirst FE. Dentilisin is part of a conserved three-gene operon. J Dent Res 2006; 85 (Spec Iss A): 2126. (www.dentalresearch.org).
115. McDowell JV, Huang B, Fenno JC, Marconi RT. Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infect Immun 2009; 77: 1417-25.
116. Leung WK, Haapasalo M, Uitto V-J, Hannam PM, McBride BC. The surface proteinase of Treponema denticola may mediate attachment of the bacteria to epithelial cells. Anaerobe 1996; 2: 39-46.
117. Weinberg A, Holt SC. Chemical and biological activities of a 64-kilodalton outer sheath protein from Treponema denticola strains. J Bacteriol 1991; 173: 6935-47.
118. Hashimoto M, Ogawa S, Asai Y, Takai Y, Ogawa T. Binding of Porphyromonas gingivalis fimbriae to Treponema denticola dentilisin. FEMS Microbiol Lett 2003; 226: 267-71.
119. Puthengady TB, Sun CX, Bajenova E, Ellen RP, Glogauer M. Modulation of human neutrophil functions in vitro by Treponema denticola major outer sheath protein. Infect Immun 2006; 74: 1954-7.
120. Miyamoto M, Ishihara K, Okuda K. The Treponema denticola surface protease Dentilisin degrades Interleukin-1{beta} (IL-1{beta}), IL-6, and Tumor Necrosis Factor Alpha. Infect Immun 2006; 74: 2462-7.
121. Mäkinen PL, Mäkinen KK, Syed SA. An endo-acting prolinespecific oligopeptidase from Treponema denticola ATCC 35405: evidence of hydrolysis of human bioactive peptides. Infect Immun 1994; 62: 4938-47.
122. Yamazaki T, Miyamoto M, Yamada S, Okuda K, Ishihara K. Surface protease of Treponema denticola hydrolyzes C3 and influences function of polymorphonuclear leukocytes. Microbes Infect 2006; 8: 1758-63.
123. McDowell JV, Frederick J, Stamm L, Marconi RT. Identification of the gene encoding the FhbB protein of Treponema denticola, a highly unique factor H-like protein 1 binding protein. Infect Immun 2007; 75: 1050-4.
124. McDowell JV, Frederick J, Goodman MP, Goetting-Minesky MP, Miller DP, Fenno JC, et al. Marconi. Identification of the primary mechanism of complement evasion by the periodontal pathogen, Treponema denticola. Mol Oral Microbiol 2011; 26: 140-9.
125. Brogden KA. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 2005; 3: 238-50.
126. Komatsuzawa H, Ouhara K, Kawai T, Yamada S, Fujiwara T, Shiba H, et al. Susceptibility of periodontopathogenic and cariogenic bacteria to defensins and potential therapeutic use of defensins in oral diseases. Curr Pharm Des 2007; 13: 3084-95.
127. Brissette CA, Lukehart SA. Treponema denticola is resistant to human beta-defensins. Infect Immun 2002; 70: 3982-4.
128. Brissette CA, Simonson LG, Lukehart SA. Resistance to human beta-defensins is common among oral treponemes. Oral Microbiol Immunol 2004; 19: 403-7.
129. Brissette CA, Lukehart SA. Mechanisms of decreased susceptibility to beta-defensins by Treponema denticola. Infect Immun 2007; 75: 2307-15.
130. Grenier D, Mayrand D. Cleavage of human immunoglobulin G by Treponema denticola. Anaerobe 2001; 7: 1-4.
131. Hollmann R, Van der Hoeven HJ. Inability of intact cells of Treponema denticola to degrade human serum proteins IgA, IgG and albumin. J Clin Periodontol 1999; 26: 477-9.
132. Von Pawel-Rammingen U, Johansson BP, Bjorck L. IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. Embo J 2002; 21: 1607-15.
133. Ishihara K, Wawrzonek K, Shaw LN, Inagaki S, Miyamoto M, Potempa J. Dentipain, a Streptococcus pyogenes IdeS protease homolog, is a novel virulence factor of Treponema denticola. Biol Chem 2010; 391: 1047-55.
134. Schultz CP, Wolf V, Lange R, Mertens E, Wecke J, Naumann D, et al. Evidence for a new type of outer membrane lipid in oral spirochete Treponema denticola. Functioning permeation barrier without lipopolysaccharides. J Biol Chem 1998; 273: 15661-6.
135. Aliprantis AO, Yang RB, Mark MR, Suggett S, Devaux B, Radolf JD, et al. Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science 1999; 285: 736-9.
136. Nussbaum G, Ben-Adi S, Genzler T, Sela M, Rosen G. Involvement of Toll-like receptors 2 and 4 in the innate immune response to Treponema denticola and its outer sheath components. Infect Immun 2009; 77: 3939-47.
137. Opitz B, Schroder NW, Spreitzer I, Michelsen KS, Kirschning CJ, Hallatschek W, et al. Toll-like receptor-2 mediates Treponema glycolipid and lipoteichoic acid-induced NF-kappaB translocation. J Biol Chem 2001; 276: 22041-7.
138. Schroder NW, Opitz B, Lamping N, Michelsen KS, Zahringer U, Gobel UB, et al. Involvement of lipopolysaccharide binding protein, CD14, and Toll-like receptors in the initiation of innate immune responses by Treponema glycolipids. J Immunol 2000; 165: 2683-93.
139. 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: 226-33.
140. Limberger RJ, Slivienski LL, Izard J, Samsonoff WA. Insertional inactivation of Treponema denticola tap1 results in a nonmotile mutant with elongated flagellar hooks. J Bacteriol 1999; 181: 3743-50.
141. Kataoka M, Li H, Arakawa S, Kuramitsu H. Characterization of a methyl-accepting chemotaxis gene, dmcA, from the oral spirochete Treponema denticola. Infect Immun 1997; 65: 4011-6.
142. Li H, Arakawa S, Deng QD, Kuramitsu H. Characterization of a novel methyl-accepting chemotaxis gene, dmcB, from the oral spirochete Treponema denticola. Infect Immun 1999; 67: 694-9.
143. Fenno JC, Wong GWK, Hannam PM, McBride BC. Mutagenesis of outer membrane virulence determinants of the oral spirochete Treponema denticola. FEMS Microbiol Lett 1998; 163: 209-15.
144. Ishihara K, Kuramitsu HK, Miura T, Okuda K. Dentilisin activity affects the organization of the outer sheath of Treponema denticola. J Bacteriol 1998; 180: 3837-44.
145. Xu X, Kolodrubetz D. Construction and analysis of hemin binding protein mutants in the oral pathogen Treponema denticola. Res Microbiol 2002; 153: 569-77.