1887

Chapter 11 : Treponomics: Genome and Functions

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Treponomics: Genome and Functions, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817107/9781555815035_Chap11-1.gif /docserver/preview/fulltext/10.1128/9781555817107/9781555815035_Chap11-2.gif

Abstract:

This chapter reviews current progress in applying genome information to the research areas and suggests some topics that have yet to be addressed adequately by the research community. A group of seven genes was identified by homology with TP0155, a fibronectin-binding protein of . While five of these proteins showed at least some fibronectin-binding activity in recombinant form, only one was clearly demonstrated to be surface localized. This study provides a rational basis for further examination of the relative contribution of these proteins to interactions with fibronectin. The repeat (tpr) genes, which encode paralogous proteins with sequence similarity to major surface protein (Msp) of , were expressed at relatively low levels. This study, as well as numerous similar studies of other pathogens, demonstrates the potential utility of in vivo microarray analysis of bacterial gene expression. The current paucity of microarray-based global expression analysis is likely the result of several factors. As in many bacteria, the genome contains genes that appear to be more closely related to those of eukaryotes or archaea than to those of other bacteria. Several groups are investigating various aspects of molecular physiology, especially as it relates to microbial community ecology and periodontal pathogenesi. In addition to the continued need to characterize putative virulence determinants very little is known about several important biological components of these cells, including nutrient uptake and processing, secretion and efflux systems, and various lipids and lipid-containing molecules.

Citation: Fenno J. 2011. Treponomics: Genome and Functions, p 149-161. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch11

Key Concept Ranking

Tumor Necrosis Factor alpha
0.46566767
Mobile Genetic Elements
0.4600662
0.46566767
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Composite immunogold transmission electron micrograph showing a ATCC 35405 dividing cell labeled with immunoglobulins raised against the PrtP protease complex (dentilisin). The hexagonal array of Msp complex is also visible in the outer membrane. The inset shows an enlargement of the indicated region. Bars, 300 nm. Original photographs courtesy of B. C. McBride.

Citation: Fenno J. 2011. Treponomics: Genome and Functions, p 149-161. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555817107.ch11
1. Baehni, P. C.,, M. Song,, C. A. McCulloch, and, R. P. Ellen. 1992. Treponema denticola induces actin rearrangement and detachment of human gingival fibroblasts. Infect. Immun. 60:33603368.
2. Bamford, C. V.,, J. C. Fenno,, H. F. Jenkinson, and, D. Dymock. 2007. The chymotrypsin-like protease complex of Treponema denticola ATCC 35405 mediates fibrinogen adherence and degradation. Infect. Immun. 75:43644372.
3. Bamford, C. V.,, T. Francescutti,, C. E. Cameron,, H. F. Jenkinson, and, D. Dymock. 2010. Characterization of a novel family of fibronectin-binding proteins with M23 peptidase domains from Treponema denticola. Mol. Oral Microbiol. 25:369383.
4. Barbieri, J. T.,, F. E. Austin, and, C. D. Cox. 1981. Distribution of glucose incorporated into macromolecular material by Treponema pallidum. Infect. Immun. 31:10711077.
5. Beauséjour, A.,, N. Deslauriers, and, D. Grenier. 1997. Activation of the interleukin-1β precursor by Treponema denticola: a potential role in chronic inflammatory periodontal diseases. Infect. Immun. 65:31993202.
6. Boehringer, H.,, P. H. Berthold, and, N. S. Taichman. 1986. Studies on the interaction of human neutrophils with plaque spirochetes. J. Periodontal Res. 21:195209.
7. Boehringer, H.,, N. S. Taichman, and, B. J. Shenker. 1984. Suppression of fibroblast proliferation by oral spirochetes. Infect. Immun. 45:155159.
8. Brown, J. R. 2003. Ancient horizontal gene transfer. Nat. Rev. Genet. 4:121132.
9. Cameron, C. E.,, J. M. Kuroiwa,, M. Yamada,, T. Francescutti,, B. Chi, and, H. K. Kuramitsu. 2008. Heterologous expression of the Treponema pallidum laminin-binding adhesin Tp0751 in the culturable spirochete Treponema phagedenis. J. Bacteriol. 190:25652571.
10. Capone, R. F.,, Y. Ning,, N. Pakulis,, T. Alhazzazi, and, J. C. Fenno. 2007. Characterization of Treponema denticola pyrF encoding orotidine-5′-monophosphate decarboxylase. FEMS Microbiol. Lett. 268:261267.
11. Chan, E. C. S.,, A. Klitorinos,, S. Gharbia,, S. D. Caudry,, M. D. Rahal, and, R. Siboo. 1996. Characterization of a 4.2-kb plasmid isolated from periodontopathic spirochetes. Oral Microbiol. Immunol. 11:365368.
12. Chauhan, S.,, and H. K. Kuramitsu. 2004. Sequence analysis of plasmid pTS1 isolated from oral spirochetes. Plasmid 51:6165.
13. Chen, T.,, K. Abbey,, W. J. Deng, and, M. C. Cheng. 2005. The bioinformatics resource for oral pathogens. Nucleic Acids Res. 33:W734W740.
14. Chen, T.,, W. H. Yu,, J. Izard,, O. V. Baranova,, A. Lakshmanan, and, F. E. Dewhirst. 2010. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) doi:10.1093/database/baq013.
15. Chi, B.,, S. Chauhan, and, H. Kuramitsu. 1999. 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. 67:36533656.
16. Choi, B. K.,, B. J. Paster,, F. E. Dewhirst, and, U. B. Gobel. 1994. Diversity of cultivable and uncultivable oral spirochetes from a patient with severe destructive periodontitis. Infect. Immun. 62:18891895.
17. Chu, L.,, A. Burgum,, D. Kolodrubetz, and, S. C. Holt. 1995. The 46-kilodalton-hemolysin gene from Treponema denticola encodes a novel hemolysin homologous to aminotransferases. Infect. Immun. 63:44484455.
18. Chu, L.,, J. L. Ebersole,, G. P. Kurzban, and, S. C. Holt. 1997. Cystalysin, a 46-kilodalton cysteine desulfhydrase from Treponema denticola, with hemolytic and hemoxidative activities. Infect. Immun. 65:32313238.
19. Chu, L.,, Y. Lai,, X. Xu,, S. Eddy,, S. Yang,, L. Song, and, D. Kolodrubetz. 2008. A 52-kDa leucyl aminopeptidase from Treponema denticola is a cysteinylglycinase that mediates the second step of glutathione metabolism. J. Biol. Chem. 283:1935119358.
20. Chu, L.,, X. Xu,, Z. Dong,, D. Cappelli, and, J. L. Ebersole. 2003. Role for recombinant γ-glutamyltransferase from Treponema denticola in glutathione metabolism. Infect. Immun. 71:335342.
21. Coleman, N.,, S. Tetu,, N. Wilson, and, A. Holmes. 2004. An unusual integron in Treponema denticola. Microbiology 150:35243526.
22. Dawson, J. R.,, and R. P. Ellen. 1990. Tiporiented adherence of Treponema denticola to fibronectin. Infect. Immun. 58:39243928.
23. De Filippo, A. B.,, R. P. Ellen, and, C. A. McCulloch. 1995. Induction of cytoskeletal rearrangements and loss of volume regulation in epithelial cells by Treponema denticola. Arch. Oral Biol. 40:199207.
24. Dewhirst, F. E.,, T. Chen,, J. Izard,, B. J. Paster,, A. C. Tanner,, W. H. Yu,, A. Lakshmanan, and, W. G. Wade. 2010. The human oral microbiome. J. Bacteriol. 192:50025017.
25. Dewhirst, F. E.,, M. A. Tamer,, R. E. Ericson,, C. N. Lau,, V. A. Levanos,, S. K. Boches,, J. L. Galvin, and, B. J. Paster. 2000. The diversity of periodontal spirochetes by 16S rRNA analysis. Oral Microbiol. Immunol. 15:196202.
26. Ding, Y.,, V.-J. Uitto,, M. Haapasalo,, K. Lounatmaa,, Y. T. Konttinen,, T. Salo,, D. Grenier, and, T. Sorsa. 1996. Membrane components of Treponema denticola trigger proteinase release from human polymorphonuclear leukocytes. J. Dent. Res. 75:19861993.
27. Doolittle, W. F. 1999. Lateral genomics. Trends Cell Biol. 9:M5M8.
28. Ebersole, J. L. 1990. Systemic humoral immune responses in periodontal disease. Crit. Rev. Oral Biol. Med. 1:283331.
29. Ellen, R. P.,, and V. B. Galimanas. 2005. Spirochetes at the forefront of periodontal infections. Periodontol. 2000 38:1332.
30. Ellen, R. P.,, M. Song, and, C. A. McCulloch. 1994. Degradation of endogenous plasma membrane fibronectin concomitant with Treponema denticola 35405 adhesion to gingival fibroblasts. Infect. Immun. 62:30333037.
31. Fenno, J. C.,, P. M. Hannam,, W. K. Leung,, M. Tamura,, V.-J. Uitto, and, B. C. McBride. 1998. Cytopathic effects of the major surface protein (Msp) and the chymotrypsinlike protease (CTLP) of Treponema denticola. Infect. Immun. 66:18691877.
32. Fenno, J. C.,, and B. C. McBride. 1998. Virulence factors of oral treponemes. Anaerobe 4:117.
33. Fenno, J. C.,, K. H. Muller, and, B. C. McBride. 1996. Sequence analysis, expression, and binding activity of recombinant major outer sheath protein (Msp) of Treponema denticola. J. Bacteriol. 178:24892497.
34. Fenno, J. C.,, M. Tamura,, P. M. Hannam,, G. W. Wong,, R. A. Chan, and, B. C. McBride. 2000. Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect. Immun. 68:18841892.
35. Figge, R. M.,, and R. Cerff. 2001. GAPDH gene diversity in spirochetes: a paradigm for genetic promiscuity. Mol. Biol. Evol. 18:22402249.
36. Fletcher, H. M.,, H. A. Schenkein,, R. M. Morgan,, K. A. Bailey,, C. R. Berry, and, F. L. Macrina. 1995. Virulence of a Porphyromonas gingivalis W83 mutant defective in the prtH gene. Infect. Immun. 63:15211528.
37. Frank, R. M. 1980. Bacterial penetration in the apical pocket wall of advanced human periodontitis. J. Periodont. Res. 15:563573.
38. Fraser, C. M.,, S. J. Norris,, G. M. Weinstock,, O. White,, G. G. Sutton,, R. Dodson,, M. Gwinn,, E. K. Hickey,, R. Clayton,, K. A. Ketchum,, E. Sodergren,, J. M. Hardham,, M. P. McLeod,, S. Salzberg,, J. Peterson,, H. Khalak,, D. Richardson,, J. K. Howell,, M. Chidambaram,, T. Utterback,, L. McDonald,, P. Artiach,, C. Bowman,, M. D. Cotton,, C. Fujii,, S. Garland,, B. Hatch,, K. Horst,, K. Roberts,, M. Sandusky,, J. Weidman,, H. O. Smith, and, J. C. Venter. 1998. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281:375388.
39. Frederick, J. R.,, E. A. Rogers, and, R. T. Marconi. 2008. Analysis of a growth-phase-regulated two-component regulatory system in the periodontal pathogen Treponema denticola. J. Bacteriol. 190:61626169.
40. Goetting-Minesky, M. P.,, and J. C. Fenno. 2010. A simplified erythromycin resistance cassette for Treponema denticola mutagenesis. J. Microbiol. Methods 83:6668.
41. Gonzalez, C. F.,, A. J. Stonestrom,, G. L. Lorca, and, M. H. Saier, Jr. 2005. Biochemical characterization of phosphoryl transfer involving HPr of the phosphoenolpyruvate-dependent phosphotransferase system in Treponema denticola, an organism that lacks PTS permeases. Biochemistry 44:598608.
42. Grenier, D. 1992. Demonstration of a bimodal coaggregation reaction between Porphyromonas gingivalis and Treponema denticola. Oral Microbiol. Immunol. 7:280284.
43. Hashimoto, M.,, S. Ogawa,, Y. Asai,, Y. Takai, and, T. Ogawa. 2003. Binding of Porphyromonas gingivalis fimbriae to Treponema denticola dentilisin. FEMS Microbiol. Lett. 226:267271.
44. Henderson, B.,, S. Poole, and, M. Wilson. 1996. Bacterial modulins: a novel class of virulence factors which cause host tissue pathology by inducing cytokine synthesis. Microbiol. Rev. 60:316341.
45. Hinton, J. C.,, I. Hautefort,, S. Eriksson,, A. Thompson, and, M. Rhen. 2004. Benefits and pitfalls of using microarrays to monitor bacterial gene expression during infection. Curr. Opin. Microbiol. 7:277282.
46. Hoepelman, A. I.,, and E. I. Tuomanen. 1992. Consequences of microbial attachment: directing host cell functions with adhesins. Infect. Immun. 60:17291733.
47. Ikegami, A.,, K. Honma,, A. Sharma, and, H. K. Kuramitsu. 2004. Multiple functions of the leucine-rich repeat protein LrrA of Treponema denticola. Infect. Immun. 72:46194627.
48. Ishihara, K.,, H. K. Kuramitsu,, T. Miura, and, K. Okuda. 1998. Dentilisin activity affects the organization of the outer sheath of Treponema denticola. J. Bacteriol. 180:38373844.
49. Kent, C.,, P. Gee,, S. Y. Lee,, X. Bian, and, J. C. Fenno. 2004. A CDP-choline pathway for phosphatidylcholine biosynthesis in Treponema denticola. Mol. Microbiol. 51:471481.
50. Kesavalu, L.,, S. Sathishkumar,, V. Bakthavatchalu,, C. Matthews,, D. Dawson,, M. Steffen, and, J. L. Ebersole. 2007. Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect. Immun. 75:17041712.
51. Kolenbrander, P. E.,, K. D. Parrish,, R. N. Andersen, and, E. P. Greenberg. 1995. Inter-generic coaggregation of oral Treponema spp. with Fusobacterium spp. and intrageneric coaggregation among Fusobacterium spp. Infect. Immun. 63:45844588.
52. Lai, C. H.,, M. A. Listgarten,, C. I. Evian, and, P. Dougherty. 1986. Serum IgA and IgG antibodies to Treponema vincentii and Treponema denticola in adult periodontitis, juvenile periodontitis and periodontally healthy subjects. J. Clin. Periodontol. 13:752757.
53. Lee, S. F.,, E. Andrian,, E. Rowland, and, I. C. Marquez. 2009. Immune response and alveolar bone resorption in a mouse model of Treponema denticola infection. Infect. Immun. 77:694698.
54. Lee, S. Y.,, Y. Ning, and, J. C. Fenno. 2002. 23S rRNA point mutation associated with erythromycin resistance in Treponema denticola. FEMS Microbiol. Lett. 207:3942.
55. Lee, W.,, L. Pankoski,, A. Zekavat, and, B. J. Shenker. 2004. Treponema denticola immunoinhibitory protein induces irreversible G1 arrest in activated human lymphocytes. Oral Microbiol. Immunol. 19:144149.
56. Li, H.,, J. Ruby,, N. Charon, and, H. Kuramitsu. 1996. Gene inactivation in the oral spirochete Treponema denticola: construction of an flgE mutant. J. Bacteriol. 178:36643667.
57. Livermore, B. P.,, and R. C. Johnson. 1974. Lipids of the Spirochaetales: comparison of the lipids of several members of the genera Spirochaeta, Treponema, and Leptospira. J. Bacteriol. 120:12681273.
58. Loesche, W. J.,, and N. S. Grossman. 2001. Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin. Microbiol. Rev. 14:727752.
59. Loesche, W. J.,, and B. E. Laughon. 1982. Role of spirochetes in periodontal disease, p. 62–75. In R. J. Genco and, S. E. Mergenhagen (ed.), Host-Parasite Interactions in Periodontal Diseases. American Society for Microbiology, Washington, DC.
60. Lopez-Lara, I. M.,, and O. Geiger. 2001. Novel pathway for phosphatidylcholine biosynthesis in bacteria associated with eukaryotes. J. Biotechnol. 91:211221.
61. Lux, R.,, J. N. Miller,, N. H. Park, and, W. Shi. 2001. Motility and chemotaxis in tissue penetration of oral epithelial cell layers by Treponema denticola. Infect. Immun. 69:62766283.
62. Lux, R.,, J. H. Sim,, J. P. Tsai, and, W. Shi. 2002. Construction and characterization of a cheA mutant of Treponema denticola. J. Bacteriol. 184:31303134.
63. MacDougall, J.,, D. Margarita, and, I. Saint Girons. 1992. Homology of a plasmid from the spirochete Treponema denticola with the singlestranded DNA plasmids. J. Bacteriol. 174:27242728.
64. Mäkinen, P. L.,, and K. K. Mäkinen. 1997. γ-Glutamyltransferase from the outer cell envelope of Treponema denticola ATCC 35405. Infect. Immun. 65:685691.
65. Mangan, D. F.,, B. E. Laughon,, B. Bower, and, D. E. Lopatin. 1982. In vitro lymphocyte blastogenic responses and titers of humoral antibodies from periodontitis patients to oral spirochete isolates. Infect. Immun. 37:445451.
66. McDowell, J. V.,, J. Frederick,, L. Stamm, and, R. T. Marconi. 2007. Identification of the gene encoding the FhbB protein of Treponema denticola, a highly unique factor H-like protein 1 binding protein. Infect. Immun. 75:10501054.
67. McDowell, J. V.,, B. Huang,, J. C. Fenno, and, R. T. Marconi. 2009. Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infect. Immun. 77:14171425.
68. McHardy, I.,, C. Keegan,, J. H. Sim,, W. Shi, and, R. Lux. 2010. Transcriptional profiles of Treponema denticola in response to environmental conditions. PLoS One 5:e13655.
69. Mitchell, H. L.,, S. G. Dashper,, D. V. Cat-mull,, R. A. Paolini,, S. M. Cleal,, N. Slakeski,, K. H. Tan, and, E. C. Reynolds. 2010. Treponema denticola biofilm-induced expression of a bacteriophage, toxin-antitoxin systems and transposases. Microbiology 156:774788.
70. Ochman, H.,, J. G. Lawrence, and, E. A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299304.
71. Reijntjens, F. M.,, F. H. Mikx,, J. M. Wolters-Lutgerhorst, and, J. C. Maltha. 1986. Adherence of oral treponemes and their effect on morphological damage and detachment of epithelial cells in vitro. Infect. Immun. 51:642647.
72. Rosen, G.,, T. Genzler, and, M. N. Sela. 2008. Coaggregation of Treponema denticola with Porphyromonas gingivalis and Fusobacterium nucleatum is mediated by the major outer sheath protein of Treponema denticola. FEMS Microbiol. Lett. 289:5966.
73. Rosen, G.,, M. N. Sela,, R. Naor,, A. Halabi,, V. Barak, and, L. Shapira. 1999. Activation of murine macrophages by lipoprotein and lipooligosaccharide of Treponema denticola. Infect. Immun. 67:11801186.
74. Rowe-Magnus, D. A.,, A. M. Guerout, and, D. Mazel. 2002. Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol. Microbiol. 43:16571669.
75. Ruby, J. D.,, R. Lux,, W. Shi,, N. W. Charon, and, A. Dasanayake. 2008. Effect of glucose on Treponema denticola cell behavior. Oral Microbiol. Immunol. 23:234238.
76. Saglie, R.,, M. G. Newman,, F. A. Carranza, Jr., and, G. L. Pattison. 1982. Bacterial invasion of gingiva in advanced periodontitis in humans. J. Periodontol. 53:217222.
77. Saint Girons, I.,, B. Chi, and, H. Kuramitsu. 2001. Development of shuttle vectors for spirochetes, p. 123–125. In M. H. Saier, Jr., and, J. Garcia-Lara (ed.), The Spirochetes: Molecular and Cellular Biology. Horizon Scientific Press, Wymondham, United Kingdom.
78. Salyers, A. A.,, and D. D. Whitt. 1994. Bacterial Pathogenesis: a Molecular Approach. ASM Press, Washington, DC.
79. Sela, M. N.,, A. Weinberg,, R. Borinsky,, S. C. Holt, and, T. Dishon. 1988. Inhibition of superoxide production in human polymorphonuclear leukocytes by oral treponemal factors. Infect. Immun. 56:589594.
80. Seshadri, R.,, G. S. Myers,, H. Tettelin,, J. A. Eisen,, J. F. Heidelberg,, R. J. Dodson,, T. M. Davidsen,, R. T. DeBoy,, D. E. Fouts,, D. H. Haft,, J. Selengut,, Q. Ren,, L. M. Brinkac,, R. Madupu,, J. Kolonay,, S. A. Durkin,, S. C. Daugherty,, J. Shetty,, A. Shvartsbeyn,, E. Gebregeorgis,, K. Geer,, G. Tsegaye,, J. Malek,, B. Ayodeji,, S. Shatsman,, M. P. McLeod,, D. Smajs,, J. K. Howell,, S. Pal,, A. Amin,, P. Vashisth,, T. Z. McNeill,, Q. Xiang,, E. Sodergren,, E. Baca,, G. M. Weinstock,, S. J. Norris,, C. M. Fraser, and, I. T. Paulsen. 2004. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc. Natl. Acad. Sci. USA 101:56465651.
81. Shenker, B. J.,, M. A. Listgarten, and, N. S. Taichman. 1984. Suppression of human lymphocyte responses by oral spirochetes: a monocyte-dependent phenomenon. J. Immunol. 132:20392045.
82. Sim, J. H.,, W. Shi, and, R. Lux. 2005. Protein-protein interactions in the chemotaxis signalling pathway of Treponema denticola. Microbiology 151:18011807.
83. Slivienski-Gebhardt, L. L.,, J. Izard,, W. A. Samsonoff, and, R. J. Limberger. 2004. Development of a novel chloramphenicol resistance expression plasmid used for genetic complementation of a fliG deletion mutant in Treponema denticola. Infect. Immun. 72:54935497.
84. Smajs, D.,, M. McKevitt,, J. K. Howell,, S. J. Norris,, W. W. Cai,, T. Palzkill, and, G. M. Weinstock. 2005. Transcriptome of Treponema pallidum: gene expression profile during experimental rabbit infection. J. Bacteriol. 187:18661874.
85. Smibert, R. M. 1976. Cultivation, composition, and physiology of avirulent treponemes, p. 49–56. In R. C. Johnson (ed.), The Biology of Parasitic Spirochetes. Academic Press, New York, NY.
86. Sohlenkamp, C.,, I. M. Lopez-Lara, and, O. Geiger. 2003. Biosynthesis of phosphatidylcholine in bacteria. Prog. Lipid Res. 42:115162.
87. Tsai, J. P.,, and W. Shi. 2000. Analysis of gene expression in Treponema denticola with differential display polymerase chain reaction. Oral Microbiol. Immunol. 15:305308.
88. Uitto, V.-J.,, Y. M. Pan,, W. K. Leung,, H. Larjava,, R. P. Ellen,, B. B. Finlay, and, B. C. McBride. 1995. Cytopathic effects of Treponema denticola chymotrypsin-like proteinase on migrating and stratified epithelial cells. Infect. Immun. 63:34013410.
89. Umemoto, T.,, Y. Nakatani,, Y. Nakamura, and, I. Namikawa. 1993. Fibronectin-binding proteins of a human oral spirochete Treponema denticola. Microbiol. Immunol. 37:7578.
90. Veith, P. D.,, S. G. Dashper,, N. M. O’Brien-Simpson,, R. A. Paolini,, R. Orth,, K. A. Walsh, and, E. C. Reynolds. 2009. Major proteins and antigens of Treponema denticola. Biochim. Biophys. Acta 1794:14211432.
91. Wang, B. Y.,, B. Chi, and, H. K. Kuramitsu. 2002. Genetic exchange between Treponema denticola and Streptococcus gordonii in biofilms. Oral Microbiol. Immunol. 17:108112.
92. Wang, Q.,, K. S. Ko,, A. Kapus,, C. A. McCulloch, and, R. P. Ellen. 2001. A spirochete surface protein uncouples store-operated calcium channels in fibroblasts: a novel cytotoxic mechanism. J. Biol. Chem. 276:2305623064.
93. Wolf, Y. I.,, L. Aravind,, N. V. Grishin, and, E. V. Koonin. 1999. Evolution of aminoacyl-tRNA synthetases—analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res. 9:689710.
94. Yamada, M.,, A. Ikegami, and, H. K. Kuramitsu. 2005. Synergistic biofilm formation by Treponema denticola and Porphyromonas gingivalis. FEMS Microbiol. Lett. 250:271277.
95. Yamazaki, T.,, M. Miyamoto,, S. Yamada,, K. Okuda, and, K. Ishihara. 2006. Surface protease of Treponema denticola hydrolyzes C3 and influences function of polymorphonuclear leukocytes. Microbes Infect. 8:17581763.
96. Yang, Y.,, P. E. Stewart,, X. Shi, and, C. Li. 2008. Development of a transposon mutagenesis system in the oral spirochete Treponema denticola. Appl. Environ. Microbiol. 74:64616464.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error