Tannerella forsythia infection-induced calvarial bone and soft tissue transcriptional profiles

Molecular Oral Microbiology

Volumn 25, Issue 5, 2010, Pages 317-330

  Bakthavatchalu, V ^a   Meka, A ^b,e   Sathishkumar, S ^a,f   Lopez, M C ^c   Bhattacharyya, I ^b   Boyce, B F ^d   Mans, J J ^b   Lamont, R J ^b   Baker, H V ^c   Ebersole, J L ^a   Kesavalu, L ^a,b  

^a UNIVERSITY OF KENTUCKY COLLEGE OF DENTISTRY   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^e NONE   (United States)

^f Genetic ID NA Inc   (United States)

Author keywords

calvarial bone; gene expression; microarray; Tannerella forsythia; tissue

Indexed keywords

CELL ADHESION MOLECULE; RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; BACTERIAL INFECTION; BAGG ALBINO MOUSE; CALVARIA; CELL JUNCTION; CELL MIGRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DEBRIDEMENT; DNA HYBRIDIZATION; DNA MICROARRAY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; GENE INTERACTION; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; HOST CELL; INFLAMMATION; LEUKOCYTE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOCLAST; OSTEOLYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; SOFT TISSUE; TANNERELLA FORSYTHENSIS;

ALVEOLAR BONE LOSS; ANIMALS; BACTEROIDES INFECTIONS; CELL ADHESION MOLECULES; CHRONIC PERIODONTITIS; FEMALE; GENE EXPRESSION PROFILING; LEUKOCYTES; MICE; MICE, INBRED BALB C; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, CELL SURFACE; SKULL; TRANSCRIPTION, GENETIC; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 77956370067     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/j.2041-1014.2010.00583.x     Document Type: Article

References (52)

1. Arakawa, S., Nakajima, T., Ishikura, H., Ichinose, S., Ishikawa, I. Tsuchida, N. (2000) Novel apoptosis-inducing activity in Bacteroides forsythus: a comparative study with three serotypes of Actinobacillus actinomycetemcomitans. Infect Immun 68 : 4611 4615.
2. Bakthavatchalu, V., Meka, A., Sathishkumar, S. et al. (2010) Molecular characterization of Treponema denticola infection-induced bone and tissue transcriptional profiles. Mol Oral Microbiol 25 : 1 15.
3. Boyce, B.F., Aufdemorte, T.B., Garrett, I.R., Yates, A.J. Mundy, G.R. (1989) Effects of interleukin-1 on bone turnover in normal mice. Endocrinology 125 : 1142 1150.
4. Chou, H.H., Yumoto, H., Davey, M. et al. (2005) Porphyromonas gingivalis fimbria-dependent activation of inflammatory genes in human aortic endothelial cells. Infect Immun 73 : 5367 5378.
5. Cohen, P., Bouaboula, M., Bellis, M. et al. (2000) Monitoring cellular responses to Listeria monocytogenes with oligonucleotide arrays. J Biol Chem 275 : 11181 11190.
6. Demmer, R.T., Behle, J.H., Wolf, D.L. et al. (2008) Transcriptomes in healthy and diseased gingival tissues. J Periodontol 79 : 2112 2124.
7. Draghici, S., Khatri, P., Tarca, A.L. et al. (2007) A systems biology approach for pathway level analysis. Genome Res 17 : 1537 1545.
8. Eisen, M.B., Spellman, P.T., Brown, P.O. Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95 : 14863 14868.
9. Eskra, L., Mathison, A. Splitter, G. (2003) Microarray analysis of mRNA levels from RAW264.7 macrophages infected with Brucella abortus. Infect Immun 71 : 1125 1133.
10. Feezor, R.J., Oberholzer, C., Baker, H.V. et al. (2003) Molecular characterization of the acute inflammatory response to infections with gram-negative versus gram-positive bacteria. Infect Immun 71 : 5803 5813.
11. Gemmell, E., Walsh, L.J., Savage, N.W. Seymour, G.J. (1994) Adhesion molecule expression in chronic inflammatory periodontal disease tissue. J Periodontal Res 29 : 46 53.
12. Haffajee, A.D., Teles, R.P. Socransky, S.S. (2006) Association of Eubacterium nodatum and Treponema denticola with human periodontitis lesions. Oral Microbiol Immunol 21 : 269 282.
13. Handfield, M., Mans, J.J., Zheng, G. et al. (2005) Distinct transcriptional profiles characterize oral epithelium-microbiota interactions. Cell Microbiol 7 : 811 823.
14. Handfield, M., Baker, H.V. Lamont, R.J. (2008) Beyond good and evil in the oral cavity: insights into host-microbe relationships derived from transcriptional profiling of gingival cells. J Dent Res 87 : 203 223.
15. Hannas, A.R., Pereira, J.C., Granjeiro, J.M. Tjaderhane, L. (2007) The role of matrix metalloproteinases in the oral environment. Acta Odontol Scand 65 : 1 13.
16. Hannigan, E., O'Connell, D.P., Hannigan, A. Buckley, L.A. (2004) Soluble cell adhesion molecules in gingival crevicular fluid in periodontal health and disease. J Periodontol 75 : 546 550.
17. Hasegawa, Y., Tribble, G.D., Baker, H.V., Mans, J.J., Handfield, M. Lamont, R.J. (2008) Role of Porphyromonas gingivalis SerB in gingival epithelial cell cytoskeletal remodeling and cytokine production. Infect Immun 76 : 2420 2427.
18. Hayashi, J., Saito, I., Ishikawa, I. Miyasaka, N. (1994) Effects of cytokines and periodontopathic bacteria on the leukocyte function-associated antigen 1intercellular adhesion molecule 1 pathway in gingival fibroblasts in adult periodontitis. Infect Immun 62 : 5205 5212.
19. Higgins, M.A., Berridge, B.R., Mills, B.J. et al. (2003) Gene expression analysis of the acute phase response using a canine microarray. Toxicol Sci 74 : 470 484.
20. Hughes, C.V., Malki, G., Loo, C.Y., Tanner, A.C. Ganeshkumar, N. (2003) Cloning and expression of alpha-d-glucosidase and N-acetyl - glucosaminidase from the periodontal pathogen, Tannerella forsythensis (Bacteroides forsythus). Oral Microbiol Immunol 18 : 309 312.
21. Inagaki, S., Onishi, S., Kuramitsu, H.K. Sharma, A. (2006) Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by "Tannerella forsythia". Infect Immun 74 : 5023 5028.
22. Ishikura, H., Arakawa, S., Nakajima, T., Tsuchida, N. Ishikawa, I. (2003) Cloning of the Tannerella forsythensis (Bacteroides forsythus) siaHI gene and purification of the sialidase enzyme. J Med Microbiol 52 : 1101 1107.
23. Karim, A.Y., Kulczycka, M., Kantyka, T. et al. (2010) A novel matrix metalloprotease-like enzyme (karilysin) of the periodontal pathogen Tannerella forsythia ATCC 43037. Biol Chem 391 : 105 117.
24. Khatri, P., Voichita, C., Kattan, K. et al. (2007) Onto-Tools: new additions and improvements in 2006. Nucleic Acids Res 35 : W206 W211.
25. Kiili, M., Cox, S.W., Chen, H.Y. et al. (2002) Collagenase-2 (MMP-8) and collagenase-3 (MMP-13) in adult periodontitis: molecular forms and levels in gingival crevicular fluid and immunolocalisation in gingival tissue. J Clin Periodontol 29 : 224 232.
26. Li, C. Wong, W.H. (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98 : 31 36.
27. Maiden, M.F., Pham, C. Kashket, S. (2004) Glucose toxicity effect and accumulation of methylglyoxal by the periodontal anaerobe Bacteroides forsythus. Anaerobe 10 : 27 32.
28. Matsuyama, T., Kawai, T., Izumi, Y. Taubman, M.A. (2005) Expression of major histocompatibility complex class II and CD80 by gingival epithelial cells induces activation of CD4+ T cells in response to bacterial challenge. Infect Immun 73 : 1044 1051.
29. Meka, A., Bakthavatchalu, V., Sathishkumr, S. et al. (2010) Porphyromonas gingivalis infection-induced tissue and bone transcriptional profiles. Mol Oral Microbiol 25 : 61 74.
30. Murakami, Y., Higuchi, N., Nakamura, H., Yoshimura, F. Oppenheim, F.G. (2002) Bacteroides forsythus hemagglutinin is inhibited by N- acetylneuraminyllactose. Oral Microbiol Immunol 17 : 125 128.
31. Nakajima, T., Tomi, N., Fukuyo, Y. et al. (2006) Isolation and identification of a cytopathic activity in Tannerella forsythia. Biochem Biophys Res Commun 351 : 133 139.
32. Offenbacher, S., Barros, S.P., Paquette, D.W. et al. (2009) Gingival transcriptome patterns during induction and resolution of experimental gingivitis in humans. J Periodontol 80 : 1963 1982.
33. Onishi, S., Honma, K., Liang, S. et al. (2008) Toll-like receptor 2-mediated interleukin-8 expression in gingival epithelial cells by the Tannerella forsythia leucine-rich repeat protein BspA. Infect Immun 76 : 198 205.
34. Papapanou, P.N., Behle, J.M., Kebschull, M. et al. (2009) Subgingival bacterial colonization profiles correlate with gingival tissue gene expression. BMC Microbiol 9 : 221.
35. Piana, C., Wirth, M., Gerbes, S., Viernstein, H., Gabor, F. Toegel, S. (2008) Validation of reference genes for qPCR studies on Caco-2 cell differentiation. Eur J Pharm Biopharm 69 : 1187 1192.
36. Rachman, H., Kim, N., Ulrichs, T. et al. (2006) Critical role of methylglyoxal and AGE in mycobacteria-induced macrophage apoptosis and activation. PLoS ONE 1 : e29.
37. Rios, H., Koushik, S.V., Wang, H. et al. (2005) Periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol 25 : 11131 11144.
38. Rios, H.F., Ma, D., Xie, Y. et al. (2008) Periostin is essential for the integrity and function of the periodontal ligament during occlusal loading in mice. J Periodontol 79 : 1480 1490.
39. Sabet, M., Lee, S.W., Nauman, R.K., Sims, T. Um, H.S. (2003) The surface (S-) layer is a virulence factor of Bacteroides forsythus. Microbiology 149 : 3617 3627.
40. Saito, T., Ishihara, K., Kato, T. Okuda, K. (1997) Cloning, expression, and sequencing of a protease gene from Bacteroides forsythus ATCC 43037 in Escherichia coli. Infect Immun 65 : 4888 4891.
41. Sharma, A., Sojar, H.T., Glurich, I., Honma, K., Kuramitsu, H.K. Genco, R.J. (1998) Cloning, expression, and sequencing of a cell surface antigen containing a leucine-rich repeat motif from Bacteroides forsythus ATCC 43037. Infect Immun 66 : 5703 5710.
42. Sharma, A., Inagaki, S., Honma, K., Sfintescu, C., Baker, P.J. Evans, R.T. (2005) Tannerella forsythia-induced alveolar bone loss in mice involves leucine-rich-repeat BspA protein. J Dent Res 84 : 462 467.
43. Socransky, S.S., Haffajee, A.D., Cugini, M.A., Smith, C. Kent, R.L. Jr. (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25 : 134 144.
44. Tamai, R., Asai, Y. Ogawa, T. (2005) Requirement for intercellular adhesion molecule 1 and caveolae in invasion of human oral epithelial cells by Porphyromonas gingivalis. Infect Immun 73 : 6290 6298.
45. Tamai, R., Asai, Y., Kawabata, A., Akisaka, T. Ogawa, T. (2007) Possible requirement of intercellular adhesion molecule-1 for invasion of gingival epithelial cells by Treponema medium. Can J Microbiol 53 : 1232 1238.
46. Tanner, A.C. Izard, J. 2006) Tannerella forsythia, a periodontal pathogen entering the genomic era. Periodontol 2000 42 : 88 113.
47. Tanner, A., Maiden, M.F., Macuch, P.J., Murray, L.L. Kent, R.L. Jr. (1998) Microbiota of health, gingivitis, and initial periodontitis. J Clin Periodontol 25 : 85 98.
48. Tervahartiala, T., Pirila, E., Ceponis, A. et al. (2000) The in vivo expression of the collagenolytic matrix metalloproteinases (MMP-2, -8, -13, and -14) and matrilysin (MMP-7) in adult and localized juvenile periodontitis. J Dent Res 79 : 1969 1977.
49. Wang, P.L., Ohura, K., Fujii, T. et al. (2003) DNA microarray analysis of human gingival fibroblasts from healthy and inflammatory gingival tissues. Biochem Biophys Res Commun 305 : 970 973.
50. Yoneda, M., Yoshikane, T., Motooka, N. et al. (2005) Stimulation of growth of Porphyromonas gingivalis by cell extracts from Tannerella forsythia. J Periodontal Res 40 : 105 109.
51. Yoo, J.Y., Kim, H.C., Zhu, W. et al. (2007) Identification of Tannerella forsythia antigens specifically expressed in patients with periodontal disease. FEMS Microbiol Lett 275 : 344 352.
52. Zubery, Y., Dunstan, C.R., Story, B.M. et al. (1998) Bone resorption caused by three periodontal pathogens in vivo in mice is mediated in part by prostaglandin. Infect Immun 66 : 4158 4162.