Journal of Periodontal and Implant Science

  • 제52권2호
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  • Pages.141-154
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  • 2022
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  • 2093-2278(pISSN)
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  • 2093-2286(eISSN)
대한치주과학회 (Korean Academy of Periodontology)
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A murine periodontitis model using coaggregation between human pathogens and a predominant mouse oral commensal bacterium

  • Liu, Mengmeng (Department of Immunology and Molecular Microbiology, School of Dentistry and Dental Research Institute, Seoul National University) ;
  • Choi, Youngnim (Department of Immunology and Molecular Microbiology, School of Dentistry and Dental Research Institute, Seoul National University)
  • 투고 : 2021.08.09
  • 심사 : 2021.10.25
  • 발행 : 2022.04.30
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초록

Purpose: C57BL/6 mice, which are among the most common backgrounds for genetically engineered mice, are resistant to the induction of periodontitis by oral infection with periodontal pathogens. This study aimed to develop a periodontitis model in C57BL/6 mice using coaggregation between human pathogens and the mouse oral commensal Streptococcus danieliae (Sd). Methods: The abilities of Porphyromonas gingivalis ATCC 33277 (Pg33277), P. gingivalis ATCC 49417 (Pg49417), P. gingivalis KUMC-P4 (PgP4), Fusobacterium nucleatum subsp. nucleatum ATCC 25586 (Fnn), and F. nucleatum subsp. animalis KCOM 1280 (Fna) to coaggregate with Sd were tested by a sedimentation assay. The Sd-noncoaggregating Pg33277 and 2 Sd-coaggregating strains, PgP4 and Fna, were chosen for animal experiments. Eighty C57BL/6 mice received oral gavage with Sd once and subsequently received vehicle alone (sham), Fna, Pg33277, PgP4, or Fna+PgP4 6 times at 2-day intervals. Mice were evaluated at 5 or 8 weeks after the first gavage of human strains. Results: Fnn, Fna, and PgP4 efficiently coaggregated with Sd, but Pg33277 and Pg49417 did not. Alveolar bone loss was significantly higher in the PgP4 group at both time points (weeks 5 and 8) and in all experimental groups at week 8 compared with the sham group. The PgP4 group presented greater alveolar bone loss than the other experimental groups at both time points. A higher degree of alveolar bone loss accompanied higher bacterial loads in the oral cavity, the invasion of not only PgP4 but also Sd and Fna, and the serum antibody responses to these bacteria. Conclusions: Periodontitis was successfully induced in C57BL/6 mice by oral infection with a P. gingivalis strain that persists in the oral cavity through coaggregation with a mouse oral commensal bacterium. This new model will be useful for studying the role of human oral bacteria-host interactions in periodontitis using genetically engineered mice.

키워드

과제정보

We acknowledge Professor Hyun-Man Kim at the Department of Cell and Developmental Biology for providing histologic expertise on gingival inflammation.

참고문헌

  1. Graves DT, Kang J, Andriankaja O, Wada K, Rossa C Jr. Animal models to study host-bacteria interactions involved in periodontitis. Front Oral Biol 2012;15:117-32. https://doi.org/10.1159/000329675
  2. Gurumurthy CB, Lloyd KC. Generating mouse models for biomedical research: technological advances. Dis Model Mech 2019;12:dmm029462. https://doi.org/10.1242/dmm.029462
  3. Marchesan J, Girnary MS, Jing L, Miao MZ, Zhang S, Sun L, et al. An experimental murine model to study periodontitis. Nat Protoc 2018;13:2247-67. https://doi.org/10.1038/s41596-018-0035-4
  4. Baker PJ, Dixon M, Roopenian DC. Genetic control of susceptibility to Porphyromonas gingivalis-induced alveolar bone loss in mice. Infect Immun 2000;68:5864-8. https://doi.org/10.1128/IAI.68.10.5864-5868.2000
  5. Hajishengallis G, Diaz PI. Porphyromonas gingivalis: Immune subversion activities and role in periodontal dysbiosis. Curr Oral Health Rep 2020;7:12-21. https://doi.org/10.1007/s40496-020-00249-3
  6. Chun J, Kim KY, Lee JH, Choi Y. The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer. BMC Microbiol 2010;10:101. https://doi.org/10.1186/1471-2180-10-101
  7. Clavel T, Charrier C, Haller D. Streptococcus danieliae sp. nov., a novel bacterium isolated from the caecum of a mouse. Arch Microbiol 2013;195:43-9. https://doi.org/10.1007/s00203-012-0846-6
  8. Lee J, Alam J, Choi E, Ko YK, Lee A, Choi Y. Association of a dysbiotic oral microbiota with the development of focal lymphocytic sialadenitis in IκB-ζ-deficient mice. NPJ Biofilms Microbiomes 2020;6:49. https://doi.org/10.1038/s41522-020-00158-4
  9. Baek KJ, Ji S, Kim YC, Choi Y. Association of the invasion ability of Porphyromonas gingivalis with the severity of periodontitis. Virulence 2015;6:274-81. https://doi.org/10.1080/21505594.2014.1000764
  10. Ji S, Shin JE, Kim YC, Choi Y. Intracellular degradation of Fusobacterium nucleatum in human gingival epithelial cells. Mol Cells 2010;30:519-26. https://doi.org/10.1007/s10059-010-0142-8
  11. Parikh N, Nagarajan P, Sei-ichi M, Sinha S, Garrett-Sinha LA. Isolation and characterization of an immortalized oral keratinocyte cell line of mouse origin. Arch Oral Biol 2008;53:1091-100. https://doi.org/10.1016/j.archoralbio.2008.07.002
  12. Choi YS, Kim YC, Baek KJ, Choi Y. In situ detection of bacteria within paraffin-embedded tissues using a digoxin-labeled DNA probe targeting 16S rRNA. J Vis Exp 2015;99:e52836.
  13. Lee A, Kim YC, Baek K, Alam J, Choi YS, Rheu Y, et al. Treponema denticola enolase contributes to the production of antibodies against ENO1 but not to the progression of periodontitis. Virulence 2018;9:1263-72. https://doi.org/10.1080/21505594.2018.1496775
  14. Tribble GD, Lamont RJ. Bacterial invasion of epithelial cells and spreading in periodontal tissue. Periodontol 2000 2010;52:68-83. https://doi.org/10.1111/j.1600-0757.2009.00323.x
  15. 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;66:4729-32. https://doi.org/10.1128/iai.66.10.4729-4732.1998
  16. Rickard AH, Gilbert P, High NJ, Kolenbrander PE, Handley PS. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 2003;11:94-100. https://doi.org/10.1016/S0966-842X(02)00034-3
  17. Lamont RJ, El-Sabaeny A, Park Y, Cook GS, Costerton JW, Demuth DR. Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology (Reading) 2002;148:1627-36. https://doi.org/10.1099/00221287-148-6-1627
  18. Hajishengallis G, Liang S, Payne MA, Hashim A, Jotwani R, Eskan MA, et al. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 2011;10:497-506. https://doi.org/10.1016/j.chom.2011.10.006
  19. Baek K, Ji S, Choi Y. Complex intratissue microbiota forms biofilms in periodontal lesions. J Dent Res 2018;97:192-200. https://doi.org/10.1177/0022034517732754
  20. Baek KJ, Choi YS, Kang CK, Choi Y. The proteolytic activity of Porphyromonas gingivalis is critical in a murine model of periodontitis. J Periodontol 2017;88:218-24. https://doi.org/10.1902/jop.2016.160262
  21. Wu RQ, Zhang DF, Tu E, Chen QM, Chen W. The mucosal immune system in the oral cavity-an orchestra of T cell diversity. Int J Oral Sci 2014;6:125-32. https://doi.org/10.1038/ijos.2014.48
  22. Tsuzuno T, Takahashi N, Yamada-Hara M, Yokoji-Takeuchi M, Sulijaya B, Aoki-Nonaka Y, et al. Ingestion of Porphyromonas gingivalis exacerbates colitis via intestinal epithelial barrier disruption in mice. J Periodontal Res 2021;56:275-88. https://doi.org/10.1111/jre.12816