Journal of Food Hygiene and Safety (한국식품위생안전성학회지)

The Korean Society of Food Hygiene and Safety (한국식품위생안전성학회)
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Anti-periodontitic Effects of Weissella cibaria SPM402 and Lactobacillus paracasei SPM412 Isolated from Korean Traditional Foods

한국전통식품에서 분리한 Weissella cibaria SPM402와 Lactobacillus SPM412의 항치주염 효능

  • Received : 2024.07.15
  • Accepted : 2024.08.20
  • Published : 2024.08.30
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Abstract

This study aimed to develop probiotics with anti-periodontitic effects to help treat inflammation in the tissues surrounding the teeth. We isolated Weisiella cibaria (W. cibareia) SPM402 and Lactobacillus paracasei (L. paracasei) SPM412 from homemade kimchi and used their cell-free supernatants. At a concentration of 10 mg/mL of L. paracasei SPM412 (LP412) inhibited the formation of Fusobacterium nucleatum (F. nucleatum) biofilm by 95.99±0.73%. In addition, 10 mg/mL of LP412 reduced the RQ value of fimA, an adhesin gene of Porphyromonas gingivalis (P. gingivalis) to 0.08±0.05, and the RQ value of radD, an adhesin gene of F. nucleatum, to 0.08±0.008. When the P. gingivalis outer membrane vehicle (Pg OMV) induced inflammation in YD-38 cells, the RQ value of TNF-α was increased to 36.68±1.85, but was reduced to 4.15±0.37 in the presence of 1 mg/mL of W. cibareia SPM402 (WC402). Similarly, in Pg OMV-induced inflammation in THP-1 cells, the RQ value of IL-1β increased to 2,330.65±204.61 but was reduced to 15.19±4.57 in the presence of 15 mg/mL of WC402. In F. nucleatum-induced inflammation in YD-38 cells, the RQ value of IL-8 increased to 15.10±1.11 and was decreased to 2.67±0.50 in the presence of 1 mg/mL of LP412. In conclusion, W. cibaria SPM402 and L. paracasei SPM412 showed potent anti-inflammatory effects against oral pathogenic bacteria and hold promise as functional probiotics with anti-periodontitic activity.

본 연구는 한국전통식품인 김치에서 분리한 W. cibaria SPM402, L. paracasei SPM412의 포괄적인 항 치주염 효과를 확인하였다. WC402 10 mg/mL농도에서 P. gingivalis 의 생물막 형성이 37.30±8.23%, LP412 10 mg/mL에서 51.36±5.95% 억제되었고, F. nucleatum의 생물막 형성의 경우 WC402 10 mg/mL에서 76.77±2.77%, LP412 10 mg/mL에서 95.99± 0.73% 억제되었다. LP412 10 mg/mL에서 P. gingivalis 부착소인 fimA의 RQ값이 0.08±0.05로 약 12배 감소함을 확인하였고, F. nucleatum의 부착소인 radD의 RQ값은 0.08±0.008으로 radD는 거의 90배 이상 억제되었다. 사람 잇몸 상피세포주인 YD-38에 Pg OMV에 의한 염증반응을 유도 후 WC402 15 mg/mL 처리 결과 IL-1β유전자 발현이 약 150배 가량 억제되었고, LP412 0.1 mg/mL 처리 결과 IL-1β유전자 발현이 약 3.6배 가량 억제됨을 확인하였다. YD-38세포주에 F. nucleatum에 의한 염증반응을 유도 후 1 mg/mL의 WC402를 처리한 결과 IL-8유전자 발현이 약 3배 정도, 1 mg/mL의 LP412를 처리한 결과 IL-8유전자 발현이 약 5.6배 정도 억제되었다. 이상의 결과를 볼 때 W. cibaria SPM402, L. paracasei SPM412는 구강병원성 세균의 생물막 형성 관련 병인인자 발현 억제, 직접적인 생물막 형성 억제 및 병원성 세균에 의해 유도된 염증반응을 효과적으로 억제하는 기능을 보유한 균주로 구강질환에 대한 치료제나 구강 건강에 도움이 되는 구강 건강기능성 식품으로 사용될 가능성이 있음을 확인하였다.

Keywords

Acknowledgement

본 연구는 삼육대학교 교내연구비 지원으로 수행되었으며, 이에 감사드립니다.

References

  1. Bernabe, E., Marcenes, W., Hernandez, C.R., Bailey, J., Abreu, L.G., Alipour, V., Amini, S., Arabloo, J., Arefi, Z., Arora, A., Ayanore, M.A., Barnighausen, T.W., Bijani, A., Cho, D.Y., Chu, D.T., Crowe, C.S., Demoz, G.T., Demsie, D.G., Forooshani, Z.S., Du, M., El Tantawi, M., Fischer, F., Folayan, M.O., Futran, N.D., Geramo, Y.C.D., Haj-Mirzaian, A., Hariyani, N., Hasanzadeh, A., Hassanipour, S,. Hay, S.I., Hole, M.K., Hostiuc, S., Ilic, M.D., James, S.L., Kalhor, R., Kemmer, L., Keramati, M., Khader, Y.S., Kisa, S., Kisa, A., Koyanagi, A., Lalloo, R., Le Nguyen. Q., London, S.D., Manohar, N.D., Massenburg, B.B., Mathur, M.R., Meles, H.G., Mestrovic, T., Mohammadian-Hafshejani, A., Mohammadpourhodki, R., Mokdad, A.H., Morrison, S.D., Nazari, J., Nguyen, T.H., Nguyen, C.T., Nixon, M.R., Olagunju, T.O., Pakshir, K., Pathak, M., Rabiee, N., Rafiei, A., Ramezanzadeh, K., Rios-Blancas, M.J., Roro, E.M., Sabou,r S., Samy, A.M., Sawhney, M., Schwendicke, F., Shaahmadi, F., Shaikh, M.A., Stein, C., Tovani-Palone, M.R., Tran, B.X., Unnikrishnan, B., Vu, G.T., Vukovic, A., Warouw, T.S.S., Zaidi, Z., Zhang, Z.J., Kassebaum, N.J., Global, regional, and national levels and trends in burden of oral conditions from 1990 to 2017: a systematic analysis for the global burden of disease 2017 study. J. Dent. Res., 99, 362-373 (2020). https://doi.org/10.1177/0022034520908533
  2. Hasturk, H., Schulte, F., Martins, M., Sherzai, H., Floros, C., Cugini, M., Chiu, C.J., Hardt, M., Van Dyke, T., Safety and preliminary efficacy of a novel host-modulatory therapy for reducing gingival inflammation. Front. Immunol., 12, 704163 (2021).
  3. Olsen, I., Potempa, J.. Strategies for the inhibition of gingipains for the potential treatment of periodontitis and associated systemic diseases. J. Oral Microbiol., 6, 24800 (2014).
  4. Peng, X., Cheng, L., You, Y., Tang, C., Ren, B., Li, Y., Xu, X., Zhou, X., Oral microbiota in human systematic diseases. Int. J. Oral Sci., 14, 14 (2022).
  5. Yamamoto, M., Aizawa, R., Maintaining a protective state for human periodontal tissue. Periodontol., 86, 142-156 (2021). https://doi.org/10.1111/prd.12367
  6. Graves, D., Cytokines that promote periodontal tissue destruction. J. Periodontol., 79, 1585-1591 (2008). https://doi.org/10.1902/jop.2008.080183
  7. Moutsopoulos, N.M., Konkel, J.E., Tissue-specific immunity at the oral mucosal barrier. Trends Immunol., 39, 276-287 (2018). https://doi.org/10.1016/j.it.2017.08.005
  8. Mohanty, R., Asopa, S.J., Joseph, M.D., Singh, B., Rajguru, J.P., Saidath, K., Sharma, U., Red complex: Polymicrobial conglomerate in oral flora: A review. J. Family Med. Prim. Care, 8, 3480-3486 (2019). https://doi.org/10.4103/jfmpc.jfmpc_759_19
  9. de Andrade, K.Q., Almeida-da-Silva, C.L.C., Coutinho-Silva, R., Immunological pathways triggered by Porphyromonas gingivalis and Fusobacterium nucleatum: therapeutic possibilities? Mediators Inflamm., 2019, 7241312 (2019).
  10. Jia, L., Han, N., Du, J., Guo, L., Luo, Z., Liu, Y., Pathogenesis of important virulence factors of Porphyromonas gingivalis via toll-like receptors. Front. Cell Infect. Microbiol., 9, 262 (2019).
  11. Belanger, M., Kozarov, E., Song, H., Whitlock, J., Progulske-Fox, A., Both the unique and repeat regions of the Porphyromonas gingivalis hemagglutin A are involved in adhesion and invasion of host cells. Anaerobe, 18, 128-134 (2011). https://doi.org/10.1016/j.anaerobe.2011.10.005
  12. Wang, H., Zhang, W., Wang, W., Zhang, L., The prevalence of fimA genotypes of Porphyromonas gingivalis in patients with chronic periodontitis: A meta-analysis. PLoS One, 15, e0240251 (2020).
  13. Signat, B., Roques, C., Poulet, P., Duffaut, D., Role of Fusobacterium nucleatum in periodontal health and disease. Curr. Issues Mol. Biol., 13, 25-36 (2011).
  14. Liu, P., Liu, Y., Wang, J., Guo, Y., Zhang, Y., Xiao, S., Detection of Fusobacterium nucleatum and fadA adhesin gene in patients with orthodontic gingivitis and non-orthodontic periodontal inflammation PLoS One, 9, e85280 (2014).
  15. Kaplan, C., Lux, R., Shi, W., The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Mol. Microbiol., 1, 35-47 (2009). https://doi.org/10.1111/j.1365-2958.2008.06503.x
  16. Jansen, P.M., Abdelbary, M.M.H., Conrads, G., A concerted probiotic activity to inhibit periodontitis-associated bacteria. PLoS One, 16, e0248308 (2021).
  17. Kazmierczyk-Winciorek, M., Nedzi-Gora, M., Slotwinska, S.M., The immunomodulating role of probiotics in the prevention and treatment of oral diseases. Cent. Eur. J. Immunol., 46, 99-104 (2021). https://doi.org/10.5114/ceji.2021.104412
  18. Seminario-Amez, M., Lopez-Lopez, J., Estrugo-Devesa, A., Ayuso-Montero, R., Jane-Salas, E., Probiotics and oral health: A systematic review. Med. Oral Patol. Oral Cir. Bucal., 22, e282-e288 (2017).
  19. Park, H.E., Kang, K.W., Kim, B.S., Lee, S.M., Lee, W.K., Immunomodulatory potential of Weissella cibaria in aged C57BL/6J Mice. J. Microbiol. Biotechnol., 27, 2094-2103 (2017). https://doi.org/10.4014/jmb.1708.08016
  20. Kang, M.S., Park, G.Y., In vitro evaluation of the effect of oral probiotic Weissella cibaria on the formation of multispecies oral biofilms on dental implant surfaces. Microorganisms, 9, 2482 (2021).
  21. de Alvarenga, J.A., de Barros, P.P., de Camargo, Ribeiro F., Rossoni, R.D., Garcia, M.T., Dos Santos Velloso, M., Shukla, S., Fuchs, B.B., Shukla, A., Mylonakis, E., Junqueira, J.C., Probiotic effects of Lactobacillus paracasei 28.4 to inhibit Streptococcus mutans in a gellan-based formulation probiotics. Antimicrob. Probiotics Antimicrob. Proteins, 13, 506-517 (2021). https://doi.org/10.1007/s12602-020-09712-0
  22. Livshits, M.A., Khomyakova, E., Evtushenko, E.G., Lazarev, VN., Kulemin, N.A., Semina, S.E., Generozov, E.V., Govorun, V.M., Isolation of exosomes by differential centrifugation: theoretical analysis of a commonly used protocol. Sci. Rep., 5, 17319 (2015).
  23. Kim, J.H., Jang, H.J., Lee, N.K., Paik, H.D., Antibacterial and antibiofilm effect of cell-free supernatant of Lactobacillus brevis KCCM 202399 isolated from Korean fermented food against Streptococcus mutans KCTC 5458. J. Microbiol. Biotechnol., 32, 56-63 (2021).
  24. Seo, C.H., Kang, S.W., Choi, S.S., Inhibition Effects of Weisiella cibaria SPM402 and Lactobacillus paracasei SPM412 against Gingipains as a Major Virulence Factor for Porphyromonas gingivalis. J. Food Hyg. Saf., 38, 544-550 (2023). https://doi.org/10.13103/JFHS.2023.38.6.544
  25. Rao, X., Huang, X., Zhou, Z., Lin, X., An improvement of the 2ˆ(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat. Bioinforma. Biomath., 3, 71-85 (2013).
  26. Lee, J.H., Yim, D.S., Choi, S.S., Antibacterial activity and anti-inflammatory effect of methanol extracts of Saliva miltiorrhiza against oral pathogenic bacteria. Kor. J. Pharmacogn., 52, 41-48 (2021).
  27. Vermilyea, D.M., Ottenberg, G.K., Davey, M.E., Citrullination mediated by PPAD constrains biofilm formation in P. gingivalis strain 381. NPJ Biofilms Microbiomes., 5, 7 (2019).
  28. Chen, Y., Shi, T., Li, Y., Huang, L., Yin, D., Fusobacterium nucleatum: The opportunistic pathogen of periodontal and peri-implant diseases. Front Microbiol., 13, 860149 (2022).
  29. Albuquerque-Souza, E., Balzarini, D., Ando-Suguimoto, E.S., Ishikawa, K.H., Simionato, M.R.L., Holzhausen, M., Mayer, M.P.A., Probiotics alter the immune response of gingival epithelial cells challenged by Porphyromonas gingivalis. J. Periodontal Res., 54, 115-127 (2019). https://doi.org/10.1111/jre.12608
  30. Khattri, S., Kumbargere Nagraj, S., Arora, A., Eachempati, P., Kusum, C.K., Bhat, K.G., Johnson, T.M., Lodi, G., Adjunctive systemic antimicrobials for the non-surgical treatment of periodontitis. Cochrane Database Syst. Rev., 11, CD012568 (2020).