Skip to main content
SpringerLink
Log in

Effects of Lactobacillus curvatus MG5246 on inflammatory markers in Porphyromonas gingivalis lipopolysaccharide-sensitized human gingival fibroblasts and periodontitis rat model

  • Research Article
  • Published:
Food Science and Biotechnology Aims and scope Submit manuscript

Abstract

This study investigated the effects of Lactobacillus curvatus MG5246 on periodontitis inflammation. Cell-free supernatants (CFS) prepared from L. curvatus MG5246 decreased prostaglandin E2 production and cyclooxygenase-2 gene expression by 60% and 78% in Porphyromonas gingivalis-lipopolysaccharide stimulated human gingival fibroblasts at 400 μg/mL. Gene expressions of tumor necrosis factor-α, interleukin-6, matrix metalloproteinases, and chemokines were significantly downregulated by CFS treatment (p < 0.05). L. curvatus MG5246 (2 × 108 CFU/day, 8 weeks) administration significantly improved alveolar bone loss in the ligature-induced periodontitis rat model. Elevated mRNA expression of the receptor activator of nuclear factor-κB ligand/osteoprotegerin ratio in the gingival tissue was significantly decreased by L. curvatus MG5246 administration (p < 0.05). Moreover, L. curvatus MG5246 showed sufficient tolerance in simulated gastrointestinal conditions (gastric tolerance: 89.48%, intestinal tolerance: 98.62%) and did not show antibiotic resistance and hemolytic activity. Therefore, L. curvatus MG5246 has the potential as novel oral probiotics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abe T, Hajishengallis G. Optimization of the ligature-induced periodontitis model in mice. Journal of Immunological Methods. 294: 49-54 (2013)

    Article  Google Scholar 

  • Aguilar-Toalá J. E, Garcia-Varela R, Garcia HS, Mata-Haro V, González-Córdova AF, Vallejo-Cordoba B, Hernández-Mendoza A. Postbiotics: An evolving term within the functional foods field. Trends in Food Science & Technology. 75: 105-114 (2018)

    Article  Google Scholar 

  • Allaker RP, Stephen AS. Use of probiotics and oral health. Current Oral Health Reports. 4: 309–318 (2017)

    Article  Google Scholar 

  • Bartold PM, Marshall RI, Haynes DR. Periodontitis and rheumatoid arthritis: a review. Journal of Periodontology. 76: 2066-2074 (2005)

    Article  CAS  Google Scholar 

  • Beck JD, Offenbacher S. Systemic effects of periodontitis: epidemiology of periodontal disease and cardiovascular disease. Journal of Periodontology. 76: 2089-2100 (2005)

    Article  Google Scholar 

  • Belibasakis GN, Bostanci N. The RANKL-OPG system in clinical periodontology. Journal of Clinical Periodontology. 39: 239-248 (2012)

    Article  CAS  Google Scholar 

  • Bostanci N, Ilgenli T, Emingli G, Afacan B, Han B, Toz H, Berdeli A, Atilla G, McKay IJ, Hughes FJ, Belibasakis GN. Differential expression of receptor activator of nuclear factor-κB ligand and osteoprotegerin mRNA in periodontal diseases. Journal of Periodontal Research. 42: 287-293 (2007)

    Article  CAS  Google Scholar 

  • Buxton R. Blood agar plates and hemolysis protocols. American Society for Microbiology. 1–9 (2005)

  • Choi Y, Park E, Kim S, Ha J, Oh H, Kim Y, Choi KH. Alleviation of periodontal disease using Lactobacillus curvatus SMFM2016-NK. Journal of Functional Foods. 83: 104531 (2021a)

    Article  CAS  Google Scholar 

  • Choi Y, Park E, Kim S, Ha J, Oh H, Kim Y, Choi KH. Fermented milk with Lactobacillus curvatus SMFM2016-NK alleviates periodontal and gut inflammation, and alters oral and gut microbiota. Journal of Dairy Science. 104: 5197-5207 (2021b)

    Article  CAS  Google Scholar 

  • Chu ZX, Chen HQ, Ma YL, Zhou YK, Zhang M, Zhang P, Qin HL. Lactobacillus plantarum prevents the upregulation of adhesion molecule expression in an experimental colitis model. Digestive Diseases and Sciences. 55: 2505-2513 (2010)

    Article  CAS  Google Scholar 

  • FAO, WHO. Guidelines for the evaluation of probiotics in food, report of a joint FAO/WHO working group on drafting guideline for the evaluation of probiotic in food. World Health Organization, Geneva. (2002).

  • Gatej SM, Marino V, Bright R, Fitzsimmons TR, Gully N, Zilm P, Bartold PM. Probiotic Lactobacillus rhamnosus GG prevents alveolar bone loss in a mouse model of experimental periodontitis. Journal of Clinical Periodontology. 45: 204-212 (2018)

    Article  CAS  Google Scholar 

  • Grassi F, Cristino S, Toneguzzi S, Piacentini A, Facchini A, Lisignoli G. CXCL12 chemokine up‐regulates bone resorption and MMP‐9 release by human osteoclasts: CXCL12 levels are increased in synovial and bone tissue of rheumatoid arthritis patients. Journal of Cellular Physiology. 199: 244-251 (2004)

    Article  CAS  Google Scholar 

  • Hosokawa Y, Hosokawa I, Ozaki K, Nakae H, Matsuo T. Cytokines differentially regulate ICAM‐1 and VCAM‐1 expression on human gingival fibroblasts. Clinical & Experimental Immunology. 144: 494-502 (2006)

    Article  CAS  Google Scholar 

  • Kitamoto S, Nagoa-Kitamoto H, Hein R, Schmidt TM, Kamada N. (2020). The bacterial connection between the oral cavity and the gut diseases. Journal of Dental Research. 99: 1021–1029 (2020)

    Article  CAS  Google Scholar 

  • Kim H., Kim J-S, Kim Y, Jeong Y, Kim J-E, Paek N-S, Kang C-H. Antioxidant and probiotic properties of Lactobacilli and Bifidobacteria of human origins. Biotechnology and Bioprocess Engineering. 25: 421-430 (2020)

    Article  CAS  Google Scholar 

  • Kim S, Choi S-I, Kim G-H, Imm J-Y. Anti-inflammatory effect of Ecklonia cava extract on Porphyromonas gingivalis lipopolysaccharide-stimulated macrophages and a periodontitis rat model. Nutrients 11: 1143 (2019)

    Article  CAS  Google Scholar 

  • Klare I, Konstabel C, Müller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, Swings J, Goossens H, Witte W. Evaluation of new broth media for microdilution antibiotic susceptibility testing of lactobacilli, pediococci, lactococci, and bifidobacteria. Applied and Environmental Microbiology. 71: 8982-8986 (2005)

    Article  CAS  Google Scholar 

  • Kobayashi R, Kobayashi T, Sakai F, Hosoya T, Yamamoto M, Kurita-Ochiai T. Oral administration of Lactobacillus gasseri SBT2055 is effective in preventing Porphyromonas gingivalis-accelerated periodontal disease. Scientific Reports. 7: 1-10 (2017)

    Article  Google Scholar 

  • Makela M, Salo T, Uitto V-J, Larjava H. Matrix metalloproteinases (MMP-2 andMMP-9) of the oral cavity: cellular originand relationship to periodontal status. Journal of Dental Research.73: 1397–1406 (1994)

    Article  CAS  Google Scholar 

  • Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E. Probiotic potential of Lactobacillus strains isolated from dairy products. International Dairy Journal 16: 189-199 (2006)

    Article  CAS  Google Scholar 

  • Morton RS, Dongari‐Bagtzoglou AI. Cyclooxygenase‐2 is upregulated in inflamed gingival tissues. Journal of Periodontology. 72: 461-469 (2001)

    Article  CAS  Google Scholar 

  • Nagashima H, Shinoda M, Honda K, Kamio N, Hasuike A, Sugano N, Iwata K. CXCR4 signaling contributes to alveolar bone resorption in Porphyromonas gingivalis-induced periodontitis in mice. Journal of Oral Science. 59: 571-577 (2017)

    Article  Google Scholar 

  • Offenbacher S, Heasman PA, Collins JG. Modulation of host PGE2 secretion as a determinant of periodontal disease expression. Journal of Periodontology. 64: 432-444 (1993)

    CAS  PubMed  Google Scholar 

  • Oliveira LF, Salvador SL, Silva PH, Furlaneto FA, Figueiredo L, Casarin R, Messora MR. Benefits of Bifidobacterium animalis subsp. lactis probiotic in experimental periodontitis. Journal of Periodontology. 88: 197-208 (2017)

    Article  Google Scholar 

  • Shokryazdan P, Faseleh JM, Liang JB, Kalavathy R, Sieo CC, Ho YW. Safety assessment of two new Lactobacillus strains as probiotic for human using a rat model. PLoS ONE, 11: e0159851 (2016)

    Article  Google Scholar 

  • Sorsa T, Tervahartiala T, Leppilahti J, Hernandez M, Gamonal J, Tuomainen AM, Lauhio A, Pussinen PJ, Mäntylä, P. Collagenase-2 (MMP-8) as a point-of-care biomarker in periodontitis and cardiovascular diseases. Therapeutic response to non-antimicrobial properties of tetracyclines. Pharmacological Research. 63: 108-113 (2011)

    Article  CAS  Google Scholar 

  • Sun J, Nemoto E, Hong G, Sasaki K. Modulation of stromal cell-derived factor 1 alpha (SDF-1α) and its receptor CXCR4 in Porphyromonas gingivalis-induced periodontal inflammation. BMC Oral Health. 17: 1-8 (2017)

    Article  Google Scholar 

  • Sun Y, Shu R, Li CL, Zhang MZ. Gram‐negative periodontal bacteria induce the activation of Toll‐like receptors 2 and 4, and cytokine production in human periodontal ligament cells. Journal of Periodontology. 81: 1488-1496 (2010)

    Article  CAS  Google Scholar 

  • Szkaradkiewicz AK, Stopa J, Karpiński TM. Effect of oral administration involving a probiotic strain of Lactobacillus reuteri on pro-inflammatory cytokine response in patients with chronic periodontitis. Archivum Immunologiae et Therapiae Experimentalis. 62: 495-500 (2014)

    Article  CAS  Google Scholar 

  • Teame T, Wang A, Xie M, Zhang Z, Yang Y, Ding Q, Zhou Z. Paraprobiotics and postbiotics of probiotic Lactobacilli, their positive effects on the host and action mechanisms: A review. Frontiers in nutrition. 7. (2020)

  • Teng YTA, Nguyen H, Gao X, Kong YY, Gorczynski RM, Singh B, Penninger JM. Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. The Journal of Clinical Investigation. 106: R59-R67 (2000).

    Article  CAS  Google Scholar 

  • Terán LC, Coeuret G, Raya R, Zagorec M, Champomier-Vergès MC, Chaillou S. Phylogenomic analysis of Lactobacillus curvatus reveals two lineages distinguished by genes for fermenting plant-derived carbohydrates. Genome Biology and Evolution 10: 1516-1525 (2018)

    Article  Google Scholar 

  • Tokatlı M, Gülgör G, Bağder Elmacı S, Arslankoz İşleyen N, Özçelik F. In vitro properties of potential probiotic indigenous lactic acid bacteria originating from traditional pickles. BioMed Research International. Article ID 315819 (2015)

  • Wang PL, Azuma Y, Shinohara M, Ohura K. Toll-like receptor 4-mediated signal pathway induced by Porphyromonas gingivalis lipopolysaccharide in human gingival fibroblasts. Biochemical and Biophysical Research Communications. 273: 1161–1167 (2000)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was financially supported by the Ministry of Small and Medium Sized Enterprises (SEMs) and Startups (MSS), Korea, under the “Regional Star-Enterprise Development Program (R&D, S2908142)” supervised by the Korea Institute for Advancement of Technology (KIAT)

Author information

Authors and Affiliations

  1. Kookmin University, Seoul, Republic of Korea

    Jae-In Jung, Yong Gyeong Kim, Chang-Ho Kang & Jee-Young Imm

  2. Mediogen, Co., Ltd., Jecheon, 27159, Korea

    Yong Gyeong Kim & Chang-Ho Kang

Authors
  1. Jae-In Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yong Gyeong Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chang-Ho Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jee-Young Imm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jee-Young Imm.

Ethics declarations

Conflicts of interest

YongGyeong Kim and Chang-Ho Kang are employees of Mediogen. The authors declare that they had no role in the design of the study; in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jung, JI., Kim, Y.G., Kang, CH. et al. Effects of Lactobacillus curvatus MG5246 on inflammatory markers in Porphyromonas gingivalis lipopolysaccharide-sensitized human gingival fibroblasts and periodontitis rat model. Food Sci Biotechnol 31, 111–120 (2022). https://doi.org/10.1007/s10068-021-01009-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-021-01009-4

Keywords

Search

Navigation