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Lactiplantibacillus plantarum EIR/IF-1 Kaynaklı Biyotiklerin Periodontal İnflamasyonun Modülasyonu Üzerindeki Etkileri

Year 2025, Volume: 11 Issue: 1, 1 - 15, 30.04.2025

Abstract

Amaç: Bu çalışma, bebek fekal mikrobiyotasından izole edilen Lactiplantibacillus plantarum EIR/IF-1 suşundan elde edilen postbiyotiklerin ve paraprobiyotiklerin immünmodülatör etkilerini araştırmayı amaçlamaktadır.

Materyal ve Yöntem: İnsan periodontal ligament fibroblast (iPDLF) hücreleri, Lactiplantibacillus plantarum EIR/IF-1 kaynaklı salınan ve bağlı formlarda bulunan eksopolizakkaritler (10–1.000 μg/mL), hücre lizatı (0,1–1.000 μg/mL), hücre yüzeyi proteinleri (0,1–100 μg/mL) ve inaktif hücreler (10⁶–10¹⁰ KOB/mL) ile 24 saat süreyle birlikte inkübe edilmiştir. Hücre canlılığı MTT testi ile değerlendirilmiştir. Periodontal hastalıkla ilişkili önemli bir patojen olan Porphyromonas gingivalis’ten elde edilen lipopolisakkarit (LPS), iPDLF hücrelerinde inflamasyonu indüklemek için kullanılmıştır. Biyotiklerin, LPS ile uyarılmış iPDLF hücrelerinde sitokin üretimine olan etkisi, toksik olmayan dozlarla birlikte inkübasyon neticesinde test edilmiştir. Sitokin seviyeleri (IL-10, IL-8 ve IFN-γ) ELİZA protokolü ile belirlenmiştir.

Bulgular: Hücreler 1 µg/mL LPS ve toksik etkisi olmayan seçilen biyotik dozları ile 24 saat inkübe edildikten sonra, P. gingivalis kaynaklı LPS’nin IL-8 üretimini indüklediği gözlemlenmiştir. Ancak, EIR/IF-1 suşundan elde edilen biyotikler, IL-8 üretimini önemli ölçüde azaltmıştır (p<0.0001). Ayrıca, bu biyotikler anti-inflamatuvar bir sitokin olan IL-10 üretimini artırmıştır (p<0.0001).

Sonuç: Elde edilen veriler, biyotiklerin LPS’nin oluşturduğu pro-inflamatuvar etkileri azaltabilecek potansiyele sahip olduğunu göstermektedir. Bu bulgular, biyolojik olarak aktif ve etkin bileşenler içeren postbiyotikler ve paraprobiyotiklerin periodontal inflamasyonu azaltmak ve önlemek için umut verici, doğal ve güvenilir bir yaklaşım olarak kullanılabileceğini vurgulamaktadır. Sonuç olarak, mikrobiyota kaynaklı biyotiklerin periodontal hastalıkların yönetiminde etkili yardımcı bir tedavi olarak kullanılabileceği önerilmektedir.

Project Number

TÜBİTAK 119S865

References

  • Chen MX, Zhong YJ, Dong QQ, Wong HM, Wen YF. Global, regional, and national burden of severe periodontitis, 1990- 2019: An analysis of the Global Burden of Disease Study 2019. J Clin Periodontol. 2021;48(9):1165-88. doi: 10.1111/ jcpe.13506.
  • Internet: Global oral health status report, Towards universal health coverage for oral health by 2030. URL: https://www.who.int/ team/noncommunicable-diseases/globalstatus- report-on-oral-health-2022
  • Wu CZ, Yuan YH, Liu HH, et al. Epidemiologic relationship between periodontitis and type 2 diabetes mellitus. BMC Oral Health. 2020;20(1):204. doi: 10.1186/s12903-020-01180-w.
  • Hajishengallis G, Chavakis T. Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities. Nat Rev Immunol. 2021;21(7):426-40. doi: 10.1038/s41577-020-00488-6.
  • Gotsman I, Lotan C, Soskolne WA, et al. Periodontal destruction is associated with coronary artery disease and periodontal infection with acute coronary syndrome. J Periodontol. 2007;78(5):849-58. doi: 10.1902/jop.2007.060301.
  • Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases. Nat Rev Dis Primers. 2017;3:17038. doi: 10.1038/nrdp.2017.38.
  • Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366(9499):1809-1820. doi: 10.1016/ S0140-6736(05)67728-8.
  • Martínez-García M, Hernández-Lemus E. Periodontal inflammation and systemic diseases: An Overview. Front Physiol. 2021;12:709438. doi: 10.3389/ fphys.2021.709438.
  • Aggarwal S, Sabharwal V, Kaushik P, Joshi A, Aayushi A, Suri M. Postbiotics: From emerging concept to application. Front Sustain Food Syst. 2022; 6:887642. doi: 10.3389/fsufs.2022.887642
  • Nataraj BH, Ali SA, Behare PV, Yadav H. Postbiotics-parabiotics: the new horizons in microbial biotherapy and functional foods. Microb Cell Fact. 2020;19(1):168. doi: 10.1186/s12934-020-01426-w.
  • Tsilingiri K, Rescigno M. Postbiotics: what else? Benef Microbes. 2013;4(1):101-7. doi: 10.3920/BM2012.0046.
  • Aguilar-Toalá JE, Garcia-Varela R, Garcia HS, et al. Postbiotics: An evolving term within the functional foods field. Trends Food Sci Technol. 2018;75:105-114. doi: 10.1016/j.tifs.2018.03.009.
  • Teame T, Wang A, Xie M, et al. Paraprobiotics and postbiotics of probiotic Lactobacilli, their positive effects on the host and action mechanisms: A review. Front Nutr. 2020;7:570344. doi:10.3389/ fnut.2020.570344.
  • Żółkiewicz J, Marzec A, Ruszczyński M, Feleszko W. Postbiotics-a step beyond preand probiotics. Nutrients. 2020;12(8):2189. doi: 10.3390/nu12082189.
  • Taverniti V, Guglielmetti S. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr. 2011;6(3):261-74. doi: 10.1007/s12263-011-0218-x.
  • OmerOglou E, Karaca B, Kibar H, Haliscelik O, Kiran F. The role of microbiota-derived postbiotic mediators on biofilm formation and quorum sensing-mediated virulence of Streptococcus mutans: A perspective on preventing dental caries. Microb Pathog. 2022;164:105390. doi: 10.1016/j. micpath.2022.105390.
  • Karaca B, Haliscelik O, Gursoy M, et al. Analysis of chemical structure and antibiofilm properties of exopolysaccharides from Lactiplantibacillus plantarum EIR/IF-1 postbiotics. Microorg. 2022;10(11):2200. doi: 10.3390/microorganisms10112200.
  • Karaca B, Gursoy M, Kiran F, Loimaranta V, Söderling E, Gursoy UK. Postbiotics of the Lactiplantibacillus plantarum EIR/ IF-1 Strain show antimicrobial activity against oral microorganisms with ph adaptation capability. MicrobiolRes. 2023;14(3):1442-56. https://doi. org/10.3390/microbiolres14030098.
  • Todorov S, Onno B, Sorokine O, Chobert JM, Ivanova I, Dousset X. Detection and characterization of a novel antibacterial substance produced by Lactobacillus plantarum ST 31 isolated from sourdough. Int J Food Microbiol. 1999;48(3):167-77. doi: 10.1016/s0168-1605(99)00048-3.
  • Ou CC, Lin SL, Tsai JJ, Lin MY. Heatkilled lactic acid bacteria enhance immunomodulatory potential by skewing the immune response toward Th1 polarization. J Food Sci. 2011;76(5):260-267. doi: 10.1111/j.1750-3841.2011.02161.x.
  • Duché O, Trémoulet F, Glaser P, Labadie J. Salt stress proteins induced in Listeria monocytogenes. Appl Environ Microbiol. 2002;68(4):1491-8. doi: 10.1128/ AEM.68.4.1491-1498.2002.
  • Tallon R, Bressollier P, Urdaci MC. Isolation and characterization of two exopolysaccharides produced by Lactobacillus plantarum EP56. Res Microbiol. 2003;154(10):705-12. doi: 10.1016/j.resmic.2003.09.006.
  • Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F. A colorimetric method for the determination of sugars. Nature. 1951;168(4265):167. doi: 10.1038/168167a0.
  • Johnson B, Selle K, O'Flaherty S, Goh YJ, Klaenhammer T. Identification of extracellular surface-layer associated proteins in Lactobacillus acidophilus NCFM. Microbiol. 2013;159(11):2269-82. doi: 10.1099/mic.0.070755-0.
  • Kibar H, Arslan YE, Ceylan A, Karaca B, Haliscelik O, Kiran F. Weissella cibaria EIR/P2-derived exopolysaccharide: A novel alternative to conventional biomaterials targeting periodontal regeneration. Int J Biol Macromol. 2020;165:2900-8. doi: 10.1016/j. ijbiomac.2020.10.106.
  • Denizot F, Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods. 1986;89(2):271-7. doi: 10.1016/0022-1759(86)90368-6.
  • Liu J, Tang X, Li C, et al. Porphyromonas gingivalis promotes the cell cycle and inflammatory cytokine production in periodontal ligament fibroblasts. Arch Oral Biol. 2015;60(8):1153-61. doi: 10.1016/j. archoralbio.2015.05.004.
  • Dixon DR, Darveau RP. Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid a structure. J Dent Res. 2005;84(7):584-95. doi: 10.1177/154405910508400702.
  • Herath TD, Wang Y, Seneviratne CJ, Darveau RP, Wang CY, Jin L. The expression and regulation of matrix metalloproteinase-3 is critically modulated by Porphyromonas gingivalis lipopolysaccharide with heterogeneous lipid A structures in human gingival fibroblasts. BMC Microbiol. 2013;13:73. doi: 10.1186/1471-2180-13-73.
  • Zhang Y, Ding Y, Guo Q. Probiotic species in the management of periodontal diseases: An overview. Front Cell Infect Microbiol. 2022;12:806463. doi: 10.3389/ fcimb.2022.806463.
  • Singh D, Singh A, Kumar S. Probiotics: friend or foe to the human immune system. Bull Natl Res Cent. 2023;47:126. doi:10.1186/ s42269-023-01098-7.
  • Tezuka H, Ohteki T. Regulation of IgA Production by ıntestinal dendritic cells and related cells. Front Immunol. 2019;10:1891. doi: 10.3389/fimmu.2019.01891.
  • 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. Sci Rep. 2017;7(1):545. doi: 10.1038/s41598-017-00623-9.
  • Chen X, Daliri EB, Kim N, Kim JR, Yoo D, Oh DH. Microbial etiology and prevention of dental caries: Exploiting natural products to ınhibit cariogenic biofilms. Pathogens. 2020;9(7):569. doi: 10.3390/ pathogens9070569.
  • Moraes RM, Schlagenhauf U, Anbinder AL. Outside the limits of bacterial viability: Postbiotics in the management of periodontitis. Biochem Pharmacol. 2022;201:115072. doi: 10.1016/j.bcp.2022.115072.
  • Favero C, Giordano L, Mihaila SM, Masereeuw R, Ortiz A, Sanchez-Niño MD. Postbiotics and Kidney Disease. Toxins. 2022;14(9):623. doi: 10.3390/ toxins14090623.
  • Cuevas-González PF, Liceaga AM, Aguilar- Toalá JE. Postbiotics and paraprobiotics: From concepts to applications. Food Res Int. 2020;136:109502. doi: 10.1016/j. foodres.2020.109502.
  • Wells JM. Immunomodulatory mechanisms of lactobacilli. Microb Cell Fact. 2011;10(1):17. doi: 10.1186/1475-2859-10- S1-S17.
  • Du X, Rodriguez J, Wee J. Dietary postbiotics reduce cytotoxicity and inflammation induced by crystalline silica in an in vitro RAW 264.7 Macrophage Model. Foods. 2022;11(6):877. doi: 10.3390/foods11060877.
  • Gao K, Wang C, Liu L, et al. Immunomodulation and signaling mechanism of Lactobacillus rhamnosus GG and its components on porcine intestinal epithelial cells stimulated by lipopolysaccharide. J Microbiol Immunol Infect. 2017;50(5):700-13. doi: 10.1016/j. jmii.2015.05.002.
  • De Marco S, Sichetti M, Muradyan D, et al. Probiotic cell-free supernatants exhibited anti-ınflammatory and antioxidant activity on human gut epithelial cells and macrophages stimulated with LPS. Evid Based Complement Alternat Med. 2018;2018:1756308. doi: 10.1155/2018/1756308.
  • Jensen GS, Benson KF, Carter SG, Endres JR. GanedenBC30 cell wall and metabolites: anti-inflammatory and immune modulating effects in vitro. BMC Immunol. 2010;11:15. doi: 10.1186/1471-2172-11-15.
  • Hoarau C, Martin L, Faugaret D, et al. Supernatant from bifidobacterium differentially modulates transduction signaling pathways for biological functions of human dendritic cells. PLoS One. 2008;3(7):e2753. doi: 10.1371/journal.pone.0002753.
  • Ohlrich EJ, Cullinan MP, Seymour GJ. The immunopathogenesis of periodontal disease. Aust Dent J. 2009;54(1):2-10. doi: 10.1111/j.1834-7819.2009.01139.x.
  • Taylor JJ. Cytokine regulation of immune responses to Porphyromonas gingivalis. Periodontol 2000. 2010;54(1):160-94. doi: 10.1111/j.1600-0757.2009.00344.x.
  • Giorgetti G, Brandimarte G, Fabiocchi F, et al. Interactions between innate immunity, microbiota, and probiotics. J Immunol Res. 2015;2015:501361. doi: 10.1155/2015/501361.
  • Canonici A, Siret C, Pellegrino E, et al. Saccharomyces boulardii improves intestinal cell restitution through activation of the α2β1 integrin collagen receptor. PLoS One. 2011;6(3):e18427. doi: 10.1371/journal. pone.0018427.
  • Castro-Bravo N, Wells JM, Margolles A, Ruas-Madiedo P. Interactions of surface exopolysaccharides peptidoglycan-derived muropeptide. Gut. 2011;60(8):1050-9. doi: 10.1136/gut.2010.232918.
  • Mohamadzadeh M, Pfeiler EA, Brown JB, et al. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA. 2011;108(1):4623-30. doi: 10.1073/pnas.1005066107.
  • Noh SY, Kang SS, Yun CH, Han SH. Lipoteichoic acid from Lactobacillus plantarum inhibits Pam2CSK4-induced IL-8 production in human intestinal epithelial cells. Mol Immunol. 2015;64(1):183-9. doi: 10.1016/j.molimm.2014.11.014.
  • Chandhni PR, Pradhan D, Sowmya K, et al. Ameliorative effect of surface proteins of probiotic Lactobacilli in colitis mouse models. Front Microbiol. 2021;12:679773. doi: 10.3389/fmicb.2021.679773.
  • Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G. Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J. 2006;30(2):55-60.
  • Vivekananda MR, Vandana KL, Bhat KG. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: A preliminary randomized clinical trial. J Oral Microbiol. 2010;2:5344. doi: 10.3402/jom.v2i0.5344.
  • Amizic IP, Cigić L, Gavić L, Radić M, Barišić IG. Antimicrobial efficacy of probiotic-containing toothpastes: An in vitro evaluation. Med Glas. 2017;14:139-44. doi: 10.17392/870-16.
  • Kuru BE, Laleman I, Yalnızoğlu T, Kuru L, Teughels W. The influence of a Bifidobacterium animalis probiotic on gingival health: A randomized controlled clinical trial. J Periodontol. 2017;88:1115- 23. doi: 10.1902/jop.2017.170213.
  • Zhang Y, Pu F, Cheng R, et al. Effect of heatinactivated Lactobacillus paracasei N1115 on microbiota and gut-brain axis related molecules. Biosci Microbiota Food Health. 2020;39(3):89-99. doi: 10.12938/ bmfh.2019-025.
  • Chuang L, Wu KG, Pai C, et al. Heat-killed cells of lactobacilli skew the immune response toward T helper 1 polarization in mouse splenocytes and dendritic cell-treated T cells. J Agric Food Chem. 2007;55(26):11080-6. doi: 10.1021/jf071786o.
  • Kaczynska A, Klosinska M, Janeczek K, Zarobkiewicz M, Emeryk A. Promising immunomodulatory effects of bacterial lysates in allergic diseases. Front Immunol. 2022;13:907149. doi: 10.3389/ fimmu.2022.907149.
  • Coviello S, Wimmenauer V, Polack FP, Irusta PM. Bacterial lysates improve the protective antibody response against respiratory viruses through Toll-like receptor 4. Hum Vaccin Immunother. 2014;10(10):2896-902. doi: 10.4161/hv.29784.
  • Shida K, Kiyoshima-Shibata J, Kaji R, Nagaoka M, Nanno M. Peptidoglycan from lactobacilli inhibits interleukin-12 production by macrophages induced by Lactobacillus casei through Toll-like receptor 2-dependent and independent mechanisms. Immunology. 2009;128:e858-69. doi: 10.1111/j.1365- 2567.2009.03095.x.
  • Macho Fernandez E, Valenti V, Rockel C, et al. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut. 2011;60(8):1050-9. doi: 10.1136/ gut.2010.232918.
  • Mohamadzadeh M, Pfeiler EA, Brown JB, et al. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA. 2011;108(1):4623-30. doi: 10.1073/pnas.1005066107.
  • Noh SY, Kang SS, Yun CH, Han SH. Lipoteichoic acid from Lactobacillus plantarum inhibits Pam2CSK4-induced IL-8 production in human intestinal epithelial cells. Mol Immunol. 2015;64(1):183-9. doi: 10.1016/j.molimm.2014.11.014.
  • Chandhni PR, Pradhan D, Sowmya K, et al. Ameliorative effect of surface proteins of probiotic Lactobacilli in colitis mouse models. Front Microbiol. 2021;12:679773. doi: 10.3389/fmicb.2021.679773.
  • Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G. Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J. 2006;30(2):55-60.
  • Vivekananda MR, Vandana KL, Bhat KG. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: A preliminary randomized clinical trial. J Oral Microbiol. 2010;2:5344. doi: 10.3402/jom.v2i0.5344.
  • Amizic IP, Cigić L, Gavić L, Radić M, Barišić IG. Antimicrobial efficacy of probiotic-containing toothpastes: An in vitro evaluation. Med Glas. 2017;14:139-44. doi: 10.17392/870-16.
  • Kuru BE, Laleman I, Yalnızoğlu T, Kuru L, Teughels W. The influence of a Bifidobacterium animalis probiotic on gingival health: A randomized controlled clinical trial. J Periodontol. 2017;88:1115- 23. doi: 10.1902/jop.2017.170213.

The Effects of Biotics Derived from Lactiplantibacillus plantarum EIR/IF-1 on the Modulation of Periodontal Inflammation

Year 2025, Volume: 11 Issue: 1, 1 - 15, 30.04.2025

Abstract

Objective: This study aims to investigate the immunomodulatory effects of postbiotics and paraprobiotics derived from Lactiplantibacillus plantarum EIR/IF-1, isolated from infant fecal microbiota.

Materials and Methods: Human periodontal ligament fibroblast (hPDLF) cells were co-incubated with the release and bound forms of exopolysaccharides (10-1,000 μg/mL), cell lysate (0.1-1,000 μg/mL), cell surface proteins (0.1-100 μg/mL), and inactivated cells (10⁶-10¹⁰ CFU/mL) derived from Lactiplantibacillus plantarum EIR/IF-1 for 24 hours. Cell viability was assessed using the MTT assay. Lipopolysaccharide (LPS) from Porphyromonas gingivalis, a key pathogen involved in periodontal disease, was used to induce inflammation in hPDLF cells. Non-toxic doses of the biotics were subsequently tested for their impact on cytokine production in LPS induced hPDLF cells. Cytokine levels (IL-10, IL-8, and IFN-γ) were quantified using the ELISA protocol.

Results: After 24 hours incubation of hPDLF cells with 1 µg/mL LPS and selected concentrations of the biotics derived from the EIR/IF-1 strain that did not exhibit toxic effects, it was observed that LPS from P. gingivalis induced IL-8 production. However, the biotics extracted from the EIR/IF-1 strain significantly reduced IL-8 production (p<0.0001). Furthermore, these biotics increased the production of the anti-inflammatory cytokine IL-10 (p<0.0001).

Conclusion: The obtained data suggest that the biotics have the potential to counteract the pro-inflammatory effects induced by LPS. The findings highlight the potential of postbiotics and paraprobiotics, containing biologically active and effective components, as a promising natural and reliable approach for reducing and preventing periodontal inflammation. In conclusion, our results suggest that microbiota-derived biotics could serve as effective adjuncts in the management of periodontal diseases.

Project Number

TÜBİTAK 119S865

References

  • Chen MX, Zhong YJ, Dong QQ, Wong HM, Wen YF. Global, regional, and national burden of severe periodontitis, 1990- 2019: An analysis of the Global Burden of Disease Study 2019. J Clin Periodontol. 2021;48(9):1165-88. doi: 10.1111/ jcpe.13506.
  • Internet: Global oral health status report, Towards universal health coverage for oral health by 2030. URL: https://www.who.int/ team/noncommunicable-diseases/globalstatus- report-on-oral-health-2022
  • Wu CZ, Yuan YH, Liu HH, et al. Epidemiologic relationship between periodontitis and type 2 diabetes mellitus. BMC Oral Health. 2020;20(1):204. doi: 10.1186/s12903-020-01180-w.
  • Hajishengallis G, Chavakis T. Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities. Nat Rev Immunol. 2021;21(7):426-40. doi: 10.1038/s41577-020-00488-6.
  • Gotsman I, Lotan C, Soskolne WA, et al. Periodontal destruction is associated with coronary artery disease and periodontal infection with acute coronary syndrome. J Periodontol. 2007;78(5):849-58. doi: 10.1902/jop.2007.060301.
  • Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases. Nat Rev Dis Primers. 2017;3:17038. doi: 10.1038/nrdp.2017.38.
  • Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366(9499):1809-1820. doi: 10.1016/ S0140-6736(05)67728-8.
  • Martínez-García M, Hernández-Lemus E. Periodontal inflammation and systemic diseases: An Overview. Front Physiol. 2021;12:709438. doi: 10.3389/ fphys.2021.709438.
  • Aggarwal S, Sabharwal V, Kaushik P, Joshi A, Aayushi A, Suri M. Postbiotics: From emerging concept to application. Front Sustain Food Syst. 2022; 6:887642. doi: 10.3389/fsufs.2022.887642
  • Nataraj BH, Ali SA, Behare PV, Yadav H. Postbiotics-parabiotics: the new horizons in microbial biotherapy and functional foods. Microb Cell Fact. 2020;19(1):168. doi: 10.1186/s12934-020-01426-w.
  • Tsilingiri K, Rescigno M. Postbiotics: what else? Benef Microbes. 2013;4(1):101-7. doi: 10.3920/BM2012.0046.
  • Aguilar-Toalá JE, Garcia-Varela R, Garcia HS, et al. Postbiotics: An evolving term within the functional foods field. Trends Food Sci Technol. 2018;75:105-114. doi: 10.1016/j.tifs.2018.03.009.
  • Teame T, Wang A, Xie M, et al. Paraprobiotics and postbiotics of probiotic Lactobacilli, their positive effects on the host and action mechanisms: A review. Front Nutr. 2020;7:570344. doi:10.3389/ fnut.2020.570344.
  • Żółkiewicz J, Marzec A, Ruszczyński M, Feleszko W. Postbiotics-a step beyond preand probiotics. Nutrients. 2020;12(8):2189. doi: 10.3390/nu12082189.
  • Taverniti V, Guglielmetti S. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr. 2011;6(3):261-74. doi: 10.1007/s12263-011-0218-x.
  • OmerOglou E, Karaca B, Kibar H, Haliscelik O, Kiran F. The role of microbiota-derived postbiotic mediators on biofilm formation and quorum sensing-mediated virulence of Streptococcus mutans: A perspective on preventing dental caries. Microb Pathog. 2022;164:105390. doi: 10.1016/j. micpath.2022.105390.
  • Karaca B, Haliscelik O, Gursoy M, et al. Analysis of chemical structure and antibiofilm properties of exopolysaccharides from Lactiplantibacillus plantarum EIR/IF-1 postbiotics. Microorg. 2022;10(11):2200. doi: 10.3390/microorganisms10112200.
  • Karaca B, Gursoy M, Kiran F, Loimaranta V, Söderling E, Gursoy UK. Postbiotics of the Lactiplantibacillus plantarum EIR/ IF-1 Strain show antimicrobial activity against oral microorganisms with ph adaptation capability. MicrobiolRes. 2023;14(3):1442-56. https://doi. org/10.3390/microbiolres14030098.
  • Todorov S, Onno B, Sorokine O, Chobert JM, Ivanova I, Dousset X. Detection and characterization of a novel antibacterial substance produced by Lactobacillus plantarum ST 31 isolated from sourdough. Int J Food Microbiol. 1999;48(3):167-77. doi: 10.1016/s0168-1605(99)00048-3.
  • Ou CC, Lin SL, Tsai JJ, Lin MY. Heatkilled lactic acid bacteria enhance immunomodulatory potential by skewing the immune response toward Th1 polarization. J Food Sci. 2011;76(5):260-267. doi: 10.1111/j.1750-3841.2011.02161.x.
  • Duché O, Trémoulet F, Glaser P, Labadie J. Salt stress proteins induced in Listeria monocytogenes. Appl Environ Microbiol. 2002;68(4):1491-8. doi: 10.1128/ AEM.68.4.1491-1498.2002.
  • Tallon R, Bressollier P, Urdaci MC. Isolation and characterization of two exopolysaccharides produced by Lactobacillus plantarum EP56. Res Microbiol. 2003;154(10):705-12. doi: 10.1016/j.resmic.2003.09.006.
  • Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F. A colorimetric method for the determination of sugars. Nature. 1951;168(4265):167. doi: 10.1038/168167a0.
  • Johnson B, Selle K, O'Flaherty S, Goh YJ, Klaenhammer T. Identification of extracellular surface-layer associated proteins in Lactobacillus acidophilus NCFM. Microbiol. 2013;159(11):2269-82. doi: 10.1099/mic.0.070755-0.
  • Kibar H, Arslan YE, Ceylan A, Karaca B, Haliscelik O, Kiran F. Weissella cibaria EIR/P2-derived exopolysaccharide: A novel alternative to conventional biomaterials targeting periodontal regeneration. Int J Biol Macromol. 2020;165:2900-8. doi: 10.1016/j. ijbiomac.2020.10.106.
  • Denizot F, Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods. 1986;89(2):271-7. doi: 10.1016/0022-1759(86)90368-6.
  • Liu J, Tang X, Li C, et al. Porphyromonas gingivalis promotes the cell cycle and inflammatory cytokine production in periodontal ligament fibroblasts. Arch Oral Biol. 2015;60(8):1153-61. doi: 10.1016/j. archoralbio.2015.05.004.
  • Dixon DR, Darveau RP. Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid a structure. J Dent Res. 2005;84(7):584-95. doi: 10.1177/154405910508400702.
  • Herath TD, Wang Y, Seneviratne CJ, Darveau RP, Wang CY, Jin L. The expression and regulation of matrix metalloproteinase-3 is critically modulated by Porphyromonas gingivalis lipopolysaccharide with heterogeneous lipid A structures in human gingival fibroblasts. BMC Microbiol. 2013;13:73. doi: 10.1186/1471-2180-13-73.
  • Zhang Y, Ding Y, Guo Q. Probiotic species in the management of periodontal diseases: An overview. Front Cell Infect Microbiol. 2022;12:806463. doi: 10.3389/ fcimb.2022.806463.
  • Singh D, Singh A, Kumar S. Probiotics: friend or foe to the human immune system. Bull Natl Res Cent. 2023;47:126. doi:10.1186/ s42269-023-01098-7.
  • Tezuka H, Ohteki T. Regulation of IgA Production by ıntestinal dendritic cells and related cells. Front Immunol. 2019;10:1891. doi: 10.3389/fimmu.2019.01891.
  • 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. Sci Rep. 2017;7(1):545. doi: 10.1038/s41598-017-00623-9.
  • Chen X, Daliri EB, Kim N, Kim JR, Yoo D, Oh DH. Microbial etiology and prevention of dental caries: Exploiting natural products to ınhibit cariogenic biofilms. Pathogens. 2020;9(7):569. doi: 10.3390/ pathogens9070569.
  • Moraes RM, Schlagenhauf U, Anbinder AL. Outside the limits of bacterial viability: Postbiotics in the management of periodontitis. Biochem Pharmacol. 2022;201:115072. doi: 10.1016/j.bcp.2022.115072.
  • Favero C, Giordano L, Mihaila SM, Masereeuw R, Ortiz A, Sanchez-Niño MD. Postbiotics and Kidney Disease. Toxins. 2022;14(9):623. doi: 10.3390/ toxins14090623.
  • Cuevas-González PF, Liceaga AM, Aguilar- Toalá JE. Postbiotics and paraprobiotics: From concepts to applications. Food Res Int. 2020;136:109502. doi: 10.1016/j. foodres.2020.109502.
  • Wells JM. Immunomodulatory mechanisms of lactobacilli. Microb Cell Fact. 2011;10(1):17. doi: 10.1186/1475-2859-10- S1-S17.
  • Du X, Rodriguez J, Wee J. Dietary postbiotics reduce cytotoxicity and inflammation induced by crystalline silica in an in vitro RAW 264.7 Macrophage Model. Foods. 2022;11(6):877. doi: 10.3390/foods11060877.
  • Gao K, Wang C, Liu L, et al. Immunomodulation and signaling mechanism of Lactobacillus rhamnosus GG and its components on porcine intestinal epithelial cells stimulated by lipopolysaccharide. J Microbiol Immunol Infect. 2017;50(5):700-13. doi: 10.1016/j. jmii.2015.05.002.
  • De Marco S, Sichetti M, Muradyan D, et al. Probiotic cell-free supernatants exhibited anti-ınflammatory and antioxidant activity on human gut epithelial cells and macrophages stimulated with LPS. Evid Based Complement Alternat Med. 2018;2018:1756308. doi: 10.1155/2018/1756308.
  • Jensen GS, Benson KF, Carter SG, Endres JR. GanedenBC30 cell wall and metabolites: anti-inflammatory and immune modulating effects in vitro. BMC Immunol. 2010;11:15. doi: 10.1186/1471-2172-11-15.
  • Hoarau C, Martin L, Faugaret D, et al. Supernatant from bifidobacterium differentially modulates transduction signaling pathways for biological functions of human dendritic cells. PLoS One. 2008;3(7):e2753. doi: 10.1371/journal.pone.0002753.
  • Ohlrich EJ, Cullinan MP, Seymour GJ. The immunopathogenesis of periodontal disease. Aust Dent J. 2009;54(1):2-10. doi: 10.1111/j.1834-7819.2009.01139.x.
  • Taylor JJ. Cytokine regulation of immune responses to Porphyromonas gingivalis. Periodontol 2000. 2010;54(1):160-94. doi: 10.1111/j.1600-0757.2009.00344.x.
  • Giorgetti G, Brandimarte G, Fabiocchi F, et al. Interactions between innate immunity, microbiota, and probiotics. J Immunol Res. 2015;2015:501361. doi: 10.1155/2015/501361.
  • Canonici A, Siret C, Pellegrino E, et al. Saccharomyces boulardii improves intestinal cell restitution through activation of the α2β1 integrin collagen receptor. PLoS One. 2011;6(3):e18427. doi: 10.1371/journal. pone.0018427.
  • Castro-Bravo N, Wells JM, Margolles A, Ruas-Madiedo P. Interactions of surface exopolysaccharides peptidoglycan-derived muropeptide. Gut. 2011;60(8):1050-9. doi: 10.1136/gut.2010.232918.
  • Mohamadzadeh M, Pfeiler EA, Brown JB, et al. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA. 2011;108(1):4623-30. doi: 10.1073/pnas.1005066107.
  • Noh SY, Kang SS, Yun CH, Han SH. Lipoteichoic acid from Lactobacillus plantarum inhibits Pam2CSK4-induced IL-8 production in human intestinal epithelial cells. Mol Immunol. 2015;64(1):183-9. doi: 10.1016/j.molimm.2014.11.014.
  • Chandhni PR, Pradhan D, Sowmya K, et al. Ameliorative effect of surface proteins of probiotic Lactobacilli in colitis mouse models. Front Microbiol. 2021;12:679773. doi: 10.3389/fmicb.2021.679773.
  • Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G. Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J. 2006;30(2):55-60.
  • Vivekananda MR, Vandana KL, Bhat KG. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: A preliminary randomized clinical trial. J Oral Microbiol. 2010;2:5344. doi: 10.3402/jom.v2i0.5344.
  • Amizic IP, Cigić L, Gavić L, Radić M, Barišić IG. Antimicrobial efficacy of probiotic-containing toothpastes: An in vitro evaluation. Med Glas. 2017;14:139-44. doi: 10.17392/870-16.
  • Kuru BE, Laleman I, Yalnızoğlu T, Kuru L, Teughels W. The influence of a Bifidobacterium animalis probiotic on gingival health: A randomized controlled clinical trial. J Periodontol. 2017;88:1115- 23. doi: 10.1902/jop.2017.170213.
  • Zhang Y, Pu F, Cheng R, et al. Effect of heatinactivated Lactobacillus paracasei N1115 on microbiota and gut-brain axis related molecules. Biosci Microbiota Food Health. 2020;39(3):89-99. doi: 10.12938/ bmfh.2019-025.
  • Chuang L, Wu KG, Pai C, et al. Heat-killed cells of lactobacilli skew the immune response toward T helper 1 polarization in mouse splenocytes and dendritic cell-treated T cells. J Agric Food Chem. 2007;55(26):11080-6. doi: 10.1021/jf071786o.
  • Kaczynska A, Klosinska M, Janeczek K, Zarobkiewicz M, Emeryk A. Promising immunomodulatory effects of bacterial lysates in allergic diseases. Front Immunol. 2022;13:907149. doi: 10.3389/ fimmu.2022.907149.
  • Coviello S, Wimmenauer V, Polack FP, Irusta PM. Bacterial lysates improve the protective antibody response against respiratory viruses through Toll-like receptor 4. Hum Vaccin Immunother. 2014;10(10):2896-902. doi: 10.4161/hv.29784.
  • Shida K, Kiyoshima-Shibata J, Kaji R, Nagaoka M, Nanno M. Peptidoglycan from lactobacilli inhibits interleukin-12 production by macrophages induced by Lactobacillus casei through Toll-like receptor 2-dependent and independent mechanisms. Immunology. 2009;128:e858-69. doi: 10.1111/j.1365- 2567.2009.03095.x.
  • Macho Fernandez E, Valenti V, Rockel C, et al. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut. 2011;60(8):1050-9. doi: 10.1136/ gut.2010.232918.
  • Mohamadzadeh M, Pfeiler EA, Brown JB, et al. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA. 2011;108(1):4623-30. doi: 10.1073/pnas.1005066107.
  • Noh SY, Kang SS, Yun CH, Han SH. Lipoteichoic acid from Lactobacillus plantarum inhibits Pam2CSK4-induced IL-8 production in human intestinal epithelial cells. Mol Immunol. 2015;64(1):183-9. doi: 10.1016/j.molimm.2014.11.014.
  • Chandhni PR, Pradhan D, Sowmya K, et al. Ameliorative effect of surface proteins of probiotic Lactobacilli in colitis mouse models. Front Microbiol. 2021;12:679773. doi: 10.3389/fmicb.2021.679773.
  • Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G. Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J. 2006;30(2):55-60.
  • Vivekananda MR, Vandana KL, Bhat KG. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: A preliminary randomized clinical trial. J Oral Microbiol. 2010;2:5344. doi: 10.3402/jom.v2i0.5344.
  • Amizic IP, Cigić L, Gavić L, Radić M, Barišić IG. Antimicrobial efficacy of probiotic-containing toothpastes: An in vitro evaluation. Med Glas. 2017;14:139-44. doi: 10.17392/870-16.
  • Kuru BE, Laleman I, Yalnızoğlu T, Kuru L, Teughels W. The influence of a Bifidobacterium animalis probiotic on gingival health: A randomized controlled clinical trial. J Periodontol. 2017;88:1115- 23. doi: 10.1902/jop.2017.170213.
There are 68 citations in total.

Details

Primary Language English
Subjects Periodontics
Journal Section Research Article
Authors

Hikmet Can 0009-0009-8251-1958

Hazal Kibar Demirhan 0000-0002-5188-7698

Emine Omer Oglou 0000-0001-9345-7875

Fadime Kıran 0000-0002-4536-2959

Project Number TÜBİTAK 119S865
Publication Date April 30, 2025
Submission Date December 2, 2024
Acceptance Date February 27, 2025
Published in Issue Year 2025 Volume: 11 Issue: 1

Cite

Vancouver Can H, Kibar Demirhan H, Omer Oglou E, Kıran F. The Effects of Biotics Derived from Lactiplantibacillus plantarum EIR/IF-1 on the Modulation of Periodontal Inflammation. Aydin Dental Journal. 2025;11(1):1-15.

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