Glycerol strengthens probiotic effect of Limosilactobacillus reuteri in oral biofilms: A synergistic synbiotic approach.
ATCC PTA 5289
Limosilactobacillus reuteri
glycerol
periodontitis
probiotic
synbiotics
Journal
Molecular oral microbiology
ISSN: 2041-1014
Titre abrégé: Mol Oral Microbiol
Pays: Denmark
ID NLM: 101524770
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
revised:
13
07
2022
received:
30
03
2022
accepted:
16
08
2022
pubmed:
9
9
2022
medline:
29
11
2022
entrez:
8
9
2022
Statut:
ppublish
Résumé
Both in vitro and in vivo studies have shown that the probiotic Limosilactobacillus reuteri can improve oral health. Limosilactobacillus reuteri species are known to produce the antimicrobial "reuterin" from glycerol. In order to further increase its antimicrobial activity, this study evaluated the effect of the combined use of glycerol and Limosilactobacillus reuteri (ATCC PTA 5289) in view of using a synergistic synbiotic over a probiotic. An antagonistic agar growth and a multispecies biofilm model showed that the antimicrobial potential of the probiotic was significantly enhanced against periodontal pathobionts and anaerobic commensals when supplemented with glycerol. Synbiotic biofilms also showed a significant reduction in inflammatory expression of human oral keratinocytes (HOK-18A), but only when the keratinocytes were preincubated with the probiotic. Probiotic preincubation of keratinocytes or probiotic and synbiotic treatment of biofilms alone was insufficient to significantly reduce inflammatory expression. Overall, this study shows that combining glycerol with the probiotic L. reuteri into a synergistic synbiotic can greatly improve the effectiveness of the latter.
Substances chimiques
Glycerol
PDC6A3C0OX
Anti-Bacterial Agents
0
Anti-Infective Agents
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Pagination
266-275Informations de copyright
© 2022 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Castiblanco, A., Yucel-Lindberg, G., Roos, T., & Twetman, S. (2017). Effect of lactobacillus reuteri on cell viability and PGE2 production in human gingival fibroblasts. Probiotics and Antimicrobial Proteins, 9(3), 278-283. https://doi.org/10.1007/s12602-016-9246-6
Baker, J. L., Tang, X., & Labonte, S. (2022). mucG, mucH, and mucI modulate production of mutanocyclin and reutericyclins in Streptococcus mutans B04Sm5. Journal of Bacteriology, 204(5), e0004222.
Çaglar, E., Kuscu, O. O., Cildir, S. K., Kuvvetli, S. S., & Sandalli, N. (2008). A probiotic lozenge administered medical device and its effect on salivary mutans streptococci and lactobacilli. International Journal of Paediatric Dentistry, 18(1), 35-39. https://doi.org/10.1111/j.1365-263X.2007.00866.x
Dame, Z. T., Aziat, F., Mandal, R., Krishnamurthy, R., Bouatra, S., Borzouie, S., Guo, A. C., Sajed, T., Deng, L., Lin, H., Liu, P., Dong, E., & Wishart, D. S. (2015). The human saliva metabolome. Metabolomics, 11(6), 1864-1883. https://doi.org/10.1007/s11306-015-0840-5
Darveau, R. P. (2010). Periodontitis: A polymicrobial disruption of host homeostasis. Nature Reviews Microbiology, 8(7), 481-490. https://doi.org/10.1038/nrmicro2337
De Weirdt, R., Possemiers, S., Vermeulen, G., Moerdijk-Poortvliet, T. C. W., Boschker, H. T. S., Verstraete, W., & Van De Wiele, T. (2010). Human faecal microbiota display variable patterns of glycerol metabolism. FEMS Microbiology Ecology, 74(3), 601-611. https://doi.org/10.1111/j.1574-6941.2010.00974.x
Dewhirst, F. E., Chen, T., Izard, J., Paster, B. J., Tanner, A. C. R., Yu, W., Lakshmanan, A., & Wade, W. G. (2010). The human oral microbiome. Journal of Bacteriology, 192(19), 5002-5017. https://doi.org/10.1128/JB.00542-10
Engels, C., Schwab, C., Zhang, J., Stevens, M. J. A., Bieri, C., Ebert, M., McNeill, K., Sturla, S. J., & Lacroix, C. (2016). Acrolein contributes strongly to antimicrobial and heterocyclic amine transformation activities of reuterin. Scientific Reports, 6, 36246. https://doi.org/10.1038/srep36246
Ezraty, B., Gennaris, A., Barras, F., & Collet, J. F. (2017). Oxidative stress, protein damage and repair in bacteria. Nature Reviews Microbiology, 15(7), 385-396. https://doi.org/10.1038/nrmicro.2017.26
Finoti, L. S., Nepomuceno, R., Pigossi, S. C., Corbi, S. C., Secolin, R., & Scarel-Caminaga, R. M. (2017). Association between interleukin-8 levels and chronic periodontal disease. Medicine, 96(22), e6932. https://doi.org/10.1097/MD.0000000000006932
Gänzle, M. G. (2004). Reutericyclin: Biological activity, mode of action, and potential applications. Applied Microbiology and Biotechnology, 64(3), 326-332. https://doi.org/10.1007/s00253-003-1536-8
Gibson, G. R., Hutkins, R., Sanders, M. E., Prescott, S. L., Reimer, R. A., Salminen, S. J., Scott, K., Stanton, C., Swanson, K. S., Cani, P. D., Verbeke, K., & Reid, G. (2017). Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nature Reviews Gastroenterology and Hepatology, 14(8), 491-502. https://doi.org/10.1038/nrgastro.2017.75
Graves, D. T., & Cochran, D. (2003). The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. Journal of Periodontology, 74(3), 391-401. https://doi.org/10.1902/jop.2003.74.3.391
Gruner, D., Paris, S., & Schwendicke, F. (2016). Probiotics for managing caries and periodontitis: Systematic review and meta-analysis. Journal of Dentistry, 48, 16-25. https://doi.org/10.1016/j.jdent.2016.03.002
Herrero, E. R., Fernandes, S., Verspecht, T., Ugarte-Berzal, E., Boon, N., Proost, P., Bernaerts, K., Quirynen, M., & Teughels, W. (2018). Dysbiotic biofilms deregulate the periodontal inflammatory response. Journal of Dental Research, 97(5), 547-555. https://doi.org/10.1177/0022034517752675
Herrero, E. R., Slomka, V., Bernaerts, K., Boon, N., Hernandez-sanabria, E., Born, B., Quirynen, M., & Teughels, W. (2016). Antimicrobial effects of commensal oral species are regulated by environmental factors. Journal of Dentistry, 47, 23-33.
Herrero, E. R., Slomka, V., Boon, N., Bernaerts, K., Hernandez-sanabria, E., Quirynen, M., & Teughels, W. (2016). Dysbiosis by neutralizing commensal mediated inhibition of pathobionts. Scientific Reports, 6, 38179. https://doi.org/10.1038/srep38179
Iniesta, M., Herrera, D., Montero, E., Zurbriggen, M., Matos, A. R., Marin, M. J., Sánchez-Beltrán, M. C., Llama-Palacio, A., & Sanz, M. (2012). Probiotic effects of orally administered Lactobacillus reuteri-containing tablets on the subgingival and salivary microbiota in patients with gingivitis. A randomized clinical trial. Journal of Clinical Periodontology, 39, 736-744. https://doi.org/10.1111/j.1600-051X.2012.01914.xProbiotic
Jansen, P. M., Abdelbary, M. M. H., & Conrads, G. (2021). A concerted probiotic activity to inhibit periodontitis-associated bacteria. PLoS ONE, 16(3), e0248308. https://doi.org/10.1371/journal.pone.0248308
Jochum, L., & Stecher, B. (2020). Label or concept - What is a pathobiont? Trends in Microbiology, 28(10), 789-792. https://doi.org/10.1016/j.tim.2020.04.011
Jørgensen, M. R., Keller, M. K., Camilla, K., Hamberg, K., Ericson, D., Nielsen, C. H., & Twetman, S. (2016). Lactobacillus reuteri supplements do not affect salivary IgA or cytokine levels in healthy subjects: A randomized, double-blind, placebo-controlled, cross-over trial. Acta Odontologica Scandinavica, 74(5), 399-404. https://doi.org/10.3109/00016357.2016.1169439
Kang, M. S., Oh, J. S., Lee, H. C., Lim, H. S., Lee, S. W., Yang, K. H., Choi, N.-K., & Kim, S. M. (2011). Inhibitory effect of Lactobacillus reuteri on periodontopathic and cariogenic bacteria. Journal of Microbiology, 49(2), 193-199. https://doi.org/10.1007/s12275-011-0252-9
Keller, M. K., Hasslöf, P., Dahlén, G., & Stecksén-Blicks, C. T. S. (2012). Probiotic supplements (Lactobacillus reuteri DSM 17938 and ATCC PTA 5289) do not affect regrowth of mutans streptococci after full-mouth disinfection with chlorhexidine: A randomized controlled multicenter trial. Caries Research, 46, 140-146. https://doi.org/10.1159/000337098
Kinane, D. F., Stathopoulou, P. G., & Papapanou, P. N. (2017). Periodontal diseases. Nature Reviews Disease Primers, 3, 17038. https://doi.org/10.1038/nrdp.2017.38
Laleman, I., Pauwels, M., Quirynen, M., & Teughels, W. (2019). A dual-strain Lactobacilli reuteri probiotic improves the treatment of residual pockets: A randomized controlled clinical trial. Journal of Clinical Periodontology, 47, 43-53. https://doi.org/10.1111/jcpe.13198
Lamont, R. J., Koo, H., & Hajishengallis, G. (2018). The oral microbiota: Dynamic communities and host interactions. Nature Reviews Microbiology, 16(12), 745-759. https://doi.org/10.1038/s41579-018-0089-x
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods, 25(4), 402-408. https://doi.org/10.1006/meth.2001.1262
Ma, D., Forsythe, P., & Bienenstock, J. (2004). Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infection and Immunity, 72(9), 5308-5314. https://doi.org/10.1128/IAI.72.9.5308
Marsh, P. D. (2018). In sickness and in health - What does the oral microbiome mean to us? An ecological perspective. Advances in Dental Research, 29(1), 60-65. https://doi.org/10.1177/0022034517735295
McFarland, L. V., Evans, C. T., & Goldstein, E. J. C. (2018). Strain-specificity and disease-specificity of probiotic efficacy: A systematic review and meta-analysis. Frontiers in Medicine, 5, 124. https://doi.org/10.3389/fmed.2018.00124
Mu, Q., Tavella, V. J., & Luo, X. M. (2018). Role of Lactobacillus reuteri in human health and diseases. Frontiers in Microbiology, 9, 757. https://doi.org/10.3389/fmicb.2018.00757
Noh, M. K., Jung, M., Kim, S. H., Lee, S. R., Park, K. H., Kim, D. H., Kim, H. H., & Park, Y. G. (2013). Assessment of IL-6, IL-8 and TNF-α levels in the gingival tissue of patients with periodontitis. Experimental and Therapeutic Medicine, 6(3), 847-851. https://doi.org/10.3892/etm.2013.1222
Ouwehand, A. C., Forssten, S., Hibberd, A. A., Lyra, A., & Stahl, B. (2016). Probiotic approach to prevent antibiotic resistance. Annals of Medicine, 48(4), 246-255. https://doi.org/10.3109/07853890.2016.1161232
Penala, S., Kalakonda, B., Pathakota, K., Jayakumar, A., Koppolu, P., Lakshmi, B., Pandey, R., & Mishra, A. (2016). Efficacy of local use of probiotics as an adjunct to scaling and root planing in chronic periodontitis and halitosis: A randomized controlled trial. Journal of Research in Pharmacy Practice, 5(2), 86-93. https://doi.org/10.4103/2279-042x.179568
Ramsey, M. M., & Whiteley, M. (2009). Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proceedings of the National Academy of Sciences of the United States of America, 106(5), 1578-1583. https://doi.org/10.1073/pnas.0809533106
Romani Vestman, N., Hasslöf, P., Keller, M. K., Granström, E., Roos, S., Twetman, S., & Stecksén-Blicks, C. (2013). Lactobacillus reuteri influences regrowth of mutans streptococci after full-mouth disinfection: A double-blind, randomised controlled trial. Caries Research, 47(4), 338-345. https://doi.org/10.1159/000347233
Schaefer, L., Auchtung, T. A., Hermans, K. E., Whitehead, D., Borhan, B., & Britton, R. A. (2010). The antimicrobial compound reuterin (3- hydroxypropionaldehyde) induces oxidative stress via interaction with thiol groups. Microbiology, 156, 1589-1599. https://doi.org/10.1099/mic.0.035642-0
Sliepen, I., Van Damme, J., Van Esshe, M., Loozen, G., Quirynen, M., & Teughels, W. (2009). Microbial interactions influence inflammatory host cell responses. Journal of Dental Research, 88(11), 1026-1030. https://doi.org/10.1177/0022034509347296
Slomka, V., Herrero, E. R., Daep, C., Boon, N., Bernaerts, K., Quirynen, M., & Teughels, W. (2018). Oral prebiotics and the influence of environmental conditions in vitro. Journal of Periodontology, 89, 708-717. https://doi.org/10.1002/JPER.17-0437
Swanson, K. S., Gibson, G. R., Hutkins, R., Reimer, R. A., Reid, G., Verbeke, K., Scott, K. P., Holscher, H. D., Azad, M. B., Delzenne, N. M., & Sanders, M. E. (2020). The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nature Reviews Gastroenterology and Hepatology, 17(11), 687-701. https://doi.org/10.1038/s41575-020-0344-2
Teughels, W., Durukan, A., Ozcelik, O., Pauwels, M., Quirynen, M., & Haytac, M. C. (2013). Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: A randomized placebo-controlled study. Journal of Clinical Periodontology, 40(11), 1025-1035. https://doi.org/10.1111/jcpe.12155
Thomas, C. M., Hong, T., van Pijkeren, J. P., Hemarajata, P., Trinh, D. V., Hu, W., Britton, R. A., Kalkum, M., & Versalovic, J. (2012). Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS ONE, 7(2), e31951. https://doi.org/10.1371/journal.pone.0031951
Twetman, S., Derawi, B., Keller, M., Ekstrand, K., Yucel-Lindberg, T., & Stecksén-Blicks, C. (2009). Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontologica Scandinavica, 67(1), 19-24. https://doi.org/10.1080/00016350802516170
Van Holm, W., Ghesquière, J., Boon, N., Verspecht, T., Bernaerts, K., Zayed, N., Chatzigiannidou, I., & Teughels, W. (2021). A viability quantitative PCR dilemma: Are longer amplicons better? Applied and Environmental Microbiology, 87(5), e0265320. https://doi.org/10.1128/AEM.02653-20
Verspecht, T., Holm, W. Van, Boon, N., Bernaerts, K., Carlo, A., Masters, J. G., Zayed, N., Quirynen, M., & Bernaerts, K. (2021). Potential prebiotic substrates modulate composition, metabolism, virulence and inflammatory potential of an in vitro multi-species oral biofilm. Journal of Oral Microbiology, 13(1), 1910462. https://doi.org/10.1080/20002297.2021.1910462
Vestman, N. R., Chen, T., Holgerson, P. L., & Öhman, C. (2015). Oral microbiota shift after 12-week supplementation with Lactobacillus reuteri DSM 17938 and PTA 5289 ; a randomized control trial. PLoS ONE, 10(5), e0125812. https://doi.org/10.1371/journal.pone.0125812
Vollenweider, S., Evers, S., Zurbriggen, K., & Lacroix, C. (2010). Unraveling the hydroxypropionaldehyde (HPA) system: An active antimicrobial agent against human pathogens. Journal of Agricultural and Food Chemistry, 58(19), 10315-10322. https://doi.org/10.1021/jf1010897
Widyarman, A. S., Bachtiar, W., Bachtiar, B. M., & Seneviratne, C. J. (2019). Inhibitory effect of probiotic lactobacilli against Streptococcus mutans and Porphyromonas gingivalis biofilms. Scientific Dental Journal, 3, 50-55. https://doi.org/10.4103/SDJ.SDJ
Widyarman, A. S., & Theodorea, C. F. (2022). Novel indigenous probiotic Lactobacillus reuteri strain produces anti-biofilm reuterin against pathogenic periodontal bacteria. European Journal of Dentistry, 16(1), 96-101. https://doi.org/10.1055/s-0041-1731591
Yu, H., Ganas, P., & Schwendicke, F. (2020). Environment-specific probiotic supernatants modify the metabolic activity and survival of Streptococcus mutans in vitro. Frontiers in Microbiology, 11, 1447. https://doi.org/10.3389/fmicb.2020.01447
Zheng, J., Wittouck, S., Salvetti, E., Franz, C. M. A. P., Harris, H. M. B., Mattarelli, P., O'Toole, P. W., Pot, B., Vandamme, P., Walter, J., Watanabe, K., Wuyts, S., Felis, G. E., Gänzle, M. G., & Lebeer, S. (2020). A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. International Journal of Systematic and Evolutionary Microbiology, 70(4), 2782-2858. https://doi.org/10.1099/ijsem.0.004107