Probiotic Lactobacillus sp. inhibit growth, biofilm formation and gene expression of caries-inducing Streptococcus mutans
dc.Affiliation | October University for modern sciences and Arts (MSA) | |
dc.contributor.author | Wasfi R. | |
dc.contributor.author | Abd El-Rahman O.A. | |
dc.contributor.author | Zafer M.M. | |
dc.contributor.author | Ashour H.M. | |
dc.contributor.other | Department of Microbiology and Immunology | |
dc.contributor.other | Faculty of Pharmacy | |
dc.contributor.other | October University for Modern Sciences and Arts (MSA) | |
dc.contributor.other | Giza | |
dc.contributor.other | Egypt; Department of Microbiology and Immunology | |
dc.contributor.other | Faculty of Pharmacy | |
dc.contributor.other | Al-Azhar University (Girls) | |
dc.contributor.other | Cairo | |
dc.contributor.other | Egypt; Department of Microbiology and Immunology | |
dc.contributor.other | Faculty of Pharmacy | |
dc.contributor.other | Ahram Canadian University (ACU) | |
dc.contributor.other | Giza | |
dc.contributor.other | Egypt; Department of Biological Sciences | |
dc.contributor.other | College of Arts and Sciences | |
dc.contributor.other | University of South Florida St. Petersburg | |
dc.contributor.other | St. Petersburg | |
dc.contributor.other | FL | |
dc.contributor.other | United States; Department of Microbiology and Immunology | |
dc.contributor.other | Faculty of Pharmacy | |
dc.contributor.other | Cairo University | |
dc.contributor.other | Cairo | |
dc.contributor.other | Egypt | |
dc.date.accessioned | 2020-01-09T20:40:59Z | |
dc.date.available | 2020-01-09T20:40:59Z | |
dc.date.issued | 2018 | |
dc.description | Scopus | |
dc.description | MSA Google Scholar | |
dc.description.abstract | Streptococcus mutans contributes significantly to dental caries, which arises from homoeostasic imbalance between host and microbiota. We hypothesized that Lactobacillus sp. inhibits growth, biofilm formation and gene expression of Streptococcus mutans. Antibacterial (agar diffusion method) and antibiofilm (crystal violet assay) characteristics of probiotic Lactobacillus sp. against Streptococcus mutans (ATCC 25175) were evaluated. We investigated whether Lactobacillus casei (ATCC 393), Lactobacillus reuteri (ATCC 23272), Lactobacillus plantarum (ATCC 14917) or Lactobacillus salivarius (ATCC 11741) inhibit expression of Streptococcus mutans genes involved in biofilm formation, quorum sensing or stress survival using quantitative real-time polymerase chain reaction (qPCR). Growth changes (OD600) in the presence of pH-neutralized, catalase-treated or trypsin-treated Lactobacillus sp. supernatants were assessed to identify roles of organic acids, peroxides and bacteriocin. Susceptibility testing indicated antibacterial (pH-dependent) and antibiofilm activities of Lactobacillus sp. against Streptococcus mutans. Scanning electron microscopy revealed reduction in microcolony formation and exopolysaccharide structural changes. Of the oral normal flora, L.salivarius exhibited the highest antibiofilm and peroxide-dependent antimicrobial activities. All biofilm-forming cells treated with Lactobacillus sp. supernatants showed reduced expression of genes involved in exopolysaccharide production, acid tolerance and quorum sensing. Thus, Lactobacillus sp. can inhibit tooth decay by limiting growth and virulence properties of Streptococcus mutans. � 2018 The Authors. Journal of Cellular and Molecular Medicine published by John Wiley & Sons Ltd and Foundation for Cellular and Molecular Medicine. | en_US |
dc.description.uri | https://www.scimagojr.com/journalsearch.php?q=15852&tip=sid&clean=0 | |
dc.identifier.doi | https://doi.org/10.1111/jcmm.13496 | |
dc.identifier.doi | PubMed ID 29316223 | |
dc.identifier.issn | 15821838 | |
dc.identifier.other | https://doi.org/10.1111/jcmm.13496 | |
dc.identifier.other | PubMed ID 29316223 | |
dc.identifier.uri | https://t.ly/OXMmM | |
dc.language.iso | English | en_US |
dc.publisher | Blackwell Publishing Inc. | en_US |
dc.relation.ispartofseries | Journal of Cellular and Molecular Medicine | |
dc.relation.ispartofseries | 22 | |
dc.subject | biofilm | en_US |
dc.subject | dental caries | en_US |
dc.subject | probiotic Lactobacillus | en_US |
dc.subject | Streptococcus mutans | en_US |
dc.subject | bacteriocin | en_US |
dc.subject | exopolysaccharide | en_US |
dc.subject | gamma interferon | en_US |
dc.subject | interleukin 10 | en_US |
dc.subject | probiotic agent | en_US |
dc.subject | bacterial polysaccharide | en_US |
dc.subject | bacteriocin | en_US |
dc.subject | catalase | en_US |
dc.subject | gamma interferon | en_US |
dc.subject | IL10 protein, human | en_US |
dc.subject | interleukin 10 | en_US |
dc.subject | peroxide | en_US |
dc.subject | probiotic agent | en_US |
dc.subject | trypsin | en_US |
dc.subject | agar diffusion | en_US |
dc.subject | antibiotic sensitivity | en_US |
dc.subject | antimicrobial activity | en_US |
dc.subject | Article | en_US |
dc.subject | bacterial growth | en_US |
dc.subject | biofilm | en_US |
dc.subject | colony formation | en_US |
dc.subject | colony forming unit | en_US |
dc.subject | controlled study | en_US |
dc.subject | enzyme linked immunosorbent assay | en_US |
dc.subject | gene expression | en_US |
dc.subject | human | en_US |
dc.subject | human cell | en_US |
dc.subject | Lactobacillus | en_US |
dc.subject | Lactobacillus casei | en_US |
dc.subject | Lactobacillus plantarum | en_US |
dc.subject | Lactobacillus reuteri | en_US |
dc.subject | Lactobacillus salivarius | en_US |
dc.subject | nonhuman | en_US |
dc.subject | normal human | en_US |
dc.subject | priority journal | en_US |
dc.subject | quorum sensing | en_US |
dc.subject | real time polymerase chain reaction | en_US |
dc.subject | scanning electron microscopy | en_US |
dc.subject | Streptococcus mutans | en_US |
dc.subject | zone of inhibition | en_US |
dc.subject | antibiosis | en_US |
dc.subject | biofilm | en_US |
dc.subject | biosynthesis | en_US |
dc.subject | chemistry | en_US |
dc.subject | culture medium | en_US |
dc.subject | cytology | en_US |
dc.subject | drug effect | en_US |
dc.subject | genetics | en_US |
dc.subject | growth, development and aging | en_US |
dc.subject | immunology | en_US |
dc.subject | metabolism | en_US |
dc.subject | microbial sensitivity test | en_US |
dc.subject | microbiology | en_US |
dc.subject | mononuclear cell | en_US |
dc.subject | pathogenicity | en_US |
dc.subject | pH | en_US |
dc.subject | primary cell culture | en_US |
dc.subject | Streptococcus mutans | en_US |
dc.subject | Antibiosis | en_US |
dc.subject | Bacteriocins | en_US |
dc.subject | Biofilms | en_US |
dc.subject | Catalase | en_US |
dc.subject | Culture Media | en_US |
dc.subject | Humans | en_US |
dc.subject | Hydrogen-Ion Concentration | en_US |
dc.subject | Interferon-gamma | en_US |
dc.subject | Interleukin-10 | en_US |
dc.subject | Lactobacillus casei | en_US |
dc.subject | Lactobacillus plantarum | en_US |
dc.subject | Lactobacillus reuteri | en_US |
dc.subject | Lactobacillus salivarius | en_US |
dc.subject | Leukocytes, Mononuclear | en_US |
dc.subject | Microbial Sensitivity Tests | en_US |
dc.subject | Peroxides | en_US |
dc.subject | Polysaccharides, Bacterial | en_US |
dc.subject | Primary Cell Culture | en_US |
dc.subject | Probiotics | en_US |
dc.subject | Quorum Sensing | en_US |
dc.subject | Streptococcus mutans | en_US |
dc.subject | Trypsin | en_US |
dc.title | Probiotic Lactobacillus sp. inhibit growth, biofilm formation and gene expression of caries-inducing Streptococcus mutans | en_US |
dc.type | Article | en_US |
dcterms.isReferencedBy | Ben Taheur, F., Kouidhi, B., Fdhila, K., Anti-bacterial and anti-biofilm activity of probiotic bacteria against oral pathogens (2016) Microb Pathog, 97, pp. 213-220; Mathews, M.J., Mathews, E.H., Mathews, G.E., Oral health and coronary heart disease (2016) BMC Oral Health, 16, pp. 1-10; Dietrich, T., Webb, I., Stenhouse, L., Evidence summary: the relationship between oral and cardiovascular disease (2017) Br Dent J, 222, pp. 381-385; Takahashi, N., Nyvad, B., Caries ecology revisited: microbial dynamics and the caries process (2008) Caries Res, 42, pp. 409-418; Tong, Z., Zhou, L., Li, J., An in�vitro investigation of Lactococcus lactis antagonizing cariogenic bacterium Streptococcus mutans (2012) Arch Oral Biol, 57, pp. 376-382; Abranches, J., Miller, J.H., Martinez, A.R., The collagen-binding protein Cnm is required for streptococcus mutans adherence to and intracellular invasion of human coronary artery endothelial cells (2011) Infect Immun, 79, pp. 2277-2284; Kreth, J., Merritt, J., Qi, F., Bacterial and host interactions of oral streptococci (2009) DNA Cell Biol, 28, pp. 397-403; Forssten, S.D., Bj�rklund, M., Ouwehand, A.C., Streptococcus mutans, caries and simulation models (2010) Nutrients, 2, pp. 290-298; Bezerra, D.S., Stipp, R.N., Neves, B.G., Insights into the virulence traits of streptococcus mutans in dentine carious lesions of children with early childhood caries (2016) Caries Res, 50, pp. 279-287; Nguyen, P.T., Falsetta, M.L., Hwang, G., alpha-Mangostin disrupts the development of Streptococcus mutans biofilms and facilitates its mechanical removal (2014) PLoS ONE, 9; Koo, H., Xiao, J., Klein, M.I., Exopolysaccharides produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms (2010) J Bacteriol, 192, pp. 3024-3032; Xiao, J., Klein, M.I., Falsetta, M.L., The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm (2012) PLoS Pathog, 8; Senadheera, D., Krastel, K., Mair, R., Inactivation of VicK affects acid production and acid survival of Streptococcus mutans (2009) J Bacteriol, 191, pp. 6415-6424; Smith, E.G., Spatafora, G.A., Gene regulation in S. mutans: complex control in a complex environment (2012) J Dent Res, 91, pp. 133-141; Cagetti, M.G., Mastroberardino, S., Milia, E., The use of probiotic strains in caries prevention: a systematic review (2013) Nutrients, 5, pp. 2530-2550; (2002) Guidelines for the evaluation of probiotics in food, , Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. Ontario, Canada; Vuotto, C., Longo, F., Donelli, G., Probiotics to counteract biofilm-associated infections: promising and conflicting data (2014) Int J Oral Sci, 6, pp. 189-194; Badet, C., Thebaud, N.B., Ecology of lactobacilli in the oral cavity: a review of literature (2008) Open Microbiol J, 2, pp. 38-48; Marsh, P., Martin, M.V., Lewis, M., (2009) Oral Microbiology, , China, Churchill Livingstone; Twetman, S., Stecksen-Blicks, C., Probiotics and oral health effects in children (2008) Int J Paediatr Dent, 18, pp. 3-10; Teanpaisan, R., Piwat, S., Tianviwat, S., Effect of long-term consumption of Lactobacillus paracasei SD1 on reducing mutans streptococci and caries risk: a randomized placebo-controlled trial (2015) Dent J, 3, pp. 43-54; Sidhu, G.K., Mantha, S., Murthi, S., Evaluation of Lactobacillus and Streptococcus mutans by addition of Probiotics in the form of curd in the diet (2015) J Int Oral Health, 7, pp. 85-89; Stamatova, I., Meurman, J.H., Probiotics: health benefits in the mouth (2009) Am J Dent, 22, pp. 329-338; Compare, D., Rocco, A., Coccoli, P., Lactobacillus casei DG and its postbiotic reduce the inflammatory mucosal response: an ex-vivo organ culture model of post-infectious irritable bowel syndrome (2017) BMC Gastroenterol, 17, pp. 1-8; Lin, X., Chen, X., Chen, Y., The effect of five probiotic lactobacilli strains on the growth and biofilm formation of Streptococcus mutans (2015) Oral Dis, 21, pp. e128-e134; Shokryazdan, P., Sieo, C.C., Kalavathy, R., Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains (2014) Biomed Res Int, pp. 1-16; Cadirci, B.H., Citak, S., A comparison of two methods used for measuring antagonistic activity of lactic acid bacteria (2005) Pak J Nutr, 4, pp. 237-241; Chew, S.Y., Cheah, Y.K., Seow, H.F., Probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 exhibit strong antifungal effects against vulvovaginal candidiasis-causing Candida glabrata isolates (2015) J Appl Microbiol, 118, pp. 1180-1190; Wasfi, R., Abd El-Rahman, O.A., Mansour, L.E., Antimicrobial activities against biofilm formed by Proteus mirabilis isolates from wound and urinary tract infections (2012) Indian J Med Microbiol, 30, pp. 76-80; Wu, C.C., Lin, C.T., Wu, C.Y., Inhibitory effect of Lactobacillus salivarius on Streptococcus mutans biofilm formation (2015) Mol Oral Microbiol, 30, pp. 16-26; Pfaffl, M.W., Tichopad, A., Prgomet, C., Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper�Excel-based tool using pair-wise correlations (2004) Biotechnol Lett, 26, pp. 509-515; Pfaffl, M.W., Relative quantification (2004) Real-Time PCR, , In, Dorak T, editor., International University Line; Kilian, M., Chapple, I.L.C., Hannig, M., The oral microbiome�an update for oral healthcare professionals (2016) Br Dent J, 221, pp. 657-666; Petrova, M.I., Lievens, E., Malik, S., Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health (2015) Front Physiol, 6, pp. 1-18; Floch, M.H., Walker, W.A., Madsen, K., Recommendations for probiotic use-2011 update (2011) J Clin Gastroenterol, 45, pp. S168-S171; Donelli, G., Activity of probiotics on biofilm-growing pathogens of the oral cavity (2013) Microb Ecol Health Dis, 24, p. 6; Lin, Y.-T.J., Chou, C.-C., Hsu, C.-Y.S., Effects of Lactobacillus casei Shirota intake on caries risk in children (2017) J Dent Sci, 12, pp. 179-184; Imran, F., Das, S., Padmanabhan, S., Evaluation of the efficacy of a probiotic drink containing Lactobacillus casei on the levels of periodontopathic bacteria in periodontitis: a clinico-microbiologic study (2015) Indian J Dent Res, 26, pp. 462-468; Caglar, E., Cildir, S.K., Ergeneli, S., Salivary mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55730 by straws and tablets (2006) Acta Odontol Scand, 64 (5), pp. 314-318; Saha, S., Tomaro-Duchesneau, C., Rodes, L., Investigation of probiotic bacteria as dental caries and periodontal disease biotherapeutics (2014) Benef Microbes, 5, pp. 447-460; Baca-Castanon, M.L., De la Garza-Ramos, M.A., Alcazar-Pizana, A.G., Antimicrobial effect of Lactobacillus reuteri on cariogenic bacteria Streptococcus gordonii, Streptococcus mutans, and periodontal diseases Actinomyces naeslundii and Tannerella forsythia (2015) Probiotics Antimicrob Proteins, 7, pp. 1-8; Hassl�f, P., (2013) Probiotic Lactobacilli in the Context of Dental Caries as a Biofilm-Mediated Disease, , [Doctoral thesis, comprehensive summary]., Ume�, Ume� universitet; Ishikawa, H., Aiba, Y., Nakanishi, M., Suppression of periodontal pathogenic bacteria in the saliva of humans by the administration of Lactobacillus salivarius TI 2711 (2003) Nihon Shishubyo Gakkai Kaishi (J Japanese Soc Periodontol), 45, pp. 105-112; Nishihara, T., Suzuki, N., Yoneda, M., Effects of Lactobacillus salivarius-containing tablets on caries risk factors: a randomized open-label clinical trial (2014) BMC Oral Health, 14, pp. 1-7; Oldak, A., Zielinska, D., Rzepkowska, A., Comparison of antibacterial activity of Lactobacillus plantarum strains isolated from two different kinds of regional cheeses from Poland: Oscypek and Korycinski Cheese (2017) Biomed Res Int, pp. 1-10; Taheri, P., Samadi, N., Ehsani, M.R., An evaluation and partial characterization of a bacteriocin produced by Lactococcus lactis subsp lactis ST1 isolated from goat milk (2012) Braz J Microbiol, 43, pp. 1452-1462; Guo, L., McLean, J.S., Lux, R., The well-coordinated linkage between acidogenicity and aciduricity via insoluble glucans on the surface of Streptococcus mutans (2015) Sci Rep, 5, pp. 1-11; Liu, Y., Burne, R.A., Multiple two-component systems of Streptococcus mutans regulate agmatine deiminase gene expression and stress tolerance (2009) J Bacteriol, 191, pp. 7363-7366; Dali�, D.K.D., Deschamps, A.M., Richard-Forget, F., Lactic acid bacteria � potential for control of mould growth and mycotoxins: a review (2010) Food Control, 21, pp. 370-380; Xu, X., Zhou, X.D., Wu, C.D., The tea catechin epigallocatechin gallate suppresses cariogenic virulence factors of Streptococcus mutans (2011) Antimicrob Agents Chemother, 55, pp. 1229-1236; Dasari, S., Shouri, R.N.D., Wudayagiri, R., Antimicrobial activity of Lactobacillus against microbial flora of cervicovaginal infections (2014) Asian Pac J Trop Dis, 4, pp. 18-24; Tahmourespour, A., Salehi, R., Kasra, K.R., Lactobacillus Acidophilus-derived biosurfactant effect on GTFB and GTFC expression level in Streptococcus mutans biofilm cells (2011) Braz J Microbiol, 42, pp. 330-339; Hassl�f, P., Hedberg, M., Twetman, S., Growth inhibition of oral mutans streptococci and candida by commercial probiotic lactobacilli�an in�vitro study (2010) BMC Oral Health, 10, pp. 1-6; Leung, V., Dufour, D., L�vesque, C.M., Death and survival in Streptococcus mutans: differing outcomes of a quorum-sensing signaling peptide (2015) Front Microbiol, 6, pp. 1-6; Banu, L.D., (2010) Gene expression in Streptococcus mutans biofilms, , University of Zurich; L�, X., Hu, P., Dang, Y., Purification and partial characterization of a novel bacteriocin produced by Lactobacillus casei TN-2 isolated from fermented camel milk (Shubat) of Xinjiang Uygur Autonomous region, China (2014) Food Control, 43, pp. 276-283; Morita, H., Toh, H., Fukuda, S., Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production (2008) DNA Res, 15, pp. 151-161; da Silva, S.S., Vitolo, M., Gonz�lez, J.M.D., Oliveira RPdS. Overview of Lactobacillus plantarum as a promising bacteriocin producer among lactic acid bacteria (2014) Food Res Int, 64, pp. 527-536; O'Shea, E.F., O'Connor, P.M., O'Sullivan, O., Bactofencin A, a new type of cationic bacteriocin with unusual immunity (2013) MBio, 4, pp. e00413-e00498; Decker, E.-M., Klein, C., Schwindt, D., Metabolic activity of Streptococcus mutans biofilms and gene expression during exposure to xylitol and sucrose (2014) Int J Oral Sci, 6, pp. 195-204; Shemesh, M., Tam, A., Feldman, M., Differential expression profiles of Streptococcus mutans ftf, gtf and vicR genes in the presence of dietary carbohydrates at early and late exponential growth phases (2006) Carbohydr Res, 341, pp. 2090-2097; Narisawa, N., Kawarai, T., Suzuki, N., Competence-dependent endogenous DNA rearrangement and uptake of extracellular DNA give a natural variant of Streptococcus mutans without biofilm formation (2011) J Bacteriol, 193, pp. 5147-5154; Jeon, J.G., Klein, M.I., Xiao, J., Influences of naturally occurring agents in combination with fluoride on gene expression and structural organization of Streptococcus mutans in biofilms (2009) BMC Microbiol, 9, p. 228; Welin-Neilands, J., Svensater, G., Acid tolerance of biofilm cells of Streptococcus mutans (2007) Appl Environ Microbiol, 73, pp. 5633-5638; Senadheera, M.D., Guggenheim, B., Spatafora, G.A., A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development (2005) J Bacteriol, 187, pp. 4064-4076; Krzysciak, W., Jurczak, A., Koscielniak, D., The virulence of Streptococcus mutans and the ability to form biofilms (2014) Eur J Clin Microbiol Infect Dis, 33, pp. 499-515; Bowen, W.H., Koo, H., Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms (2011) Caries Res, 45, pp. 69-86; Savabi, O., Kazemi, M., Kamali, S., Effects of biosurfactant produced by Lactobacillus casei on gtfB, gtfC, and ftf gene expression level in S. mutans by real-time RT-PCR (2014) Adv Biomed Res, 3, pp. 1-16; Xiao, J., Koo, H., Structural organization and dynamics of exopolysaccharide matrix and microcolonies formation by Streptococcus mutans in biofilms (2010) J Appl Microbiol, 108, pp. 2103-2113; Yamashita, Y., Bowen, W.H., Burne, R.A., Role of the Streptococcus mutans gtf genes in caries induction in the specific-pathogen-free rat model (1993) Infect Immun, 61, pp. 3811-3817; Ullrich, M., (2009) Bacterial Polysaccharide: Current Innovations and Future Trends, , Norfolk UK, Caister Academic Press; Farges, J.C., Alliot-Licht, B., Renard, E., Dental pulp defence and repair mechanisms in dental caries (2015) Mediators Inflamm, p. 16; Trinchieri, G., Interleukin-12 and the regulation of innate resistance and adaptive immunity (2003) Nat Rev Immunol, 3, pp. 133-146; Lee, S.H., Kim, Y.J., A comparative study of the effect of probiotics on cariogenic biofilm model for preventing dental caries (2014) Arch Microbiol, 196, pp. 601-609; Salehi, R., Savabi, O., Kazemi, M., Effects of Lactobacillus reuteri-derived biosurfactant on the gene expression profile of essential adhesion genes (gtfB, gtfC and ftf) of Streptococcus mutans (2014) Adv Biomed Res, 3, p. 14 | |
dcterms.source | Scopus |