Effects of caffeic acid phenethyl ester against multi-species cariogenic biofilms

. 2023 Dec ; 68 (6) : 977-989. [epub] 20230608

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37289416

Grantová podpora
81970931 National Natural Science Foundation of China

Odkazy

PubMed 37289416
DOI 10.1007/s12223-023-01064-w
PII: 10.1007/s12223-023-01064-w
Knihovny.cz E-zdroje

Dental caries is a biofilm-related disease, widely perceived to be caused by oral ecological imbalance when cariogenic/aciduric bacteria obtain an ecological advantage. Compared with planktonic bacteria, dental plaques are difficult to remove under extracellular polymeric substance protection. In this study, the effect of caffeic acid phenethyl ester (CAPE) on a preformed cariogenic multi-species biofilm was evaluated, which was comprised of cariogenic bacteria (Streptococcus mutans), commensal bacteria (Streptococcus gordonii), and a pioneer colonizer (Actinomyces naeslundii). Our result revealed that treatment with 0.08 mg/mL CAPE reduced live S. mutans in the preformed multi-species biofilm while not significantly changing the quantification of live S. gordonii. CAPE significantly reduced the production of lactic acid, extracellular polysaccharide, and extracellular DNA and made the biofilm looser. Moreover, CAPE could promote the H2O2 production of S. gordonii and inhibit the expression of SMU.150 encoding mutacin to modulate the interaction among species in biofilms. Overall, our results suggested that CAPE could inhibit the cariogenic properties and change the microbial composition of the multi-species biofilms, indicating its application potential in dental caries prevention and management.

Zobrazit více v PubMed

Abranches J, Zeng L, Kajfasz JK, Palmer S, Chakraborty B, Wen Z, Richards VP, Brady LJ, Lemos JA (2018) Biology of oral streptococci. Microbiol Spectr 6:GPP3–0042–2018. https://doi.org/10.1128/microbiolspec.GPP3-0042-2018

Bijle MN, Ashraf U, Abdalla MM, Neelakantan P, Yiu CKY (2022) Biofilm modulatory response of arginine-fluoride varnish on multi-species biofilm. J Dent 122:104096. https://doi.org/10.1016/j.jdent.2022.104096

Bitoun JP, Liao S, Yao X, Ahn SJ, Isoda R, Nguyen AH, Brady LJ, Burne RA, Abranches J, Wen ZT (2012) BrpA Is involved in regulation of cell envelope stress responses in Streptococcus mutans. Appl Environ Microbiol 78:2914–2922. https://doi.org/10.1128/AEM.07823-11 PubMed DOI PMC

Bowen WH, Burne RA, Wu H, Koo H (2018) Oral biofilms:pathogens, matrix, and polymicrobial interactions in microenvironments. Trends Microbiol 26:229–242. https://doi.org/10.1016/j.tim.2017.09.008 PubMed DOI

Bowen WH, Koo H (2011) Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms Caries Res 45:69-86.  https://doi.org/10.1159/000324598

Chen X, Daliri EB-M, Tyagi A, Oh D-H (2021) Cariogenic biofilm: pathology-related phenotypes and targeted therapy. Microorganisms 9:1311. https://doi.org/10.3390/microorganisms9061311 PubMed DOI PMC

Cheng X, Redanz S, Treerat P, Qin H, Choi D, Zhou X, Xu X, Merritt J, Kreth J (2020) Magnesium-dependent promotion of H PubMed DOI PMC

Chi Y, Wang Y, Ji M, Li Y, Zhu H, Yan Y, Fu D, Zou L, Ren B (2022) Natural products from traditional medicine as promising agents targeting at different stages of oral biofilm development. Front Microbiol 13:955459.   https://doi.org/10.3389/fmicb.2022.955459 .

Cieplik F, Jakubovics NS, Buchalla W, Maisch T, Hellwig E, Al-Ahmad A (2019) Resistance toward chlorhexidine in oral bacteria is there cause for concern? Front Microbiol 10:587–587. https://doi.org/10.3389/fmicb.2019.00587 PubMed DOI PMC

Clinical and Laboratory Standards Institute (2019) Performance standards for antimicrobial susceptibility testing, 29th edn. CLSI document M100. Clinical and Laboratory Standards Institute, Wayne

Collins W, Lowen N, Blake DJ (2019) Caffeic acid esters are effective bactericidal compounds against Paenibacillus larvae by altering intracellular oxidant and antioxidant levels. Biomolecules 9:312.  https://doi.org/10.3390/biom9080312

Craigen B, Dashiff A, Kadouri DE (2011) The use of commercially available alpha-amylase compounds to inhibit and remove Staphylococcus aureus biofilms. Open Microbiol J 5:21–31. https://doi.org/10.2174/1874285801105010021 PubMed DOI PMC

Deng Y, Yang Y, Zhang B, Chen H, Lu Y, Ren S, Lei L, Hu T (2021) The vicK gene of Streptococcus mutans mediates its cariogenicity via exopolysaccharides metabolism. Int J Oral Sci 13:45. https://doi.org/10.1038/s41368-021-00149-x PubMed DOI PMC

Eick S, Lussi A (2021) Arginine: a weapon against cariogenic biofilm? Monogr Oral Sci 29:80–90. https://doi.org/10.1159/000510203 PubMed DOI

Forma E, Brys M (2021) Anticancer activity of propolis and its compounds. Nutrients 13:2594. https://doi.org/10.3390/nu13082594 PubMed DOI PMC

Guo B, Yang F, Jia Y, Xia Q, Zhou XD (2010) The genotypic diversity of oral Actinomyces naeslundii of root caries in aged people. West China Journal of Stomatology 28:646–652 PubMed

Guo H, Chen Y, Guo W, Chen J (2021) Effects of extracellular DNA on dual-species biofilm formed by Streptococcus mutans and Candida albicans. Microb Pathog 154:104838. https://doi.org/10.1016/j.micpath.2021.104838

He J, Hwang G, Liu Y, Gao L, Kilpatrick-Liverman L, Santarpi P, Zhou X, Koo H (2016) L-arginine modifies the exopolysaccharide matrix and thwarts Streptococcus mutans outgrowth within mixed-species oral biofilms. J Bacteriol 198:2651–2661. https://doi.org/10.1128/JB.00021-16 PubMed DOI PMC

Innes NP, Frencken JE, Bjorndal L, Maltz M, Manton DJ, Ricketts D, Van Landuyt K, Banerjee A, Campus G, Domejean S, Fontana M, Leal S, Lo E, Machiulskiene V, Schulte A, Splieth C, Zandona A, Schwendicke F (2016) Managing carious lesions: consensus recommendations on terminology. Adv Dent Res 28:49–57. https://doi.org/10.1177/0022034516639276 PubMed DOI

Kalogeropoulos N, Konteles SJ, Troullidou E, Mourtzinos I, Karathanos VT (2009) Chemical composition, antioxidant activity and antimicrobial properties of propolis extracts from Greece and Cyprus. Food Chem 116:452–461. https://doi.org/10.1016/j.foodchem.2009.02.060 DOI

Kassebaum NJ, Smith AGC, Bernabe E, Fleming TD, Reynolds AE, Vos T, Murray CJL, Marcenes W (2017) Global, regional, and national prevalence, incidence, and disability-adjusted life years for oral conditions for 195 countries, 1990–2015: a systematic analysis for the global burden of diseases, injuries, and risk factors. J Dent Res 96:380–387. https://doi.org/10.1177/0022034517693566 PubMed DOI

Koo H, Rosalen PL, Cury JA, Park YK, Bowen WH (2002) Effects of compounds found in propolis on Streptococcus mutans growth and on glucosyltransferase activity. Antimicrob Agents Chemother 46:1302–1309. https://doi.org/10.1128/AAC.46.5.1302-1309.2002 PubMed DOI PMC

Lee HS, Lee SY, Park SH, Lee JH, Ahn SK, Choi YM, Choi DJ, Chang JH (2013) Antimicrobial medical sutures with caffeic acid phenethyl ester and their in vitro/in vivo biological assessment. Medchemcomm 4:777–782. https://doi.org/10.1039/c2md20289a DOI

Li X, Yin L, Ramage G, Li B, Tao Y, Zhi Q, Lin H, Zhou Y (2019) Assessing the impact of curcumin on dual‐species biofilms formed by Streptococcus mutans and Candida albicans. Microbiologyopen 8:e937. https://doi.org/10.1002/mbo3.937

Liu Y, Burne RA (2009) Multiple two-component systems modulate alkali generation in Streptococcus gordonii in response to environmental stresses. J Bacteriol 191:7353–7362. https://doi.org/10.1128/JB.01053-09 PubMed DOI PMC

Lobo CIV, Rinaldi TB, Christiano CMS, De Sales LL, Barbugli PA, Klein MI (2019) Dual-species biofilms of Streptococcus mutans and Candida albicans exhibit more biomass and are mutually beneficial compared with single-species biofilms. J Oral Microbiol 11:1581520. https://doi.org/10.1080/20002297.2019.1581520 PubMed DOI PMC

Magnavacca A, Sangiovanni E, Racagni G, Dell’Agli M (2022) The antiviral and immunomodulatory activities of propolis: an update and future perspectives for respiratory diseases. Med Res Rev 42:897–945. https://doi.org/10.1002/med.21866 PubMed DOI

Marsh PD, Head DA, Devine DA (2015) Dental plaque as a biofilm and a microbial community—implications for treatment. J Oral Biosci 57:185–191. https://doi.org/10.1016/j.job.2015.08.002 DOI

Merritt J, Qi F, Goodman SD, Anderson MH, Shi W (2003) Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect Immun 71:1972–1979. https://doi.org/10.1128/IAI.71.4.1972-1979.2003 PubMed DOI PMC

Meto A, Colombari B, Meto A, Boaretto G, Pinetti D, Marchetti L, Benvenuti S, Pellati F, Blasi E (2020) Propolis affects Pseudomonas aeruginosa growth, biofilm formation, eDNA release and phenazine production: potential involvement of polyphenols. Microorganisms 8:243. https://doi.org/10.3390/microorganisms8020243 PubMed DOI PMC

Murtaza G, Karim S, Akram MR, Khan SA, Azhar S, Mumtaz A, Bin Asad MHH (2014) Caffeic acid phenethyl ester and therapeutic potentials. Biomed Res Int 2014:145342. https://doi.org/10.1155/2014/145342

Nieva Moreno MI, Isla MI, Cudmani NG, Vattuone MA, Sampietro AR (1999) Screening of antibacterial activity of Amaicha del Valle (Tucumán, Argentina) propolis. J Ethnopharmacol 68:97–102. https://doi.org/10.1016/S0378-8741(99)00051-3

Niu Y, Wang K, Zheng S, Wang Y, Ren Q, Li H, Ding L, Li W, Zhang L (2020) Antibacterial effect of caffeic acid phenethyl ester on cariogenic bacteria and streptococcus mutans biofilms. Antimicrob Agents Chemother 64:e00251-e320. https://doi.org/10.1128/AAC.00251-20 PubMed DOI PMC

Olgierd B, Kamila Z, Anna B, Emilia M (2021) The pluripotent activities of caffeic acid phenethyl ester. Molecules 26:1335. https://doi.org/10.3390/molecules26051335 PubMed DOI PMC

Ophori EA, Eriagbonye BN, Ugbodaga P (2010) Antimicrobial activity of propolis against Streptococcus mutans. Afr J Biotechnol 9:4966–4969

Pan T, Liu F-S, Lin H, Zhou Y (2022) Anti-biofilm studies of synthetic imidazolium salts on dental biofilm in vitro. J Oral Microbiol 14:2075309. https://doi.org/10.1080/20002297.2022.2075309 PubMed DOI PMC

Parolia A, Bapat RA, Chaubal T, Yang HJ, Panda S, Mohan M, Sahebkar A, Kesharwani P (2022) Recent update on application of propolis as an adjuvant natural medication in management of gum diseases and drug delivery approaches. Process Biochem 112:254–268. https://doi.org/10.1016/j.procbio.2021.12.009 DOI

Quivey RG Jr, Grayhack EJ, Faustoferri RC, Hubbard CJ, Baldeck JD, Wolf AS, MacGilvray ME, Rosalen PL, Scott-Anne K, Santiago B, Gopal S, Payne J, Marquis RE (2015) Functional profiling in Streptococcus mutans: construction and examination of a genomic collection of gene deletion mutants. Mol Oral Microbiol 30:474–495. https://doi.org/10.1111/omi.12107 PubMed DOI PMC

Segura-Egea JJ, Gould K, Şen BH, Jonasson P, Cotti E, Mazzoni A, Sunay H, Tjäderhane L, Dummer PMH (2017) Antibiotics in endodontics: a review. Int Endod J 50:1169–1184. https://doi.org/10.1111/iej.12741 PubMed DOI

Takahashi N, Nyvad B (2008) Caries ecology revisited: microbial dynamics and the caries process. Caries Res 42:409–418. https://doi.org/10.1159/000159604 PubMed DOI

Takahashi N, Nyvad B (2011) The role of bacteria in the caries process: ecological perspectives. J Dent Res 90:294–303. https://doi.org/10.1177/0022034510379602 PubMed DOI

Takaisi kikuni NB, Schilcher H (1994) Electron microscopic and microcalorimetric investigations of the possible mechanism of the antibacterial action of a defined propolis provenance. Planta Med 60:222–227. https://doi.org/10.1055/s-2006-959463

Tsuda T, Kumazawa S (2021) Propolis: chemical constituents, plant origin, and possible role in the prevention and treatment of obesity and diabetes. J Agric Food Chem 69:15484–15494. https://doi.org/10.1021/acs.jafc.1c06194 PubMed DOI

Tsutsumi K, Maruyama M, Uchiyama A, Shibasaki K (2018) Characterisation of a sucrose-independent in vitro biofilm model of supragingival plaque. Oral Dis 24:465–475. https://doi.org/10.1111/odi.12779 PubMed DOI

Wang X, Li X, Ling J (2017) Streptococcus gordonii luxS/autoinducer-2 quorum-sensing system modulates the dual-species biofilm formation with Streptococcus mutans. J Basic Microbiol 57:605–616. https://doi.org/10.1002/jobm.201700010 PubMed DOI

Xiao J, Klein MI, Falsetta ML, Lu B, Delahunty CM, Yates Iii JR, Heydorn A, Koo H (2012) The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm. Plos Pathog 8:e1002623. https://doi.org/10.1371/journal.ppat.1002623

Zhang J, Chen C, Chen J, Zhou S, Zhao Y, Xu M, Xu H (2020) Dual mode of anti-biofilm action of G3 against Streptococcus mutans. ACS Appl Mater Interfaces 12:27866–27875. https://doi.org/10.1021/acsami.0c00771 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...