1887

Abstract

The present study explores the efficacy of limonene, a cyclic terpene found in the rind of citrus fruits, for antibiofilm potential against species of the genus , which have been deeply studied worldwide owing to their multiple pathogenic efficacy. Limonene showed a concentration-dependent reduction in the biofilm formation of (SF370), with minimal biofilm inhibitory concentration (MBIC) of 400 μg ml. Limonene was found to possess about 75–95 % antibiofilm activity against all the pathogens tested, viz. (SF370 and 5 clinical isolates), (UA159) and (ATCC 6249) at 400 μg ml concentration. Microscopic analysis of biofilm architecture revealed a quantitative breach in biofilm formation. Results of a surface-coating assay suggested that the possible mode of action of limonene could be by inhibiting bacterial adhesion to surfaces, thereby preventing the biofilm formation cascade. Susceptibility of limonene-treated to healthy human blood goes in unison with gene expression studies in which the gene was found to be downregulated. Anti-cariogenic efficacy of limonene against was confirmed, with inhibition of acid production and downregulation of the gene. Downregulation of the and genes, which play a critical role in regulating surface-associated proteins in and , respectively, is yet further evidence to show that limonene targets surface-associated proteins. The results of physiological assays and gene expression studies clearly show that the surface-associated antagonistic mechanism of limonene also reduces surface-mediated virulence factors.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000105
2015-08-01
2020-03-31
Loading full text...

Full text loading...

/deliver/fulltext/jmm/64/8/879.html?itemId=/content/journal/jmm/10.1099/jmm.0.000105&mimeType=html&fmt=ahah

References

  1. Adukwu E.C., Allen S.C., Phillips C.A. 2012; The anti-biofilm activity of lemongrass (Cymbopogon flexuosus) and grapefruit (Citrus paradisi) essential oils against five strains of Staphylococcus aureus . J Appl Microbiol 113:1217–1227 [CrossRef][PubMed]
    [Google Scholar]
  2. Baldassarri L., Creti R., Recchia S., Imperi M., Facinelli B., Giovanetti E., Pataracchia M., Alfarone G., Orefici G. 2006; Therapeutic failures of antibiotics used to treat macrolide-susceptible Streptococcus pyogenes infections may be due to biofilm formation. J Clin Microbiol 44:2721–2727 [CrossRef][PubMed]
    [Google Scholar]
  3. Ban S.H., Kim J.E., Pandit S., Jeon J.G. 2012; Influences of Dryopteris crassirhizoma extract on the viability, growth and virulence properties of Streptococcus mutans . Molecules 17:9231–9244 [CrossRef][PubMed]
    [Google Scholar]
  4. Bandara H.M.H.N., Lam O.L.T., Watt R.M., Jin L.J., Samaranayake L.P. 2010; Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species. J Med Microbiol 59:1225–1234 [CrossRef][PubMed]
    [Google Scholar]
  5. Bisno A.L. 1991; Group A streptococcal infections and acute rheumatic fever. N Engl J Med 325:783–793 [CrossRef][PubMed]
    [Google Scholar]
  6. Bjarnsholt T. 2013; The role of bacterial biofilms in chronic infections. APMIS Suppl 121:(Suppl. 136)1–51 [CrossRef][PubMed]
    [Google Scholar]
  7. Brown T.A. Jr, Ahn S.J., Frank R.N., Chen Y.Y.M., Lemos J.A., Burne R.A. 2005; A hypothetical protein of Streptococcus mutans is critical for biofilm formation. Infect Immun 73:3147–3151 [CrossRef][PubMed]
    [Google Scholar]
  8. Budzyńska A., Wieckowska-Szakiel M., Sadowska B., Kalemba D., Rózalska B. 2011; Antibiofilm activity of selected plant essential oils and their major components. Pol J Microbiol 60:35–41[PubMed] [CrossRef]
    [Google Scholar]
  9. Chaturvedi T. 2013; Allergy related to dental implant and its clinical significance. Clin Cosmet Investig Dent 5:57–61 [CrossRef][PubMed]
    [Google Scholar]
  10. Chee H.Y., Kim H., Lee M.H. 2009; In vitro antifungal activity of limonene against Trichophyton rubrum . Mycobiology 37:243–246 [CrossRef][PubMed]
    [Google Scholar]
  11. Chen Y., Zeng H., Tian J., Ban X., Ma B., Wang Y. 2013; Antifungal mechanism of essential oil from Anethum graveolens seeds against Candida albicans . J Med Microbiol 62:1175–1183 [CrossRef][PubMed]
    [Google Scholar]
  12. Chen Z., He D., Deng J., Zhu J., Mao Q. 2015; Chemical composition and antibacterial activity of the essential oil from Agathis dammara (Lamb.) rich fresh leaves. Nat Prod Res 29: (in press) [CrossRef][PubMed]
    [Google Scholar]
  13. Cho K.H., Caparon M.G. 2005; Patterns of virulence gene expression differ between biofilm and tissue communities of Streptococcus pyogenes . Mol Microbiol 57:1545–1556 [CrossRef][PubMed]
    [Google Scholar]
  14. Collin M., Olsén A. 2003; Extracellular enzymes with immunomodulating activities: variations on a theme in Streptococcus pyogenes . Infect Immun 71:2983–2992 [CrossRef][PubMed]
    [Google Scholar]
  15. Conley J., Olson M.E., Cook L.S., Ceri H., Phan V., Davies H.D. (1996); Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis . Mol Microbiol 20:1083–1091 [CrossRef][PubMed]
    [Google Scholar]
  16. Hendry E.R., Worthington T., Conway B.R., Lambert P.A. 2009; Antimicrobial efficacy of eucalyptus oil and 1,8-cineole alone and in combination with chlorhexidine digluconate against microorganisms grown in planktonic and biofilm cultures. J Antimicrob Chemother 64:1219–1225 [CrossRef][PubMed]
    [Google Scholar]
  17. Hsieh P.C., Siegel S.A., Rogers B., Davis D., Lewis K. 1998; Bacteria lacking a multidrug pump: a sensitive tool for drug discovery. Proc Natl Acad Sci U S A 95:6602–6606 [CrossRef][PubMed]
    [Google Scholar]
  18. Hsu C.Y., Lin M.H., Chen C.C., Chien S.C., Cheng Y.H., Su I.N., Shu J.C. 2011; Vancomycin promotes the bacterial autolysis, release of extracellular DNA, and biofilm formation in vancomycin-non-susceptible Staphylococcus aureus . FEMS Immunol Med Microbiol 63:236–247 [CrossRef][PubMed]
    [Google Scholar]
  19. Hübner N.O., Matthes R., Koban I., Rändler C., Müller G., Bender C., Kindel E., Kocher T., Kramer A. 2010; Efficacy of chlorhexidine, polihexanide and tissue-tolerable plasma against Pseudomonas aeruginosa biofilms grown on polystyrene and silicone materials. Skin Pharmacol Physiol 23:(Suppl)28–34 [CrossRef][PubMed]
    [Google Scholar]
  20. Iwasa K., Lee D.U., Kang S.I., Wiegrebe W. 1998; Antimicrobial activity of 8-alkyl- and 8-phenyl-substituted berberines and their 12-bromo derivatives. J Nat Prod 61:1150–1153 [CrossRef][PubMed]
    [Google Scholar]
  21. Kim M.B., Shaw J.T. 2010; Synthesis of antimicrobial natural products targeting FtsZ: (+)-totarol and related totarane diterpenes. Org Lett 12:3324–3327 [CrossRef][PubMed]
    [Google Scholar]
  22. Koziel J., Maciag-Gudowska A., Mikolajczyk T., Bzowska M., Sturdevant D.E., Whitney A.R., Shaw L.N., DeLeo F.R., Potempa J. 2009; Phagocytosis of Staphylococcus aureus by macrophages exerts cytoprotective effects manifested by the upregulation of antiapoptotic factors. PLoS One 4:e5210 [CrossRef][PubMed]
    [Google Scholar]
  23. Kubo I., Muroi H., Himejima M. 1992; Antibacterial activity of totarol and its potentiation. J Nat Prod 55:1436–1440 [CrossRef][PubMed]
    [Google Scholar]
  24. Lewis K. 2001; In search of natural substrates and inhibitors of MDR pumps. J Mol Microbiol Biotechnol 3:247–254[PubMed]
    [Google Scholar]
  25. Lou Q., Zhu T., Hu J., Ben H., Yang J., Yu F., Liu J., Wu Y., Fischer A., other authors. 2011; Role of the SaeRS two-component regulatory system in Staphylococcus epidermidis autolysis and biofilm formation. BMC Microbiol 11:146 [CrossRef][PubMed]
    [Google Scholar]
  26. Marquez B. 2005; Bacterial efflux systems and efflux pumps inhibitors. Biochimie 87:1137–1147 [CrossRef][PubMed]
    [Google Scholar]
  27. Muroi H., Kubo I. 1996; Antibacterial activity of anacardic acid and totarol, alone and in combination with methicillin, against methicillin-resistant Staphylococcus aureus . J Appl Bacteriol 80:387–394 [CrossRef][PubMed]
    [Google Scholar]
  28. Nguyen H.M., Graber C.J. 2010; Limitations of antibiotic options for invasive infections caused by methicillin-resistant Staphylococcus aureus: is combination therapy the answer?. J Antimicrob Chemother 65:24–36 [CrossRef][PubMed]
    [Google Scholar]
  29. Odds F.C. 2003; Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother 52:1 [CrossRef][PubMed]
    [Google Scholar]
  30. Oo T.Z., Cole N., Garthwaite L., Willcox M.D., Zhu H. 2010; Evaluation of synergistic activity of bovine lactoferricin with antibiotics in corneal infection. J Antimicrob Chemother 65:1243–1251 [CrossRef][PubMed]
    [Google Scholar]
  31. Pagès J.M., Masi M., Barbe J. 2005; Inhibitors of efflux pumps in Gram-negative bacteria. Trends Mol Med 11:382–389 [CrossRef][PubMed]
    [Google Scholar]
  32. Panizzi P., Nahrendorf M., Figueiredo J.L., Panizzi J., Marinelli B., Iwamoto Y., Keliher E., Maddur A.A., Waterman P., other authors. 2011; In vivo detection of Staphylococcus aureus endocarditis by targeting pathogen-specific prothrombin activation. Nat Med 17:1142–1146 [CrossRef][PubMed]
    [Google Scholar]
  33. Park K.D., Lee J.H., Kim S.H., Kang T.H., Moon J.S., Kim S.U. 2006; Synthesis of 13-(substituted benzyl) berberine and berberrubine derivatives as antifungal agents. Bioorg Med Chem Lett 16:3913–3916 [CrossRef][PubMed]
    [Google Scholar]
  34. Qiu J., Feng H., Lu J., Xiang H., Wang D., Dong J., Wang J., Wang X., Liu J., Deng X. 2010; Eugenol reduces the expression of virulence-related exoproteins in Staphylococcus aureus . Appl Environ Microbiol 76:5846–5851 [CrossRef][PubMed]
    [Google Scholar]
  35. Rice K.C., Mann E.E., Endres J.L., Weiss E.C., Cassat J.E., Smeltzer M.S., Bayles K.W. 2007; The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus . Proc Natl Acad Sci U S A 104:8113–8118 [CrossRef][PubMed]
    [Google Scholar]
  36. Sarkar A.K., Appidi S., Ranganath A.S. 2011; Evaluation of berberine chloride as a new antibacterial agent against Gram-positive bacteria for medical textiles. Fibres & Textiles in Eastern Europe 19:131–134
    [Google Scholar]
  37. Smith E.C., Kaatz G.W., Seo S.M., Wareham N., Williamson E.M., Gibbons S. 2007; The phenolic diterpene totarol inhibits multidrug efflux pump activity in Staphylococcus aureus . Antimicrob Agents Chemother 51:4480–4483 [CrossRef][PubMed]
    [Google Scholar]
  38. Steinberger R.E., Holden P.A. 2005; Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol 71:5404–5410 [CrossRef][PubMed]
    [Google Scholar]
  39. Stermitz F.R., Lorenz P., Tawara J.N., Zenewicz L.A., Lewis K. 2000; Synergy in a medicinal plant: antimicrobial action of berberine potentiated by 5′-methoxyhydnocarpin, a multidrug pump inhibitor. Proc Natl Acad Sci U S A 97:1433–1437 [CrossRef][PubMed]
    [Google Scholar]
  40. Stewart P.S., Franklin M.J. 2008; Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210 [CrossRef][PubMed]
    [Google Scholar]
  41. Wang I.N., Deaton J., Young R. 2003; Sizing the holin lesion with an endolysin-β-galactosidase fusion. J Bacteriol 185:779–787 [CrossRef][PubMed]
    [Google Scholar]
  42. Wang D., Yu L., Xiang H., Fan J., He L., Guo N., Feng H., Deng X. 2008; Global transcriptional profiles of Staphylococcus aureus treated with berberine chloride. FEMS Microbiol Lett 279:217–225 [CrossRef][PubMed]
    [Google Scholar]
  43. Wang X., Yao X., Zhu Z., Tang T., Dai K., Sadovskaya I., Flahaut S., Jabbouri S. 2009; Effect of berberine on Staphylococcus epidermidis biofilm formation. Int J Antimicrob Agents 34:60–66 [CrossRef][PubMed]
    [Google Scholar]
  44. Whitchurch C.B., Tolker-Nielsen T., Ragas P.C., Mattick J.S. 2002; Extracellular DNA required for bacterial biofilm formation. Science 295:1487 [CrossRef][PubMed]
    [Google Scholar]
  45. Xing M., Shen F., Liu L., Chen Z., Guo N., Wang X., Wang W., Zhang K., Wu X., other authors. 2012; Antimicrobial efficacy of the alkaloid harmaline alone and in combination with chlorhexidine digluconate against clinical isolates of Staphylococcus aureus grown in planktonic and biofilm cultures. Lett Appl Microbiol 54:475–482 [CrossRef][PubMed]
    [Google Scholar]
  46. Yu Y., Yi Z.B., Liang Y.Z. 2007; Validate antibacterial mode and find main bioactive components of traditional Chinese medicine Aquilegia oxysepala . Bioorg Med Chem Lett 17:1855–1859 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000105
Loading
/content/journal/jmm/10.1099/jmm.0.000105
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error