1887

Abstract

This work studied the antifungal mechanism of dill seed essential oil (DSEO) against . Flow cytometric analysis and inhibition of ergosterol synthesis were performed to clarify the mechanism of action of DSEO on . Upon treatment of cells with DSEO, propidium iodide penetrated through a lesion in its plasma membrane. DSEO also significantly reduced the amount of ergosterol. These findings indicate that the plasma membrane of was damaged by DSEO. The effect of DSEO on the functions of the mitochondria in was also studied. We assayed the mitochondrial membrane potential (mtΔψ) using rhodamine 123 and determined the production of mitochondrial dysfunction-induced reactive oxygen species (ROS) via flow cytometry. The effects of the antioxidant -cysteine (Cys) on DSEO-induced ROS production and the antifungal effect of DSEO on were investigated. Exposure to DSEO increased mtΔψ. Dysfunctions in the mitochondria caused ROS accumulation in . This increase in the level of ROS production and DSEO-induced decrease in cell viability were prevented by the addition of Cys, indicating that ROS are an important mediator of the antifungal action of DSEO. These findings indicate that the cytoplasmic membrane and mitochondria are the main anti- targets of DSEO.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.055467-0
2013-08-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/8/1175.html?itemId=/content/journal/jmm/10.1099/jmm.0.055467-0&mimeType=html&fmt=ahah

References

  1. Ahmad N., Alam M. K., Shehbaz A., Khan A., Mannan A., Hakim S. R., Bisht D., Owais M. 2005; Antimicrobial activity of clove oil and its potential in the treatment of vaginal candidiasis. J Drug Target 13:555–561 [View Article][PubMed]
    [Google Scholar]
  2. Arthington-Skaggs B. A., Jradi H., Desai T., Morrison C. J. 1999; Quantitation of ergosterol content: novel method for determination of fluconazole susceptibility of Candida albicans. J Clin Microbiol 37:3332–3337[PubMed]
    [Google Scholar]
  3. Bailer J., Aichinger T., Hackl G., de Hueber K., Dachler M. 2001; Essential oil content and composition in commercially available dill cultivars in comparison to caraway. Ind Crops Prod 14:229–239 [View Article]
    [Google Scholar]
  4. Bakkali F., Averbeck S., Averbeck D., Idaomar M. 2008; Biological effects of essential oils – a review. Food Chem Toxicol 46:446–475 [View Article][PubMed]
    [Google Scholar]
  5. Balietti M., Fattoretti P., Skalicky M., Viidik A., Giorgetti B., Grossi Y., Bertoni-Freddari C. 2005; The effect of chronic physical exercise on succinic dehydrogenase activity in the heart muscle of old rats. Biogerontology 6:95–100 [View Article][PubMed]
    [Google Scholar]
  6. Baratta T. M., Dorman D. H. J., Deans S. G., Figueiredo A. C., Barroso J. G., Ruberto G. 1998; Antimicrobial and antioxidant properties of some commercial essential oils. Flavour Fragr J 13:235–244 [View Article]
    [Google Scholar]
  7. Bauer K. D. 1993; Quality control issues in DNA content flow cytometry. Ann N Y Acad Sci 677:1 Clinical Flow59–77 [View Article][PubMed]
    [Google Scholar]
  8. Bonini M. G., Rota C., Tomasi A., Mason R. P. 2006; The oxidation of 2′,7′-dichlorofluorescin to reactive oxygen species: a self-fulfilling prophesy?. Free Radic Biol Med 40:968–975 [View Article][PubMed]
    [Google Scholar]
  9. Brand M. D., Chien L. F., Ainscow E. K., Rolfe D. F., Porter R. K. 1994; The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1187:132–139 [View Article][PubMed]
    [Google Scholar]
  10. Chinese Pharmacopoeia Commission 2010 Pharmacopoeia of the People’s Republic of China vol. I. Beijing, China: China Medical Science and Technology Press;
    [Google Scholar]
  11. Costa T. R., Fernandes O. F. L., Santos S. C., Oliveira C. M. A., Lião L. M., Ferri P. H., Paula J. R., Ferreira H. D., Sales B. H. N., Silva M. R., R. 2000; Antifungal activity of volatile constituents of Eugenia dysenterica leaf oil. J Ethnopharmacol 72:111–117 [View Article][PubMed]
    [Google Scholar]
  12. Cox S. D., Mann C. M., Markham J. L., Bell H. C., Gustafson J. E., Warmington J. R., Wyllie S. G. 2000; The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). J Appl Microbiol 88:170–175 [View Article][PubMed]
    [Google Scholar]
  13. Cox S. D., Mann C. M., Markham J. L., Gustafson J. E., Warmington J. R., Wyllie S. G. 2001; Determining the antimicrobial actions of tea tree oil. Molecules 6:87–91 [View Article]
    [Google Scholar]
  14. Crompton M. 1999; The mitochondrial permeability transition pore and its role in cell death. Biochem J 341:233–249 [View Article][PubMed]
    [Google Scholar]
  15. Dalleau S., Cateau E., Bergès T., Berjeaud J. M., Imbert C. 2008; In vitro activity of terpenes against Candida biofilms. Int J Antimicrob Agents 31:572–576 [View Article][PubMed]
    [Google Scholar]
  16. Douglas L. J. 2003; Candida biofilms and their role in infection. Trends Microbiol 11:30–36 [View Article][PubMed]
    [Google Scholar]
  17. Duarte M. C. T., Figueira G. M., Sartoratto A., Rehder V. L. G., Delarmelina C. 2005; Anti-Candida activity of Brazilian medicinal plants. J Ethnopharmacol 97:305–311 [View Article][PubMed]
    [Google Scholar]
  18. Duru M. E., Oztürk M., Uğur A., Ceylan Ö. 2004; The constituents of essential oil and in vitro antimicrobial activity of Micromeria cilicica from Turkey. J Ethnopharmacol 94:43–48 [View Article][PubMed]
    [Google Scholar]
  19. Editor Committee of National Chinese Medical Manage Bureau 2005; Chinese Herbal, Uighur Volume. Shanghai: Shanghai Scientific & Technical Publishers;
    [Google Scholar]
  20. Filipowicz N., Kamiński M., Kurlenda J., Asztemborska M., Ochocka J. R. 2003; Antibacterial and antifungal activity of juniper berry oil and its selected components. Phytother Res 17:227–231 [View Article][PubMed]
    [Google Scholar]
  21. Giordani R., Regli P., Kaloustian J., Mikaïl C., Abou L., Portugal H. 2004; Antifungal effect of various essential oils against Candida albicans. Potentiation of antifungal action of amphotericin B by essential oil from Thymus vulgaris.. Phytother Res 18:990–995 [View Article][PubMed]
    [Google Scholar]
  22. Hammer K. A., Carson C. F., Riley T. V. 1998; In-vitro activity of essential oils, in particular Melaleuca alternifolia (tea tree) oil and tea tree oil products, against Candida spp. J Antimicrob Chemother 42:591–595 [View Article][PubMed]
    [Google Scholar]
  23. Helmerhorst E. J., Troxler R. F., Oppenheim F. G. 2001; The human salivary peptide histatin 5 exerts its antifungal activity through the formation of reactive oxygen species. Proc Natl Acad Sci U S A 98:14637–14642 [View Article][PubMed]
    [Google Scholar]
  24. Jirovetz L., Buchbauer G., Stoyanova A. S., Georgiev E. V., Damianova S. T. 2003; Composition, quality control, and antimicrobial activity of the essential oil of long-time stored dill (Anethum graveolens L.) seeds from Bulgaria. J Agric Food Chem 51:3854–3857 [View Article][PubMed]
    [Google Scholar]
  25. Jouaville L. S., Pinton P., Bastianutto C., Rutter G. A., Rizzuto R. 1999; Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc Natl Acad Sci U S A 96:13807–13812 [View Article][PubMed]
    [Google Scholar]
  26. Karaman S., Digrak M., Ravid U., Ilcim A. 2001; Antibacterial and antifungal activity of the essential oils of Thymus revolutus Celak from Turkey. J Ethnopharmacol 76:183–186 [View Article][PubMed]
    [Google Scholar]
  27. Kauffman C. A. 2006; Fungal infections. Proc Am Thorac Soc 3:35–40 [View Article][PubMed]
    [Google Scholar]
  28. Kobayashi D., Kondo K., Uehara N., Otokozawa S., Tsuji N., Yagihashi A., Watanabe N. 2002; Endogenous reactive oxygen species is an important mediator of miconazole antifungal effect. Antimicrob Agents Chemother 46:3113–3117 [View Article][PubMed]
    [Google Scholar]
  29. Kordali S., Kotan R., Mavi A., Cakir A., Ala A., Yildirim A. 2005; Determination of the chemical composition and antioxidant activity of the essential oil of Artemisia dracunculus and of the antifungal and antibacterial activities of Turkish Artemisia absinthium, A. dracunculus, Artemisia santonicum, and Artemisia spicigera essential oils. J Agric Food Chem 53:9452–9458 [View Article][PubMed]
    [Google Scholar]
  30. Kuhn D. M., Balkis M., Chandra J., Mukherjee P. K., Ghannoum M. A. 2003; Uses and limitations of the XTT assay in studies of Candida growth and metabolism. J Clin Microbiol 41:506–508 [View Article][PubMed]
    [Google Scholar]
  31. Lenaz G. 2001; The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 52:159–164 [View Article][PubMed]
    [Google Scholar]
  32. Lesnefsky E. J., Moghaddas S., Tandler B., Kerner J., Hoppel C. L. 2001; Mitochondrial dysfunction in cardiac disease: ischemia–reperfusion, aging, and heart failure. J Mol Cell Cardiol 33:1065–1089 [View Article][PubMed]
    [Google Scholar]
  33. Lippold H. J. 1982; Quantitative succinic dehydrogenases histochemistry. Histochemistry 76:381–405 [View Article][PubMed]
    [Google Scholar]
  34. López P., Sánchez C., Batlle R., Nerín C. 2005; Solid- and vapor-phase antimicrobial activities of six essential oils: susceptibility of selected foodborne bacterial and fungal strains. J Agric Food Chem 53:6939–6946 [View Article][PubMed]
    [Google Scholar]
  35. Machida K., Tanaka T. 1999; Farnesol-induced generation of reactive oxygen species dependent on mitochondrial transmembrane potential hyperpolarization mediated by F0F1-ATPase in yeast. FEBS Lett 462:108–112 [View Article][PubMed]
    [Google Scholar]
  36. Machida K., Tanaka T., Fujita K., Taniguchi M. 1998; Farnesol-induced generation of reactive oxygen species via indirect inhibition of the mitochondrial electron transport chain in the yeast Saccharomyces cerevisiae.. J Bacteriol 180:4460–4465[PubMed]
    [Google Scholar]
  37. Magiatis P., Melliou E., Skaltsounis A. L., Chinou I. B., Mitaku S. 1999; Chemical composition and antimicrobial activity of the essential oils of Pistacia lentiscus var. chia. Planta Med 65:749–752 [View Article][PubMed]
    [Google Scholar]
  38. Magwa M. L., Gundidza M., Gweru N., Humphrey G. 2006; Chemical composition and biological activities of essential oil from the leaves of Sesuvium portulacastrum.. J Ethnopharmacol 103:85–89 [View Article][PubMed]
    [Google Scholar]
  39. Manohar V., Ingram C., Gray J., Talpur N. A., Echard B. W., Bagchi D., Preuss H. G. 2001; Antifungal activities of origanum oil against Candida albicans.. Mol Cell Biochem 228:111–117 [View Article][PubMed]
    [Google Scholar]
  40. Martins A. P., Salgueiro L. R., Gonçalves M. J., Vila R., Tomi F., Adzet T., Proença da Cunha A., Cañigueral S., Casanova J. 2000; Antimicrobial activity and chemical composition of the bark oil of Croton stellulifer, an endemic species from S. Tomé e Príncipe. Planta Med 66:647–650 [View Article][PubMed]
    [Google Scholar]
  41. Moradas-Ferreira P., Costa V., Piper P., Mager W. 1996; The molecular defences against reactive oxygen species in yeast. Mol Microbiol 19:651–658 [View Article][PubMed]
    [Google Scholar]
  42. Oliva B., Piccirilli E., Ceddia T., Pontieri E., Aureli P., Ferrini A. M. 2003; Antimycotic activity of Melaleuca alternifolia essential oil and its major components. Lett Appl Microbiol 37:185–187 [View Article][PubMed]
    [Google Scholar]
  43. Oumzil H., Ghoulami S., Rhajaoui M., Ilidrissi A., Fkih-Tetouani S., Faid M., Benjouad A. 2002; Antibacterial and antifungal activity of essential oils of Mentha suaveolens. Phytother Res 16:727–731 [View Article][PubMed]
    [Google Scholar]
  44. Perrone G. G., Tan S. X., Dawes I. W. 2008; Reactive oxygen species and yeast apoptosis. Biochim Biophys Acta 1783:1354–1368 [View Article][PubMed]
    [Google Scholar]
  45. Pfaller M. A., Diekema D. J., Andes D., Arendrup M. C., Brown S. D., Lockhart S. R., Motyl M., Perlin D. S.CLSI Subcommittee for Antifungal Testing 2011; Clinical breakpoints for the echinocandins and Candida revisited: integration of molecular, clinical, and microbiological data to arrive at species-specific interpretive criteria. Drug Resist Updat 14:164–176 [View Article][PubMed]
    [Google Scholar]
  46. Pina-Vaz C., Sansonetty F., Rodrigues A. G., Costa-Oliveira S., Tavares C., Martinez-de-Oliveira J. 2001; Cytometric approach for a rapid evaluation of susceptibility of Candida strains to antifungals. Clin Microbiol Infect 7:609–618 [View Article][PubMed]
    [Google Scholar]
  47. Pina-Vaz C., Gonçalves Rodrigues A. G., Pinto E., Costa-de-Oliveira S., Tavares C., Salgueiro L., Cavaleiro C., Gonçalves M. J., Martinez-de-Oliveira J. 2004; Antifungal activity of Thymus oils and their major compounds. J Eur Acad Dermatol Venereol 18:73–78 [View Article][PubMed]
    [Google Scholar]
  48. Pinto E., Pina-Vaz C., Salgueiro L., Gonçalves M. J., Costa-de-Oliveira S., Cavaleiro C., Palmeira A., Rodrigues A., Martinez-de-Oliveira J. 2006; Antifungal activity of the essential oil of Thymus pulegioides on Candida, Aspergillus and dermatophyte species. J Med Microbiol 55:1367–1373 [View Article][PubMed]
    [Google Scholar]
  49. Pinto E., Vale-Silva L., Cavaleiro C., Salgueiro L. 2009; Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J Med Microbiol 58:1454–1462 [View Article][PubMed]
    [Google Scholar]
  50. Rapp R. P. 2004; Changing strategies for the management of invasive fungal infections. Pharmacotherapy 24:4S–28S, quiz 29S–32S [View Article][PubMed]
    [Google Scholar]
  51. Rodriguez R. J., Low C., Bottema C. D., Parks L. W. 1985; Multiple functions for sterols in Saccharomyces cerevisiae. Biochim Biophys Acta 837:336–343 [View Article][PubMed]
    [Google Scholar]
  52. Runyoro D. K. B., Matee M. I. N., Ngassapa O. D., Joseph C. C., Mbwambo Z. H. 2006; Screening of Tanzanian medicinal plants for anti-Candida activity. BMC Complement Altern Med 6:11–20 [View Article][PubMed]
    [Google Scholar]
  53. Salgueiro L. R., Pinto E., Gonçalves M. J., Pina-Vaz C., Cavaleiro C., Rodrigues A. G., Palmeira A., Tavares C., Costa-de-Oliveira S., Martinez-de-Oliveira J. 2004; Chemical composition and antifungal activity of the essential oil of Thymbra capitata.. Planta Med 70:572–575 [View Article][PubMed]
    [Google Scholar]
  54. Sardi J. C. O., Scorzoni L., Bernardi T., Fusco-Almeida A. M., Mendes Giannini M. J. S. 2013; Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol 62:10–24 [View Article][PubMed]
    [Google Scholar]
  55. Simbula G., Glascott P. A. Jr, Akita S., Hoek J. B., Farber J. L. 1997; Two mechanisms by which ATP depletion potentiates induction of the mitochondrial permeability transition. Am J Physiol 273:C479–C488[PubMed]
    [Google Scholar]
  56. Starkov A. A., Fiskum G. 2003; Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state. J Neurochem 86:1101–1107 [View Article][PubMed]
    [Google Scholar]
  57. Tampieri M. P., Galuppi R., Macchioni F., Carelle M. S., Falcioni L., Cioni P. L., Morelli I. 2005; The inhibition of Candida albicans by selected essential oils and their major components. Mycopathologia 159:339–345 [View Article][PubMed]
    [Google Scholar]
  58. Tang X. Q., Feng J. Q., Chen J., Chen P. X., Zhi J. L., Cui Y., Guo R. X., Yu H. M. 2005; Protection of oxidative preconditioning against apoptosis induced by H2O2 in PC12 cells: mechanisms via MMP, ROS, and Bcl-2. Brain Res 1057:57–64 [View Article][PubMed]
    [Google Scholar]
  59. Tavares A. C., Gonçalves M. J., Cavaleiro C., Cruz M. T., Lopes M. C., Canhoto J., Salgueiro L. R. 2008; Essential oil of Daucus carota subsp. halophilus: composition, antifungal activity and cytotoxicity. J Ethnopharmacol 119:129–134 [View Article][PubMed]
    [Google Scholar]
  60. Tian J., Ban X. Q., Zeng H., Huang B., He J. S., Wang Y. W. 2011; In vitro and in vivo activity of essential oil from dill (Anethum graveolens L.) against fungal spoilage of cherry tomatoes. Food Control 22:1992–1999 [View Article]
    [Google Scholar]
  61. Tian J., Ban X. Q., Zeng H., He J. S., Chen Y. X., Wang Y. W. 2012; The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. PLoS ONE 7:e30147 [View Article][PubMed]
    [Google Scholar]
  62. Tzakou O., Pitarokili D., Chinou I. B., Harvala C. 2001; Composition and antimicrobial activity of the essential oil of Salvia ringens. Planta Med 67:81–83 [View Article][PubMed]
    [Google Scholar]
  63. Xing M. Z., Zhang X. Z., Sun Z. L., Zhang H. Y. 2003; Perylenequinones act as broad-spectrum fungicides by generating reactive oxygen species both in the dark and in the light. J Agric Food Chem 51:7722–7724 [View Article][PubMed]
    [Google Scholar]
  64. Yili A., Aisa H. A., Maksimov V. V., Veshkurova O. N., Salikhov Sh. I. 2009; Chemical composition and antimicrobial activity of essential oil from seeds of Anethum graveolens growing in Uzebkistan. Chem Nat Compd 45:280–281 [View Article]
    [Google Scholar]
  65. Zeng H., Tian J., Zheng Y. C., Ban X. Q., Zeng J. S., Mao Y. H., Wang Y. W. 2011; In vitro and in vivo activities of essential oil from the seed of Anethum graveolens L. against Candida spp. Evid Based Complement Alternat Med 2011:659704 [View Article][PubMed]
    [Google Scholar]
  66. Zorov D. B., Krasnikov B. F., Kuzminova A. E., Vysokikh M. Y., Zorova L. D. 1997; Mitochondria revisited. Alternative functions of mitochondria. Biosci Rep 17:507–520 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.055467-0
Loading
/content/journal/jmm/10.1099/jmm.0.055467-0
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