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Antifungal activity of Ferulago capillaris essential oil against Candida, Cryptococcus, Aspergillus and dermatophyte species

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Abstract

This study evaluates the composition, antifungal activity and mechanism of action of the essential oil of Ferulago capillaris (Link ex Spreng.) Cout. and its main components, limonene and α-pinene, against clinically relevant yeasts and moulds. Essential oil from the plant’s aerial parts was obtained by hydrodistillation and analysed by gas chromatography (GC) and gas chromatography/mass spectrometry (GC-MS). Essential oil showed high contents of limonene (30.9 %) and α-pinene (35.8 %). Minimum inhibitory concentrations (MICs) were measured according to the reference Clinical and Laboratory Standards Institute (CLSI) broth macrodilution protocols. Cell suspensions were subcultured in solid medium and the minimum fungicidal concentrations (MFCs) were rendered. The effect of essential oil on germ tube formation, mitochondrial function and ergosterol biosynthesis was investigated. Essential oil and α-pinene displayed low and similar MIC and MFC values against tested organisms (0.08 to 5.0 μL/mL), while limonene showed a weaker activity (0.32 to 20 μL/mL). Essential oil inhibited germ tube formation at sub-inhibitory concentrations on Candida albicans. The exposure of C. albicans to the essential oil resulted in impairment of mitochondrial functions in a dose-dependent manner. No difference in ergosterol content was observed in essential oil-treated C. albicans. F. capillaris and α-pinene display a broad fungicidal activity. The fungicidal activity of F. capillaris on C. albicans can be related to an induced oxidative stress which affects enzymes activity and the membrane potential of mitochondria. The essential oil of F. capillaris was shown to have potential for use in the development of clinically useful therapeutic preparations, particularly for topical application in the management of superficial mycoses.

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References

  1. Kavanagh K (2007) Medical mycology: cellular and molecular techniques. Wiley, Chichester

    Google Scholar 

  2. Cavaleiro C, Pinto E, Gonçalves MJ, Salgueiro L (2006) Antifungal activity of Juniperus essential oils against dermatophyte, Aspergillus and Candida strains. J Appl Microbiol 100:1333–1338

    Article  PubMed  CAS  Google Scholar 

  3. Zuzarte M, Vale-Silva L, Gonçalves MJ, Cavaleiro C, Vaz S, Canhoto J, Pinto E, Salgueiro L (2012) Antifungal activity of phenolic-rich Lavandula multifida L. essential oil. Eur J Clin Microbiol Infect Dis 31:1359–1366

    Article  PubMed  CAS  Google Scholar 

  4. Vale-Silva L, Silva M-J, Oliveira D, Gonçalves M-J, Cavaleiro C, Salgueiro L, Pinto E (2012) Correlation of the chemical composition of essential oils from Origanum vulgare subsp. virens with their in vitro activity against pathogenic yeasts and filamentous fungi. J Med Microbiol 61:252–260

    Article  PubMed  CAS  Google Scholar 

  5. Başer KHC, Demirci F (2007) Chemistry of essential oils. In: Berger RG (ed) Flavours and fragrances: chemistry, bioprocessing and sustainability. Springer, Berlin, pp 43–86

    Google Scholar 

  6. Rechinger KH, Hedge IC, Lamond JM (1987) Flora Iranica. Graz: Akademische Druck- und Verlagsanstalt 162:428–430

    Google Scholar 

  7. Başer KHC, Demirci B, Demirci F, Hashimoto T, Asakawa Y, Noma Y (2002) Ferulagone: a new monoterpene ester from Ferulago thirkeana essential oil. Planta Med 68:564–567

    Article  PubMed  Google Scholar 

  8. Ozturk B, Gur S, Coskun M, Kosan M, Erdurak C, Hafez G, Ozgunes O, Cetinkaya M (2004) Relaxant effect of Ferulago syriaca root extract on human corpus cavernosum. Eur Urol Suppl 3:62

    Article  Google Scholar 

  9. Khalighi-Sigaroodi F, Hadjiakhoondi A, Shafiee A, Mozaffarian VA, Shahverdi AR, Alavi SHR (2006) Phytochemical analysis of Ferulogo bernardii Tomk and M. Pimen. DARU 14:214–221

    CAS  Google Scholar 

  10. Taran M, Ghasempour HR, Shirinpour E (2011) Antimicrobial activity of essential oils of Ferulago angulata subsp. carduchorum. Jundishapur J Microbiol 3:10–14

    Google Scholar 

  11. Demetzos C, Perdetzoglou D, Gazouli M, Tan K, Economakis C (2000) Chemical analysis and antimicrobial studies on three species of Ferulago from Greece. Planta Med 66:560–563

    Article  PubMed  CAS  Google Scholar 

  12. Khalighi-Sigaroodi F, Hadjiakhoondi A, Shahverdi AR, Mozaffarian VA, Shafiee A (2005) Chemical composition and antimicrobial activity of the essential oil of Ferulago bernardii Tomk. and M. Pimen. DARU 13:100–104

    CAS  Google Scholar 

  13. Özkan AMG, Demirci B, Demirci F, Başer KHC (2008) Composition and antimicrobial activity of essential oil of Ferulago longistylis Boiss. fruits. J Essent Oil Res 20:569–573

    Article  Google Scholar 

  14. Castroviejo S (2003) Flora Ibérica, Real Jardín Botánico, vol X. CSIC, Madrid

    Google Scholar 

  15. Jiménez B, Grande MC, Anaya J, Torres P, Grande M (2000) Coumarins from Ferulago capillaris and F. brachyloba. Phytochemistry 53:1025–1031

    Article  PubMed  Google Scholar 

  16. Council of Europe (1997) European pharmacopoeia, 3rd edn. Council of Europe, Strasbourg

    Google Scholar 

  17. Cavaleiro C, Salgueiro LR, Miguel MG, Proença da Cunha A (2004) Analysis by gas chromatography–mass spectrometry of the volatile components of Teucrium lusitanicum and Teucrium algarbiensis. J Chromatogr A 1033:187–190

    Article  PubMed  CAS  Google Scholar 

  18. Adams RP (1995) Identification of essential oil components by gas chromatography/mass spectrometry. Allured Publishing Corporation, Carol Stream

    Google Scholar 

  19. Joulain D, König WA (1998) The atlas of spectral data of sesquiterpene hydrocarbons. E.B. Verlag, Hamburg

    Google Scholar 

  20. Clinical and Laboratory Standards Institute (CLSI) (2008) Reference method for broth dilution antifungal susceptibility testing of yeasts; Approved standard—Third edition. CLSI document M27-A3. CLSI, Wayne, PA

  21. Clinical and Laboratory Standards Institute (CLSI) (2008) Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; Approved standard—Second edition. CLSI document M38-A2. CLSI, Wayne, PA

  22. Pinto E, Afonso C, Duarte S, Vale-Silva L, Costa E, Sousa E, Pinto M (2011) Antifungal activity of xanthones: evaluation of their effect on ergosterol biosynthesis by high-performance liquid chromatography. Chem Biol Drug Des 77:212–222

    Article  PubMed  CAS  Google Scholar 

  23. Marichal P, Gorrens J, Van Cutsem J, Vanden Bossche H (1986) Culture media for the study of the effects of azole derivatives on germ tube formation and hyphal growth of C. albicans. Mykosen 29:76–81

    Article  PubMed  CAS  Google Scholar 

  24. Lopes G, Sousa C, Silva LR, Pinto E, Andrade PB, Bernardo J, Mouga T, Valentão P (2012) Can phlorotannins purified extracts constitute a novel pharmacological alternative for microbial infections with associated inflammatory conditions? PloS One 7:e31145. doi:10.1371/journal.pone.0031145

    Article  PubMed  CAS  Google Scholar 

  25. Ludovico P, Sansonetty F, Côrte-Real M (2001) Assessment of mitochondrial membrane potential in yeast cell populations by flow cytometry. Microbiology 147:3335–3343

    PubMed  CAS  Google Scholar 

  26. Ahmad A, Khan A, Manzoor N, Khan LA (2010) Evolution of ergosterol biosynthesis inhibitors as fungicidal against Candida. Microb Pathog 48:35–41

    Article  PubMed  CAS  Google Scholar 

  27. Pfaller MA, Diekema DJ, Sheehan DJ (2006) Interpretive breakpoints for fluconazole and Candida revisited: a blueprint for the future of antifungal susceptibility testing. Clin Microbiol Rev 19:435–447

    Article  PubMed  CAS  Google Scholar 

  28. Brand MD, Nicholls DG (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435:297–312

    Article  PubMed  CAS  Google Scholar 

  29. Erdurak C, Coşkun M, Demirci B, Başer KHC (2006) Composition of the essential oil of fruits and roots of Ferulago isaurica Peşmen andF. syriaca Boiss. (Umbelliferae) from Turkey. Flav Fragr J 21:118–121

    Article  CAS  Google Scholar 

  30. Mitchell AP (1998) Dimorphism and virulence in Candida albicans. Curr Opin Microbiol 1:687–692

    Article  PubMed  CAS  Google Scholar 

  31. Shepherd MG (1987) Cell envelope of Candida albicans. Crit Rev Microbiol 15:7–25

    Article  PubMed  CAS  Google Scholar 

  32. Hector RF (1993) Compounds active against cell walls of medically important fungi. Clin Microbiol Rev 6:1–21

    PubMed  CAS  Google Scholar 

  33. Brayman TG, Wilks JW (2003) Sensitive assay for antifungal activity of glucan synthase inhibitors that uses germ tube formation in Candida albicans as an end point. Antimicrob Agents Chemother 47:3305–3310

    Article  PubMed  CAS  Google Scholar 

  34. Saville SP, Lazzell AL, Bryant AP, Fretzen A, Monreal A, Solberg EO, Monteagudo C, Lopez-Ribot JL, Milne GT (2006) Inhibition of filamentation can be used to treat disseminated candidiasis. Antimicrob Agents Chemother 50:3312–3316

    Article  PubMed  CAS  Google Scholar 

  35. Rodriguez RJ, Low C, Bottema CD, Parks LW (1985) Multiple functions for sterols in Saccharomyces cerevisiae. Biochim Biophys Acta 837:336–343

    Article  PubMed  CAS  Google Scholar 

  36. Kelly SL, Lamb DC, Corran AJ, Baldwin BC, Kelly DE (1995) Mode of action and resistance to azole antifungals associated with the formation of 14 alpha-methylergosta-8,24(28)-dien-3 beta,6 alpha-diol. Biochem Biophys Res Commun 207:910–915

    Article  PubMed  CAS  Google Scholar 

  37. Onyewu C, Blankenship JR, Del Poeta M, Heitman J (2003) Ergosterol biosynthesis inhibitors become fungicidal when combined with calcineurin inhibitors against Candida albicans, Candida glabrata, and Candida krusei. Antimicrob Agents Chemother 47:956–964

    Article  PubMed  CAS  Google Scholar 

  38. Ahmad A, Khan A, Akhtar F, Yousuf S, Xess I, Khan LA, Manzoor N (2011) Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida. Eur J Clin Microbiol Infect Dis 30:41–50

    Article  PubMed  CAS  Google Scholar 

  39. Diao L, Mei Q, Xu JM, Liu XC, Hu J, Jin J, Yao Q, Chen ML (2012) Rebamipide suppresses diclofenac-induced intestinal permeability via mitochondrial protection in mice. World J Gastroenterol 18:1059–1066

    Article  PubMed  CAS  Google Scholar 

  40. Lemasters JJ, Nieminen A-L, Qian T, Trost LC, Herman B (1997) The mitochondrial permeability transition in toxic, hypoxic and reperfusion injury. Mol Cell Biochem 174:159–165

    Article  PubMed  CAS  Google Scholar 

  41. Vander Heiden MGV, Thompson CB (1999) Bcl-2 proteins: regulators of apoptosis or of mitochondrial homeostasis? Nat Cell Biol 1:E209–E216

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Fundação para a Ciência e a Tecnologia (FCT) through grants PEst-OE/SAU/UI0177/2011, CEQUIMED-PEst-OE/SAU/UI4040/2011 and PEst-C/EQB/LA0006/2011. G. Lopes (SFRH/BD/61565/2009) is indebted to FCT, FSE and POPH for the grant.

Thanks are also due to Dra Ana Cristina Tavares (CEF/Faculty of Pharmacy, University of Coimbra) for her help in prospecting plant material, and Prof. Alice Santos Silva and Dr. Elísio Costa for their help in the toxicity assays.

Conflict of interest

No conflict to disclose.

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Authors and Affiliations

  1. CEQUIMED-UP/Serviço de Microbiologia, Departamento de Ciências Biológicas, Faculdade de Farmácia, Universidade do Porto, Rua Jorge Viterbo Ferreira, 228, 4050-313, Porto, Portugal

    E. Pinto, K. Hrimpeng & S. Vaz

  2. REQUIMTE/Laboratório de Farmacognosia, Departamento de Química, Faculdade de Farmácia, Universidade do Porto, Rua Jorge Viterbo Ferreira, 228, 4050-313, Porto, Portugal

    G. Lopes

  3. CEF/Laboratório de Farmacognosia, Faculdade de Farmácia, Universidade de Coimbra, 3000-548, Coimbra, Portugal

    M. J. Gonçalves, C. Cavaleiro & L. Salgueiro

  4. Department of Microbiology, Faculty of Science, Burapha University, Chon-Buri, Thailand

    K. Hrimpeng

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  1. E. Pinto
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  2. K. Hrimpeng
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  5. M. J. Gonçalves
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  6. C. Cavaleiro
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  7. L. Salgueiro
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Correspondence to E. Pinto.

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Pinto, E., Hrimpeng, K., Lopes, G. et al. Antifungal activity of Ferulago capillaris essential oil against Candida, Cryptococcus, Aspergillus and dermatophyte species. Eur J Clin Microbiol Infect Dis 32, 1311–1320 (2013). https://doi.org/10.1007/s10096-013-1881-1

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  • DOI: https://doi.org/10.1007/s10096-013-1881-1

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