View More View Less
  • 1 University of Pécs, Pécs, Hungary
  • 2 University of Pécs, Pécs, Hungary
Restricted access

The present study investigated the linalool (Lol)-induced effects in acute toxicity tests in the human pathogen Candida albicans (C. albicans). Lol treatments induced reduced germ tube formation of the pathogen, which plays a crucial role in the virulence. In comparison with the untreated control, the exposure of 107 cells ml−1 to 0.7 mM or 1.4 mM Lol for one hour induced 20% and 30% decrements, respectively, in the colony-forming ability. At the same time, these treatments caused dose-dependent decrease in the levels of superoxide anion radical and total reactive oxygen species, while there was 1.5 and 1.8-fold increases in the concentrations of peroxides and lipid peroxides, respectively, indicating oxidative stress induction in the presence of Lol. Lol treatments resulted in different adaptive modifications of the antioxidant system. In 0.7 mM-treated cells, decreased specific activities of superoxide dismutase and catalase were detected, while exposure to 1.4 mM Lol resulted in the up-regulation of catalase, glutathione reductase and glutathione peroxidases.

  • 1.

    Anderson, M. E. (1985) Determination of glutathione and glutathione disulphide in biological samples. Methods Enzymol. 113, 548555.

  • 2.

    Ao, Y., Satoh, K., Shibano, K., Kawahito, Y., Shioda, S. (2008) Singlet oxygen scavenging activity and cytotoxicity of essential oils of Rutaceae. J. Clin. Biochem. Nutr. 43, 612.

    • Search Google Scholar
    • Export Citation
  • 3.

    Bakkali, F., Averbeck, S., Idaomar, M. (2008) Biological effects of essential oils — A review. Food Chem. Toxicol. 46, 446475.

  • 4.

    Bickers, D., Calowb, P., Greimc, H., Hanifind, J. M. et al. (2003) A toxicologic and dermatologic assessment of linalool and related esters when used as fragrance ingredients. Food Chem. Toxicol. 41, 919942.

    • Search Google Scholar
    • Export Citation
  • 5.

    Blaskó, Á., Gazdag, Z., Gróf, P., Máté, G. et al. (2017) Effects of clary sage oil and its main components, linalool and linalyl acetate, on the plasma membrane of Candida albicans: an in vivo EPR study. Apoptosis 22, 175187.

    • Search Google Scholar
    • Export Citation
  • 6.

    Carmel-Harel, O., Storz, G. (2000) Roles of the glutathione-and thioredoxin-dependent reduction system in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Ann. Rev. Microbiol. 54, 439461.

    • Search Google Scholar
    • Export Citation
  • 7.

    Casao, A., Cebrián, I., Asumpção, M. E., Pérez-Pé, R. et al. (2010) Seasonal variations of melatonin in ram seminalplasma are correlated to those of testosterone and antioxidant enzymes. Reprod. Biol. Endocrin. 59, 19.

    • Search Google Scholar
    • Export Citation
  • 8.

    Celik, S., Özkaya, A. (2002) Effects of intraperitoneally administered lipoic acid, vitamin E, and linalool on the level of total lipid and fatty acids in guinea pig brain with oxidative stress induced by H2O2. J. Biochem. Mol. Biol. 35, 547552.

    • Search Google Scholar
    • Export Citation
  • 9.

    Chiu, D. T. Y., Stults, F. H., Tappel, A. L. (1976) Purification and properties of rat lung soluble glutathione peroxidase. Biochim. Biophys. Acta 445, 558566.

    • Search Google Scholar
    • Export Citation
  • 10.

    Cho, S. Y., Jun, H. J., Lee, J. H., Lee, J. H. et al. (2011) Linalool reduces the expression of 3-hydroxy-3-methylglutaryl CoA reductase via sterol regulatory element binding protein-2-and ubiquitindependent mechanisms. FEBS Lett. 585, 32893296.

    • Search Google Scholar
    • Export Citation
  • 11.

    Emri, T., Bartók, G., Szentirmai, A. (1994) Regulation of specific activity of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase in Penicillium chrysogenum. FEMS Microbiol. Lett. 117, 6770.

    • Search Google Scholar
    • Export Citation
  • 12.

    Erdogan, A., Ozkan, A. (2013) A comparative study of cytotoxic, membrane and DNA damaging effects of Origanum majorana’s essential oil and its oxygenated monoterpene component linalool on parental and epirubicin-resistant H1299 cells. Biologia 68, 754761.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ferguson, L. R., von Borstel, R. C. (1992) Induction of the cytoplasmatic ‘petite’ mutation by chemical and physical agents in Saccharomyces cerevisiae. Mutat. Res. 265, 103148.

    • Search Google Scholar
    • Export Citation
  • 14.

    Fisher, K., Phillips, C. A. (2006) The effects of lemon, orange and bergamot essential oils and their components on the survival of Campylobacter jejuni, Escherichia coli O157, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus in vitro and in food systems. J. Appl. Microbiol. 101, 12321240.

    • Search Google Scholar
    • Export Citation
  • 15.

    Gazdag, Z., Fujs, S., Kőszegi, B., Kálmán, N. et al. (2011) The abc1-/coq8-respiratory-deficient mutant of Schizosaccharomyces pombe suffers from glutathione underproduction and hyperaccumulates Cd2+. Folia Microbiol. 56, 353359.

    • Search Google Scholar
    • Export Citation
  • 16.

    Gazdag, Z., Máté, G., Čertik, M., Türmer, K. et al. (2014) Tert-Butyl hydroperoxide-induced differing plasma membrane and oxidative stress processes in yeast strains BY4741 and erg5Δ. J. Basic Microbiol. 54, 5062.

    • Search Google Scholar
    • Export Citation
  • 17.

    Gille, G., Sigler, K. (1995) Oxidative stress and living cells. Folia Microbiol. 40, 131152.

  • 18.

    Gónzalez-Párraga, P., Alonso-Monge, R., Plá, J., Argüelles, J. C. (2010) Adaptive tolerance to oxidative stress and the induction of antioxidant enzymatic activities in Candida albicans are independent of the Hog1 and Cap1-mediated pathways. FEMS Yeast Res. 10, 747756.

    • Search Google Scholar
    • Export Citation
  • 19.

    Gu, Y., Ting, Z., Qiu, X., Zhang, X. et al. (2010) Linalool preferentially induces robust apoptosis of variety of leukaemia cells via upregulating p53 and cyclin-dependent kinase inhibitors. Toxicol. 268, 1924.

    • Search Google Scholar
    • Export Citation
  • 20.

    Halliwell, B., Gutteridge, J. M. C. (2007) Free Radicals in Biology and Medicine. Oxford University Press, New York.

  • 21.

    Jones, C. M., Lawrence, A., Wardman, P., Burkitt, M. J. (2003) Kinetics of superoxide scavenging by glutathione: an evaluation of its role in the removal of mitochondrial superoxide. Biochem. Soc. T. 31, 13371339.

    • Search Google Scholar
    • Export Citation
  • 22.

    Khan, A., Ahmad, A., Akhtar, F., Yousuf, S. et al. (2010) Ocimum sanctum essential oil and its active principles exert their antifungal activity by disrupting ergosterol biosynthesis and membrane integrity. Microbiol. 161, 816823.

    • Search Google Scholar
    • Export Citation
  • 23.

    Kim, D., Shin, W. S., Lee, K. H., Kim, K. et al. (2002) Rapid differentiation of Candida albicans from other Candida species using its unique germ tube formation at 39 °C. Yeast 19, 957962.

    • Search Google Scholar
    • Export Citation
  • 24.

    Kladniew, B. R., Polo, M., Villegas, S. M., Galle, M. et al. (2014) Synergistic antiproliferative and anticholesterogenic effects of linalool, 1, 8-cineole, and simvastatin on human cell lines. Chem-Biol. Interact. 214, 5768.

    • Search Google Scholar
    • Export Citation
  • 25.

    Lee, J., Dawes, I. W., Roe, J. H. (1995) Adaptive response of Schizosaccharomyces pombe to hydrogen peroxide and menadione. Microbiol. 141, 31273132.

    • Search Google Scholar
    • Export Citation
  • 26.

    Letizia, C. S., Cocchiara, J., Lalko, J., Api, A. M. (2003) Fragrance material review on linalool. Food Chem. Toxicol. 41, 943964.

  • 27.

    Martin, H. L., Teismann, P. (2009) Glutathione — a review on its role and significance in Parkinson’s disease. FASEB J. 23, 32633272.

    • Search Google Scholar
    • Export Citation
  • 28.

    Mayer, F. L., Wilson, D., Hube, B. (2013) Candida albicans pathogenicity mechanisms. Virulence 4, 119128.

  • 29.

    Máté, G., Gazdag, Z., Mike, N., Papp, G. et al. (2014) Regulation of oxidative stress-induced cytotoxic processes of citrinin in the fission yeast Schizosaccharomyces pombe. Toxicon 90, 155166.

    • Search Google Scholar
    • Export Citation
  • 30.

    Mirata, M. A., Wüst, M., Mosandl, A., Schrader, J. (2008) Fungal biotransformation of (±)-linalool. J. Agric. Food Chem. 56, 32873296.

    • Search Google Scholar
    • Export Citation
  • 31.

    Mitić-Ćulafić, D., Žegura, B., Nikolic, B., Vuković-Gacić, B. et al. (2009) Protective effect of linalool, myrcene and eucalyptol against t-butyl hydroperoxide induced genotoxicity in bacteria and cultured human cells. Food Chem. Toxicol. 47, 260266.

    • Search Google Scholar
    • Export Citation
  • 32.

    Oberley, L. W., Spitz, D. R. (1984) Assay of superoxide dismutase activity in tumor tissue. Methods Enzymol. 105, 457464.

  • 33.

    Pesti, M., Horváth, L., Vígh, L., Farkas, T. (1985) Lipid content and ESR determination of plasma membrane order parameter in Candida albicans sterol mutants. Acta Microbiol. Hung. 32, 305313.

    • Search Google Scholar
    • Export Citation
  • 34.

    Peterson, G. L. (1983) Determination of total protein. Methods Enzymol. 91, 86105.

  • 35.

    Pinto, M. C., Mata, A. M., Lopez-Barea, I. (1984) Reversible inactivation of Saccharomyces cerevisiae glutathione reductase under reducing conditions. Arch. Biochem. Biophys. 228, 112.

    • Search Google Scholar
    • Export Citation
  • 36.

    Pócsi, I., Prade, R. A., Penninckx, M. J. (2004) Glutathione, altruistic metabolite in fungi. Adv. Microb. Physiol. 49, 176.

  • 37.

    Rahman, K. (2007) Studies on free radicals, antioxidants, and co-factors. Clin. Inertv. Aging 2, 219236.

  • 38.

    Roggenkamp, R., Sahm, H., Wagner, F. (1974) Microbial assimilation of methanol induction and function of catalase in Candida boidinii. FEBS Lett. 41, 283286.

    • Search Google Scholar
    • Export Citation
  • 39.

    Royall, J. A., Ischiropoulos, H. (1993) Evaluation of 2’, 7’-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch. Biochim. Biophys. 302, 348355.

    • Search Google Scholar
    • Export Citation
  • 40.

    Sardi, J. C. O., Scorzoni, L., Bernardi, T., Fusco-Almeida, A. M. et al. (2013) Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J. Med. Microbiol. 62, 1024.

    • Search Google Scholar
    • Export Citation
  • 41.

    Simić, A., Manoljović, D., Šegan, D., Todorić, M. (2007) Electrochemical behavior and antioxidant and prooxidant activity of natural phenolics. Molecules 12, 23272340.

    • Search Google Scholar
    • Export Citation
  • 42.

    Stanojević, J., Kneževic-Vukcević, J., Miloshev, G. (2004) Inhibition of oxidative DNA damage by plant antioxidants. Arch. Biol. Sci. Belgrade 56, 1718.

    • Search Google Scholar
    • Export Citation
  • 43.

    Usta, J., Kreydiyyeh, S., Knio, K., Barnabe, P. et al. (2009) Linalool decreases HepG2 viability by inhibiting mitochondrial complexes I and II, increasing reactive oxygen species and decreasing ATP and GSH levels. Chem-Biol. Interact. 180, 3946.

    • Search Google Scholar
    • Export Citation
  • 44.

    Warholm, M., Guthenberg, C., von Bahr, C., Mannervik, B. (1985) Glutathione transferases from human liver. Methods Enzymol. 113, 499504.

    • Search Google Scholar
    • Export Citation
  • 45.

    Zengin, H., Baysal, A. H. (2014) Antibacterial and antioxidant activity of essential oil terpenes against pathogenic and spoilage-forming bacteria and cell structure-activity relationships evaluated by SEM microscopy. Molecules 19, 1777317798.

    • Search Google Scholar
    • Export Citation
  • 46.

    Zore, G. B., Thakre, A. D., Rathod, V., Karuppayil, S. M. (2011) Evaluation of anti-Candida potential of geranium oil constituents against clinical isolates of Candida albicans differentially sensitive to fluconazole: inhibition of growth, dimorphism and sensitization. Mycoses 54, 99109.

    • Search Google Scholar
    • Export Citation