Effect of Carum carvi essential oil on ERG6 gene expression and virulence factors in Candida albicans

Document Type : Original Articles

Authors

1 Department of Mycology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

2 Department of Mycology, Pasteur Institute of Iran, Tehran, Iran

Abstract

Background and Purpose: The present study was conducted to investigate the inhibitory effects of Carum carvi essential oil (EO) against ERG6 gene expression in relation to fungal growth and some important virulence factors in Candida albicans.
Materials and Methods: The minimum inhibitory concentration (MIC) of C. carvi EO against C. albicans was determined by the Clinical and Laboratory Standards Institute M27-A4 method at a concentration range of 20-1280 μg/ml. Furthermore, the expression of ERG6 gene was studied at the 0.5× MIC concentration of C. carvi EO using real-time polymerase chain reaction. The proteinase and phospholipase activities, cell surface hydrophobicity (CSH), and cell membrane ergosterol (CME) content of C. albicans were also assessed at the 0.5× MIC concentration of the plant EO using the approved methods. In addition, fluconazole (FLC) was used as a control antifungal drug.
Results: The results indicated that the MIC and minimum fungicidal concentration of C. carvi EO for C. albicans growth were 320 and 640 μg/ml, respectively. The expression of fungal ERG6 at an mRNA level and ergosterol content of yeast cells were significantly decreased by both C. carvi EO (640 μg/ml) and FLC (2 μg/ml). The proteinase and phospholipase activities were also reduced in C. carvi EO by 49.82% and 53.26%, respectively, while they were inhibited in FLC-treated cultures by 27.72% and 34.67%, respectively. Furthermore, the CSH was inhibited in EO- and FLC-treated cultures by 12.75% and 20.80%, respectively.
Conclusion: Our findings revealed that C. carvi EO can be considered a potential natural compound in the development of an efficient antifungal agent against C. albicans.
 

Keywords

References

1. Costa-de-Oliveira S, Rodrigues AG. Candida albicans antifungal resistance and tolerance in bloodstream infections: the triad yeast-host-antifungal. Microorganisms. 2020; 8(2):E154. 
2. Chin VK, Lee TY, Rusliza B, Chong PP. Dissecting Candida albicans infection from the perspective of C. albicans virulence and omics approaches on host-pathogen interaction: a Review. Int J Mol Sci. 2016; 17(10):E1643.
3. Sardi JC, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJ. Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol. 2013; 62(Pt 1):10-24.
4. Sadeghi G, Mousavi SF, Ebrahimi-Rad M, Ardakani E, Eslamifar A, Shams-Ghahfarokhi M, et al. In vivo and in vitro pathogenesis and virulence factors of Candida albicans strains isolated from cutaneous candidiasis. Iran Biomed J. 2020; 25:257-66.
5. Yu Q, Zhang B, Ma F, Jia C, Xiao C, Zhang B, et al. Novel
mechanisms of surfactants against Candida albicans growth and morphogenesis. Chem Biol Interact. 2015; 227:1-6.
6. Marcos-Zambrano L, Escribano P, Bouzaa E, Guineaa J. Production of biofilm by Candida and non-Candida spp. isolates causing fungemia: comparison of biomass production and metabolic activity and development of cut-off points. Int J Med Microbiol. 2014; 304(8):1192-8.
7. Jahanshiri Z, Shams-Ghahfarokhi M, Asghari-Paskiabi F, Saghiri R, Razzaghi-Abyaneh M. α-Bisabolol inhibits Aspergillus fumigatus Af239 growth via affecting microsomal Δ24-sterol methyltransferase as a crucial enzyme in ergosterol biosynthesis pathway. World J Microbiol Biotechnol. 2017; 33(3):55.
8. Khan M, Ahmad I. Antibiofilm activity of certain phytocompounds and their synergy with fluconazole against Candida albicans biofilms. J Antimicrob Chemother. 2012; 67(3):618-21.
9. Patel M, Gulube Z, Dutton M. The effect of Dodonaea viscosa var. angustifolia on Candida albicans proteinase and phospholipase production and adherence to oral epithelial cells. J Ethnopharmacol. 2009; 124(3):562-5.
10. Consolaro ME, Gasparetto A, Svidzinski TI, Peralta RM. Effect of pepstatin A on the virulence factors of Candida albicans strains isolated from vaginal environment of patients in three different clinical conditions. Mycopathologia. 2006; 162(2):75-82.
11. Dabiri S, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. Comparative analysis of proteinase, phospholipase, hydrophobicity and biofilm forming ability in Candida species isolated from clinical specimens. J Mycol Med. 2018; 28(3):437-42.
12. Razzaghi-Abyaneh M, Shams-Ghahfarokhi M, Rai M. Antifungal plants of Iran: an insight into ecology, chemistry, and molecular biology, in Antifungal Metabolites from Plants. Berlin: Springer; 2013. P. 27-57.
13. Shams-Ghahfarokhi M, Shokoohamiri MR, Amirrajab N, Moghadasi B, Ghajari A, Zeini F, et al. In vitro antifungal activities of Allium cepa, Allium sativum and ketoconazole against some pathogenic yeasts and dermatophytes. Fitoterapia. 2006; 77(4):321-3. 
14. Alves M, Gonçalves MJ, Zuzarte M, Alves-Silva JM, Cavaleiro C, Cruz MT, et al. Unveiling the antifungal potential of two iberian thyme essential oils: effect on C. albicans germ tube and preformed biofilms. Front Pharmacol. 2019; 10:446. 
15. Serra E, Hidalgo-Bastida LA, Verran J, Williams D, Malic S. Antifungal activity of commercial essential oils and biocides against Candida albicans. Pathogens. 2018; 7(1):E15. 
16. Freire JC, Júnior JK, Silva DF, de Sousa JP, Guerra FQ, de Oliveira Lima E. Antifungal activity of essential oils against Candida albicans strains isolated from users of dental prostheses. Evid Based Complement Alternat Med. 2017; 2017:7158756.
17. Hassanpour P, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. Antifungal activity of eugenol against Cryptococcus neoformans biological activity and Cxt1p gene expression. Curr Med Mycol. 2020; 6(1):9-14.
18. Panda H. Handbook on spices and condiments (cultivation, processing and extraction). New Delhi, India: Asia Pacific Business Press Inc; 2010.
19. Grigore A, Colceru-Mihul SV, Paraschiv I, Nita SU, Christof RA, Iuksel RA, et al. Chemical analysis and antimicrobial activity of indigenous medicinal species volatile oils. Roman Biotechnol Lett. 2012; 17(5):7620-7.
20. Nasiri S, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. Inhibitory effect of Carum carvi essential oils on growth of Candida albicans. Sci J Microb. 2014; 3(7):74-7.
21. Razzaghi-Abyaneh M, Shams-Ghahfarokhi M, Rezaee MB, Jaimand K, Alinezhad S, Saberi R, et al. Chemical composition and antiaflatoxigenic activity of Carum carvi L., Thymus vulgaris and Citrus aurantifolia essential oils. Food Control. 2009; 20(11):1018-24.
22. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts. CLSI standard M27-A4. 4th ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2017.
23. Price MF, Wikinson ID, Gentry LO. Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia. 1982; 20(1):7-14.
24. Samaranayake YH, Dassanayake RS, Jayatilake JA, Chgeung BP, Yau JY, Yeung KW, et al. Phospholipase B enzyme experission is not associated with other virulence attributes in Candida albicans isolates from patints with human immunodeficiency virus infection. J Med Microbiol. 2005; 54(6):583-93.
25. Jahanshiri Z, Shams-Ghahfarokhi M, Allameh A, Razzaghi-Abyaneh M. Inhibitory effect of eugenol on aflatoxin B1 production in Aspergillus parasiticus by downregulating the expression of major genes in the toxin biosynthetic pathway. World J Microbiol Biotechnol. 2015; 31(7):1071-8.
26. Jensen-Pergakes KL, Kennedy MA, Lees ND, Barbuch R, Koegel C, Bard M. Sequencing, disruption, and characterization of the Candida albicans sterol methyltransferase (ERG6) gene: drug susceptibility studies in ERG6 mutants. Antimicrob Agents Chemother. 1998; 42(5):1160-7.
27. Razzaghi-Abyaneh M, Shams-Ghahfarokhi M, Rai M. Medical mycology: current trends and future prospects. Florida: CRC Press; 2015. P. 442.
28. Pakshir K, Zomorodian K, Karamitalab M, Jafari M, Taraz H, Ebrahimi H. Phospholipase, esterase and hemolytic activities of Candida spp. isolated from onychomycosis and oral lichen planus lesions. J Mycol Med. 2013; 23(2):113-8.
29. Razzagh-parast A, Shams Ghahfarokhi, Yadegari MH, Razzaghi Abyaneh M. Antifungal effects of Allium cepa and some azoles in intact forms and in combinations to each other against pathogenic yeasts. Kowsar Med J. 2008; 13(2):103-13.
30. Nehiri M, Aouane EM, Tarfaoui K, Choukri S, Chaib Y, Inekach S, et al. Evaluation of the antibacterial activity of Carum Carvi L. essential oil. Am J Innovat Res Appl Sci. 2017; 5(6):67-70.
31. Razzaghi-Abyaneh M, Yoshinari T, Shams-Ghahfarokhi M,
Rezaee MB, Nagasawa H, Sakuda S. Dillapiol and apiol as specific inhibitors of the biosynthesis of aflatoxin G1 in Aspergillus parasiticus. Biosci Biotechnol Biochem. 2007; 71(9):2329-32.
32. Ibrahim GS, Kiki MJ. Chemical composition, antifungal and antioxidant activity of some spice essential oils. Int J Life Sci Pharma Res. 2020; 10(1):L43-50.
33. Iacobellis N, Cantore P, Capasso F, Felice S, Antibacterial activity of Cuminum cyminum L. and Carum carvi essential oils. J Agric Food Chem. 2005; 53(1):57-61.
34. Begum J, Bhuiyan MN, Chowdhury JU, Hoque MN, Anwar MN. Antimicrobial activity of essential oil from seeds of Carum carvi and its composition. Bangladesh J Microbiol. 2008; 25(2):85-9.
35. Siripornvisal S, Thawornluk P, Rungprom W. Screening for antifungal activity and active components of crude extracts from 6 Umbelliferae. Agric Sci J. 2011; 42(2):361-4.
36. Ben Salha G, Herrera Díaz R, Lengliz O, Abderrabba M, Labidi J. Effect of the chemical composition of free-terpene hydrocarbons essential oils on antifungal activity. Molecules. 2019; 24(19):E3532.
37. Sanglard D, Ischer F, Parkinson T, Falconer D, Bille J. Candida albicans mutations in the ergosterol biosynthetic pathway and resistance to several antifungal agents. Antimicrob Agents Chemother. 2003; 47(8):2404-12.
38. Naderi-Kalali B, Allameh A, Rasaee MJ, Bach HJ, Behechti A, Doods K, et al. Suppressive effects of caraway (Carum carvi) extracts on 2, 3, 7, 8-tetrachloro-dibenzo-p-dioxin-dependent gene expression of cytochrome P450 1A1 in the rat H4IIE cells. Toxicol in Vitro. 2005; 19(3):373-7.
39. Korashy HM, Shayeganpour A, Brocks DR, El-Kadi AO. Induction of cytochrome P450 1A1 by ketoconazole and itraconazole but not fluconazole in murine and human hepatoma cell lines. Toxicol Sci. 2007; 97(1):32-43.
Current Medical Mycology
Volume 6, Issue 2
June 2020
Pages 30-36

Files

History

  • Receive Date: 04 March 2020
  • Revise Date: 13 May 2020
  • Accept Date: 20 June 2020
  • Publish Date: 01 June 2020

Share

How to cite

Statistics