Abstract
Phlorotannins from the brown alga, Eisenia bicyclis, are known to possess strong antimicrobial activity against several microbial pathogens. In this study, the antifungal activity of phlorotannins against Candida albicans was evaluated. Among the six phlorotannins tested in the present study, fucofuroeckol-A (FF) exhibited potent antifungal activity with minimum inhibitory concentration (MIC) value of 512 μg mL−1 against C. albicans strains. It is also observed that FF restored the antifungal effect of fluconazole against fluconazole-resistant C. albicans in the combination mode. The MIC values of fluconazole against C. albicans strains drastically decreased by three- to fourfold in the combination of FF-fluconazole. Furthermore, analysis of fractional inhibitory concentration (FIC) indices revealed that the median ΣFIC against C. albicans strains ranged from 0.287 to 0.508 with FF-A and fluconazole combination indicating synergistic antifungal effects with restoring antifungal activity of fluconazole. The results obtained in this study imply that phlorotannins especially FF derived from E. bicyclis can be a potential source to develop an antifungal agent against drug-resistant C. albicans infection.
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Cao Y, Huang S, Dai B, Zhu Z, Lu H, Dong L, Cao Y, Wang Y, Gao P, Chai Y, Jiang Y (2009) Candida albicans cells lacking CaMCA1-encoded metacaspase show resistance to oxidative stress-induced death and change in energy metabolism. Fungal Genet Biol 46:183–189
Clinical and Laboratory Standards Institute (CLSI) (2012) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved Standard-Ninth Edition. Wayne, Pennsylvania, pp 07-A9
de Aquino LJ, Costa CR, de Araújo CR, Souza LK, Silva Mdo R (2009) Susceptibility testing of Candida albicans isolated from oropharyngeal mucosa of HIV(+) patients to fluconazole, amphotericin B and caspofungin. Killing kinetics of caspofungin and amphotericin B against fluconazole resistant and susceptible isolates. Braz J Microbiol 40:163–169
Eom SH, Kim DH, Lee SH, Yoon NY, Kim JH, Kim TH, Chung YH, Kim SB, Kim YM, Kim HW, Lee MS, Kim YM (2012a) In vitro antibacterial activity and synergistic antibiotic effects of phlorotannins isolated from Eisenia bicyclis against methicillin-resistant Staphylococcus aureus. Phytother Res 27:1260–1264
Eom SH, Lee SH, Yoon NY, Jung WK, Jeon YJ, Kim SK, Lee MS, Kim YM (2012b) α-glucosidase-and α-amylase-inhibitory activities of phlorotannins from Eisenia bicyclis. J Sci Food Agric 92:2084–2090
Eom SH, Lee DS, Kang YM, Son KT, Jeon YJ, Kim YM (2013a) Application of yeast Candida utilis to ferment Eisenia bicyclis for enhanced antibacterial effect. Appl Biochem Biotechnol 171:569–582
Eom SH, Lim KS, Kim YM (2013b) Potential of Candida utilis to ferment Ecklonia cava by-product for enhanced anti-methicillin-resistant Staphylococcus aureus (MRSA) activity. J Appl Phycol 25:1949–1956
Eom SH, Moon SY, Lee DS, Kim HJ, Park K, Lee EW, Kim TH, Chung YH, Lee MS, Kim YM (2015) In vitro antiviral activity of dieckol and phlorofucofuroeckol-A isolated from edible brown alga Eisenia bicyclis against murine norovirus. Algae 30:241–246
Eom SH, Lee EH, Park K, Kwon JY, Kim PH, Jung WK, Kim YM (2017) Eckol from Eisenia bicyclis inhibits inflammation through the Akt/NF-κB signaling in Propionibacterium acnes-induced human keratinocyte Hacat cells. J Food Biochem 41:e12312. doi:10.1111/jfbc.12312
Ghannoum MA, Elewski B (1999) Successful treatment of fluconazole-resistant oropharyngeal candidiasis by a combination of fluconazole and terbinafine. Clin Diagn Lab Immunol 6:921–923
Hsieh MH, Yu CM, Yu VL, Chow JW (1993) Synergy assessed by checkerboard. A critical analysis. Diagn Microbiol Infect Dis 16:343–349
Kim KH, Eom SH, Kim HJ, Lee DS, Nshimiyumukiza O, Kim SD, Kim YM, Lee MS (2014) Antifungal and synergistic effects of an ethyl acetate extract of the edible brown seaweed Eisenia bicyclis against Candida species. Fish Aquat Sci 17:209–214
Lee W, Lee DG (2014) An antifungal mechanism of curcumin lies in membrane-targeted action within Candida albicans. IUBMB Life 66:780–785
Lee JH, Eom SH, Lee EH, Jung YJ, Kim HJ, Jo MR, Son KT, Lee HJ, Kim JH, Lee MS, Kim YM (2014) In vitro antibacterial and synergistic effect of phlorotannins isolated from edible brown seaweed Eisenia bicyclis against acne-related bacteria. Algae 29:47–55
Liu H, Wang L, Li Y, Liu J, An M, Zhu S, Cao Y, Jiang Z, Zhao M, Cai Z, Dai L, Ni T, Liu W, Chen S, Wei C, Zang C, Tian S, Yang J, Wu C, Zhang D, Liu H, Jiang Y (2014) Structural optimization of berberine as a synergist to restore antifungal activity of fluconazole against drug-resistant Candida albicans. ChemMedChem 9:207–216
Martins CV, da Silva DL, Neres AT, Magalhães TF, Watanabe GA, Modolo LV, Sabino AA, de Fátima A, de Resende MA (2009) Curcumin as a promising antifungal of clinical interest. J Antimicrob Chemother 63:337–339
Meletiadis J, Pournaras S, Roilides E, Walsh TJ (2010) Defining fractional inhibitory concentration index cutoffs for additive interactions based on self-drug additive combinations, Monte Carlo simulation analysis, and in vitro-in vivo correlation data for antifungal drug combinations against Aspergillus fumigatus. Antimicrob Agents Chemother 54:602–609
Neelofar K, Shreaz S, Rimple B, Muralidhar S, Nikhat M, Khan LA (2011) Curcumin as a promising anticandidal of clinical interest. Can J Microbiol 57:204–210
Nshmiyumukiza O, Kang SK, Kim HJ, Lee EH, Han HN, Kim YH, Kim DH, Kim JH, Eom SH, Kim YM (2015) Synergistic antibacterial activity of Ecklonia cava (Phaeophyceae: Laminariales) against Listeria monocytogenes (Bacillales: Listeriaceae). Fish Aquat Sci 18:1–6
Pfaller MA (2012) Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am J Med 125:S3–S13
Rex JH, Pfaller MA, Galgiani JN, Bartlett MS, Espinel-Ingroff A, Ghannoum MA, Lancaster M, Odds FC, Rinaldi MG, Walsh TJ, Barry AL (1997) Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data for fluconazole, itraconazole, and candida infections. Subcommittee on antifungal susceptibility testing of the National Committee for Clinical Laboratory Standards. Clin Infect Dis 24:235–247
Sharma M, Manoharlal R, Puri N, Prasad R (2010) Antifungal curcumin induces reactive oxygen species and triggers an early apoptosis but prevents hyphae development by targeting the global repressor TUP1 in Candida albicans. Biosci Rep 30:391–404
Treyvaud-Amiguet V, Petit P, Ta CA, Nuñez R, Sánchez-Vindas P, Alvarez LP, Smith ML, Arnason JT, Durst T (2006) Phytochemistry and antifungal properties of the newly discovered tree Pleodendron costaricense. J Nat Prod 69:1005–1009
Tsao SM, Yin MC (2000) Enhanced inhibitory effect from interaction of curcumin with amphotericin B or fluconazole against Candida species. J Food Drug Anal 8:208–212
Vengurlekar S, Sharma R, Trivedi P (2012) Efficacy of some natural compounds as antifungal agents. Pharmacogn Rev 6:91–99
Xie CF, Qu JB, Wu XZ, Liu N, Ji M, Lou HX (2010) Antifungal macrocyclic bis (bibenzyls) from the Chinese liverwort Ptagiochasm intermedlum L. Nat Prod Res 24:515–552
Acknowledgements
This research was supported by Marine Biotechnology Program (20150220) funded by Ministry of Oceans and Fisheries, Republic of Korea. The pathogen for this study was provided by the Gyeongsang National University Hospital Branch of National Culture Collection for pathogens (GNUH-NCCP).
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Kim, KH., Yu, D., Eom, SH. et al. Fucofuroeckol-A from edible marine alga Eisenia bicyclis to restore antifungal activity of fluconazole against fluconazole-resistant Candida albicans . J Appl Phycol 30, 605–609 (2018). https://doi.org/10.1007/s10811-017-1232-1
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DOI: https://doi.org/10.1007/s10811-017-1232-1