Could Flavonoids Compete with Synthetic Azoles in Diminishing Candida albicans Infections? A Comparative Review Based on In Vitro Studies

Author(s): Marija Smiljković , Marina Kostić , Dejan Stojković , Jasmina Glamočlija , Marina Soković* .

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 14 , 2019

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Abstract:

Flavonoids are polyphenolic compounds with already confirmed various health benefits. This review will shed light on flavonoids as potential antifungals in Candida albicans infections. C. albicans is an opportunistic pathogen able to cause serious health issues due to numerous virulence factors amplifying its pathogenicity. One of the most important virulence factors is Candida ability to form biofilms which are highly resistant to the treatment of antifungal drugs; making diminishing of this pathogen even more challenging. This review will focus on current knowledge on individual flavonoid compounds having the potential to deal with C. albicans in vitro, with special turn on antibiofilm potential and insight into the mode of action, where available. Majority of the commercial drugs for the treatment of candidiasis belong to azole class, so the activity of flavonoids will be compared with the activity of newly synthetized azole compounds, as well as with azole drugs that are already on the market as official therapeutics. This literature review will provide pros and cons for pushing future research towards exploring novel synthetic azoles or further examination of a wide pallet of natural flavonoids.

Keywords: Flavonoids, azoles, candidiasis, Candida sp., virulence factors, antifungals, biofilms.

[1]
Sawant, B.; Khan, T. Recent advances in delivery of antifungal agents for therapeutic management of candidiasis. Biomed. Pharmacother., 2017, 96, 1478-1490. [http://dx.doi.org/10.1016/j.biopha.2017.11.127]. [PMID: 29223551].
[2]
Mayer, F.L.; Wilson, D.; Hube, B. Candida albicans pathogenicity mechanisms. Virulence, 2013, 4(2), 119-128. [http://dx.doi.org/10.4161/viru.22913]. [PMID: 23302789].
[3]
Tsui, C.; Kong, E.F.; Jabra-Rizk, M.A. Pathogenesis of Candida albicans biofilm. Pathog. Dis., 2016, 74(4)ftw018 [http://dx.doi.org/10.1093/femspd/ftw018]. [PMID: 26960943].
[4]
Antinori, S.; Milazzo, L.; Sollima, S.; Galli, M.; Corbellino, M. Candidemia and invasive candidiasis in adults: A narrative review. Eur. J. Intern. Med., 2016, 34, 21-28. [http://dx.doi.org/10.1016/j.ejim.2016.06.029]. [PMID: 27394927].
[5]
Neves, N.A.; Carvalho, L.P.; De Oliveira, M.A.M.; Giraldo, P.C.; Bacellar, O.; Cruz, Á.A.; Carvalho, E.M. Association between atopy and recurrent vaginal candidiasis. Clin. Exp. Immunol., 2005, 142(1), 167-171. [http://dx.doi.org/10.1111/j.1365-2249.2005.02891.x]. [PMID: 16178872].
[6]
Pappas, P.G.; Kauffman, C.A.; Andes, D.R.; Clancy, C.J.; Marr, K.A.; Ostrosky-Zeichner, L.; Reboli, A.C.; Schuster, M.G.; Vazquez, J.A.; Walsh, T.J.; Zaoutis, T.E.; Sobel, J.D. Clinical practice guideline for the management of Candidiasis: 2016 update by the Infectious Diseases Society of America. Clin. Infect. Dis., 2016, 62(4), 1-50. [http://dx.doi.org/10.1093/cid/civ1194].
[7]
Whaley, S.G.; Berkow, E.L.; Rybak, J.M.; Nishimoto, A.T.; Barker, K.S.; Rogers, P.D. Azole Antifungal Resistance in Candida albicans and Emerging Non-albicans Candida Species. Front. Microbiol., 2017, 7(7), 2173. [http://dx.doi.org/10.3389/fmicb.2016.02173]. [PMID: 28127295].
[8]
Campoy, S.; Adrio, J.L. Antifungals. Biochem. Pharmacol., 2017, 133, 86-96. [http://dx.doi.org/10.1016/j.bcp.2016.11.019]. [PMID: 27884742].
[9]
Sheehan, D.J.; Hitchcock, C.A.; Sibley, C.M. Current and emerging azole antifungal agents. Clin. Microbiol. Rev., 1999, 12(1), 40-79. [http://dx.doi.org/10.1128/CMR.12.1.40]. [PMID: 9880474].
[10]
Bondaryk, M.; Kurzątkowski, W.; Staniszewska, M. Antifungal agents commonly used in the superficial and mucosal candidiasis treatment: mode of action and resistance development. Postepy Dermatol. Alergol., 2013, 30(5), 293-301. [http://dx.doi.org/10.5114/pdia.2013.38358]. [PMID: 24353489].
[11]
Kanafani, Z.A.; Perfect, J.R. Antimicrobial resistance: resistance to antifungal agents: mechanisms and clinical impact. Clin. Infect. Dis., 2008, 46(1), 120-128. [http://dx.doi.org/10.1086/524071]. [PMID: 18171227].
[12]
Berkow, E.L.; Lockhart, S.R. Fluconazole resistance in Candida species: A current perspective. Infect. Drug Resist., 2017, 10(10), 237-245. [http://dx.doi.org/10.2147/IDR.S118892]. [PMID: 28814889].
[13]
Marcos-Zambrano, L.J.; Escribano, P.; Sánchez, C.; Muñoz, P.; Bouza, E.; Guinea, J. Antifungal resistance to fluconazole and echinocandins is not emerging in yeast isolates causing fungemia in a Spanish tertiary care center. Antimicrob. Agents Chemother., 2014, 58(8), 4565-4572. [http://dx.doi.org/10.1128/AAC.02670-14]. [PMID: 24867979].
[14]
Müller, F.M.; Weig, M.; Peter, J.; Walsh, T.J. Azole cross-resistance to ketoconazole, fluconazole, itraconazole and voriconazole in clinical Candida albicans isolates from HIV-infected children with oropharyngeal candidosis. J. Antimicrob. Chemother., 2000, 46(2), 338-340. [http://dx.doi.org/10.1093/jac/46.2.338]. [PMID: 10933673].
[15]
García Rodríguez, L.A.; Duque, A.; Castellsague, J.; Pérez-Gutthann, S.; Stricker, B.H. A cohort study on the risk of acute liver injury among users of ketoconazole and other antifungal drugs. Br. J. Clin. Pharmacol., 1999, 48(6), 847-852. [http://dx.doi.org/10.1046/j.1365-2125.1999.00095.x]. [PMID: 10594489].
[16]
Kathiravan, M.K.; Salake, A.B.; Chothe, A.S.; Dudhe, P.B.; Watode, R.P.; Mukta, M.S.; Gadhwe, S. The biology and chemistry of antifungal agents: A review. Bioorg. Med. Chem., 2012, 20(19), 5678-5698. [http://dx.doi.org/10.1016/j.bmc.2012.04.045]. [PMID: 22902032].
[17]
Gao, M.; Wang, H.; Zhu, L. Quercetin assists fluconazole to inhibit biofilm formations of fluconazole-resistant Candida albicans in in vitro and in vivo antifungal managements of vulvovaginal candidiasis. Cell. Physiol. Biochem., 2016, 40(3-4), 727-742. [http://dx.doi.org/10.1159/000453134]. [PMID: 27915337].
[18]
Yordanov, M.; Dimitrova, P.; Patkar, S.; Saso, L.; Ivanovska, N. Inhibition of Candida albicans extracellular enzyme activity by selected natural substances and their application in Candida infection. Can. J. Microbiol., 2008, 54(6), 435-440. [http://dx.doi.org/10.1139/W08-029]. [PMID: 18535628].
[19]
Seleem, D.; Benso, B.; Noguti, J.; Pardi, V.; Murata, R.M. In vitro and in vivo antifungal activity of lichochalcone-A against Candida albicans biofilms. PLoS One, 2016, 11(6)e0157188 [http://dx.doi.org/10.1371/journal.pone.0157188]. [PMID: 27284694].
[20]
Rai Rima, S.; Singha, R.; Brahma, P.; Sanyal, K. Epigenetic determinants of phenotypic plasticity in Candida albicans. Fungal Biol. Rev., 2018, 32, 10-19. [http://dx.doi.org/10.1016/j.fbr.2017.07.002].
[21]
Lagree, K.; Desai, J.V.; Finkel, J.S.; Lanni, F. Microscopy of fungal biofilms. Curr. Opin. Microbiol., 2018, 43, 100-107. [http://dx.doi.org/10.1016/j.mib.2017.12.008]. [PMID: 29414442].
[22]
Hirota, K.; Yumoto, H.; Sapaar, B.; Matsuo, T.; Ichikawa, T.; Miyake, Y. Pathogenic factors in Candida biofilm-related infectious diseases. J. Appl. Microbiol., 2017, 122(2), 321-330. [http://dx.doi.org/10.1111/jam.13330]. [PMID: 27770500].
[23]
Nobile, C.J.; Johnson, A.D. Candida albicans biofilms and human disease. Annu. Rev. Microbiol., 2015, 69, 71-92. [http://dx.doi.org/10.1146/annurev-micro-091014-104330]. [PMID: 26488273].
[24]
Sun, D.; Hurdle, J.G.; Lee, R.; Lee, R.; Cushman, M.; Pezzuto, J.M. Evaluation of flavonoid and resveratrol chemical libraries reveals abyssinone II as a promising antibacterial lead. ChemMedChem, 2012, 7(9), 1541-1545. [http://dx.doi.org/10.1002/cmdc.201200253]. [PMID: 22847956].
[25]
Tsao, R. Chemistry and biochemistry of dietary polyphenols. Nutrients, 2010, 2(12), 1231-1246. [http://dx.doi.org/10.3390/nu2121231]. [PMID: 22254006].
[26]
Vetrani, C.; Vitale, M.; Bozzetto, L.; Della Pepa, G.; Cocozza, S.; Costabile, G.; Mangione, A.; Cipriano, P.; Annuzzi, G.; Rivellese, A.A. Association between different dietary polyphenol subclasses and the improvement in cardiometabolic risk factors: evidence from a randomized controlled clinical trial. Acta Diabetol., 2018, 55(2), 149-153. [http://dx.doi.org/10.1007/s00592-017-1075-x]. [PMID: 29151225].
[27]
Vitale, M.; Vaccaro, O.; Masulli, M.; Bonora, E.; Del Prato, S.; Giorda, C.B.; Nicolucci, A.; Squatrito, S.; Auciello, S.; Babini, A.C.; Bani, L.; Buzzetti, R.; Cannarsa, E.; Cignarelli, M.; Cigolini, M.; Clemente, G.; Cocozza, S.; Corsi, L.; D’Angelo, F.; Dall’Aglio, E.; Di Cianni, G.; Fontana, L.; Gregori, G.; Grioni, S.; Giordano, C.; Iannarelli, R.; Iovine, C.; Lapolla, A.; Lauro, D.; Laviola, L.; Mazzucchelli, C.; Signorini, S.; Tonutti, L.; Trevisan, R.; Zamboni, C.; Riccardi, G.; Rivellese, A.A. Polyphenol intake and cardiovascular risk factors in a population with type 2 diabetes: The TOSCA.IT study. Clin. Nutr., 2017, 36(6), 1686-1692. [http://dx.doi.org/10.1016/j.clnu.2016.11.002]. [PMID: 27890487].
[28]
Luo, Y.; Shang, P.; Li, D. Luteolin: a flavonoid that has multiple cardio-protective effects and its molecular mechanisms. Front. Pharmacol., 2017, 8, 692. [http://dx.doi.org/10.3389/fphar.2017.00692]. [PMID: 29056912].
[29]
Farhat, G.; Drummond, S.; Al-Dujaili, E.A.S. Polyphenols and their role in obesity management: a systematic review of randomized clinical trials. Phytother. Res., 2017, 31(7), 1005-1018. [http://dx.doi.org/10.1002/ptr.5830]. [PMID: 28493374].
[30]
Li, M.; Shi, A.; Pang, H.; Xue, W.; Li, Y.; Cao, G.; Yan, B.; Dong, F.; Li, K.; Xiao, W.; He, G.; Du, G.; Hu, X. Safety, tolerability, and pharmacokinetics of a single ascending dose of baicalein chewable tablets in healthy subjects. J. Ethnopharmacol., 2014, 156, 210-215. [http://dx.doi.org/10.1016/j.jep.2014.08.031]. [PMID: 25219601].
[31]
Bondonno, N.P.; Bondonno, C.P.; Blekkenhorst, L.C.; Considine, M.J.; Maghzal, G.; Stocker, R.; Woodman, R.J.; Ward, N.C.; Hodgson, J.M.; Croft, K.D. Flavonoid-rich apple improves endothelial function in individuals at risk for cardiovascular disease: a randomized controlled clinical trial. Mol. Nutr. Food Res., 2018, 62(3)1700674 [http://dx.doi.org/10.1002/mnfr.201700674]. [PMID: 29086478].
[32]
Eicher, T.; Hauptmann, S. The Chemistry of Heterocycles: Structure, Reactions, Synthesis, and Applications., 2nd ed; Richard, A.H.; Pamela, C., Eds.; Lippincott Williams and Wilkins: New York. 2006.
[33]
Kumar, V.; Kaur, K.; Gupta, G.K.; Sharma, A.K. Pyrazole containing natural products: Synthetic preview and biological significance. Eur. J. Med. Chem., 2013, 69, 735-753. [http://dx.doi.org/10.1016/j.ejmech.2013.08.053]. [PMID: 24099993].
[34]
Jiang, N.; Doseff, A.I.; Grotewold, E. Flavones: From Biosynthesis to Health Benefits. Plants (Basel), 2016, 5(2), 27. [http://dx.doi.org/10.3390/plants5020027]. [PMID: 27338492].
[35]
Shankar, E.; Goel, A.; Gupta, K.; Gupta, S. Plant flavone apigenin: An emerging anticancer agent. Curr. Pharmacol. Rep., 2017, 3(6), 423-446. [http://dx.doi.org/10.1007/s40495-017-0113-2]. [PMID: 29399439].
[36]
Lee, H.; Woo, E.R.; Lee, D.G. Apigenin induces cell shrinkage in Candida albicans by membrane perturbation. FEMS Yeast Res., 2018, 18(1)foy003 [http://dx.doi.org/10.1093/femsyr/foy003]. [PMID: 29346565].
[37]
Ozçelik, B.; Kartal, M.; Orhan, I. Cytotoxicity, antiviral and antimicrobial activities of alkaloids, flavonoids, and phenolic acids. Pharm. Biol., 2011, 49(4), 396-402. [http://dx.doi.org/10.3109/13880209.2010.519390]. [PMID: 21391841].
[38]
Smiljkovic, M.; Stanisavljevic, D.; Stojkovic, D.; Petrovic, I.; Marjanovic Vicentic, J.; Popovic, J.; Golic Grdadolnik, S.; Markovic, D.; Sankovic-Babice, S.; Glamoclija, J.; Stevanovic, M.; Sokovic, M. Apigenin-7-O-glucoside versus apigenin: Insight into the modes of anticandidal and cytotoxic actions. EXCLI J., 2017, 16(16), 795-807. [PMID: 28827996].
[39]
Cheah, H.L.; Lim, V.; Sandai, D. Inhibitors of the glyoxylate cycle enzyme ICL1 in Candida albicans for potential use as antifungal agents. PLoS One, 2014, 9(4)e95951 [http://dx.doi.org/10.1371/journal.pone.0095951]. [PMID: 24781056].
[40]
Mamadalieva, N.Z.; Herrmann, F.; El-Readi, M.Z.; Tahrani, A.; Hamoud, R.; Egamberdieva, D.R.; Azimova, S.S.; Wink, M. Flavonoids in Scutellaria immaculata and S. ramosissima (Lamiaceae) and their biological activity. J. Pharm. Pharmacol., 2011, 63(10), 1346-1357. [http://dx.doi.org/10.1111/j.2042-7158.2011.01336.x]. [PMID: 21899551].
[41]
Martins, N.; Ferreira, I.C.F.R.; Henriques, M.; Silva, S. In vitro anti-candida activity of Glycyrrhiza glabra L. Ind. Crops Prod., 2016, 83, 81-85. [http://dx.doi.org/10.1016/j.indcrop.2015.12.029].
[42]
Shahzad, M.; Sherry, L.; Rajendran, R.; Edwards, C.A.; Combet, E.; Ramage, G. Utilising polyphenols for the clinical management of Candida albicans biofilms. Int. J. Antimicrob. Agents, 2014, 44(3), 269-273. [http://dx.doi.org/10.1016/j.ijantimicag.2014.05.017]. [PMID: 25104135].
[43]
Mendes, A.; Mores, A.U.; Carvalho, A.P.; Rosa, R.T.; Samaranayake, L.P.; Rosa, E.A. Candida albicans biofilms produce more secreted aspartyl protease than the planktonic cells. Biol. Pharm. Bull., 2007, 30(9), 1813-1815. [http://dx.doi.org/10.1248/bpb.30.1813]. [PMID: 17827747].
[44]
Zhou, X.; Wang, F.; Zhou, R.; Song, X.; Xie, M. Apigenin: A current review on its beneficial biological activities J. Food Biochem, 2017, 41, e12376. [http://dx.doi.org/10.1111/jfbc.12376].
[45]
Xu, Y.; Xin, Y.; Diao, Y.; Lu, C.; Fu, J.; Luo, L.; Yin, Z. Synergistic effects of apigenin and paclitaxel on apoptosis of cancer cells. PLoS One, 2011, 6(12)e29169 [http://dx.doi.org/10.1371/journal.pone.0029169]. [PMID: 22216199].
[46]
Venigalla, M.; Gyengesi, E.; Münch, G. Curcumin and Apigenin - novel and promising therapeutics against chronic neuroinflammation in Alzheimer’s disease. Neural Regen. Res., 2015, 10(8), 1181-1185. [http://dx.doi.org/10.4103/1673-5374.162686]. [PMID: 26487830].
[47]
Shukla, S.; Gupta, S. Apigenin: A promising molecule for cancer prevention. Pharm. Res., 2010, 27(6), 962-978. [http://dx.doi.org/10.1007/s11095-010-0089-7]. [PMID: 20306120].
[48]
Cao, Y.; Dai, B.; Wang, Y.; Huang, S.; Xu, Y.; Cao, Y.; Gao, P.; Zhu, Z.; Jiang, Y. In vitro activity of baicalein against Candida albicans biofilms. Int. J. Antimicrob. Agents, 2008, 32(1), 73-77. [http://dx.doi.org/10.1016/j.ijantimicag.2008.01.026]. [PMID: 18374543].
[49]
Huang, S.; Cao, Y.Y.; Dai, B.D.; Sun, X.R.; Zhu, Z.Y.; Cao, Y.B.; Wang, Y.; Gao, P.H.; Jiang, Y.Y. In vitro synergism of fluconazole and baicalein against clinical isolates of Candida albicans resistant to fluconazole. Biol. Pharm. Bull., 2008, 31(12), 2234-2236. [http://dx.doi.org/10.1248/bpb.31.2234]. [PMID: 19043205].
[50]
Shirley, K.P.; Windsor, L.J.; Eckert, G.J.; Gregory, R.L. In Vitro effects of plantago major extract, aucubin, and baicalein on Candida albicans biofilm formation, metabolic activity, and cell surface hydrophobicity. J. Prosthodont., 2017, 26(6), 508-515. [http://dx.doi.org/10.1111/jopr.12411]. [PMID: 26618515].
[51]
Fu, Z.; Lu, H.; Zhu, Z.; Yan, L.; Jiang, Y.; Cao, Y. Combination of baicalein and Amphotericin B accelerates Candida albicans apoptosis. Biol. Pharm. Bull., 2011, 34(2), 214-218. [http://dx.doi.org/10.1248/bpb.34.214]. [PMID: 21415530].
[52]
Salazar-Aranda, R.; Granados-Guzmán, G.; Pérez-Meseguer, J.; González, G.M.; de Torres, N.W. Activity of polyphenolic compounds against Candida glabrata. Molecules, 2015, 20(10), 17903-17912. [http://dx.doi.org/10.3390/molecules201017903]. [PMID: 26426003].
[53]
Seleem, D.; Pardi, V.; Murata, R.M. Review of flavonoids: A diverse group of natural compounds with anti-Candida albicans activity in vitro. Arch. Oral Biol., 2017, 76, 76-83. [http://dx.doi.org/10.1016/j.archoralbio.2016.08.030]. [PMID: 27659902].
[54]
Miyazaki, Y.; Ichimura, A.; Sato, S.; Fujii, T.; Oishi, S.; Sakai, H.; Takeshima, H. The natural flavonoid myricetin inhibits gastric H+, K+-ATPase. Eur. J. Pharmacol., 2018, 820, 217-221. [http://dx.doi.org/10.1016/j.ejphar.2017.12.042]. [PMID: 29274333].
[55]
Rocha, G.R.; Florez Salamanca, E.J.; de Barros, A.L.; Lobo, C.I.V.; Klein, M.I. Effect of tt-farnesol and myricetin on in vitro biofilm formed by Streptococcus mutans and Candida albicans. BMC Complement. Altern. Med., 2018, 18(1), 61. [http://dx.doi.org/10.1186/s12906-018-2132-x]. [PMID: 29444673].
[56]
Kashyap, D.; Sharma, A.; Singh Tuli, H.; Sak, K.; Punia, S.; Mukherjee, T. Kaempferol – A dietary anticancer molecule with multiple mechanisms of action: Recent trends and advancements. J. Funct. Foods, 2017, 30, 203-219. [http://dx.doi.org/10.1016/j.jff.2017.01.022].
[57]
Shao, J.; Zhang, M.; Wang, T.; Li, Y.; Wang, C. The roles of CDR1, CDR2, and MDR1 in kaempferol-induced suppression with fluconazole-resistant Candida albicans. Pharm. Biol., 2016, 54(6), 984-992. [http://dx.doi.org/10.3109/13880209.2015.1091483]. [PMID: 26459663].
[58]
Li, X.; Tian, Y.; Wang, T.; Lin, Q.; Feng, X.; Jiang, Q.; Liu, Y.; Chen, D. Role of the p-coumaroyl moiety in the antioxidant and cytoprotective effects of flavonoid glycosides: comparison of astragalin and tiliroside. Molecules, 2017, 22(7)E1165 [http://dx.doi.org/10.3390/molecules22071165]. [PMID: 28704976].
[59]
Süzgeç-Selçuka, S.; Birteksöz, A.S. Flavonoids of Helichrysum chasmolycicum and its antioxidant and antimicrobial activities. S. Afr. J. Bot., 2011, 77(1), 170-174. [http://dx.doi.org/10.1016/j.sajb.2010.07.017].
[60]
Lee, J.; Mitchell, A.E. Pharmacokinetics of quercetin absorption from apples and onions in healthy humans. J. Agric. Food Chem., 2012, 60(15), 3874-3881. [http://dx.doi.org/10.1021/jf3001857]. [PMID: 22439822].
[61]
Gehrke, I.T.; Neto, A.T.; Pedroso, M.; Mostardeiro, C.P.; Da Cruz, I.B.; Silva, U.F.; Ilha, V.; Dalcol, I.I.; Morel, A.F. Antimicrobial activity of Schinus lentiscifolius (Anacardiaceae). J. Ethnopharmacol., 2013, 148(2), 486-491. [http://dx.doi.org/10.1016/j.jep.2013.04.043]. [PMID: 23684720].
[62]
Singh, B.N.; Upreti, D.K.; Singh, B.R.; Pandey, G.; Verma, S.; Roy, S.; Naqvi, A.H.; Rawat, A.K. Quercetin sensitizes fluconazole-resistant candida albicans to induce apoptotic cell death by modulating quorum sensing. Antimicrob. Agents Chemother., 2015, 59(4), 2153-2168. [http://dx.doi.org/10.1128/AAC.03599-14]. [PMID: 25645848].
[63]
Vashisth, P.; Nikhil, K.; Pemmaraju, S.; Pruthi, P.; Mallick, V.; Singh, H. Antibiofilm activity of quercetin-encapsulated cytocompatible nanofibers against Candida albicans. J. Bioact. Compat. Polym., 2013, 28(6), 652-665. [http://dx.doi.org/10.1177/0883911513502279].
[64]
Wagner, C.; Fachinetto, R.; Dalla Corte, C.L.; Brito, V.B.; Severo, D.; de Oliveira Costa Dias, G.; Morel, A.F.; Nogueira, C.W.; Rocha, J.B. Quercitrin, a glycoside form of quercetin, prevents lipid peroxidation in vitro. Brain Res., 2006, 1107(1), 192-198. [http://dx.doi.org/10.1016/j.brainres.2006.05.084]. [PMID: 16828712].
[65]
Valentová, K.; Vrba, J.; Bancířová, M.; Ulrichová, J.; Křen, V. Isoquercitrin: pharmacology, toxicology, and metabolism. Food Chem. Toxicol., 2014, 68, 267-282. [http://dx.doi.org/10.1016/j.fct.2014.03.018]. [PMID: 24680690].
[66]
Jun, J.E.; Woo, E.R.; Lee, D.G. Isoquercitrin, isolated from Aster yomena triggers ROS-mediated apoptosis in Candida albicans. J. Funct. Foods, 2016, 22, 347-357. [http://dx.doi.org/10.1016/j.jff.2016.01.041].
[67]
Yun, J.; Lee, H.; Ko, H.J.; Woo, E.R.; Lee, D.G. Fungicidal effect of isoquercitrin via inducing membrane disturbance. Biochim. Biophys. Acta, 2015, 1848(2), 695-701. [http://dx.doi.org/10.1016/j.bbamem.2014.11.019]. [PMID: 25445674].
[68]
Gullon, B.; Lu-Chau, T.; Moreira, M.T.; Lema, J.; Eibes, G. Rutin: A review on extraction, identification and purification methods, biological activities and approaches to enhance its bioavailability. Trends Food Sci. Technol., 2017, 67, 220-235. [http://dx.doi.org/10.1016/j.tifs.2017.07.008].
[69]
Han, Y. Rutin has therapeutic effect on septic arthritis caused by Candida albicans. Int. Immunopharmacol., 2009, 9(2), 207-211. [http://dx.doi.org/10.1016/j.intimp.2008.11.002]. [PMID: 19041425].
[70]
Siler, B.; Zivković, S.; Banjanac, T.; Cvetković, J.; Nestorović Živković, J.; Cirić, A.; Soković, M.; Mišić, D. Centauries as underestimated food additives: antioxidant and antimicrobial potential. Food Chem., 2014, 147, 367-376. [http://dx.doi.org/10.1016/j.foodchem.2013.10.007]. [PMID: 24206732].
[71]
Araruna, M.K.; Brito, S.A.; Morais-Braga, M.F.; Santos, K.K.; Souza, T.M.; Leite, T.R.; Costa, J.G.; Coutinho, H.D. Evaluation of antibiotic & antibiotic modifying activity of pilocarpine & rutin. Indian J. Med. Res., 2012, 135, 252-254. [PMID: 22446871].
[72]
Johann, S.; Mendes, B.G.; Missau, F.C.; de Resende, M.A.; Pizzolatti, M.G. Antifungal activity of five species of Polygala. Braz. J. Microbiol., 2011, 42(3), 1065-1075. [http://dx.doi.org/10.1590/S1517-83822011000300027]. [PMID: 24031724].
[73]
Xia, E.; He, X.; Li, H.; Wu, S.; Li, S.; Deng, G. Biological activities of polyphenols from grapes. In Polyphenols in human health and disease; Watson, R.R.; Preedy, V.R.; Zibadi S., Ed.; Academic Press San Diego. 2014, 5, pp. 47-58. http://dx.doi.org/10.1016/B978-0-12-398456-2.00005-0]
[74]
Yilmaz, Y. Novel uses of catechin in foods. Trends Food Sci. Technol., 2006, 17, 64-71. [http://dx.doi.org/10.1016/j.tifs.2005.10.005].
[75]
Anand, J.; Rai, N. Anticandidal synergistic activity of green tea catechins, antimycotics and copper sulphate as a mean of combinational drug therapy against candidiasis. J. Mycol. Med., 2017, 27(1), 33-45. [http://dx.doi.org/10.1016/j.mycmed.2016.08.004]. [PMID: 27743771].
[76]
Mendes de Toledo, C.E.; Santos, P.R.; Palazzo de Mello, J.C.; Dias Filho, B.P.; Nakamura, C.V.; Ueda-Nakamura, T. Antifungal properties of crude extracts, fractions and purified compounds from bark of Curatella americana L. (Dilleniaceae) against Candida species. Evid. Based Complement. Alternat. Med., 2015.2015673962 [http://dx.doi.org/10.1155/2015/673962]. [PMID: 26347790].
[77]
Navarro-Martínez, M.D.; García-Cánovas, F.; Rodríguez-López, J.N. Tea polyphenol epigallocatechin-3-gallate inhibits ergosterol synthesis by disturbing folic acid metabolism in Candida albicans. J. Antimicrob. Chemother., 2006, 57(6), 1083-1092. [http://dx.doi.org/10.1093/jac/dkl124]. [PMID: 16585130].
[78]
Chen, M.; Zhai, L.; Arendrup, M.C. In vitro activity of 23 tea extractions and epigallocatechin gallate against Candida species. Med. Mycol., 2015, 53(2), 194-198. [http://dx.doi.org/10.1093/mmy/myu073]. [PMID: 25605775].
[79]
CLSI. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard—Second Edition, M27-A2 Vol. 22 No. 15, Clinical and Laboratory Standards Institute Standards, Wayne, PA.
[80]
EUCAST. European Committee on Antimicrobial Susceptibility Testing, Antifungal Agents Breakpoint tables for interpretation of MICs. Version 9.0, valid from 2018-02-12.
[81]
Esch, H.L.; Kleider, C.; Scheffler, A.; Lehmann, L. Isoflavones: Toxicological Aspects and Efficacy.Nutraceuticals efficacy, safety and toxicity; Gupta, R.C., Ed.; Elsevier Science, Academic press, 2016, Vol. 34, pp. 465-478.
[82]
Kang, M.R.; Park, K.H.; Oh, S.J.; Yun, J.; Lee, C.W.; Lee, M.Y.; Han, S.B.; Kang, J.S. Cardiovascular protective effect of glabridin: Implications in LDL oxidation and inflammation. Int. Immunopharmacol., 2015, 29(2), 914-918. [http://dx.doi.org/10.1016/j.intimp.2015.10.020]. [PMID: 26526087].
[83]
Liu, W.; Li, L.P.; Zhang, J.D.; Li, Q.; Shen, H.; Chen, S.M.; He, L.J.; Yan, L.; Xu, G.T.; An, M.M.; Jiang, Y.Y. Synergistic antifungal effect of glabridin and fluconazole. PLoS One, 2014, 9(7)e103442 [http://dx.doi.org/10.1371/journal.pone.0103442]. [PMID: 25058485].
[84]
Messier, C.; Grenier, D. Effect of licorice compounds licochalcone A, glabridin and glycyrrhizic acid on growth and virulence properties of Candida albicans. Mycoses, 2011, 54(6), e801-e806. [http://dx.doi.org/10.1111/j.1439-0507.2011.02028.x]. [PMID: 21615543].
[85]
das Neves. M.V.; da Silva, T.M.; Lima, Ede.O.; da Cunha, E.V.; Oliveira, Ede.J. Isoflavone formononetin from red propolis acts as a fungicide against Candida sp. Braz. J. Microbiol., 2016, 47(1), 159-166. [http://dx.doi.org/10.1016/j.bjm.2015.11.009]. [PMID: 26887239].
[86]
Mbaveng, A.T.; Kuete, V.; Ngameni, B.; Beng, V.P.; Ngadjui, B.T.; Meyer, J.J.; Lall, N. Antimicrobial activities of the methanol extract and compounds from the twigs of Dorstenia mannii (Moraceae). BMC Complement. Altern. Med., 2012, 12, 83. [http://dx.doi.org/10.1186/1472-6882-12-83]. [PMID: 22747736].
[87]
Belofsky, G.; Kolaczkowski, M.; Adams, E.; Schreiber, J.; Eisenberg, V.; Coleman, C.M.; Zou, Y.; Ferreira, D. Fungal ABC transporter-associated activity of isoflavonoids from the root extract of Dalea formosa. J. Nat. Prod., 2013, 76(5), 915-925. [http://dx.doi.org/10.1021/np4000763]. [PMID: 23631483].
[88]
Shakhatreh, M.A.; Al-Smadi, M.L.; Khabour, O.F.; Shuaibu, F.A.; Hussein, E.I.; Alzoubi, K.H. Study of the antibacterial and antifungal activities of synthetic benzyl bromides, ketones, and corresponding chalcone derivatives. Drug Des. Devel. Ther., 2016, 10, 3653-3660. [http://dx.doi.org/10.2147/DDDT.S116312]. [PMID: 27877017].
[89]
Gabriela, N.; Rosa, A.M.; Catiana, Z.I.; Soledad, C.; Mabel, O.R.; Esteban, S.J.; Veronica, B.; Daniel, W.; Ines, I.M. The effect of Zuccagnia punctata, an Argentine medicinal plant, on virulence factors from candida species. Nat. Prod. Commun., 2014, 9(7), 933-936. [http://dx.doi.org/10.1177/1934578X1400900712]. [PMID: 25230496].
[90]
Sun, J.; Ding, W-X.; Hong, X-P.; Zang, K-Y.; Zou, Y. Synthesis and antimicrobial activities of 4-aryl-3,4-dihydrocoumarins and 4-arylcoumarins. Chem. Nat. Compd., 2012, 48(1), 16-22. [http://dx.doi.org/10.1007/s10600-012-0149-9].
[91]
Khan, M.K. E-Huma, Z.; Dangles, O. A comprehensive review on flavanones, the major citrus polyphenols. J. Food Compos. Anal., 2014, 33(1), 85-104. [http://dx.doi.org/10.1016/j.jfca.2013.11.004].
[92]
Das, S.; Ghosh, P.; Koley, S.; Singha Roy, A. Binding of naringin and naringenin with hen egg white lysozyme: A spectroscopic investigation and molecular docking study. Spectrochim. Acta A Mol. Biomol. Spectrosc., 2018, 192, 211-221. [http://dx.doi.org/10.1016/j.saa.2017.11.015]. [PMID: 29145059].
[93]
Funari, C.S.; Gullo, F.P.; Napolitano, A.; Carneiro, R.L.; Mendes-Giannini, M.J.; Fusco-Almeida, A.M.; Piacente, S.; Pizza, C.; Silva, D.H. Chemical and antifungal investigations of six Lippia species (Verbenaceae) from Brazil. Food Chem., 2012, 135(3), 2086-2094. [http://dx.doi.org/10.1016/j.foodchem.2012.06.077]. [PMID: 22953960].
[94]
Rauha, J.P.; Remes, S.; Heinonen, M.; Hopia, A.; Kähkönen, M.; Kujala, T.; Pihlaja, K.; Vuorela, H.; Vuorela, P. Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. Int. J. Food Microbiol., 2000, 56(1), 3-12. [http://dx.doi.org/10.1016/S0168-1605(00)00218-X]. [PMID: 10857921].
[95]
Takemoto, J.K.; Remsberg, C.M.; Yáñez, J.A.; Vega-Villa, K.R.; Davies, N.M. Stereospecific analysis of sakuranetin by high-performance liquid chromatography: pharmacokinetic and botanical applications. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2008, 875(1), 136-141. [http://dx.doi.org/10.1016/j.jchromb.2008.07.019]. [PMID: 18676186].
[96]
Gong, Y.; Qin, X.Y.; Zhai, Y.Y.; Hao, H.; Lee, J.; Park, Y.D. Inhibitory effect of hesperetin on α-glucosidase: Molecular dynamics simulation integrating inhibition kinetics. Int. J. Biol. Macromol., 2017, 101, 32-39. [http://dx.doi.org/10.1016/j.ijbiomac.2017.03.072]. [PMID: 28322965].
[97]
Golfakhrabadi, F.; Shams Ardakani, M.R.; Saeidnia, S.; Akbarzadeh, T.; Yousefbeyk, F.; Jamalifar, H.; Khanavi, M. In vitro antimicrobial and acetylcholinesterase inhibitory activities of coumarins from Ferulago carduchorum. Med. Chem. Res., 2016, 25, 1623-1629. [http://dx.doi.org/10.1007/s00044-016-1595-x].
[98]
Mandalari, G.; Bennett, R.N.; Bisignano, G.; Trombetta, D.; Saija, A.; Faulds, C.B.; Gasson, M.J.; Narbad, A. Antimicrobial activity of flavonoids extracted from bergamot (Citrus bergamia Risso) peel, a byproduct of the essential oil industry. J. Appl. Microbiol., 2007, 103(6), 2056-2064. [http://dx.doi.org/10.1111/j.1365-2672.2007.03456.x]. [PMID: 18045389].
[99]
Vega-Villa, K.R.; Remsberg, C.M.; Podelnyk, K.L.; Davies, N.M. Stereospecific high-performance liquid chromatographic assay of isosakuranetin in rat urine. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2008, 875(1), 142-147. [http://dx.doi.org/10.1016/j.jchromb.2008.05.018]. [PMID: 18514595].
[100]
Finger, D.; Machado, C.S.; Torres, Y.R.; Quináia, S.P.; Thomaz, A.C.G.; Gobbo, A.R.; Monteiro, M.C.; Ferreira, A.G.; Sawaya, A.C.H.F.; Eberlin, M.N. Antifungal bioassay-guided fractionation of an oil extract of propolis. J. Food Qual., 2013, 36(5), 291-301. [http://dx.doi.org/10.1111/jfq.12039].
[101]
Kasote, D.; Ahmad, A.; Chen, W.; Combrinck, S.; Viljoen, A. HPTLC-MS as an efficient hyphenated technique for the rapid identification of antimicrobial compounds from propolis. Phytochem. Lett., 2015, 11, 326-331. [http://dx.doi.org/10.1016/j.phytol.2014.08.017].
[102]
Katerere, D.R.; Gray, A.I.; Nash, R.J.; Waigh, R.D. Phytochemical and antimicrobial investigations of stilbenoids and flavonoids isolated from three species of Combretaceae. Fitoterapia, 2012, 83(5), 932-940. [http://dx.doi.org/10.1016/j.fitote.2012.04.011]. [PMID: 22546149].
[103]
Peralta, M.A.; da Silva, M.A.; Ortega, M.G.; Cabrera, J.L.; Paraje, M.G. Antifungal activity of a prenylated flavonoid from Dalea elegans against Candida albicans biofilms. Phytomedicine, 2015, 22(11), 975-980. [http://dx.doi.org/10.1016/j.phymed.2015.07.003]. [PMID: 26407939].
[104]
Ge, F.; Tian, E.; Wang, L.; Li, X.; Zhu, Q.; Wang, Y.; Zhong, Y.; Ge, R.S. Taxifolin suppresses rat and human testicular androgen biosynthetic enzymes. Fitoterapia, 2018, 125, 258-265. [http://dx.doi.org/10.1016/j.fitote.2018.01.017]. [PMID: 29402482].
[105]
Mishra, S.; Singh, S.; Misra, K. Restraining pathogenicity in Candida albicans by taxifolin as an inhibitor of Ras1-pka pathway. Mycopathologia, 2017, 182(11-12), 953-965. [http://dx.doi.org/10.1007/s11046-017-0170-4]. [PMID: 28681317].
[106]
Castañeda-Ovando, A.; Pacheco-Hernández, M.; Páez-Hernández, M.E.; Rodríguez, J.A.; Galán-Vidal, C.A. Chemical studies of anthocyanins: A review. Food Chem., 2009, 113(4), 859-871. [http://dx.doi.org/10.1016/j.foodchem.2008.09.001].
[107]
Pal Singh, J.; Kaur, A.; Singh, N.; Nim, L.; Shevkani, K.; Kaur, H.; Singh Arora, D. In vitro antioxidant and antimicrobial properties of jambolan (Syzygium cumini) fruit polyphenols. Lebensm. Wiss. Technol., 2016, 65, 1025-1030. [http://dx.doi.org/10.1016/j.lwt.2015.09.038].
[108]
Maertens, J.A. History of the development of azole derivatives. Clin. Microbiol. Infect., 2004, 10(Suppl. 1), 1-10. [http://dx.doi.org/10.1111/j.1470-9465.2004.00841.x]. [PMID: 14748798].
[109]
Roemer, T.; Krysan, D.J. Antifungal drug development: challenges, unmet clinical needs, and new approaches. Cold Spring Harb. Perspect. Med., 2014, 4(5)019703 [http://dx.doi.org/10.1101/cshperspect.a019703]. [PMID: 24789878].
[110]
Pea, F.; Lewis, R.E. Overview of antifungal dosing in invasive candidiasis. J. Antimicrob. Chemother., 2018, 73(Suppl. 1), i33-i43. [PMID: 29304210].
[111]
Smiljkovic, M.; Matsoukas, M.T.; Kritsi, E.; Zelenko, U.; Grdadolnik, S.G.; Calhelha, R.C.; Ferreira, I.C.F.R.; Sankovic-Babic, S.; Glamoclija, J.; Fotopoulou, T.; Koufaki, M.; Zoumpoulakis, P.; Sokovic, M. Nitrate esters of heteroaromatic compounds as novel Candida albicans CYP51 enzyme inhibitors. ChemMedChem, 2018, 13(3), 251-258. [http://dx.doi.org/10.1002/cmdc.201700602]. [PMID: 29235267].
[112]
Thamban Chandrika, N.; Shrestha, S.K.; Ngo, H.X.; Howard, K.C.; Garneau-Tsodikova, S. Novel fluconazole derivatives with promising antifungal activity. Bioorg. Med. Chem., 2018, 26(3), 573-580. [http://dx.doi.org/10.1016/j.bmc.2017.12.018]. [PMID: 29279242].
[113]
Shrestha, S.K.; Garzan, A.; Garneau-Tsodikova, S. Novel alkylated azoles as potent antifungals. Eur. J. Med. Chem., 2017, 133, 309-318. [http://dx.doi.org/10.1016/j.ejmech.2017.03.075]. [PMID: 28395217].
[114]
Fakhim, H.; Emami, S.; Vaezi, A.; Hashemi, S.M.; Faeli, L.; Diba, K.; Dannaoui, E.; Badali, H. In vitro activities of novel azole compounds ATTAF-1 and ATTAF-2 against fluconazole-susceptible and -resistant isolates of Candida species. Antimicrob. Agents Chemother., 2016, 61(1), 01106-001116. [PMID: 27795371].
[115]
Thamban Chandrika, N.; Shrestha, S.K.; Ngo, H.X.; Tsodikov, O.V.; Howard, K.C.; Garneau-Tsodikova, S. Alkylated piperazines and piperazine-azole hybrids as antifungal agents. J. Med. Chem., 2018, 61(1), 158-173. [http://dx.doi.org/10.1021/acs.jmedchem.7b01138]. [PMID: 29256601].
[116]
Yates, C.M.; Garvey, E.P.; Shaver, S.R.; Schotzinger, R.J.; Hoekstra, W.J. Design and optimization of highly-selective, broad spectrum fungal CYP51 inhibitors. Bioorg. Med. Chem. Lett., 2017, 27(15), 3243-3248. [http://dx.doi.org/10.1016/j.bmcl.2017.06.037]. [PMID: 28651982].
[117]
Mellado, E.; Diaz-Guerra, T.M.; Cuenca-Estrella, M.; Rodriguez-Tudela, J.L. Identification of two different 14-alpha sterol demethylase-related genes (cyp51A and cyp51B) in Aspergillus fumigatus and other Aspergillus species. J. Clin. Microbiol., 2001, 39(7), 2431-2438. [http://dx.doi.org/10.1128/JCM.39.7.2431-2438.2001]. [PMID: 11427550].
[118]
Fu, B.; Wu, M.; Huang, L.; Wu, Q.; Wang, S.; Chai, X. Synthesis and bioactivity evaluation of novel azoles containing dithiocarbamate moieties. Med. Chem. Res., 2017, 26(10), 2491-2498. [http://dx.doi.org/10.1007/s00044-017-1948-0].
[119]
Zhao, D.; Zhao, S.; Zhao, L.; Zhang, X.; Wei, P.; Liu, C.; Hao, C.; Sun, B.; Su, X.; Cheng, M. Discovery of biphenyl imidazole derivatives as potent antifungal agents: Design, synthesis, and structure-activity relationship studies. Bioorg. Med. Chem., 2017, 25(2), 750-758. [http://dx.doi.org/10.1016/j.bmc.2016.11.051]. [PMID: 27955926].
[120]
Uppuluri, P.; Srinivasan, A.; Ramasubramanian, A.; Lopez-Ribot, J.L. Effects of fluconazole, amphotericin B, and caspofungin on Candida albicans biofilms under conditions of flow and on biofilm dispersion. Antimicrob. Agents Chemother., 2011, 55(7), 3591-3593. [http://dx.doi.org/10.1128/AAC.01701-10]. [PMID: 21518839].
[121]
Lamfon, H.; Porter, S.R.; McCullough, M.; Pratten, J. Susceptibility of Candida albicans biofilms grown in a constant depth film fermentor to chlorhexidine, fluconazole and miconazole: a longitudinal study. J. Antimicrob. Chemother., 2004, 53(2), 383-385. [http://dx.doi.org/10.1093/jac/dkh071]. [PMID: 14729749].
[122]
Brito, G.N.; Inocêncio, A.C.; Querido, S.M.; Jorge, A.O.; Koga-Ito, C.Y. In vitro antifungal susceptibility of Candida spp. oral isolates from HIV-positive patients and control individuals. Braz. Oral Res., 2011, 25(1), 28-33. [http://dx.doi.org/10.1590/S1806-83242011005000001]. [PMID: 21271179].
[123]
Douglas, L.J. Candida biofilms and their role in infection. Trends Microbiol., 2003, 11(1), 30-36. [http://dx.doi.org/10.1016/S0966-842X(02)00002-1]. [PMID: 12526852].
[124]
Katragkou, A.; Chatzimoschou, A.; Simitsopoulou, M.; Dalakiouridou, M.; Diza-Mataftsi, E.; Tsantali, C.; Roilides, E. Differential activities of newer antifungal agents against Candida albicans and Candida parapsilosis biofilms. Antimicrob. Agents Chemother., 2008, 52(1), 357-360. [http://dx.doi.org/10.1128/AAC.00856-07]. [PMID: 17938192].
[125]
El-Azizi, M.; Farag, N.; Khardori, N. Antifungal activity of amphotericin B and voriconazole against the biofilms and biofilm-dispersed cells of Candida albicans employing a newly developed in vitro pharmacokinetic model. Ann. Clin. Microbiol. Antimicrob., 2015, 3, 14-21. [http://dx.doi.org/10.1186/s12941-015-0083-3].


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