Antifungal activity, antibiofilm, synergism and molecular docking of Allium sativum essential oil against clinical isolates of C. albicans
DOI:
https://doi.org/10.33448/rsd-v10i12.20457Keywords:
Pathogenesis; Biofilms; Modelling; Virulence; Mycology.Abstract
The aim of the present study was to investigate the biological activity of A. sativum essential oil against clinical isolates of C. albicans and, in addition, a computational study of the action of two main compounds of the essential oil on the protein of the fungus CYP51 was carried out. The Minimum Inhibitory Concentration and the Minimum Fungicidal Concentration were determined by the broth microdilution method. The biofilm formation was evaluated by biomass quantification using the violet crystal staining method. For the study of molecular docking computer simulations of interaction between CYP51 and ligands were performed using the AutoDock Vina code. The main constituents were diallyl disulfide, followed by diallyl disulfide. The essential oil demonstrated activity against clinical isolates of C. albicans. The essential oil showed a reduction progressive increase in the biomass produced from the biofilms of all yeasts tested in this study. The ligands Diallyl disulfide, Diallyl trisulfide and fluconazole formed complexes with the protein target. Based on the results, the essential oil of A. sativum can be considered promising product for the development of new drugs in the prevention of infections associated with C. albicans. This study characterizes the effects of A. sativum essential oil against clinical isolates of C. albicans responsible for the development of pathologies in humans.
References
A. Hess and L. Smentek, “The concerted nature of the cyclization of squalene oxide to the protosterol cation,” Angew. Chemie - Int. Ed., 2013, doi: 10.1002/anie.201302886.
Aala F, Yusuf UM, Khodavandi A & Jamal F (2010) In vitro antifungal activity of allicin alone and in combination with two medications against six dermatophytic fungi. Afr J Microbiol Res 4: 380–385.
Alorainy, M. S. (2011). Evaluation of antimicrobial activity of garlic (Allium sativum) against E. coli O 157:H 7. Journal of Agriculture and Veterinary Science, 4, 149–157
Amin M, Kapadnis BP. Heat stable antimicrobial activity of Allium ascalonicum against bacteria and fungi. Indian J Exp Biol. 2005; 43(8):751-4.
Amin M, Kapadnis BP. Heat stable antimicrobial activity of Allium ascalonicum against bacteria and fungi. Indian J Exp Biol. 2005; 43(8):751-4.
An M, Shen H, Cao Y, Zhang J, Cai Y, Wang R & Jiang Y (2009) Allicin enhances the oxidative damage effect of amphotericin B against Candida albicans. Int J Antimicrob Ag 33: 258–263.
Ankri S & Mirelman D (1999) Antimicrobial properties of allicin from garlic. Microbes Infect 1: 125–129.
Armstrong-James D., Brown G.D., Netea M.G., Zelante T., Gresnigt M., van de Veerdonk F., Levitz S.M (2017) Immunotherapeutic approaches to treatment of fungal diseases. Lancet Infect Dis 17, 393-402.
Banerjee, S. K., Mukherjee, P. K., & Maulik, S. K. (2003). Garlic as an antioxidant: The good, the bad and the ugly. Phytotherapy Research, 17, 97–106.
Behbahani B A, Fooladi A A I. Evaluation of phytochemical analysis and antimicrobial activities Allium essential oil against the growth of some microbial pathogens. Microbial Pathogenesis, 2017.
Behbahani B A, Fooladi A A I. Evaluation of phytochemical analysis and antimicrobial activities Allium essential oil against the growth of some microbial pathogens. Microbial Pathogenesis, 2017.
Block, E., Naganathan, S., Putman, D., & Zhao, S.-H. (1993). Organo-sulfur chemistry of garlic and onion: Recent results. Pure and Applied Chemistry, 65, 625–632.
Borlinghaus, J., Albrecht, F., Gruhlke, M. C. H., Nwachukwu, I. D., & Slusarenko, A. J. (2014). Allicin: Chemistry and biological properties. Molecules, 19, 12591–12618.
C. Milite et al., “Novel 2-substituted-benzimidazole-6-sulfonamides as carbonic anhydrase inhibitors: synthesis, biological evaluation against isoforms I, II, IX and XII and molecular docking studies,” J. Enzyme Inhib. Med. Chem., 2019, doi: 10.1080/14756366.2019.1666836.
Capasso, A. (2013). Antioxidant action and therapeutic efficacy of Allium sativum L. Molecules, 18, 690–700.
Casella, S. et al. The role of diallyl sulfides and dipropyl sulfides in the in vitro antimicrobial activity of the essential oil of garlic, Allium sativum L., and leek, Allium porrum L. Phytotherapy Research, 2012.
Chen, S., Shen, X., Cheng, S., Li, P., Du, J., Chang, Y., & Meng, H. (2013). Evaluation of garlic cultivars for polyphenolic content and antioxidant properties. PLoS ONE, 8, e79730.
Clinical and Laboratory Standards Institute, 2008a. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts (Approved Standard. Document M27. CLSI). Third ed. vol. M27-A3. Clinical and Laboratory Standards Institute, Wayne, PA.
Clinical and Laboratory Standards Institute, 2008b. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi (Approved Standard. Document M38. CLSI). Second ed. vol. M38-A2. Clinical and Laboratory Standards Institute, Wayne, PA
Cohain, JS. Cases series: Symptomatic Group B Rev. Bras. Pl. Med., Campinas, v.16, n.3, supl. I, p.679-684, 2014. Streptococcus vaginitis treated with fresh garlic. Integrative Medicine, v.9, n.3, p. 40-3, 2010.
D. S. Biovia et al., “Dassault Systèmes BIOVIA, Discovery Studio Visualizer, v.17.2, San Diego: Dassault Systèmes, 2016. ,” J. Chem. Phys., 2000, doi: 10.1016/0021-9991(74)90010-2.
D. Yusuf, A. M. Davis, G. J. Kleywegt, and S. Schmitt, “An alternative method for the evaluation of docking performance: RSR vs RMSD,” J. Chem. Inf. Model., vol. 48, no. 7, pp. 1411–1422, 2008, doi: 10.1021/ci800084x.
E. F. Pettersen et al., “UCSF Chimera - A visualization system for exploratory research and analysis,” J. Comput. Chem., vol. 25, no. 13, pp. 1605–1612, 2004, doi: 10.1002/jcc.20084.
F. W. Q. Almeida-Neto et al., “Characterization of the structural, spectroscopic, nonlinear optical, electronic properties and antioxidant activity of the N-{4’-[(E)-3-(Fluorophenyl)-1-(phenyl)-prop-2-en-1-one]}-acetamide,” J. Mol. Struct., vol. 1220, p. 128765, 2020, doi: 10.1016/j.molstruc.2020.128765.
FAO (2013). Production and trade statistics.Rome, Italy: FAO.
Fasihzadeh S, Lorigooini Z, Jivad N. Chemical constituents of Allium stipitatum regel 341 (persian shallot) essential oil. Der Pharmacia Lettre. 2016; 8:175-80.
Fontenelle, R. O. S.; Morais, S. M.; Brito, E. H. S.; Mendonça, M. R. K.; Brilhante, R. S. N.; Cordeiro, R. A. N.; Nascimento, N. R. F.; Sidrim, J. J. C.; Rocha, M. F. G. Chemical composition, toxicological aspects and antifungal activity of essential oil from Lippia sidoides Cham. Journal of Antimicrobial Chemotherapy, v. 59, n. 5, p. 934-940, 2007.
Fontenelle, R.O.S., Morais, S.M., Brito, E.H.S., Brilhante, R.S.N., Cordeiro, R.A., Nascimento, N.R.F., Kerntopf, M.R., Sidrim, J.J.C., Rocha, M.F.G., (2008). Antifungal activity of essential oils of Croton species from the Brazilian Caatinga biome. J. Appl. Microbiol. 104, 1383–1390.
Galdiero E, Onofrio V D, Maione A, Gambino E, Gesuele R, Menale B, Ciaravolo M, Carraturo, Guida M. Allium ursinum and Allium oschaninii against Klebsiella pneumoniae and Candida albicans Mono- and Polymicrobic Biofilms in In Vitro Static and Dynamic Models. Microorganisms 27;8(3):336, 1-12, 2020.
Guo N, Wu X, Yu L, Liu J, Meng R, Jin J, Lu H, Wang X, Yan S & Deng X (2010) In vitro and in vivo interactions between fluconazole and allicin against clinical isolates of fluconazoleresistant Candida albicans determined by alternative methods. FEMS Immunol Med Microbiol 58: 193–201.
Hornícˇková, J., Kubec, R., Cejpek, K., Velíšek, J., Ovesná, J., & Stavelíková, H. (2010). Profiles of S-alk(en)ylcysteine sulfoxides in various garlic genotypes. Czech Journal of Food Sciences, 28(4), 298–308.
Imberty, K. D. Hardman, J. P. Carver, and S. Perez, “Molecular modelling of protein-carbohydrate interactions. Docking of monosaccharides in the binding site of concanavalin A,” Glycobiology, 1991, doi: 10.1093/glycob/1.6.631.
J. J. P. Stewart, “Optimization of parameters for semiempirical methods VI: More modifications to the NDDO approximations and re-optimization of parameters,” J. Mol. Model., 2013, doi: 10.1007/s00894-012-1667-x.
Khodavandi A, Alizadeh F, Aala F, Sekawi Z & Chong PP (2010) In vitro investigation of antifungal activity of allicin alone and in combination with azoles against Candida species. Mycopathologia 169: 287–295.
Kumar, R., Chhatwal, S., Arora, S., Sharma, S., Singh, J., Singh, N., Khurana, A. (2013). Antihyperglycemic, antihyperlipidemic, anti-inflammatory and adenosine deaminase-lowering effects of garlic in patients with type 2 diabetes mellitus with obesity. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy, 6, 49–56.
L. Colombo et al., “Brazilian guidelines for the management of candidiasis - a joint meeting report of three medical societies: Sociedade Brasileira de Infectologia, Sociedade Paulista de Infectologia and Sociedade Brasileira de Medicina Tropical,” Brazilian J. Infect. Dis., 2013, doi: 10.1016/j.bjid.2013.02.001.
Lanzotti, V., Scala, F., & Bonanomi, G. (2014). Compounds from Allium species with cytotoxic and antimicrobial activity. Phytochemistry Reviews, 13, 769–791.
Lanzotti, V., Scala, F., & Bonanomi, G. (2014). Compounds from Allium species with cytotoxic and antimicrobial activity. Phytochemistry Reviews, 13, 769–791.
Lemar KM, Passa O, Aon MA, Cortassa S,M¨uller CT, Plummer S, O’Rourke B & Lloyd D (2005) Allyl alcohol and garlic (0) extract produce oxidative stress in Candida albicans. Microbiology 151: 3257–3265.
Lemar KM, Turner MP & Lloyd D (2002) Garlic (Allium sativum) as an anti-Candida agent: a comparison of the efficacy of fresh garlic and freeze-dried extracts. J Appl Microbiol 93: 398–405.
Li G, Ma X, Deng L, et al. Fresh garlic extract enhances the antimicrobial activities of antibiotics on resistant strains in vitro. Jundishapur J Microbiol 2015; 8: e14814. DOI: 10.5812/jjm.14814
Li Wen-Ru, Shi Qing-Shan, Dai Huan-Qin, Liang Qing, Xie Xiao-Bao, Huang Xiao-Mo, Zhao Guang-Ze, Zhang Li-Xin. Antifungal activity, kinetics and molecular mechanism of action of garlic oil against Candida albicans. Scientific Reports | 6:22805.
Li WR, Shi QS, Dai HQ, et al. Antifungal activity, kinetics and molecular mechanism of action of garlic oil against Candida albicans. Sci Rep 2016; 6: 22805. DOI: 10.1038/ srep22805
Lima, C.M.B.L. et al. Ultrastructural study on the morphological changes to male worms of Schistosoma mansoni after in vitro exposure to allicin. Revista da Sociedade Brasileira de Medicina Tropical, v.44, n.3, p.327-30, 2011.
Low CF, Chong PP, Yong PVC, Lim CSY, Ahmad Z & Othman F (2008) Inhibition of hyphae formation and SIR2 expression in Candida albicans treated with fresh Allium sativum (garlic) extract. J Appl Microbiol 105: 2169–2177.
M. V. Keniya et al., “Crystal Structures of Full-Length Lanosterol 14α-Demethylases of Prominent Fungal Pathogens Candida albicans and Candida glabrata Provide Tools for Antifungal Discovery,” Antimicrob. Agents Chemother., 2018, doi: 10.1128/AAC.01134-18.
Mantawy, M.M. et al. Therapeutic Effects of Allium sativum and Allium cepa in Schistosoma mansoni experimental infection. Revista do Instituto de Medicina Tropical de São Paulo, v.53, n.3, p.155-63, 2011.
Medici N, Poeta M. New insight on the development on fungal vaccines: from immunity to recent challenges. Mem Inst Oswaldo Cruz 2015;110:966e73.
Miron T, Bercovici T, Rabinkov A, Wilchek M & Mirelman D (2004) [3H]Allicin: preparation and applications. Anal Biochem 331: 364–369.
Nami S, Mohammadi R, Vakili M, Khezripour K, Mirzael H, Morovati H. Fungal vaccines, mechanism of actions and immunology: a comprehensive review. Biomed Pharm 2018; 109:333e44.
O. Trott and A. J. Olson, “AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading,” J. Comput. Chem., 2009, doi: 10.1002/jcc.21334.
P. Schimmel, J. Tao, and J. Hill, “Aminoacyl tRNA synthetases as targets for new anti‐infectives,” FASEB J., 1998, doi: 10.1096/fasebj.12.15.1599.
Q. Guo, S. Sun, J. Yu, Y. Li, and L. Cao, “Synergistic activity of azoles with amiodarone against clinically resistant Candida albicans tested by chequerboard and time-kill methods,” J. Med. Microbiol., 2008, doi: 10.1099/jmm.0.47651-0.
S. Shityakov and C. Förster, “In silico predictive model to determine vector-mediated transport properties for the blood-brain barrier choline transporter,” Adv. Appl. Bioinforma. Chem., vol. 7, no. 1, pp. 23–36, 2014, doi: 10.2147/AABC.S63749.
S. Silva, M. Negri, M. Henriques, R. Oliveira, D. W. Williams, and J. Azeredo, “Candida glabrata, Candida parapsilosis and Candida tropicalis: Biology, epidemiology, pathogenicity and antifungal resistance,” FEMS Microbiology Reviews. 2012, doi: 10.1111/j.1574-6976.2011.00278.x.
S. Stepanovic, D. Vukovic, I. Dakic, B. Savic, M. Svabic-Vlahovic, A modified microtiter-plate test for quantification of staphylococcal biofilm formation, J. Microbiol. Methods 40 (2) (2000) 175–179
Sakagami T, Kawano T, Yamashita K, Ymada E, Fujino N, Kaeriyama M, et al. Antifungal susceptibility trend and analysis of resistance mechanism for Candida species isolated from bloodstream at a Japanese university hospital. J Infect Chemother 2019;25:34 e40.
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. 24.
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. 24.
Shields, R.K.; Nguyen, M.H.; Press, E.G.; Kwa, A.L.; Cheng, S.; Du, C.; Clancy, C.J. The presence of na FKS mutation rather than MIC is an independent risk factor for failure of echinocandin therapy among patients with invasive candidiasis due to Candida glabrata. Antimicrob. Agents Chemother. 2012, 56, 4862–4869.
Silva, J.L. et al. Atividade antifúngica de extratos vegetais sobre o crescimento in vitro de fitopatógenos. Revista verde de agroecologia e desenvolvimento sustentável, v. 7, n.1, p. 80-6, 2012.
Song, J., Zhang, S., Lu, L. Fungal cytochrome P450 protein Cyp51: What we can learn from its evolution, regulons and Cyp51-based azole resistance. Fungal Biology Reviews, v. 32 (3), p. 131-142, 2018.
V. Sueth-Santiago, T. N. Franklim, N. D. Lopes, and M. E. F. Lima, “CYP51: Is it a good idea?,” Rev. Virtual Quim., vol. 7, no. 2, pp. 539–575, 2015, doi: 10.5935/1984 6835.20150024.
Venturoso, L.R. et al. Atividade antifúngica de extratos vegetais sobre o desenvolvimento de fitopatógenos. Summa Phytopathologica, v.37, n.1, p.18-23, 2011.
Yamada Y &Azuma K (1977) Evaluation of the in vitro antifungal activity of allicin. Antimicrob Agents Ch 11: 743–749
Zainal, M, Zain NM, Amin IM, Ahmad VN. The antimicrobial and antibiofilme properties of allicin against Candida albicans and Staphylococcus aureus – A therapeutic potential for denture stomatitis. The Saudi Dental Journal, 2020.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Rafael Pereira; Josilayne de Fátima Souza Mendes; Raquel Oliveira dos Santos Fontenelle; Tigressa Helena Soares Rodrigues; Hélcio Silva dos Santos; Emmanuel Silva Marinho; Márcia Machado Marinho; Selene Maia de Morais
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.