Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Biogenic Silver Nanoparticles and Stressors Generate Synergistic Growth Inhibition in Candida Species through Cell Wall Damage, Osmotic Stress, and Oxidative Stress

Author(s): José Antonio Cervantes-Chávez, Gastón García-Bouchot, Nataly García-Gutiérrez, Hayde Azeneth Vergara- Castañeda, Rufino Nava-Mendoza, Gabriel Luna-Bárcenas, Eduardo Arturo Elizalde-Peña, Edgardo Ulises Esquivel-Naranjo, Fidel Landeros-Jaime, Norma Gabriela Rojas-Avelizapa and Héctor Pool*

Volume 24, Issue 13, 2023

Published on: 29 March, 2023

Page: [1682 - 1693] Pages: 12

DOI: 10.2174/1389201024666230303145653

Price: $65

Abstract

Background: The need to combat and reduce the incidence, virulence, and drug resistance of species belonging to Candida genus, has led to the development of new strategies. Nanotechnology, through the implementation of nanomaterials, has emerged as an infallible tool to treat various diseases caused by pathogens, where its mechanisms of action prevent the development of undesirable pharmacological resistance.

Objective: The antifungal activity and adjuvant properties of biogenic silver nanoparticles in different Candida species (C. parapsilosis, C. glabrata, and C. albicans) are evaluated.

Methods: The biogenic metallic nanoparticles were developed by quercetin-mediated biological synthesis. The physicochemical properties were studied by light scattering, electrophoretic mobility, UV-vis and infrared spectroscopy, and transmission electron microscopy. The elucidation of mechanisms of antifungal action was carried out under stress conditions in Candida species at the cell wall and response to oxidative stress.

Results: Small silver nanoparticles (≈ 16.18 nm) with irregular morphology, and negative surface electrical charge (≈ -48.99 mV), were obtained through quercetin-mediated biosynthesis. Infrared spectra showed that the surface of silver nanoparticles is functionalized with the quercetin molecule. The antifungal activity of biogenic nanoparticles had efficacy in the following trend C. glabrata ≥ C. parapsilosis > C. albicans. Biogenic nanoparticles and stressors showed synergistic and potentiated antifungal effects through cell damage, osmotic stress, cell wall damage, and oxidative stress.

Conclusions: Silver nanoparticles synthesized by quercetin-mediated biosynthesis could be implemented as a powerful adjuvant agent to enhance the inhibition effects of diverse compounds over different Candida species.

« Previous Next »
Graphical Abstract

[1]
Ghrenassia, E.; Mokart, D.; Mayaux, J.; Demoule, A.; Rezine, I.; Kerhuel, L.; Calvet, L.; De Jong, A.; Azoulay, E.; Darmon, M. Candidemia in critically ill immunocompromised patients: Report of a retrospective multicenter cohort study. Ann. Intensive Care, 2019, 9(1), 62.
[http://dx.doi.org/10.1186/s13613-019-0539-2] [PMID: 31161475]
[2]
Ding, X.; Yan, D.; Sun, W.; Zeng, Z.; Su, R.; Su, J. Epidemiology and risk factors for nosocomial non-Candida albicans candidemia in adult patients at a tertiary care hospital in North China. Med. Mycol., 2015, 53(7), 684-690.
[http://dx.doi.org/10.1093/mmy/myv060] [PMID: 26229153]
[3]
Ksiezopolska, E.; Gabaldón, T. Evolutionary emergence of drug resistance in Candida opportunistic pathogens. Genes, 2018, 9(9), 461.
[http://dx.doi.org/10.3390/genes9090461] [PMID: 30235884]
[4]
Pfaller, M.A.; Moet, G.J.; Messer, S.A.; Jones, R.N.; Castanheira, M. Candida bloodstream infections: Comparison of species distributions and antifungal resistance patterns in community-onset and nosocomial isolates in the SENTRY antimicrobial surveillance program, 2008-2009. Antimicrob. Agents Chemother., 2011, 55(2), 561-566.
[http://dx.doi.org/10.1128/AAC.01079-10] [PMID: 21115790]
[5]
Morace, G.; Perdoni, F.; Borghi, E. Antifungal drug resistance in Candida species. J. Glob. Antimicrob. Resist., 2014, 2(4), 254-259.
[http://dx.doi.org/10.1016/j.jgar.2014.09.002] [PMID: 27873684]
[6]
Costa-de-Oliveira, S.; Rodrigues, A.G. Candida albicans antifungal resistance and tolerance in bloodstream infections: The triad yeast-host-antifungal. Microorganisms, 2020, 8(2), 154.
[http://dx.doi.org/10.3390/microorganisms8020154] [PMID: 31979032]
[7]
Marak, M.B.; Dhanashree, B. Antifungal susceptibility and biofilm production of Candida spp. isolated from clinical samples. Int. J. Microbiol., 2018, 2018, 1-5.
[http://dx.doi.org/10.1155/2018/7495218] [PMID: 30405717]
[8]
de Oliveira Santos, G.C.; Vasconcelos, C.C.; Lopes, A.J.O.; de Sousa Cartágenes, M.S.; Filho, A.K.D.B.; do Nascimento, F.R.F.; Ramos, R.M.; Pires, E.R.R.B.; de Andrade, M.S.; Rocha, F.M.G.; de Andrade Monteiro, C. Candida infections and therapeutic strategies: Mechanisms of action for traditional and alternative agents. Front. Microbiol., 2018, 9, 1351.
[http://dx.doi.org/10.3389/fmicb.2018.01351] [PMID: 30018595]
[9]
Castillo, H.A.P.; Castellanos, L.N.M.; Chamorro, R.M.; Martínez, R.R.; Borunda, E.O. Nanoparticles as new therapeutic agents against Candida albicans. In: Candida Albicans; IntechOpen: London, 2018.
[10]
Jebali, A.; Hajjar, F.H.E.; Pourdanesh, F.; Hekmatimoghaddam, S.; Kazemi, B.; Masoudi, A.; Daliri, K.; Sedighi, N. Silver and gold nanostructures: Antifungal property of different shapes of these nanostructures on Candida species. Med. Mycol., 2014, 52(1), 65-72.
[PMID: 23968285]
[11]
Iravani, S.; Korbekandi, H.; Mirmohammadi, S.V.; Zolfaghari, B. Synthesis of silver nanoparticles: Chemical, physical and biological methods. Res. Pharm. Sci., 2014, 9(6), 385-406.
[PMID: 26339255]
[12]
Pantidos, N.; Horsfall, L.E. Biological synthesis of metallic nanoparticles by bacteria, fungi and plants. J. Nanomed. Nanotechnol., 2014, 5(5), 1.
[http://dx.doi.org/10.4172/2157-7439.1000233]
[13]
Vergara-Castañeda, H.; Granados-Segura, L.O.; Luna-Bárcenas, G.; McClements, D.J.; Herrera-Hernández, M.G.; Arjona, N.; Hernández-Martínez, A.R.; Estevez, M.; Pool, H. Gold nanoparticles bioreduced by natural extracts of arantho (Kalanchoe daigremontiana) for biological purposes: Physicochemical, antioxidant and antiproliferative evaluations. Mater. Res. Express, 2019, 6(5)055010
[http://dx.doi.org/10.1088/2053-1591/ab0155]
[14]
Jalal, M.; Ansari, M.A.; Ali, S.G.; Khan, H.M.; Rehman, S. Anticandidal activity of bioinspired ZnO NPs: Effect on growth, cell morphology and key virulence attributes of Candida species. Artif. Cells Nanomed. Biotechnol., 2018, 46(sup1), 912-925.
[http://dx.doi.org/10.1080/21691401.2018.1439837] [PMID: 29446992]
[15]
Cervantes-Chávez, J.A.; Valdés-Santiago, L.; Bakkeren, G.; Hurtado-Santiago, E.; León-Ramírez, C.G.; Esquivel-Naranjo, E.U.; Landeros-Jaime, F.; Rodríguez-Aza, Y.; Ruiz-Herrera, J. Trehalose is required for stress resistance and virulence of the Basidiomycota plant pathogen Ustilago maydis. Microbiology, 2016, 162(6), 1009-1022.
[http://dx.doi.org/10.1099/mic.0.000287] [PMID: 27027300]
[16]
Nikolaou, E.; Agrafioti, I.; Stumpf, M.; Quinn, J.; Stansfield, I.; Brown, A.J.P. Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol. Biol., 2009, 9(1), 44.
[http://dx.doi.org/10.1186/1471-2148-9-44] [PMID: 19232129]
[17]
Vergara-Castañeda, H.; Hernandez-Martinez, A.R.; Estevez, M.; Mendoza, S.; Luna-Barcenas, G.; Pool, H. Quercetin conjugated silica particles as novel biofunctional hybrid materials for biological applications. J. Colloid Interface Sci., 2016, 466, 44-55.
[http://dx.doi.org/10.1016/j.jcis.2015.12.011] [PMID: 26704475]
[18]
Vanaraj, S.; Keerthana, B.B.; Preethi, K. Biosynthesis, characterization of silver nanoparticles using quercetin from Clitoria ternatea L to enhance toxicity against bacterial biofilm. J. Inorg. Organomet. Polym. Mater., 2017, 27(5), 1412-1422.
[http://dx.doi.org/10.1007/s10904-017-0595-8]
[19]
Link, S.; El-Sayed, M.A. Shape and size dependence of radiative, non-radiative and photothermal properties of gold nanocrystals. Int. Rev. Phys. Chem., 2000, 19(3), 409-453.
[http://dx.doi.org/10.1080/01442350050034180]
[20]
Wang, H.; Qiao, X.; Chen, J.; Ding, S. Preparation of silver nanoparticles by chemical reduction method. Colloids Surf. A Physicochem. Eng. Asp., 2005, 256(2-3), 111-115.
[http://dx.doi.org/10.1016/j.colsurfa.2004.12.058]
[21]
Mat Yusuf, S.N.A.; Che Mood, C.N.A.; Ahmad, N.H.; Sandai, D.; Lee, C.K.; Lim, V. Optimization of biogenic synthesis of silver nanoparticles from flavonoid-rich Clinacanthus nutans leaf and stem aqueous extracts. R. Soc. Open Sci., 2020, 7(7), 200065.
[http://dx.doi.org/10.1098/rsos.200065] [PMID: 32874618]
[22]
Dubey, S.P.; Lahtinen, M.; Sillanpää, M. Tansy fruit mediated greener synthesis of silver and gold nanoparticles. Process Biochem., 2010, 45(7), 1065-1071.
[http://dx.doi.org/10.1016/j.procbio.2010.03.024]
[23]
Jalal, M.; Ansari, M.A.; Alzohairy, M.A.; Ali, S.G.; Khan, H.M.; Almatroudi, A.; Siddiqui, M.I. Anticandidal activity of biosynthesized silver nanoparticles: Effect on growth, cell morphology, and key virulence attributes of Candida species. Int. J. Nanomedicine, 2019, 14, 4667-4679.
[http://dx.doi.org/10.2147/IJN.S210449] [PMID: 31308652]
[24]
Rocha, M.F.G.; Sales, J.A.; da Rocha, M.G.; Galdino, L.M.; de Aguiar, L.; Pereira-Neto, W.A.; de Aguiar Cordeiro, R.; Castelo-Branco, D.S.C.M.; Sidrim, J.J.C.; Brilhante, R.S.N. Antifungal effects of the flavonoids kaempferol and quercetin: A possible alternative for the control of fungal biofilms. Biofouling, 2019, 35(3), 320-328.
[http://dx.doi.org/10.1080/08927014.2019.1604948] [PMID: 31066306]
[25]
Silva, S.; Negri, M.; Henriques, M.; Oliveira, R.; Williams, D.W.; Azeredo, J. Candida glabrata, Candida parapsilosis and Candida tropicalis: Biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol. Rev., 2012, 36(2), 288-305.
[http://dx.doi.org/10.1111/j.1574-6976.2011.00278.x] [PMID: 21569057]
[26]
Oliveira, V.M.; Carraro, E.; Auler, M.E.; Khalil, N.M. Quercetin and rutin as potential agents antifungal against Cryptococcus spp. Braz. J. Biol., 2016, 76(4), 1029-1034.
[http://dx.doi.org/10.1590/1519-6984.07415] [PMID: 27166572]
[27]
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]
[28]
Tasca, F.; Antiochia, R. Biocide activity of green quercetin-mediated synthesized silver nanoparticles. Nanomaterials , 2020, 10(5), 909.
[http://dx.doi.org/10.3390/nano10050909] [PMID: 32397267]
[29]
Radhakrishnan, V.S.; Reddy Mudiam, M.K.; Kumar, M.; Dwivedi, S.P.; Singh, S.P.; Prasad, T. Silver nanoparticles induced alterations in multiple cellular targets, which are critical for drug susceptibilities and pathogenicity in fungal pathogen (Candida albicans). Int. J. Nanomedicine, 2018, 13, 2647-2663.
[http://dx.doi.org/10.2147/IJN.S150648] [PMID: 29760548]
[30]
Xia, Z.K.; Ma, Q.H.; Li, S.Y.; Zhang, D.Q.; Cong, L.; Tian, Y.L.; Yang, R.Y. The antifungal effect of silver nanoparticles on Trichosporon asahii. J. Microbiol. Immunol. Infect., 2016, 49(2), 182-188.
[http://dx.doi.org/10.1016/j.jmii.2014.04.013] [PMID: 24877597]
[31]
Al Aboody, M.S.; Mickymaray, S. Anti-fungal efficacy and mechanisms of flavonoids. Antibiotics, 2020, 9(2), 45.
[http://dx.doi.org/10.3390/antibiotics9020045] [PMID: 31991883]
[32]
Chaffin, W.L.; López-Ribot, J.L.; Casanova, M.; Gozalbo, D.; Martínez, J.P. Cell wall and secreted proteins of Candida albicans: Identification, function, and expression. Microbiol. Mol. Biol. Rev., 1998, 62(1), 130-180.
[http://dx.doi.org/10.1128/MMBR.62.1.130-180.1998] [PMID: 9529890]
[33]
Lopez, M.J.; Hall, C.A. Physiology. In: Osmosis; , 2020.
[34]
Abdel-Hafez, S.I.I.; Nafady, N.A.; Abdel-Rahim, I.R.; Shaltout, A.M.; Daròs, J.-A.; Mohamed, M.A. Assessment of protein silver nanoparticles toxicity against pathogenic Alternaria solani. 3 Biotech, 2016, 6(2), 199.
[35]
Kuranda, K.; Leberre, V.; Sokol, S.; Palamarczyk, G.; François, J. Investigating the caffeine effects in the yeast Saccharomyces cerevisiae brings new insights into the connection between TOR, PKC and Ras/cAMP signalling pathways. Mol. Microbiol., 2006, 61(5), 1147-1166.
[http://dx.doi.org/10.1111/j.1365-2958.2006.05300.x] [PMID: 16925551]
[36]
Quinteros, M.A.; Cano Aristizábal, V.; Dalmasso, P.R.; Paraje, M.G.; Páez, P.L. Oxidative stress generation of silver nanoparticles in three bacterial genera and its relationship with the antimicrobial activity. Toxicol. In Vitro, 2016, 36, 216-223.
[http://dx.doi.org/10.1016/j.tiv.2016.08.007] [PMID: 27530963]
[37]
Lee, B.; Lee, M.J.; Yun, S.J.; Kim, K.; Choi, I.H.; Park, S. Silver nanoparticles induce reactive oxygen species-mediated cell cycle delay and synergistic cytotoxicity with 3-bromopyruvate in Candida albicans, but not in Saccharomyces cerevisiae. Int. J. Nanomedicine, 2019, 14, 4801-4816.
[http://dx.doi.org/10.2147/IJN.S205736] [PMID: 31308659]
[38]
Cuéllar-Cruz, M.; López-Romero, E.; Ruiz-Baca, E.; Zazueta-Sandoval, R. Differential response of Candida albicans and Candida glabrata to oxidative and nitrosative stresses. Curr. Microbiol., 2014, 69(5), 733-739.
[http://dx.doi.org/10.1007/s00284-014-0651-3] [PMID: 25002360]
[39]
Kamli, M.R.; Srivastava, V.; Hajrah, N.H.; Sabir, J.S.M.; Ali, A.; Malik, M.A.; Ahmad, A. Phytogenic fabrication of Ag-Fe bimetallic nano-particles for cell cycle arrest and apoptosis signaling pathways in Candida auris by generating oxidative stress. Antioxidants, 2021, 10(2), 182.
[http://dx.doi.org/10.3390/antiox10020182] [PMID: 33513888]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy