Silver nanoparticles induce reactive oxygen species-mediated cell cycle delay and synergistic cytotoxicity with 3-bromopyruvate in Candida albicans, but not in Saccharomyces cerevisiae

References

• Ullah Khan S, Saleh TA, Wahab A, et al. Nanosilver: new ageless and versatile biomedical therapeutic scaffold. Int J Nanomed. 2018;13:733–762. doi:10.2147/IJN.S153167
   PubMed Web of Science ®Google Scholar
• Saratale RG, Saratale GD, Shin HS, et al. New insights on the green synthesis of metallic nanoparticles using plant and waste biomaterials: current knowledge, their agricultural and environmental applications. Environ Sci Pollut Res Int. 2018;25:10164–10183. doi:10.1007/s11356-017-9912-628815433
   PubMed Web of Science ®Google Scholar
• Pugazhendhi A, Edison T, Karuppusamy I, Kathirvel B. Inorganic nanoparticles: a potential cancer therapy for human welfare. Int J Pharm. 2018;539:104–111. doi:10.1016/j.ijpharm.2018.01.03429366941
   PubMed Web of Science ®Google Scholar
• De Matteis V, Cascione M, Toma CC, Leporatti S. Silver nanoparticles: synthetic routes, in vitro toxicity and theranostic applications for cancer disease. Nanomaterials (Basel). 2018;8:319. doi:10.3390/nano8050319
   PubMedGoogle Scholar
• Pugazhendhi A, Prabakar D, Jacob JM, Karuppusamy I, Saratale RG. Synthesis and characterization of silver nanoparticles using Gelidium amansii and its antimicrobial property against various pathogenic bacteria. Microb Pathog. 2018;114:41–45. doi:10.1016/j.micpath.2017.11.01329146498
   PubMed Web of Science ®Google Scholar
• Saravanan M, Arokiyaraj S, Lakshmi T, Pugazhendhi A. Synthesis of silver nanoparticles from Phenerochaete chrysosporium (MTCC-787) and their antibacterial activity against human pathogenic bacteria. Microb Pathog. 2018;117:68–72. doi:10.1016/j.micpath.2018.02.00829427709
   PubMed Web of Science ®Google Scholar
• Saravanan M, Barik SK, MubarakAli D, Prakash P, Pugazhendhi A. Synthesis of silver nanoparticles from Bacillus brevis (NCIM 2533) and their antibacterial activity against pathogenic bacteria. Microb Pathog. 2018;116:221–226. doi:10.1016/j.micpath.2018.01.03829407231
   PubMed Web of Science ®Google Scholar
• Shanmuganathan R, MubarakAli D, Prabakar D, et al. An enhancement of antimicrobial efficacy of biogenic and ceftriaxone-conjugated silver nanoparticles: green approach. Environ Sci Pollut Res Int. 2018;25:10362–10370. doi:10.1007/s11356-017-9367-928600792
   PubMed Web of Science ®Google Scholar
• Kim KJ, Sung WS, Moon SK, Choi JS, Kim JG, Lee DG. Antifungal effect of silver nanoparticles on dermatophytes. J Microbiol Biotechnol. 2008;18:1482–1484.18756112
   PubMed Web of Science ®Google Scholar
• Velluti F, Mosconi N, Acevedo A, et al. Synthesis, characterization, microbiological evaluation, genotoxicity and synergism tests of new nano silver complexes with sulfamoxole: X-ray diffraction of [Ag2(SMX)2].DMSO. J Inorg Biochem. 2014;141:58–69. doi:10.1016/j.jinorgbio.2014.08.00725217718
   PubMed Web of Science ®Google Scholar
• Sun L, Liao K, Li Y, et al. Synergy between polyvinylpyrrolidone-coated silver nanoparticles and azole antifungal against drug-resistant Candida albicans. J Nanosci Nanotech. 2016;16:2325–2335. doi:10.1166/jnn.2016.10934
   PubMedGoogle Scholar
• Kim KJ, Sung WS, Suh BK, et al. Antifungal activity and mode of action of silver nano-particles on Candida albicans. Biometals. 2009;22:235–242. doi:10.1007/s10534-008-9159-218769871
   PubMed Web of Science ®Google Scholar
• Lara HH, Romero-Urbina DG, Pierce C, Lopez-Ribot JL, Arellano-Jimenez MJ, Jose-Yacaman M. Effect of silver nanoparticles on Candida albicans biofilms: an ultrastructural study. J Nanobiotechnology. 2015;13:91. doi:10.1186/s12951-015-0147-826666378
   PubMed Web of Science ®Google Scholar
• Hwang IS, Lee J, Hwang JH, Kim KJ, Lee DG. Silver nanoparticles induce apoptotic cell death in Candida albicans through the increase of hydroxyl radicals. Febs J. 2012;279:1327–1338. doi:10.1111/j.1742-4658.2012.08527.x22324978
   PubMed Web of Science ®Google Scholar
• Radhakrishnan VS, Reddy Mudiam MK, Kumar M, Dwivedi SP, Singh SP, 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 Nanomed. 2018;13:2647–2663. doi:10.2147/IJN.S150648
   PubMed Web of Science ®Google Scholar
• Kaosaar S, Kahru A, Mantecca P, Kasemets K. Profiling of the toxicity mechanisms of coated and uncoated silver nanoparticles to yeast Saccharomyces cerevisiae BY4741 using a set of its 9 single-gene deletion mutants defective in oxidative stress response, cell wall or membrane integrity and endocytosis. Toxicol In Vitro. 2016;35:149–162. doi:10.1016/j.tiv.2016.05.01827260961
   PubMed Web of Science ®Google Scholar
• Lee YM, Kim E, An J, et al. Dissection of the HOG pathway activated by hydrogen peroxide in Saccharomyces cerevisiae. Environ Microbiol. 2017;19:584–597. doi:10.1111/1462-2920.1349927554843
   PubMed Web of Science ®Google Scholar
• Alonso-Rodriguez E, Fernandez-Pinar P, Sacristan-Reviriego A, Molina M, Martin H. An analog-sensitive version of the protein kinase Slt2 allows identification of novel targets of the yeast cell wall integrity pathway. J Biol Chem. 2016;291:5461–5472. doi:10.1074/jbc.M115.68368026786099
   PubMedGoogle Scholar
• Mulford KE, Fassler JS. Association of the Skn7 and Yap1 transcription factors in the Saccharomyces cerevisiae oxidative stress response. Eukaryot Cell. 2011;10:761–769. doi:10.1128/EC.00328-1021478431
   PubMedGoogle Scholar
• Lee J, Godon C, Lagniel G, et al. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Biol Chem. 1999;274:16040–16046. doi:10.1074/jbc.274.23.1604010347154
   PubMed Web of Science ®Google Scholar
• Brombacher K, Fischer BB, Rufenacht K, Eggen RI. The role of Yap1p and Skn7p-mediated oxidative stress response in the defence of Saccharomyces cerevisiae against singlet oxygen. Yeast. 2006;23:741–750. doi:10.1002/yea.139216862604
   PubMed Web of Science ®Google Scholar
• Lim DH, Jang J, Kim S, Kang T, Lee K, Choi IH. The effects of sub-lethal concentrations of silver nanoparticles on inflammatory and stress genes in human macrophages using cDNA microarray analysis. Biomaterials. 2012;33:4690–4699. doi:10.1016/j.biomaterials.2012.03.00622459196
   PubMed Web of Science ®Google Scholar
• Akter M, Sikder MT, Rahman MM, et al. A systematic review on silver nanoparticles-induced cytotoxicity: physicochemical properties and perspectives. J Adv Res. 2018;9:1–16. doi:10.1016/j.jare.2017.10.00830046482
   PubMed Web of Science ®Google Scholar
• Morones JR, Elechiguerra JL, Camacho A, et al. The bactericidal effect of silver nanoparticles. Nanotechnology. 2005;16:2346–2353. doi:10.1088/0957-4484/16/10/05920818017
   PubMed Web of Science ®Google Scholar
• Elechiguerra JL, Burt JL, Morones JR, et al. Interaction of silver nanoparticles with HIV-1. J Nanobiotechnology. 2005;3:6. doi:10.1186/1477-3155-3-615987516
   PubMedGoogle Scholar
• Oves M, Aslam M, Rauf MA, et al. Antimicrobial and anticancer activities of silver nanoparticles synthesized from the root hair extract of Phoenix dactylifera. Mater Sci Eng C Mater Biol Appl. 2018;89:429–443. doi:10.1016/j.msec.2018.03.03529752116
   PubMed Web of Science ®Google Scholar
• Monteiro DR, Gorup LF, Silva S, et al. Silver colloidal nanoparticles: antifungal effect against adhered cells and biofilms of Candida albicans and Candida glabrata. Biofouling. 2011;27:711–719. doi:10.1080/08927014.2011.59910121756192
   PubMed Web of Science ®Google Scholar
• Panacek A, Kolar M, Vecerova R, et al. Antifungal activity of silver nanoparticles against Candida spp. Biomaterials. 2009;30:6333–6340. doi:10.1016/j.biomaterials.2009.07.06519698988
   PubMed Web of Science ®Google Scholar
• Dziedzic A, Kubina R, Buldak RJ, Skonieczna M, Cholewa K. Silver nanoparticles exhibit the dose-dependent anti-proliferative effect against human squamous carcinoma cells attenuated in the presence of berberine. Molecules. 2016;21:365. doi:10.3390/molecules2103036526999092
   PubMed Web of Science ®Google Scholar
• Annu AS, Kaur G, Sharma P, Singh S, Ikram S. Evaluation of the antioxidant, antibacterial and anticancer (lung cancer cell line A549) activity of Punica granatum mediated silver nanoparticles. Toxicol Res (Camb). 2018;7:923–930. doi:10.1039/c8tx00103k30310669
   PubMedGoogle Scholar
• Lee YS, Kim DW, Lee YH, et al. Silver nanoparticles induce apoptosis and G2/M arrest via PKCzeta-dependent signaling in A549 lung cells. Arch Toxicol. 2011;85:1529–1540. doi:10.1007/s00204-011-0714-121611810
   PubMed Web of Science ®Google Scholar
• Correia I, Alonso-Monge R, Pla J. The Hog1 MAP kinase promotes the recovery from cell cycle arrest induced by hydrogen peroxide in Candida albicans. Front Microbiol. 2016;7:2133. doi:10.3389/fmicb.2016.0213328111572
   PubMed Web of Science ®Google Scholar
• Radhakrishnan VS, Dwivedi SP, Siddiqui MH, Prasad T. In vitro studies on oxidative stress-independent, Ag nanoparticles-induced cell toxicity of Candida albicans, an opportunistic pathogen. Int J Nanomed. 2018;13:91–96. doi:10.2147/IJN.S125010
   PubMedGoogle Scholar
• Lee AR, Lee SJ, Lee M, et al. Editor’s Highlight: a genome-wide screening of target genes against silver nanoparticles in fission yeast. Toxicol Sci. 2018;161:171–185. doi:10.1093/toxsci/kfx20829294138
   PubMed Web of Science ®Google Scholar
• Sillapawattana P, Gruhlke MC, Schaffer A. Effect of silver nanoparticles on the standard soil arthropod Folsomia candida (Collembola) and the eukaryote model organism Saccharomyces cerevisiae. Environ Sci Eur. 2016;28:27. doi:10.1186/s12302-016-0095-427882277
   PubMedGoogle Scholar
• Hanscho M, Ruckerbauer DE, Chauhan N, et al. Nutritional requirements of the BY series of Saccharomyces cerevisiae strains for optimum growth. FEMS Yeast Res. 2012;12:796–808. doi:10.1111/j.1567-1364.2012.00830.x22780918
   PubMedGoogle Scholar
• Cokol M, Weinstein ZB, Yilancioglu K, et al. Large-scale identification and analysis of suppressive drug interactions. Chem Biol. 2014;21:541–551. doi:10.1016/j.chembiol.2014.02.01224704506
   PubMedGoogle Scholar
• Dylag M, Lis P, Niedzwiecka K, et al. 3-Bromopyruvate: a novel antifungal agent against the human pathogen Cryptococcus neoformans. Biochem Biophys Res Commun. 2013;434:322–327. doi:10.1016/j.bbrc.2013.02.12523541578
   PubMed Web of Science ®Google Scholar
• Lis P, Zarzycki M, Ko YH, et al. Transport and cytotoxicity of the anticancer drug 3-bromopyruvate in the yeast Saccharomyces cerevisiae. J Bioenerg Biomembr. 2012;44:155–161. doi:10.1007/s10863-012-9421-822359102
   PubMedGoogle Scholar
• Yun SJ, Kim K, Lee ES, Park S. The suppressive effect of butyrate and bromopyruvate on inflammatory cytokine production and short chain fatty acid receptor expression by blood mononuclear cells in patients with Behçet’s disease. Ann Dermatol. 2018;30:566–574. doi:10.5021/ad.2018.30.5.566
   PubMedGoogle Scholar
• Lis P, Jurkiewicz P, Cal-Bakowska M, et al. Screening the yeast genome for energetic metabolism pathways involved in a phenotypic response to the anti-cancer agent 3-bromopyruvate. Oncotarget. 2016;7:10153–10173. doi:10.18632/oncotarget.717426862728
   PubMedGoogle Scholar
• Piao MJ, Kang KA, Lee IK, et al. Silver nanoparticles induce oxidative cell damage in human liver cells through inhibition of reduced glutathione and induction of mitochondria-involved apoptosis. Toxicol Lett. 2011;201:92–100. doi:10.1016/j.toxlet.2010.12.01021182908
   PubMed Web of Science ®Google Scholar
• Patra KC, Hay N. The pentose phosphate pathway and cancer. Trends Biochem Sci. 2014;39:347–354. doi:10.1016/j.tibs.2014.06.00525037503
   PubMed Web of Science ®Google Scholar