Publication Cover
Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 36, 2020 - Issue 1
642
Views
35
CrossRef citations to date
0
Altmetric
Original Articles

Impediment to growth and yeast-to-hyphae transition in Candida albicans by copper oxide nanoparticles

ORCID Icon, , ORCID Icon, , , & show all
Pages 56-72 | Received 15 Nov 2019, Accepted 06 Jan 2020, Published online: 30 Jan 2020

References

  • Baev D, Li XS, Dong J, Keng P, Edgerton M. 2002. Human salivary histatin 5 causes disordered volume regulation and cell cycle arrest in Candida albicans. Infect Immun. 70:4777–4784. doi:10.1128/IAI.70.9.4777-4784.2002
  • Ballo MKS, Rtimi S, Pulgarin C, Hopf N, Berthet A, Kiwi J, Moreillon P, Entenza JM, Bizzini A. 2016. In vitro and in vivo effectiveness of an innovative silver-copper nanoparticle coating of catheters to prevent methicillin-resistant Staphylococcus aureus infection. Antimicrob Agents Chemother. 60:5349–5356. doi:10.1128/AAC.00959-16
  • Berman J, Sudbery PE. 2002. Candida albicans: a molecular revolution built on lessons from budding yeast. Nature reviews. Nat Rev Genet. 3:918–930. doi:10.1038/nrg948
  • Besold AN, Culbertson EM, Culotta VC. 2016. The yin and yang of copper during infection. J Biol Inorg Chem. 21:137–144. doi:10.1007/s00775-016-1335-1
  • Bink A, Vandenbosch D, Coenye T, Nelis H, Cammue BPA, Thevissen K. 2011. Superoxide dismutases are involved in Candida albicans biofilm persistence against miconazole. Antimicrob Agents Chemother. 55:4033–4037. doi:10.1128/AAC.00280-11
  • Boyce KJ, Andrianopoulos A. 2015. Fungal dimorphism: the switch from hyphae to yeast is a specialized morphogenetic adaptation allowing colonization of a host. FEMS Microbiol Rev. 39:797–811. doi:10.1093/femsre/fuv035
  • Braun BR, Johnson AD. 2000. TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans. Genetics. 155:57–67.
  • Braun BR, Kadosh D, Johnson AD. 2001. NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 20:4753–4761. doi:10.1093/emboj/20.17.4753
  • Breivik ON, Owades JL. 1957. Yeast analysis, spectrophotometric semimicrodetermination of ergosterol in yeast. J Agric Food Chem. 5:360–363. doi:10.1021/jf60075a005
  • Castillo H, Muñoz-Castellanos L, Chamorro R, Reyes Martinez R, Borunda E. 2018. Nanoparticles as new therapeutic agents against Candida albicans. In: Candida albicans. London: IntechOpen. https://cdn.intechopen.com/pdfs/63926.pdf.
  • Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol. 183:5385–5394. doi:10.1128/JB.183.18.5385-5394.2001
  • Collart MA, Oliviero S. 2001. Preparation of yeast RNA. Curr Protocal Mol Biol. 23:13.12.1–13.12.5.
  • Csank C, SchröPpel K, Leberer E, Harcus D, Mohamed O, Meloche S, Thomas DY, Whiteway M. 1998. Roles of the Candida albicans mitogen-activated protein kinase homolog, Cek1p, in hyphal development and systemic candidiasis. Infect Immun. 66:2713–2721. doi:10.1128/IAI.66.6.2713-2721.1998
  • Cullity BD. 1978. Elements of x-ray diffraction. 2nd ed. Phillippines: Addison-Wesley Publishing Company Inc.
  • d’Ostiani CF, Del Sero G, Bacci A, Montagnoli C, Spreca A, Mencacci A, Ricciardi-Castagnoli P, Romani L. 2000. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J Experiment Med. 191:1661–1674. doi:10.1084/jem.191.10.1661
  • de Oliveira Santos GC, Vasconcelos CC, Lopes AJO, de Sousa Cartágenes MS, Filho AKDB, do Nascimento FRF, Ramos RM, Pires ERRB, de Andrade MS, Rocha FMG, et al. 2018. Candida infections and therapeutic strategies: mechanisms of action for traditional and alternative agents. Front Microbiol. 9:1351–1351. doi:10.3389/fmicb.2018.01351
  • Delaloye J, Calandra T. 2014. Invasive candidiasis as a cause of sepsis in the critically ill patient. Virulence. 5:161–169. doi:10.4161/viru.26187
  • Ethiraj AS, Kang DJ. 2012. Synthesis and characterization of CuO nanowires by a simple wet chemical method. Nanoscale Res Lett. 7:70. doi:10.1186/1556-276X-7-70
  • Festa RA, Thiele DJ. 2011. Copper: an essential metal in biology. Curr Biol. 21:R877–R883. doi:10.1016/j.cub.2011.09.040
  • Futcher B. 1996. Cyclins and the wiring of the yeast cell cycle. Yeast. 12:1635–1646. doi:10.1002/(SICI)1097-0061(199612)12:16<1635::AID-YEA83>3.0.CO;2-O
  • Gray KC, Palacios DS, Dailey I, Endo MM, Uno BE, Wilcock BC, Burke MD. 2012. Amphotericin primarily kills yeast by simply binding ergosterol. Proc Natl Acad Sci USA. 109:2234–2239. doi:10.1073/pnas.1117280109
  • Haber F, Weiss J, Pope WJ. 1934. The catalytic decomposition of hydrogen peroxide by iron salts. Proc R Soc London Ser A. 147:332–351.
  • Hsiao IL, Hsieh YK, Wang CF, Chen IC, Huang YJ. 2015. Trojan-horse mechanism in the cellular uptake of silver nanoparticles verified by direct intra- and extracellular silver speciation analysis. Environ Sci Technol. 49:3813–3821. doi:10.1021/es504705p
  • Hua Q, Cao T, Gu X-K, Lu J, Jiang Z, Pan X, Luo L, Li W-X, Huang W. 2014. Crystal-plane-controlled selectivity of Cu2O catalysts in propylene oxidation with molecular oxygen. Angew Chem Int Ed. 53:4856–4861. doi:10.1002/anie.201402374
  • Inoue M. 2013. Solvothermal synthesis of metal oxides. In: Handbook of advanced ceramics, 2nd ed. Oxford: Academic Press; p. 927–948.
  • Irving H, Williams R. 1948. Order of stability of metal complexes. Nature. 162:746–747. doi:10.1038/162746a0
  • Jabra-Rizk MA, Falkler WA, Meiller TF. 2004. Fungal biofilms and drug resistance. Emerg Infect Dis. 10:14–19. doi:10.3201/eid1001.030119
  • Jacobsen ID, Hube B. 2017. Candida albicans morphology: still in focus. Exp Rev Anti-Infect Ther. 15:327–330. doi:10.1080/14787210.2017.1290524
  • Jones L, O’Shea P. 1994. The electrostatic nature of the cell surface of Candida albicans: a role in adhesion. Experiment Mycol. 18:111–120. doi:10.1006/emyc.1994.1013
  • Kasemets K, Kaosaar S, Vija H, Fascio U, Mantecca P. 2019. Toxicity of differently sized and charged silver nanoparticles to yeast Saccharomyces cerevisiae BY4741: a nano-biointeraction perspective. Nanotoxicology. 13:1041–1059. doi:10.1080/17435390.2019.1621401
  • Kehrer JP. 2000. The Haber-Weiss reaction and mechanisms of toxicity. Toxicology. 149:43–50. doi:10.1016/S0300-483X(00)00231-6
  • Khosravi Rad K, Falahati M, Roudbary M, Farahyar S, Nami S. 2016. Overexpression of MDR-1 and CDR-2 genes in fluconazole resistance of Candida albicans isolated from patients with vulvovaginal candidiasis. Curr Med Mycol. 2:24–29.
  • Klis FM, de Groot P, Hellingwerf K. 2001. Molecular organization of the cell wall of Candida albicans. Med Mycol. 39: 1–8. doi:10.1080/mmy.39.1.1.8-0
  • Klug L, Daum G. 2014. Yeast lipid metabolism at a glance. FEMS Yeast Res. 14:369–388. doi:10.1111/1567-1364.12141
  • Koga T, Sakata Y, Terasaki N. 2019. Accumulation and analysis of cuprous ions in a copper sulfate plating solution. J Vis Exp. 2019:e59376.
  • Kojic EM, Darouiche RO. 2004. Candida infections of medical devices. Clin Microbiol Rev. 17:255–267. doi:10.1128/CMR.17.2.255-267.2004
  • Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA. 2002. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother. 46:1773–1780. doi:10.1128/AAC.46.6.1773-1780.2002
  • Kvaal C, Lachke SA, Srikantha T, Daniels K, McCoy J, Soll DR. 1999. Misexpression of the opaque- phase-specific gene PEP1 (SAP1) in the white phase of Candida albicans confers increased virulence in a mouse model of cutaneous infection. Infect Immun. 67:6652–6662.
  • Lazebnik YA, Cole S, Cooke CA, Nelson WG, Earnshaw WC. 1993. Nuclear events of apoptosis in vitro in cell-free mitotic extracts: a model system for analysis of the active phase of apoptosis. J Cell Biol. 123:7–22. doi:10.1083/jcb.123.1.7
  • Leberer E, Harcus D, Broadbent ID, Clark KL, Dignard D, Ziegelbauer K, Schmidt A, Gow NAR, Brown AJP, Thomas DY. 1996. Signal transduction through homologs of the Ste20p and Ste7p protein kinases can trigger hyphal formation in the pathogenic fungus Candida albicans. Proc Natl Acad Sci USA. 93:13217–13222. doi:10.1073/pnas.93.23.13217
  • Lee H, Woo E-R, Lee DG. 2018. Apigenin induces cell shrinkage in Candida albicans by membrane perturbation. FEMS Yeast Res. 18:foy003.
  • Li F, Palecek SP. 2003. EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryotic Cell. 2:1266–1273. doi:10.1128/EC.2.6.1266-1273.2003
  • Liu J, Rijckaert H, Zeng M, Haustraete K, Laforce B, Vincze L, Van Driessche I, Kaczmarek AM, Van, Deun R. 2018. Simultaneously excited downshifting/upconversion luminescence from lanthanide-doped core/shell fluoride nanoparticles for multimode anticounterfeiting. Adv Funct Mater. 28:1707365. doi:10.1002/adfm.201707365
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 − ΔΔCT method. Methods. 25:402–408. doi:10.1006/meth.2001.1262
  • Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell. 90:939–949. doi:10.1016/S0092-8674(00)80358-X
  • McQuillan JS, Groenaga Infante H, Stokes E, Shaw AM. 2012. Silver nanoparticle enhanced silver ion stress response in Escherichia coli K12. Nanotoxicology. 6:857–866. doi:10.3109/17435390.2011.626532
  • Merson-Davies LA, Odds FC. 1989. A morphology index for characterization of cell shape in Candida albicans. J Gen Microbiol. 135:3143–3152.
  • Miller MG, Johnson AD. 2002. White-opaque switching in Candida albicans is controlled by mating- type locus homeodomain proteins and allows efficient mating. Cell. 110:293–302. doi:10.1016/S0092-8674(02)00837-1
  • Montagner H, Montagner F, Braun KO, Peres PEC, Gomes B. 2009. In vitro antifungal action of different substances over microwaved-cured acrylic resins. J Appl Oral Sci. 17:432–435. doi:10.1590/S1678-77572009000500015
  • Moyes DL, Richardson JP, Naglik JR. 2015. Candida albicans-epithelial interactions and pathogenicity mechanisms: scratching the surface. Virulence. 6:338–346. doi:10.1080/21505594.2015.1012981
  • Mukaremera L, Lee KK, Mora-Montes HM, Gow N. 2017. Candida albicans yeast, pseudohyphal, and hyphal morphogenesis differentially affects immune recognition. Front Immunol. 8:629–629. doi:10.3389/fimmu.2017.00629
  • Mukherjee PK, Chandra J. 2004. Candida biofilm resistance. Drug Resist Updat. 7:301–309. doi:10.1016/j.drup.2004.09.002
  • Murad AM, d’Enfert C, Gaillardin C, Tournu H, Tekaia F, Talibi D, Marechal D, Marchais V, Cottin J, Brown AJ. 2001. Transcript profiling in Candida albicans reveals new cellular functions for the transcriptional repressors CaTup1, CaMig1 and CaNrg1. Mol Microbiol. 42:981–993. doi:10.1046/j.1365-2958.2001.02713.x
  • Murad AM, Leng P, Straffon M, Wishart J, Macaskill S, MacCallum D, Schnell N, Talibi D. 2001. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20:4742–4752. doi:10.1093/emboj/20.17.4742
  • Muthamil S, Balasubramaniam B, Balamurugan K, Pandian SK. 2018. Synergistic effect of quinic acid derived from Syzygium cumini and undecanoic acid against Candida spp. biofilm and virulence. Front Microbiol. 9:2835. doi:10.3389/fmicb.2018.02835
  • Nes WR, Sekula BC, Nes WD, Adler JH. 1978. The functional importance of structural features of ergosterol in yeast. J Biol Chem. 253:6218–6225.
  • Nobile CJ, Johnson AD. 2015. Candida albicans biofilms and human disease. Annu Rev Microbiol. 69:71–92. doi:10.1146/annurev-micro-091014-104330
  • Olsen I. 2014. Attenuation of Candida albicans virulence with focus on disruption of its vacuole functions. J Oral Microbiol. 6:23898. doi:10.3402/jom.v6.23898
  • Padmavathi AR, Bakkiyaraj D, Thajuddin N, Pandian SK. 2015. Effect of 2, 4-di-tert-butylphenol on growth and biofilm formation by an opportunistic fungus Candida albicans. Biofouling. 31:565–574. doi:10.1080/08927014.2015.1077383
  • Padmavathi AR, Murthy PS, Das A, Nishad PA, Pandian R, Rao TS. 2019. Copper oxide nanoparticles as an effective anti-biofilm agent against a copper tolerant marine bacterium, Staphylococcus lentus. Biofouling. 35:1007–1025. doi:10.1080/08927014.2019.1687689
  • Pham AN, Rose AL, Waite TD. 2012. Kinetics of Cu(II) reduction by natural organic matter. J Phys Chem A. 116:6590–6599. doi:10.1021/jp300995h
  • Pham AN, Xing G, Miller CJ, Waite TD. 2013. Fenton-like copper redox chemistry revisited: hydrogen peroxide and superoxide mediation of copper-catalyzed oxidant production. J Catal. 301:54–64. doi:10.1016/j.jcat.2013.01.025
  • Phan QT, Belanger PH, Filler SG. 2000. Role of hyphal formation in interactions of Candida albicans with endothelial cells. Infect Immun. 68:3485–3490. doi:10.1128/IAI.68.6.3485-3490.2000
  • Poreddy R, Engelbrekt C, Riisager A. 2015. Copper oxide as efficient catalyst for oxidative dehydrogenation of alcohols with air. Catal Sci Technol. 5:2467–2477. doi:10.1039/C4CY01622J
  • Prasad KN, Prasad N, Gupta A, Sharma RK, Verma AK, Ayyagari A. 2004. Fungal peritonitis in patients on continuous ambulatory peritoneal dialysis: a single centre Indian experience. J Infect. 48:96–101. doi:10.1016/S0163-4453(03)00119-1
  • Ramage G, Martínez JP, López-Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6:979–986. doi:10.1111/j.1567-1364.2006.00117.x
  • Ramage G, Vande Walle K, Wickes BL, Lopez-Ribot JL. 2001. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother. 45:2475–2479. doi:10.1128/AAC.45.9.2475-2479.2001
  • Ramírez-Zavala B, Weyler M, Gildor T, Schmauch C, Kornitzer D, Arkowitz R, Morschhäuser J. 2013. Activation of the cph1-dependent MAP kinase signaling pathway induces white-opaque switching in Candida albicans. PLOS Pathog. 9:e1003696. doi:10.1371/journal.ppat.1003696
  • Rathna J, Bakkiyaraj D, Pandian SK. 2016. Anti-biofilm mechanisms of 3,5-di-tert-butylphenol against clinically relevant fungal pathogens. Biofouling. 32:979–993. doi:10.1080/08927014.2016.1216103
  • Ray PD, Huang B-W, Tsuji Y. 2012. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 24:981–990. doi:10.1016/j.cellsig.2012.01.008
  • Rodrigues ML. 2018. The multifunctional fungal ergosterol. mBio. 9:e01755–01718.
  • Rossi DCP, Gleason JE, Sanchez H, Schatzman SS, Culbertson EM, Johnson CJ, McNees CA, Coelho C, Nett JE, Andes DR, et al. 2017. Candida albicans FRE8 encodes a member of the NADPH oxidase family that produces a burst of ROS during fungal morphogenesis. PLOS Pathog. 13:e1006763. doi:10.1371/journal.ppat.1006763
  • Salvatori O, Pathirana RU, Kay JG, Edgerton M. 2018. Candida albicans Ras1 inactivation increases resistance to phagosomal killing by human neutrophils. Infect Immun. 86:e00685–00618.
  • Schroeder L, Ikui AE. 2019. Tryptophan confers resistance to SDS-associated cell membrane stress in Saccharomyces cerevisiae. Plos One. 14:e0199484. doi:10.1371/journal.pone.0199484
  • Shalom Y, Perelshtein I, Perkas N, Gedanken A, Banin E. 2017. Catheters coated with Zn-doped CuO nanoparticles delay the onset of catheter-associated urinary tract infections. Nano Res. 10:520–533. doi:10.1007/s12274-016-1310-8
  • Synnott JM, Guida A, Mulhern-Haughey S, Higgins DG, Butler G. 2010. Regulation of the hypoxic response in Candida albicans. Eukaryotic Cell. 9:1734–1746. doi:10.1128/EC.00159-10
  • Taff HT, Mitchell KF, Edward JA, Andes DR. 2013. Mechanisms of Candida biofilm drug resistance. Future Microbiol. 8:1325–1337. doi:10.2217/fmb.13.101
  • Wei M, Lun N, Ma X, Wen S. 2007. A simple solvothermal reduction route to copper and cuprous oxide. Mater Lett. 61:2147–2150. doi:10.1016/j.matlet.2006.08.035
  • Winterbourn CC. 1995. Toxicity of iron and hydrogen peroxide: the Fenton reaction. Toxicol Lett. 82-83:969–974. doi:10.1016/0378-4274(95)03532-X
  • Yang YL, Cheng HH, Lo HJ. 2006. Distribution and antifungal susceptibility of Candida species isolated from different age populations in Taiwan. Med Mycol. 44:237–242. doi:10.1080/13693780500401213
  • Zafiriou OC, Voelker BM, Sedlak DL. 1998. Chemistry of the superoxide radical (O2-) in seawater: reactions with inorganic copper complexes. J Phys Chem A. 102:5693–5700. doi:10.1021/jp980709g
  • Zakikhany K, Naglik JR, Schmidt-Westhausen A, Holland G, Schaller M, Hube B. 2007. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell Microbiol. 9:2938–2954. doi:10.1111/j.1462-5822.2007.01009.x
  • Zhang Q, Zhang K, Xu D, Yang G, Huang H, Nie F, Liu C, Yang S. 2014. CuO nanostructures: synthesis, characterization, growth mechanisms, fundamental properties, and applications. Progr Mater Sci. 60:208–337. doi:10.1016/j.pmatsci.2013.09.003
  • Zheng WL, Wang BJ, Wang L, Shan YP, Zou H, Song RL, Wang T, Gu JH, Yuan Y, Liu Z-P, et al. 2018. ROS-mediated cell cycle arrest and apoptosis induced by zearalenone in mouse sertoli cells via ER stress and the ATP/AMPK Pathway. Toxins. 10:24. doi:10.3390/toxins10010024
  • Ziąbka M, Menaszek E, Tarasiuk J, Wroński S. 2018. Biocompatible nanocomposite implant with silver nanoparticles for otology in vivo evaluation. Nanomaterials (Basel). 8:764. doi:10.3390/nano8100764
  • Zimbeck AJ, Iqbal N, Ahlquist AM, Farley MM, Harrison LH, Chiller T, Lockhart SR. 2010. FKS mutations and elevated echinocandin MIC values among Candida glabrata isolates from U.S. population-based surveillance. Antimicrob Agents Chemother. 54:5042–5047. doi:10.1128/AAC.00836-10

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.