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Original Research

Size-Dependent Bioactivity of Silver Nanoparticles: Antibacterial Properties, Influence on Copper Status in Mice, and Whole-Body Turnover

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Pages 137-157 | Published online: 31 Dec 2020

References

  • Yaqoob SB, Adnan R, Rameez Khan RM, Rashid M. Gold, silver, and palladium nanoparticles: A chemical tool for biomedical applications. Front Chem. 2020;8:376.32582621
  • Zhang XF, Liu ZG, Shen W, Gurunathan S. Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci. 2016;17(9):1534. doi:10.3390/ijms17091534
  • Elbehiry A, Al-Dubaib M, Marzouk E, Moussa I. Antibacterial effects and resistance induction of silver and gold nanoparticles against Staphylococcus aureus-induced mastitis and the potential toxicity in rats. Microbiologyopen. 2019;8(4):e00698. doi:10.1002/mbo3.69830079629
  • Chowdhury NR, MacGregor-Ramiasa M, Zilm P, Majewski P, Vasilev K. ‘Chocolate’ silver nanoparticles: synthesis, antibacterial activity and cytotoxicity. J Colloid Interface Sci. 2016;482:151–158. doi:10.1016/j.jcis.2016.08.00327501038
  • Rodrigues CT, de Andrade FB, de Vasconcelos LRSM, et al. Antibacterial properties of silver nanoparticles as a root canal irrigant against Enterococcus faecalis biofilm and infected dentinal tubules. Int Endod J. 2018;51(8):901–911. doi:10.1111/iej.1290429397005
  • Durán N, Nakazato G, Seabra AB. Antimicrobial activity of biogenic silver nanoparticles, and silver chloride nanoparticles: an overview and comments. Appl Microbiol Biotechnol. 2016;100(15):6555–6570. doi:10.1007/s00253-016-7657-727289481
  • You J, Zhang Y, Hu Z. Bacteria and bacteriophage inactivation by silver and zinc oxide nanoparticles. Colloids Surf B Biointerfaces. 2011;85(2):161–167. doi:10.1016/j.colsurfb.2011.02.02321398101
  • Xiang D, Zheng Y, Duan W, et al. Inhibition of A/Human/Hubei/3/2005 (H3N2) influenza virus infection by silver nanoparticles in vitro and in vivo [published correction appears. Int J Nanomedicine. 2013;8:4703. doi:10.2147/IJN.S57432
  • Franci G, Falanga A, Galdiero S, et al. Silver nanoparticles as potential antibacterial agents. Molecules. 2015;20(5):8856–8874. doi:10.3390/molecules2005885625993417
  • Gliga AR, Skoglund S, Wallinder IO, Fadeel B, Karlsson HL. Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release. Part Fibre Toxicol. 2014;11:11. doi:10.1186/1743-8977-11-1124529161
  • Akter M, Sikder MT, Rahman MM, et al. A systematic review on silver nanoparticles-induced cytotoxicity: physicochemical properties and perspectives. J Adv Res. 2017;9:1–16. doi:10.1016/j.jare.2017.10.00830046482
  • Xin L, Wang J, Fan G, et al. Oxidative stress and mitochondrial injury-mediated cytotoxicity induced by silver nanoparticles in human A549 and HepG2 cells. Environ Toxicol. 2016;31(12):1691–1699. doi:10.1002/tox.2217126172371
  • Begum AN, Aguilar JS, Elias L, Hong Y. Silver nanoparticles exhibit coating and dose-dependent neurotoxicity in glutamatergic neurons derived from human embryonic stem cells. Neurotoxicology. 2016;57:45–53. doi:10.1016/j.neuro.2016.08.01527593553
  • Tang S, Zheng J. Antibacterial activity of silver nanoparticles: structural effects. Adv Healthc Mater. 2018;7(13):e1701503. doi:10.1002/adhm.20170150329808627
  • Pratsinis A, Hervella P, Leroux JC, Pratsinis SE, Sotiriou GA. Toxicity of silver nanoparticles in macrophages. Small. 2013;9(15):2576–2584. doi:10.1002/smll.20120212023418027
  • Soares T, Ribeiro D, Proença C, Chisté RC, Fernandes E, Freitas M. Size-dependent cytotoxicity of silver nanoparticles in human neutrophils assessed by multiple analytical approaches. Life Sci. 2016;145:247–254. doi:10.1016/j.lfs.2015.12.04626743952
  • Liu J, Li S, Fang Y, Zhu Z. Boosting antibacterial activity with mesoporous silica nanoparticles supported silver nanoclusters. J Colloid Interface Sci. 2019;555:470–479. doi:10.1016/j.jcis.2019.08.00931400539
  • Raj A, Shah P, Agrawal N. Dose-dependent effect of silver nanoparticles (AgNPs) on fertility and survival of Drosophila: an in-vivo study. PLoS One. 2017;12(5):e0178051. doi:10.1371/journal.pone.017805128542630
  • Ottoni CA, Lima Neto MC, Léo P, Ortolan BD, Barbieri E, De Souza AO. Environmental impact of biogenic silver nanoparticles in soil and aquatic organisms. Chemosphere. 2020;239:124698. doi:10.1016/j.chemosphere.2019.12469831493753
  • Abramenko N, Demidova TB, Krutyakov YA, et al. The effect of capping agents on the toxicity of silver nanoparticles to Danio rerio embryos. Nanotoxicology. 2019;13(1):1–13. doi:10.1080/17435390.2018.149893130691337
  • Caloudova H, Hodkovicova N, Sehonova P, et al. The effect of silver nanoparticles and silver ions on zebrafish embryos (Danio rerio). Neuro Endocrinol Lett. 2018;39(4):299–304.30531708
  • Roh JY, Sim SJ, Yi J, et al. Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics. Environ Sci Technol. 2009;43(10):3933–3940. doi:10.1021/es803477u19544910
  • Munger MA, Radwanski P, Hadlock GC, et al. In vivo human time-exposure study of orally dosed commercial silver nanoparticles. Nanomedicine. 2014;10(1):1–9. doi:10.1016/j.nano.2013.06.01023811290
  • Pareek V, Gupta R, Panwar J. Do physico-chemical properties of silver nanoparticles decide their interaction with biological media and bactericidal action? A review. Mater Sci Eng C Mater Biol Appl. 2018;90:739–749. doi:10.1016/j.msec.2018.04.09329853145
  • Dakal TC, Kumar A, Majumdar RS, Yadav V. Mechanistic basis of antimicrobial actions of silver nanoparticles. Front Microbiol. 2016;7:1831. doi:10.3389/fmicb.2016.0183127899918
  • Kozlowski H, Kolkowska P, Watly J, Krzywoszynska K, Potocki S. General aspects of metal toxicity. Curr Med Chem. 2014;21(33):3721–3740. doi:10.2174/092986732166614071609383825039781
  • Linder MC. Copper and genomic stability in mammals. Mutat Res. 2001;475(1–2):141–152. doi:10.1016/S0027-5107(01)00076-811295159
  • Jiménez-Lamana J, Laborda F, Bolea E, et al. An insight into silver nanoparticles bioavailability in rats. Metallomics. 2014;6(12):2242–2249. doi:10.1039/C4MT00200H25363792
  • Orlov IA, Sankova TP, Babich PS, et al. New silver nanoparticles induce apoptosis-like process in E. coli and interfere with mammalian copper metabolism. Int J Nanomedicine. 2016;11:6561–6574. doi:10.2147/IJN.S11774528008247
  • Pavelková M, Vysloužil J, Kubová K, Vetchý D. Biological role of copper as an essential trace element in the human organism. Biologická role mědi jako základního stopového prvku v lidském organismu. Ceska Slov Farm. 2018;67(4):143–153.30646728
  • Yuan S, Chen S, Xi Z, Liu Y. Copper-finger protein of Sp1: the molecular basis of copper sensing. Metallomics. 2017;9(8):1169–1175. doi:10.1039/C7MT00184C28759062
  • D’Ambrosi N, Rossi L. Copper at synapse: release, binding and modulation of neurotransmission. Neurochem Int. 2015;90:36–45. doi:10.1016/j.neuint.2015.07.00626187063
  • Li S, Ahmed L, Zhang R, et al. Smelling sulfur: copper and silver regulate the response of human odorant receptor OR2T11 to low-molecular-weight thiols. J Am Chem Soc. 2016;138(40):13281–13288. doi:10.1021/jacs.6b0698327659093
  • Riera-Romo M. COMMD1: A multifunctional regulatory protein. J Cell Biochem. 2018;119(1):34–51. doi:10.1002/jcb.2615128543362
  • Kaplan JH, Lutsenko S. Copper transport in mammalian cells: special care for a metal with special needs. J Biol Chem. 2009;284(38):25461–25465. doi:10.1074/jbc.R109.03128619602511
  • Bhattacharjee A, Chakraborty K, Shukla A. Cellular copper homeostasis: current concepts on its interplay with glutathione homeostasis and its implication in physiology and human diseases. Metallomics. 2017;9(10):1376–1388. doi:10.1039/C7MT00066A28675215
  • Puchkova LV, Broggini M, Polishchuk EV, Ilyechova EY, Polishchuk RS. Silver ions as a tool for understanding different aspects of copper metabolism. Nutrients. 2019;11(6):1364. doi:10.3390/nu11061364
  • Logeman BL, Wood LK, Lee J, Thiele DJ. Gene duplication and neo-functionalization in the evolutionary and functional divergence of the metazoan copper transporters Ctr1 and Ctr2. J Biol Chem. 2017;292(27):11531–11546. doi:10.1074/jbc.M117.79335628507097
  • Zimnicka AM, Ivy K, Kaplan JH. Acquisition of dietary copper: a role for anion transporters in intestinal apical copper uptake. Am J Physiol Cell Physiol. 2011;300(3):C588–C599. doi:10.1152/ajpcell.00054.201021191107
  • Kluska K, Peris-Díaz MD, Płonka D, et al. Formation of highly stable multinuclear AgnSn clusters in zinc fingers disrupts their structure and function. Chem Commun. 2020;56(9):1329–1332. doi:10.1039/C9CC09418K
  • Berridge MV, Herst PM, Tan AS. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev. 2005;11:127–152.16216776
  • Owen J, Smith H. Detection of ceruloplasmin after zone electrophoresis. Clin Chim Acta. 1961;6:441–444. doi:10.1016/0009-8981(61)90074-2
  • Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol. 1957;28(1):56–63. doi:10.1093/ajcp/28.1.5613458125
  • Zatulovskaia YA, Ilyechova EY, Puchkova LV. The features of copper metabolism in the rat liver during development. PLoS One. 2015;10(10):e0140797. doi:10.1371/journal.pone.014079726474410
  • Sokolov AV, Kostevich VA, Romanico DN, Zakharova ET, Vasilyev VB. Two-stage method for purification of ceruloplasmin based on its interaction with neomycin. Biochemistry (Mosc). 2012;77(6):631–638. doi:10.1134/S000629791206010722817463
  • Samygina VR, Sokolov AV, Bourenkov G, et al. Rat ceruloplasmin: a new labile copper binding site and zinc/copper mosaic. Metallomics. 2017;9(12):1828–1838. doi:10.1039/C7MT00157F29177316
  • Sharma M, Mohapatra S, Ranjann S, Dasgupta N, Kumar R, Thomas S. Transdermal and intravenous nano drug delivery systems. Appl Targeted Nano Drugs Delivery Systems. 2019;499–550.
  • Hadrup N, Loeschner K, Bergström A, et al. Subacute oral toxicity investigation of nanoparticulate and ionic silver in rats. Arch Toxicol. 2012;86(4):543–551. doi:10.1007/s00204-011-0759-121969074
  • Loeschner K, Hadrup N, Qvortrup K, et al. Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part Fibre Toxicol. 2011;8:18. doi:10.1186/1743-8977-8-1821631937
  • Katsnelson BA, Privalova LI, Sutunkova MP, et al. Some inferences from in vivo experiments with metal and metal oxide nanoparticles: the pulmonary phagocytosis response, subchronic systemic toxicity and genotoxicity, regulatory proposals, searching for bioprotectors (a self-overview). Int J Nanomedicine. 2015;10:3013–3029. doi:10.2147/IJN.S8084325945048
  • Kim YS, Song MY, Park JD, et al. Subchronic oral toxicity of silver nanoparticles. Part Fibre Toxicol. 2010;7:20. doi:10.1186/1743-8977-7-2020691052
  • Zhang Y, Wu D, Zhang X, Ma N, Liu Y. MicroRNA sponge knockdowns miR-483-5p and upregulates serum ALT/AST in transgenic mice. Biochemistry. 2018;83(1):54–59. doi:10.1134/S000629791801007829534669
  • Aldubayan MA, Elgharabawy RM, Ahmed AS, Tousson E. Antineoplastic activity and curative role of avenanthramides against the growth of ehrlich solid tumors in mice. Oxid Med Cell Longev. 2019;2019:5162687. doi:10.1155/2019/516268730755785
  • Recordati C, De Maglie M, Bianchessi S, et al. Tissue distribution and acute toxicity of silver after single intravenous administration in mice: nano-specific and size-dependent effects. Part Fibre Toxicol. 2016;13:12. doi:10.1186/s12989-016-0124-x26926244
  • Ilyechova EY, Saveliev AN, Skvortsov AN, et al. The effects of silver ions on copper metabolism in rats. Metallomics. 2014;6(10):1970–1987. doi:10.1039/C4MT00107A25008154
  • Rózga M, Sokołowska M, Protas AM, Bal W. Human serum albumin coordinates Cu(II) at its N-terminal binding site with 1 pM affinity. J Biol Inorg Chem. 2007;12(6):913–918.17516096
  • Gonzalez P, Bossak K, Stefaniak E, et al. N-terminal cu-binding motifs (Xxx-Zzz-His, Xxx-His) and their derivatives: chemistry, biology and medicinal applications. Chemistry. 2018;24(32):8029–8041. doi:10.1002/chem.20170539829336493
  • Sottrup-Jensen L, Stepanik TM, Kristensen T, et al. Primary structure of human alpha 2-macroglobulin. V. The complete structure. J Biol Chem. 1984;259(13):8318–8327.6203908
  • Hanson SR, Donley SA, Linder MC. Transport of silver in virgin and lactating rats and relation to copper. J Trace Elem Med Biol. 2001;15(4):243–253. doi:10.1016/S0946-672X(01)80040-711846014
  • Harada M, Sakisaka S, Yoshitake M, et al. Biliary copper excretion in acutely and chronically copper-loaded rats. Hepatology. 1993;17(1):111–117. doi:10.1002/hep.18401701208423032
  • Verbina IA, Puchkova LV, Gaitskhoki VS, Neifakh SA. Isolation and partial characterization of molecular forms of ceruloplasmin from human bile. FEBS Lett. 1992;298(2–3):105–108. doi:10.1016/0014-5793(92)80032-C1544429
  • Chowrimootoo GF, Ahmed HA, Seymour CA. New insights into the pathogenesis of copper toxicosis in Wilson’s disease: evidence for copper incorporation and defective canalicular transport of caeruloplasmin. Biochem J. 1996;315((Pt 3)(Pt 3)):851–855. doi:10.1042/bj31508518645167
  • Hellman NE, Gitlin JD. Ceruloplasmin metabolism and function. Annu Rev Nutr. 2002;22:439–458. doi:10.1146/annurev.nutr.22.012502.11445712055353
  • Kędziora A, Speruda M, Krzyżewska E, Rybka J, Łukowiak A, Bugla-Płoskońska G. Similarities and differences between silver ions and silver in nanoforms as antibacterial agents. Int J Mol Sci. 2018;19(2):444. doi:10.3390/ijms19020444
  • Dong Y, Zhu H, Shen Y, Zhang W, Zhang L. Antibacterial activity of silver nanoparticles of different particle size against Vibrio Natriegens. PLoS One. 2019;14(9):e0222322. doi:10.1371/journal.pone.022232231518380
  • Le Ouay B, Stellacci F. Antibacterial activity of silver nanoparticles: A surface science insight. Nano Today. 2015;10(3):339–354. doi:10.1016/j.nantod.2015.04.002
  • Sankova TP, Orlov IA, Saveliev AN, et al. The extracellular domain of human high affinity copper transporter (hNdCTR1), synthesized by E. coli cells, chelates silver and copper ions in vivo. Biomolecules. 2017;7(4):78. doi:10.3390/biom7040078
  • Juling S, Bachler G, von Götz N, et al. In vivo distribution of nanosilver in the rat: the role of ions and de novo-formed secondary particles. Food Chem Toxicol. 2016;97:327–335. doi:10.1016/j.fct.2016.08.01627523291
  • Leclerc S, Wilkinson KJ. Bioaccumulation of Nanosilver by Chlamydomonas reinhardtii-nanoparticle or the free ion? Environ Sci Technol. 2014;48(1):358–364. doi:10.1021/es404037z24320028
  • Vidmar J, Loeschner K, Correia M, et al. Translocation of silver nanoparticles in the ex vivo human placenta perfusion model characterized by single particle ICP-MS. Nanoscale. 2018;10(25):11980–11991.29904776
  • Bruneau A, Turcotte P, Pilote M, Gagné F, Gagnon C. Fate of silver nanoparticles in wastewater and immunotoxic effects on rainbow trout. Aquat Toxicol. 2016;174:70–81. doi:10.1016/j.aquatox.2016.02.01326921728
  • Rezaei A, Farzinpour A, Vaziry A, Jalili A. Effects of silver nanoparticles on hematological parameters and hepatorenal functions in laying japanese Quails. Biol Trace Elem Res. 2018;185(2):475–485. doi:10.1007/s12011-018-1267-429450680
  • El Mahdy MM, Eldin TA, Aly HS, Mohammed FF, Shaalan MI. Evaluation of hepatotoxic and genotoxic potential of silver nanoparticles in albino rats. Exp Toxicol Pathol. 2015;67(1):21–29. doi:10.1016/j.etp.2014.09.00525446800
  • Saeki K, Nakajima M, Loughlin TR, et al. Accumulation of silver in the liver of three species of pinnipeds. Environ Pollut. 2001;112(1):19–25. doi:10.1016/S0269-7491(00)00103-211202650
  • Cousins RJ. Absorption, transport, and hepatic metabolism of copper and zinc: special reference to metallothionein and ceruloplasmin. Physiol Rev. 1985;65(2):238–309. doi:10.1152/physrev.1985.65.2.2383885271
  • Harvey LJ, McArdle HJ. Biomarkers of copper status: a brief update. Br J Nutr. 2008;99(Suppl 3):S10–S13. doi:10.1017/S000711450800680618598583
  • Cabrera A, Alonzo E, Sauble E, et al. Copper binding components of blood plasma and organs, and their responses to influx of large doses of (65) Cu, in the mouse. Biometals. 2008;21(5):525–543. doi:10.1007/s10534-008-9139-618357416
  • Bernevic B, El-Khatib AH, Jakubowski N, Weller MG. Online immunocapture ICP-MS for the determination of the metalloprotein ceruloplasmin in human serum. BMC Res Notes. 2018;11(1):213. doi:10.1186/s13104-018-3324-729609633
  • Hellman NE, Kono S, Mancini GM, Hoogeboom AJ, De Jong GJ, Gitlin JD. Mechanisms of copper incorporation into human ceruloplasmin. J Biol Chem. 2002;277(48):46632–46638.12351628
  • Hirasawa F, Kawarada Y, Sato M, et al. The effect of silver administration on the biosynthesis and the molecular properties of rat ceruloplasmin. Biochim Biophys Acta. 1997;1336(2):195–201. doi:10.1016/S0304-4165(97)00026-39305790
  • Jimenez-Arroyo N, Cardona-Felix CS, Rojas-Trejo SP, Rudino-Pinera E. Structural function of the methionine-rich beta-hairpin in the laccase for T. Thermophilus. 2020.
  • Liu W, Worms IAM, Herlin-Boime N, et al. Interaction of silver nanoparticles with metallothionein and ceruloplasmin: impact on metal substitution by Ag(i), corona formation and enzymatic activity. Nanoscale. 2017;9(19):6581–6594. doi:10.1039/C7NR01075C28474724
  • Kirsipuu T, Zadorožnaja A, Smirnova J, et al. Copper(II)-binding equilibria in human blood. Sci Rep. 2020;10(1):5686. doi:10.1038/s41598-020-62560-432231266
  • Garcia-Ferrer I, Marrero A, Gomis-Rüth FX, Goulas T. α2-macroglobulins: structure and function. Subcell Biochem. 2017;83:149–183.28271476
  • Liu N, Lo LS, Askary SH, et al. Transcuprein is a macroglobulin regulated by copper and iron availability. J Nutr Biochem. 2007;18(9):597–608. doi:10.1016/j.jnutbio.2006.11.00517363239
  • Moriya M, Ho YH, Grana A, et al. Copper is taken up efficiently from albumin and alpha2-macroglobulin by cultured human cells by more than one mechanism. Am J Physiol Cell Physiol. 2008;295(3):C708–C721. doi:10.1152/ajpcell.00029.200818579803
  • Isaac L, Florido MP, Fecchio D, Singer LM. Murine alpha-2-macroglobulin increase during inflammatory responses and tumor growth. Inflamm Res. 1999;48(8):446–452. doi:10.1007/s00011005048510493162
  • Coan MH, Roberts RC. A redetermination of the concentration of alpha 2-macroglobulin in human plasma. Biol Chem Hoppe Seyler. 1989;370(7):673–676.2476158
  • Lillis AP, Mikhailenko I, Strickland DK. Beyond endocytosis: LRP function in cell migration, proliferation and vascular permeability. J Thromb Haemost. 2005;3(8):1884–1893. doi:10.1111/j.1538-7836.2005.01371.x16102056
  • Zhao F, Zhao Y, Liu Y, Chang X, Chen C, Zhao Y. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small. 2011;7(10):1322–1337. doi:10.1002/smll.20110000121520409
  • Panzarini E, Mariano S, Carata E, Mura F, Rossi M, Dini L. Intracellular transport of silver and gold nanoparticles and biological responses: an update. Int J Mol Sci. 2018;19(5):1305. doi:10.3390/ijms19051305
  • Sakurai Y, Tada H, Gonda K, et al. Development of silica-coated silver iodide nanoparticles and their biodistribution. Tohoku J Exp Med. 2012;228(4):317–323. doi:10.1620/tjem.228.31723132228
  • Gray LW, Peng F, Molloy SA, et al. Urinary copper elevation in a mouse model of Wilson’s disease is a regulated process to specifically decrease the hepatic copper load. PLoS One. 2012;7(6):e38327. doi:10.1371/journal.pone.003832722802922
  • Puchkova LV, Aleĭnikova TD, Verbina IA, Zakharova ET, Pliss MG, Gaĭtskhoki VS. Biosintez dvukh molekuliarnykh form tseruloplazmina v pecheni krysy i ikh poliarnaia sekretsiia v krovotok i v zhelch’ [Biosynthesis of two molecular forms of ceruloplasmin in rat liver and their polar secretion into the blood stream and bile]. Biokhimiia. 1993;58(12):1893–1901.8292651
  • Gregoriadis G, Morell AG, Sternlieb I, Scheinberg IH. Catabolism of desialylated ceruloplasmin in the liver. J Biol Chem. 1970;245(21):5833–5837.5472375