journal article·2016-08

Silver nanoparticles: in vivo toxicity in zebrafish embryos and a comparison to silver nitrate

Dina A. Mosselhy, Wei He, Dan Li, Yaping Meng, Qingling Feng

Journal of Nanoparticle Research· Volume 18· Issue 8
Publisher page

Abstract

The wide antimicrobial administration of silver nanoparticles (AgNPs) has raised the risks associated with their exposure. However, there is lack of robust toxicological data for the applied AgNPs to be in line with their wide antimicrobial applications. This study therefore set out to assess the in vivo toxicity of two different sizes of AgNPs using zebrafish embryos (Danio rerio) as a brilliant in vivo model. The pivotal role of size of AgNPs in the toxicity was highlighted, wherein the smaller AgNPs (Ag-9 nm) exhibited more embryo toxicities than the larger particles (Ag-30 nm). Much uncertainty still exists about whether the cause of in vivo toxicity of AgNPs is the physicochemical properties of AgNPs or the released silver ions (Ag+). Therefore, another purpose of this study is to compare the toxicity of AgNPs with silver nitrate (AgNO3) in terms of mortality, hatchability and cardiac rates, and a series of phenotypic endpoints of zebrafish embryos. Collectively, the present results point towards the remarkable size-dependent toxicity of AgNPs. Wherein, the smaller AgNPs (9 ± 2 nm) induce increased mortality rates and decreased hatchability rates than the larger particles (30 ± 5 nm) in a dose-dependent manner. Besides, AgNPs and AgNO3 induce holistic different toxic mortality and hatchability rates. We have also found striking discrepancies in the phenotypic defects that were induced by AgNPs and AgNO3. The significant phenotypic defect induced by AgNPs is the axial deformity, while it is the deposition of Ag+ on the embryonic chorion for AgNO3. Therefore, it is proposed that AgNPs and AgNO3 induce different in vivo toxicities.
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Research context

OpenAlex topics: Nanoparticles: synthesis and applications · Heavy Metal Exposure and Toxicity

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References (59)

Show source-provided references
1. Agnihotri S, Mukherji S, Mukherji S (2014) Size-controlled silver nanoparticles synthesized over the range 5–100 nm using the same protocol and their antibacterial efficacy. RSC Adv 4(8):3974–3983. doi: 10.1039/C3RA44507K10.1039/C3RA44507K ↗
2. Anker JN, Hall WP, Lyandres O, Shah NC, Zhao J, Van Duyne RP (2008) Biosensing with plasmonic nanosensors. Nat Mater 7(6):442–453. doi: 10.1038/nmat216210.1038/nmat2162 ↗
3. Asghari S, Johari SA, Lee JH, Kim YS, Jeon YB, Choi HJ, Moon MC, Yu IJ (2012) Toxicity of various silver nanoparticles compared to silver ions in Daphnia magna. J Nanobiotechnology 10(14):1–14. doi: 10.1186/1477-3155-10-1410.1186/1477-3155-10-14 ↗
4. Asharani PV, Wu YL, Gong Z, Valiyaveettil S (2008) Toxicity of silver nanoparticles in zebrafish models. Nanotechnology 19(25):255102. doi: 10.1088/09574484/19/25/25510210.1088/09574484/19/25/255102 ↗
5. Asharani PV, Lianwu Y, Gong Z, Valiyaveettil S (2011) Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology 5(1):43–54. doi: 10.3109/17435390.2010.48920710.3109/17435390.2010.489207 ↗
6. Bai W, Zhang Z, Tian W, He X, Ma Y, Zhao Y, Chai Z (2010) Toxicity of zinc oxide nanoparticles to zebrafish embryo: a physicochemical study of toxicity mechanism. J Nanopart Res 12(5):1645–1654. doi: 10.1007/s11051-009-9740-910.1007/s11051-009-9740-9 ↗
7. Bankar A, Joshi B, Kumar AR, Zinjarde S (2010) Banana peel extract mediated novel route for synthesis of silver nanoparticles. Colloids Surf A Physicochem Eng Asp 368(1):58–63. doi: 10.1016/j.colsurfa.2010.07.02410.1016/j.colsurfa.2010.07.024 ↗
8. Bar-Ilan O, Albrecht RM, Fako VE, Furgeson DY (2009) Toxicity assessments of multisized gold and silver nanoparticles in zebrafish embryos. Small 5(16):1897–1910. doi: 10.1002/smll.20080171610.1002/smll.200801716 ↗
9. Bianchini A, Grosell M, Gregory SM, Wood CM (2002) Acute silver toxicity in aquatic animals is a function of sodium uptake rate. Environ Sci Technol 36(8):1763–1766. doi: 10.1021/es011028t10.1021/es011028t ↗
10. Bilberg K, Hovgaard MB, Besenbacher F, Baatrup E (2011) In vivo toxicity of silver nanoparticles and silver ions in zebrafish (Danio rerio). J Toxicol 2012:9. doi: 10.1155/2012/29378410.1155/2012/293784 ↗
11. Bowman CR, Bailey FC, Elrod-Erickson M, Neigh AM, Otter RR (2012) Effects of silver nanoparticles on zebrafish (Danio rerio) and Escherichia coli (ATCC 25922): a comparison of toxicity based on total surface area versus mass concentration of particles in a model eukaryotic and prokaryotic system. Environ Toxicol Chem 31(8):1793–1800. doi: 10.1002/etc.188110.1002/etc.1881 ↗
12. Chae YJ, Pham CH, Lee J, Bae E, Yi J, Gu MB (2009) Evaluation of the toxic impact of silver nanoparticles on Japanese medaka (Oryzias latipes). Aquat Toxicol 94(4):320–327. doi: 10.1016/j.aquatox.2009.07.01910.1016/j.aquatox.2009.07.019 ↗
13. Chan PK, Lin CC, Cheng SH (2009) Noninvasive technique for measurement of heartbeat regularity in zebrafish (Danio rerio) embryos. BMC Biotechnol 9(1):11. doi: 10.1186/1472-6750-9-1110.1186/1472-6750-9-11 ↗
14. Choi O, Clevenger TE, Deng B, Surampalli RY, Ross L Jr, Hu Z (2009) Role of sulfide and ligand strength in controlling nanosilver toxicity. Water Res 43(7):1879–1886. doi: 10.1016/j.watres.2009.01.02910.1016/j.watres.2009.01.029 ↗
15. Cioffi N, Rai M (2012) Nano-antimicrobials: progress and prospects. Springer, Heidelberg10.1007/978-3-642-24428-5 ↗
16. Duan J, Yu Y, Li Y, Yu Y, Sun Z (2013) Cardiovascular toxicity evaluation of silica nanoparticles in endothelial cells and zebrafish model. Biomaterials 34(23):5853–5862. doi: 10.1016/j.biomaterials.2013.04.03210.1016/j.biomaterials.2013.04.032 ↗
17. Fako VE, Furgeson DY (2009) Zebrafish as a correlative and predictive model for assessing biomaterial nanotoxicity. Adv Drug Deliv Rev 61:478–486. doi: 10.1016/j.addr.2009.03.00810.1016/j.addr.2009.03.008 ↗
18. Georgantzopoulou A, Balachandran YL, Rosenkranz P, Dusinska M, Lankoff A, Wojewodzka M, Kruszewski M, Guignard C, Audinot JN, Girija S, Hoffmann L, Gutleb AC (2012) Ag nanoparticles: size-and surface-dependent effects on model aquatic organisms and uptake evaluation with NanoSIMS. Nanotoxicology 7(7):1168–1178. doi: 10.3109/17435390.2012.71531210.3109/17435390.2012.715312 ↗
19. George S, Xia T, Rallo R, Zhao Y, Ji Z, Lin S, Wang X, Zhang H, France B, Schoenfeld D, Damoiseaux R, Liu R, Lin S, Bradley KA, Cohen Y, Nel AE (2011) Use of a high-throughput screening approach coupled with in vivo zebrafish embryo screening to develop hazard ranking for engineered nanomaterials. ACS Nano 5:1805–1817. doi: 10.1021/nn102734s10.1021/nn102734s ↗
20. George S, Lin S, Ji Z, Thomas CR, Li LJ, Mecklenburg M, Meng H, Wang X, Zhang H, Xia T, Hohman JN, Lin S, Zink JI, Weiss PS, Nel AE (2012) Surface defects on plate-shaped silver nanoparticles contribute to its hazard potential in a fish gill cell line and zebrafish embryos. ACS Nano 6(5):3745–3795. doi: 10.1021/nn204671v10.1021/nn204671v ↗
21. Gliga AR, Skoglund S, Wallinder IO, Fadeel B, Karlsson HL (2014) Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release. Part Fibre Toxicol 11(1):1. doi: 10.1186/1743-8977-11-1110.1186/1743-8977-11-11 ↗
22. Gorka DE, Osterberg JS, Gwin CA, Colman BP, Meyer JN, Bernhardt ES, Gunsch CK, DiGulio RT, Liu J (2015) Reducing environmental toxicity of silver nanoparticles through shape control. Environ Sci Technol 49(16):10093–10098. doi: 10.1021/acs.est.5b0171110.1021/acs.est.5b01711 ↗
23. Gurunathan S, Kalishwaralal K, Vaidyanathan R, Venkataraman D, Pandian SRK, Muniyandi J, Hariharan N, Eom SH (2009) Biosynthesis, purification and characterization of silver nanoparticles using Escherichia coli. Colloid Surf B Biointerfaces 74(1):328–335. doi: 10.1016/j.colsurfb.2009.07.04810.1016/j.colsurfb.2009.07.048 ↗
24. Haeili M, Moore C, Davis CJC, Cochran JB, Shah S, Shrestha TB, Zhang Y, Bossmann SH, Benjamin WH, Kutsch O, Wolschendorf F (2014) Copper complexation screen reveals compounds with potent antibiotic properties against methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 58(7):3727–3736. doi: 10.1128/AAC.02316-1310.1128/AAC.02316-13 ↗
25. Han L, Wei H, Tu B, Zhao D (2011) A facile one-pot synthesis of uniform core–shell silver nanoparticle@ mesoporous silica nanospheres. Chem Commun 47(30):8536–8538. doi: 10.1039/c1cc12718g10.1039/c1cc12718g ↗
26. He R, Qian X, Yin J, Zhu Z (2002) Preparation of polychrome silver nanoparticles in different solvents. J Mater Chem 12(12):3783–3786. doi: 10.1039/b205214h10.1039/b205214h ↗
27. He W, Liu X, Kienzle A, Müller WE, Feng Q (2016) In vitro uptake of silver nanoparticles and their toxicity in human mesenchymal stem cells derived from bone marrow. J Nanosci Nanotechnol 16(1):219–228. doi: 10.1166/jnn.2016.1072810.1166/jnn.2016.10728 ↗
28. Huang H, Lu FI, Jia S, Meng S, Cao Y, Wang Y, Ma W, Yin K, Wen Z, Peng J, Thisse C, Thisse B, Meng A (2007) Amotl2 is essential for cell movements in zebrafish embryo and regulates c-Src translocation. Development 134:979–988. doi: 10.1242/dev.0278210.1242/dev.02782 ↗
29. Ivask A, ElBadawy A, Kaweeteerawat C, Boren D, Fischer H, Ji Z, Chang CH, Liu R, Tolaymat T, Telesca D, Zink JI, Cohen Y, Holden PA, Godwin HA (2013) Toxicity mechanisms in Escherichia coli vary for silver nanoparticles and differ from ionic silver. ACS Nano 8(1):374–386. doi: 10.1021/nn404404710.1021/nn4044047 ↗
30. Ivask A, Kurvet I, Kasemets K, Blinova I, Aruoja V, Suppi S, Vija H, Käkinen A, Titma T, Heinlaan M, Visnapuu M, Koller D, Kisand V, Kahru A (2014) Size-dependent toxicity of silver nanoparticles to bacteria, yeast, algae, crustaceans and mammalian cells in vitro. PLoS One 9(7):e102108. doi: 10.1371/journal.pone.010210810.1371/journal.pone.0102108 ↗
31. Jiang L, Wu Z, Wu D, Yang W, Jin R (2007) Controllable embedding of silver nanoparticles on silica nanospheres using poly (acrylic acid) as a soft template. Nanotechnology 18(18):185603. doi: 10.1088/0957-4484/18/18/18560310.1088/0957-4484/18/18/185603 ↗
32. Kalishwaralal K, Deepak V, Ramkumarpandian S, Nellaiah H, Sangiliyandi G (2008) Extracellular biosynthesis of silver nanoparticles by the culture supernatant of Bacillus licheniformis. Mater Lett 62(29):4411–4413. doi: 10.1016/j.matlet.2008.06.05110.1016/j.matlet.2008.06.051 ↗
33. Kannan RR, Jerley AJA, Ranjani M, Prakash VSG (2011) Antimicrobial silver nanoparticle induces organ deformities in the developing Zebrafish (Danio rerio) embryos. J Biomed Sci Eng 4(04):248–254. doi: 10.4236/jbise.2011.4403410.4236/jbise.2011.44034 ↗
34. Kim KT, Truong L, Wehmas L, Tanguay RL (2013) Silver nanoparticle toxicity in the embryonic zebrafish is governed by particle dispersion and ionic environment. Nanotechnology 24(11):115101. doi: 10.1088/0957-4484/24/11/11510110.1088/0957-4484/24/11/115101 ↗
35. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203(3):253–31010.1002/aja.1002030302 ↗
36. Kwok KWH, Auffan M, Badireddy AR, Nelson CM, Wiesner MR, Chilkoti A, Liu J, Marinakos SM, Hinton DE (2012) Uptake of silver nanoparticles and toxicity to early life stages of Japanese medaka (Oryzias latipes): effect of coating materials. Aquat Toxicol 120:59–66. doi: 10.1016/j.aquatox.2012.04.01210.1016/j.aquatox.2012.04.012 ↗
37. Laban G, Nies LF, Turco RF, Bickham JW, Sepúlveda MS (2010) The effects of silver nanoparticles on fathead minnow (Pimephales promelas) embryos. Ecotoxicology 19(1):185–195. doi: 10.1007/s10646-009-0404-410.1007/s10646-009-0404-4 ↗
38. Lee KJ, Browning LM, Nallathamby PD, Desai T, Cherukuri PK, Xu XHN (2012) In vivo quantitative study of sized-dependent transport and toxicity of single silver nanoparticles using zebrafish embryos. Chem Res Toxicol 25(5):1029–1046. doi: 10.1021/tx300021u10.1021/tx300021u ↗
39. Lee KJ, Browning LM, Nallathamby PD, Osgood CJ, Xu XHN (2013) Silver nanoparticles induce developmental stage-specific embryonic phenotypes in zebrafish. Nanoscale 5(23):11625–11636. doi: 10.1039/c3nr03210h10.1039/c3nr03210h ↗
40. Li L, Sun J, Li X, Zhang Y, Wang Z, Wang C, Dai J, Wang Q (2012a) Controllable synthesis of monodispersed silver nanoparticles as standards for quantitative assessment of their cytotoxicity. Biomaterials 33(6):1714–1721. doi: 10.1016/j.biomaterials.2011.11.03010.1016/j.biomaterials.2011.11.030 ↗
41. Li Z, Wang Y, Zhang M, Xu P, Huang H, Wu D, Meng A (2012b) The Amotl2 gene inhibits Wnt/β- catenin signaling and regulates embryonic development in zebrafish. J Biol Chem 287(16):13005–13015. doi: 10.1074/jbc.M112.34741910.1074/jbc.M112.347419 ↗
42. Lin JJ, Lin WC, Dong RX, Hsu SH (2012) The cellular responses and antibacterial activities of silver nanoparticles stabilized by different polymers. Nanotechnology 23(6):065102. doi: 10.1088/0957-4484/23/6/06510210.1088/0957-4484/23/6/065102 ↗
43. Lin S, Zhao Y, Nel AE, Lin S (2013) Zebrafish: an in vivo model for nano EHS studies. Small 9(9–10):1608–1618. doi: 10.1002/smll.20120211510.1002/smll.201202115 ↗
44. McGrath P, Li CQ (2008) Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov Today 13(9–10):394–401. doi: 10.1016/j.drudis.2008.03.00210.1016/j.drudis.2008.03.002 ↗
45. Mosselhy DA, El-Aziz MA, Hanna M, Ahmed MA, Husien MM, Feng Q (2015) Comparative synthesis and antimicrobial action of silver nanoparticles and silver nitrate. J Nanopart Res 17(12):1–10. doi: 10.1007/s11051-015-3279-810.1007/s11051-015-3279-8 ↗
46. Osborne OJ, Johnston BD, Moger J, Balousha M, Lead JR, Kudoh T, Tyler CR (2013) Effects of particle size and coating on nanoscale Ag and TiO2 exposure in zebrafish (Danio rerio) embryos. Nanotoxicology 7(8):1315–1324. doi: 10.3109/17435390.2012.73748410.3109/17435390.2012.737484 ↗
47. Park MVDZ, Neigh AM, Vermeulen JP, de la Fonteyne LJJ, Verharen HW, Briedé JJ, van Loveren H, de Jong WH (2011) The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. Biomaterials 32(36):9810–9817. doi: 10.1016/j.biomaterials.2011.08.08510.1016/j.biomaterials.2011.08.085 ↗
48. Powers CM, Yen J, Linney EA, Seidler FJ, Slotkin TA (2010) Silver exposure in developing zebrafish (Danio rerio): persistent effects on larval behavior and survival. Neurotoxicol Teratol 32(3):391–397. doi: 10.1016/j.ntt.2010.01.00910.1016/j.ntt.2010.01.009 ↗
49. Powers CM, Slotkin TA, Seidler FJ, Badireddy AR, Padilla S (2011) Silver nanoparticles alter zebrafish development and larval behavior: distinct roles for particle size, coating and composition. Neurotoxicol Teratol 33(6):708–714. doi: 10.1016/j.ntt.2011.02.00210.1016/j.ntt.2011.02.002 ↗
50. Prabhu S, Poulose EK (2012) Silver nanoparticles: mechanism of antimicrobial action, synthesis, medical applications, and toxicity effects. Int Nano Lett 2(1):1–10. doi: 10.1186/2228-5326-2-3210.1186/2228-5326-2-32 ↗
51. Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27:76–83. doi: 10.1016/j.biotechadv.2008.09.00210.1016/j.biotechadv.2008.09.002 ↗
52. Ribeiro F, Gallego-Urrea JA, Jurkschat K, Crossley A, Hassellöv M, Taylor C, Soares AMVM, Loureiro S (2014) Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Sci Total Environ 466:232–241. doi: 10.1016/j.scitotenv.2013.06.10110.1016/j.scitotenv.2013.06.101 ↗
53. Stebounova LV, Guio E, Grassian VH (2011) Silver nanoparticles in simulated biological media: a study of aggregation, sedimentation, and dissolution. J Nanopart Res 13(1):233–244. doi: 10.1007/s11051-010-0022-310.1007/s11051-010-0022-3 ↗
54. Suchomel P, Kvitek L, Panacek A, Prucek R, Hrbac J, Vecerova R, Zboril R (2015) Comparative study of antimicrobial activity of AgBr and Ag nanoparticles (NPs). PLoS One 10(3):e0119202. doi: 10.1371/journal.pone.011920210.1371/journal.pone.0119202 ↗
55. Truong L, Harper SL, Tanguay RL (2011) Evaluation of embryotoxicity using the zebrafish model. Method Mol Biol 691:271–279. doi: 10.1007/978-1-60761-849-2_1610.1007/978-1-60761-849-2_16 ↗
56. Verma A, Mehata MS (2015) Controllable synthesis of silver nanoparticles using Neem leaves and their antimicrobial activity. J Radiat Res Appl Sci 9(1):109–115. doi: 10.1016/j.jrras.2015.11.00110.1016/j.jrras.2015.11.001 ↗
57. Wehmas LC, Anders C, Chess J, Punnoose A, Pereira CB, Greenwood JA, Tanguay RL (2015) Comparative metal oxide nanoparticle toxicity using embryonic zebrafish. Toxicol Rep 2:702–715. doi: 10.1016/j.toxrep.2015.03.01510.1016/j.toxrep.2015.03.015 ↗
58. Wu Y, Zhou Q, Li H, Liu W, Wang T, Jiang G (2010) Effects of silver nanoparticles on the development and histopathology biomarkers of Japanese medaka (Oryzias latipes) using the partial-life test. Aquat Toxicol 100(2):160–167. doi: 10.1016/j.aquatox.2009.11.01410.1016/j.aquatox.2009.11.014 ↗
59. Xiu ZM, Zhang QB, Puppala HL, Colvin VL, Alvarez PJJ (2012) Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett 12(8):4271–4275. doi: 10.1021/nl301934w10.1021/nl301934w ↗