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Improvement Testing Strategy for Aligning Nanomaterial Safety Assessments and Oxidative Stress Responses

  • Loutfy H. MadkourEmail author
Chapter
Part of the Nanomedicine and Nanotoxicology book series (NANOMED)

Abstract

Assessing the safety of engineered nanomaterials (NMs) is paramount to the responsible and sustainable development of nanotechnology, which provides huge societal benefits. Nanoscience includes the design of materials with virtually infinite possibilities. There is a clear need to test the safety of these new materials once exposed to the environment and living organisms, avoiding toxic materials and developing healthy alternatives. The potential positive benefits of these materials should be selected according to their impact on the environment and the human population. Assessing the safety of engineered nanomaterials (NMs) is paramount to the responsible and sustainable development of nanotechnology, which provides huge societal benefits. Currently, there is no evidence that engineered NMs cause detrimental health effects in humans. However, investigation of NM toxicity using in vivo, in vitro, in chemico, and in silico models has demonstrated that some NMs stimulate oxidative stress and inflammation, which may lead to adverse health effects. Accordingly, investigation of these responses currently dominates NM safety assessments. There is a need to reduce reliance on rodent testing in nanotoxicology for ethical, financial, and legislative reasons, and due to evidence that rodent models do not always predict the human response. The development of a tiered testing strategy for NM hazard assessment that promotes the more widespread adoption of non-rodent, alternative models and focuses on investigation of inflammation and oxidative stress could make nanotoxicology testing more ethical, relevant, and cost and time efficient.

Keywords

Nanomaterial Nanoparticle Nanotoxicology Zebrafish In vitro 3Rs Inflammation Oxidative stress Neutrophil Macrophage 

References

  1. Abrikossova N, Skoglund C, Ahrén M, Bengtsson T, Uvdal K (2012) Effects of gadolinium oxide nanoparticles on the oxidative burst from human neutrophil granulocytes. Nanotechnology 23(27):275101CrossRefGoogle Scholar
  2. Afrikanova T, Serruys AS, Buenafe OE, Clinckers R, Smolders I, de Witte PA, Crawford AD, Esguerra CV (2013) Validation of the zebrafish pentylenetetrazol seizure model: locomotor versuselectrographic responses to antiepileptic drugs. PLoS ONE 8(1):e54166CrossRefGoogle Scholar
  3. Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26(9):499–509CrossRefGoogle Scholar
  4. Babin K, Antoine F, Goncalves DM, Girard D (2013) TiO2, CeO2 and ZnO nanoparticles and modulation of the degranulation process in human neutrophils. Toxicol Lett 221(1):57–63CrossRefGoogle Scholar
  5. Baktur R, Patel H, Kwon S (2011) Effect of exposure conditions on SWCNT-induced inflammatory response in human alveolar epithelial cells. Toxicol In Vitro 25(5):1153–1160.  https://doi.org/10.1016/j.tiv.2011.04.001 (Epub 2011 Apr 6)CrossRefGoogle Scholar
  6. Barros TP, Alderton WK, Reynolds HM, Roach AG, Berghmans S (2008) Zebrafish: an emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery. Br J Pharmacol 154(7):1400–1413CrossRefGoogle Scholar
  7. Beerman RW, Matty MA, Au GG, Looger LL, Choudhury KR, Keller PJ, Tobin DM (2015) Direct in vivo manipulation and imaging of calcium transients in neutrophils identify a critical role for leading-edge calcium flux. Cell Rep. 13(10):2107–2117CrossRefGoogle Scholar
  8. Benard EL, van der Sar AM, Ellett F, Lieschke GJ, Spaink HP, Meijer AH, (2012) Infection of zebrafish embryos with intracellular bacterial pathogens. J Vis Exp 15(61):3781Google Scholar
  9. Bilberg K, Hovgaard MB, Besenbacher F, Baatrup E (2012) In vivo toxicity of silver nanoparticles and silver Ions in zebrafish (Danio rerio). J Toxicol 293784Google Scholar
  10. Borm PJ, Tran L (2002) From quartz hazard to quartz risk: the coal mines revisited. Ann Occup Hyg 46(1):25–32Google Scholar
  11. Boyles MS, Young L, Brown DM, MacCalman L, Cowie H, Moisala A, Smail F, Smith PJ, Proudfoot L, Windle AH, Stone V (2015) Multi-walled carbon nanotube induced frustrated phagocytosis, cytotoxicity and pro-inflammatory conditions in macrophages are length dependent and greater than that of asbestos. Toxicol In Vitro 29(7):1513–1528CrossRefGoogle Scholar
  12. Brown T, Mackey K (2001) Analysis of RNA by northern and slot-blot hybridization. Curr Protoc Neurosci. Chapter 5: Unit 5.17.  https://doi.org/10.1002/0471142301.ns0517s15CrossRefGoogle Scholar
  13. Brown DM, Donaldson K, Borm PJ, Schins RP, Dehnhardt M, Gilmour P, Jimenez LA, Stone V (2004) Ca2+ and ROS-mediated activation of transcription factors and TNF-cytokine gene expression in macrophages exposed to ultrafine particles. Am J Physiol Lung Cell Mol Physiol 286:L344–L353CrossRefGoogle Scholar
  14. Brown DM, Kinloch IA, Bangert U, Windle AH, Walter DM, Walker GS, Scotchford CA, Donaldson K, Stone V (2007a) An in vitro study of the potential of carbon nanotubes and nanofibres to induce inflammatory mediators and frustrated phagocytosis. Carbon 45(9):1743–1756CrossRefGoogle Scholar
  15. Brown SB, Tucker CS, Ford C, Lee Y, Dunbar DR, Mullins JJ (2007b) Class III antiarrhythmic methanesulfonanilides inhibit leukocyte recruitment in zebrafish. J Leukoc Biol 82(1):79–84CrossRefGoogle Scholar
  16. Burden N, Mahony C, Müller BP, Terry C, Westmoreland C, Kimber I (2015) Aligning the 3Rs with new paradigms in the safety assessment of chemicals. Toxicology 1(330):62–66CrossRefGoogle Scholar
  17. Burden N, Benstead R, Clook M, Doyle I, Edwards P, Maynard SK, Ryder K, Sheahan D, Whale G, van Egmond R, Wheeler JR, Hutchinson TH (2016) advancing the 3Rs in regulatory ecotoxicology: a pragmatic cross-sector approach. Integr Environ Assess Manag 12(3):417–421CrossRefGoogle Scholar
  18. Burden N, Aschberger K, Chaudhry Q, Clift MJD, Doak S, Fowler P, Johnston H, Landsiedel R, Rowland J, Stone V (2017) The 3Rs as a framework to support a 21st century approach for nanosafety assessment. Nano Today 12:10–13CrossRefGoogle Scholar
  19. Burns CG, Milan DJ, Grande EJ, Rottbauer W, MacRae CA, Fishman MC (2005) High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nat Chem Biol 1(5):263–264CrossRefGoogle Scholar
  20. Chakraborty C, Sharma AR, Sharma G, Lee SS (2016) Zebrafish: a complete animal model to enumerate the nanoparticle toxicity. J Nanobiotechnology 14(1):65CrossRefGoogle Scholar
  21. Cheung CY, Webb SE, Love DR, Miller AL (2011) Visualization, characterization and modulation of calcium signaling during the development of slow muscle cells in intact zebrafish embryos. Int J Dev Biol 55(2):153–174CrossRefGoogle Scholar
  22. Cho WS, Duffin R, Poland CA, Howie SE, MacNee W, Bradley M, Megson IL, Donaldson K (2010) Metal oxide nanoparticles induce unique inflammatory footprints in the lung: important implications for nanoparticle testing. Environ Health Perspect 118(12):1699–1706CrossRefGoogle Scholar
  23. Choi JY, Ramachandran G, Kandlikar M (2009) The impact of toxicity testing costs on nanomaterial regulation. Environ Sci Technol 43(9):3030–3034CrossRefGoogle Scholar
  24. Choi JE, Kim S, Ahn JH, Youn P, Kang JS, Park K, Yi J, Ryu DY (2010) Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat Toxicol 100(2):151–159CrossRefGoogle Scholar
  25. Chu J, Sadler KC (2009) A new school in liver development: lessons from zebrafish. Hepatology 50(5):1656–1663CrossRefGoogle Scholar
  26. Clift MJ, Boyles MS, Brown DM, Stone V (2010) An investigation into the potential for different surface-coated quantum dots to cause oxidative stress and affect macrophage cell signalling in vitro. Nanotoxicology 4(2):139–149CrossRefGoogle Scholar
  27. Clift MJ, Varet J, Hankin SM, Brownlee B, Davidson AM, Brandenberger C, Rothen-Rutishauser B, Brown DM, Stone V (2011) Quantum dot cytotoxicity in vitro: an investigation into the cytotoxic effects of a series of different surface chemistries and their core/shell materials. Nanotoxicology 5(4):664–674CrossRefGoogle Scholar
  28. Costa PM, Fadeel B (2016) Emerging systems biology approaches in nanotoxicology: towards a mechanism-based understanding of nanomaterial hazard and risk. Toxicol Appl Pharmacol 299:101–111CrossRefGoogle Scholar
  29. Couto D, Freitas M, Vilas-Boas V, Dias I, Porto G, Lopez-Quintela MA, Rivas J, Freitas P, Carvalho F, Fernandes E (2014) Interaction of polyacrylic acid coated and non-coated iron oxide nanoparticles with human neutrophils. Toxicol Lett 225(1):57–65CrossRefGoogle Scholar
  30. Davis EE, Frangakis S, Katsanis N (1842) Interpreting human genetic variation with in vivo zebrafish assays. Biochim Biophys Acta 10:1960–1970Google Scholar
  31. Davis JM, Clay H, Lewis JL, Ghori N, Herbomel P, Ramakrishnan L (2002) Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formationin zebrafish embryos. Immunity 17(6):693–702CrossRefGoogle Scholar
  32. de Oliveira S, Reyes-Aldasoro CC, Candel S, Renshaw SA, Mulero V, Calado A (2013) Cxcl8 (IL-8) mediates neutrophil recruitment and behavior in the zebrafish inflammatory response. J Immunol 190(8):4349–4359CrossRefGoogle Scholar
  33. de Oliveira S, Lopez-Muñoz A, Martínez-Navarro FJ, Galindo-Villegas J, Mulero V, Calado  (2015) Cxcl8-l1 and Cxcl8-l2 are required in the zebrafish defense against Salmonella Typhimurium. Dev Comp Immunol 49(1):44–48CrossRefGoogle Scholar
  34. Deng Q, Sarris M, Bennin DA, Green JM, Herbomel P, Huttenlocher A (2013) Localized bacterial infection induces systemic activation of neutrophils through Cxcr2signaling in zebrafish. J Leukoc Biol 93(5):761–769CrossRefGoogle Scholar
  35. Dockery DW, Pope CA 3rd, Xu X, Spengler JD, Ware JH, Fay ME, Ferris BG, Speizer FE (1993) An association between air pollution and mortality in six US cites. N Engl J Med. 329(24):1753–1759CrossRefGoogle Scholar
  36. Dodd A, Curtis PM, Williams LC, Love DR (2000) Zebrafish: bridging the gap between development and disease. Hum Mol Genet 9(16):2443–2449CrossRefGoogle Scholar
  37. Donaldson K, Stone V, Borm PJ, Jimenez LA, Gilmour PS, Schins RP, Knaapen AM, Rahman I, Faux SP, Brown DM, MacNee W (2003) Oxidative stress and Ca2+ signaling in the adverse effects of environmental particles (PM10). Free Radic Biol Med 34(11):1369–1382CrossRefGoogle Scholar
  38. Driessen M, Vitins AP, Pennings JL, Kienhuis AS, Water B, van der Ven LT (2015) A transcriptomics-based hepatotoxicity comparison between the zebrafish embryo and established human and rodent in vitro and in vivo models using cyclosporine a, amiodarone and acetaminophen. Toxicol Lett 232(2):403–412CrossRefGoogle Scholar
  39. Driessen M, Kienhuis AS, Pennings JL, Pronk TE, van de Brandhof EJ, Roodbergen M, Spaink HP, van de Water B, van der Ven LT (2013) Exploring the zebrafish embryo as an alternative model for the evaluation of liver toxicity by histopathology and expression profiling. Arch Toxicol 87(5):807–23CrossRefGoogle Scholar
  40. Driscoll T, Nelson DI, Steenland K, Leigh J, Concha-Barrientos M, Fingerhut M, Prüss-Ustün A (2005) The global burden of non-malignant respiratory disease due to occupational airborne exposures. Am J Ind Med 48(6):432–445CrossRefGoogle Scholar
  41. Drummond IA, Davidson AJ (2010) Zebrafish kidney development. Methods Cell Biol 100:233–260.  https://doi.org/10.1016/B978-0-12-384892-5.00009-8CrossRefGoogle Scholar
  42. Duan J, Yu Y, Shi H, Tian L, Guo C, Huang P, Zhou X, Peng S, Sun Z (2013) Toxic effects of silica nanoparticles on zebrafish embryos and larvae. PLoS ONE 8(9):e74606CrossRefGoogle Scholar
  43. Duan J, Yu Y, Li Y, Wang Y, Sun Z (2016a) Inflammatory response and blood hypercoagulable state induced by low level co-exposure with silica nanoparticles and benzo[a]pyrene in zebrafish (Danio rerio) embryos. Chemosphere 151:152–162CrossRefGoogle Scholar
  44. Duan J, Yu Y, Li Y, Li Y, Liu H, Jing L, Yang M, Wang J, Li C, Sun Z (2016b) Low-dose exposure of silica nanoparticles induces cardiac dysfunction via neutrophil-mediated inflammation and cardiac contraction in zebrafish embryos. Nanotoxicology 10(5):575–585CrossRefGoogle Scholar
  45. Duffin AM, Johnson JA, Muyskens MA, Sevy ET (2007) Competition between photochemistry and energy transfer in UV-excited diazabenzenes. 4. UV photodissociation of 2,3-, 2,5-, and 2,6-dimethylpyrazine. J Phys Chem A 111(51):13330–13338 (Epub 2007 Nov 30)CrossRefGoogle Scholar
  46. ECHA (2011). The use of alternatives to testing on animals for the reach regulation. https://echa.europa.eu/documents/10162/13639/alternatives_test_animals_2011_en.pdf/9b0f7e93-4d61-401d-ba2c-80b3b9faaf66
  47. ECHA (2014) The use of alternatives to testing on animals for the reach regulation. second report under article 117(3) of the reach regulation. https://echa.europa.eu/documents/10162/13639/alternatives_test_animals_2014_en.pdf
  48. ECHA (2016a) Reach testing requirements and the ban on animal testing for cosmetics: reply to Peta campaign. http://ec.europa.eu/environment/chemicals/reach/animal_en.htm
  49. ECHA (2016b). Practical Guide: how to use alternatives to animal testing. https://echa.europa.eu/documents/10162/13655/practical_guide_how_to_use_alternatives_en.pdf
  50. Eimon PM, Rubinstein AL (2009) The use of in vivo zebrafish assays in drug toxicity screening. Expert Opin Drug Metab Toxicol 5(4):393–401.  https://doi.org/10.1517/17425250902882128CrossRefGoogle Scholar
  51. Ellett F, Pase L, Hayman JW, Andrianopoulos A, Lieschke GJ (2011) mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117(4):e49–e56CrossRefGoogle Scholar
  52. Ellett F, Elks PM, Robertson AL, Ogryzko NV, Renshaw SA (2015) Defining the phenotype of neutrophils following reverse migration in zebrafish. J Leukoc Biol 98(6):975–981CrossRefGoogle Scholar
  53. Ermak G, Davies KJ (2002) Ca2+ and oxidative stress: from cell signaling to cell death. Mol Immunol 38(10):713–721CrossRefGoogle Scholar
  54. European Commission (2011) Recommendation on the definition of a nanomaterial. http://ec.europa.eu/environment/chemicals/nanotech/pdf/commission_recommendation.pdf
  55. European Parliament (2010) Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32010L0063
  56. Fairbrother A, Fairbrother JR (2009) Are environmental regulations keeping up with innovation? A case study of the nanotechnology industry. Ecotoxicol Environ Saf 72(5):1327–1330CrossRefGoogle Scholar
  57. Fang L, Green SR, Baek JS, Lee SH, Ellett F, Deer E, Lieschke GJ, Witztum JL, Tsimikas S, Miller YI (2011) In vivo visualization and attenuation of oxidized lipid accumulation in hypercholesterolemic zebrafish. J Clin Invest 121(12):4861–4869CrossRefGoogle Scholar
  58. Farcal L, Torres Andón F, Di Cristo L, Rotoli BM, Bussolati O, Bergamaschi E, Mech A, Hartmann NB, Rasmussen K, Riego-Sintes J, Ponti J, Kinsner-Ovaskainen A, Rossi F, Oomen A, Bos P, Chen R, Bai R, Chen C, Rocks L, Fulton N, Ross B, Hutchison G, Tran L, Mues S, Ossig R, Schnekenburger J, Campagnolo L, Vecchione L, Pietroiusti A, Fadeel B (2015) Comprehensive in vitro toxicity testing of a panel of representative oxide nanomaterials: first steps towards an intelligent testing strategy. PLoS ONE 10(5):e0127174CrossRefGoogle Scholar
  59. Faria M, Navas JM, Ráldua D, Soares AM, Barata C (2014) Oxidative stress effects of titanium dioxide nanoparticle aggregates in zebrafish embryos. Sci Total Environ 470–471:379–389CrossRefGoogle Scholar
  60. Feng Y, Santoriello C, Mione M, Hurlstone A, Martin P (2010) Live imaging of innate immune cell sensing of transformed cells in zebrafish larvae: parallels between tumor initiation and wound inflammation. PLoS Biol 8(12):e1000562CrossRefGoogle Scholar
  61. Filep JG, El Kebir D (2009) Neutrophil apoptosis: a target for enhancing the resolution of inflammation. J Cell Biochem 108(5):1039–1046.  https://doi.org/10.1002/jcb.22351CrossRefGoogle Scholar
  62. Foucaud L, Wilson MR, Brown DM, Stone V (2007) Measurement of reactive species production by nanoparticles prepared in biologically relevant media. Toxicol Lett 174(1–3):1–9 (Epub 2007 Aug 7)CrossRefGoogle Scholar
  63. Ganesan S, Anaimalai Thirumurthi N, Raghunath A, Vijayakumar S, Perumal E (2016) Acute and sub-lethal exposure to copper oxide nanoparticles causes oxidative stress and teratogenicity in zebrafish embryos. J Appl Toxicol 36(4):554–567CrossRefGoogle Scholar
  64. Geiser LH, Ingersoll AR, Bytnerowicz A, Copeland SA (2008) Evidence of enhanced atmospheric ammoniacal nitrogen in Hells Canyon national recreation area: implications for natural and cultural resources. J Air Waste Manag Assoc 58(9):1223–1234CrossRefGoogle Scholar
  65. Gerloff K, Pereira DI, Faria N, Boots AW, Kolling J, Förster I, Albrecht C, Powell JJ, Schins RP (2013) Influence of simulated gastrointestinal conditions on particle-induced cytotoxicity and interleukin-8 regulation in differentiated and undifferentiated Caco-2 cells. Nanotoxicology 7(4):353–366CrossRefGoogle Scholar
  66. Goldsmith JR, Jobin C (2012) Think small: zebrafish as a model system of human pathology. J Biomed Biotechnol 817341Google Scholar
  67. Gonçalves DM, Girard D (2011) Titanium dioxide (TiO2) nanoparticles induce neutrophil influx and local production of several pro-inflammatory mediators in vivo. Int Immunopharmacol 11(8):1109–1115CrossRefGoogle Scholar
  68. Gonçalves DM, Chiasson S, Girard D (2010) Activation of human neutrophils by titanium dioxide (TiO2) nanoparticles. Toxicol In Vitro 24(3):1002–1008CrossRefGoogle Scholar
  69. Goodhead RM, Moger J, Galloway TS, Tyler CR (2015) Tracing engineered nanomaterials in biological tissues using Coherent Anti-stokes Raman Scattering (CARS) microscopy—A critical review. Nanotoxicology 9(7):928–939.  https://doi.org/10.3109/17435390.2014.991773CrossRefGoogle Scholar
  70. Gosens I, Kermanizadeh A, Jacobsen NR, Lenz AG, Bokkers B, de Jong WH, Krystek P, Tran L, Stone V, Wallin H, Stoeger T, Cassee FR (2015) Comparative hazard identification by a single dose lung exposure of zinc oxide and silver nanomaterials in mice. PLoS ONE 10(5):e0126934CrossRefGoogle Scholar
  71. Gratacap RL, Scherer AK, Seman BG, Wheeler RT (2017) Control of mucosal candidiasis in the zebrafish swim bladder depends on neutrophils that block filament invasion and drive extracellular-trap production. Infect Immun 85(9):Pii: e00276-17.  https://doi.org/10.1128/iai.00276-17 (Print 2017 Sept)
  72. Haase H, Fahmi A, Mahltig B (2014) Impact of silver nanoparticles and silver ions on innate immune cells. J Biomed Nanotechnol 10(6):1146–1156CrossRefGoogle Scholar
  73. Hall CJ, Boyle RH, Astin JW, Flores MV, Oehlers SH, Sanderson LE, Ellett F, Lieschke GJ, Crosier KE, Crosier PS (2013) Immunoresponsive gene 1 augments bactericidal activity of macrophage-lineage cells by regulating β-oxidation-dependent mitochondrial ROS production. Cell Metab 18(2):265–278CrossRefGoogle Scholar
  74. Halpern BN, Benacerraf B, Biozzi G (1953) Quantitative study of the granulopectic activity of the reticulo-endothelial system. I. The effect of the ingredients presents in India Ink and of substances affecting blood clotting in vivo on the fate of carbon particles administered intravenously in rats, mice and rabbits. Br J Exp Pathol 34(4):426–440Google Scholar
  75. Han X, Corson N, Wade-Mercer P, Gelein R, Jiang J, Sahu M, Biswas P, Finkelstein JN, Elder A, Oberdörster G (2012) Assessing the relevance of in vitro studies in nanotoxicology by examining correlations between in vitro and in vivo data. Toxicology 297(1–3):1–9CrossRefGoogle Scholar
  76. Hartung T (2009) Toxicology for the twenty-first century. Nature 460:208–212CrossRefGoogle Scholar
  77. Harvie EA, Huttenlocher A (2015) Non-invasive imaging of the innate immune response in a zebrafish larval model of Streptococcus iniae infection. J Vis Exp 98Google Scholar
  78. He JH, Gao JM, Huang CJ, Li CQ (2014) Zebrafish models for assessing developmental and reproductive toxicity. Neurotoxicol Teratol 42:35–42CrossRefGoogle Scholar
  79. Henry M, Beguin M, Requier F, Rollin O, Odoux J-F, Aupinel P et al (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336:348–350.  https://doi.org/10.1126/science.1215039CrossRefGoogle Scholar
  80. Herbomel P, Thisse B, Thisse C (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126(17):3735–3745Google Scholar
  81. Hermann AC, Millard PJ, Blake SL, Kim CH (2004) Development of a respiratory burst assay using zebrafish kidneys and embryos. J Immunol Methods 292(1–2):119–129CrossRefGoogle Scholar
  82. Hill AJ, Teraoka H, Heideman W, Peterson RE (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86(1):6–19CrossRefGoogle Scholar
  83. Hoodless LJ, Lucas CD, Duffin R, Denvir MA, Haslett C, Tucker CS, Rossi AG (2016) Genetic and pharmacological inhibition of CDK9 drives neutrophil apoptosis to resolve inflammation in zebrafish in vivo. Sci Rep 5:36980CrossRefGoogle Scholar
  84. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assunção JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G, Whitehead S, Kay M, Brown J, Murnane C, Gray E, Humphries M, Sycamore N, Barker D, Saunders D, Wallis J, Babbage A, Hammond S, Mashreghi-Mohammadi M, Barr L, Martin S, Wray P, Ellington A, Matthews N, Ellwood M, Woodmansey R, Clark G, Cooper J, Tromans A, Grafham D, Skuce C, Pandian R, Andrews R, Harrison E, Kimberley A, Garnett J, Fosker N, Hall R, Garner P, Kelly D, Bird C, Palmer S, Gehring I, Berger A, Dooley CM, Ersan-Ürün Z, Eser C, Geiger H, Geisler M, Karotki L, Kirn A, Konantz J, Konantz M, Oberländer M, Rudolph-Geiger S, Teucke M, Lanz C, Raddatz G, Osoegawa K, Zhu B, Rapp A, Widaa S, Langford C, Yang F, Schuster SC, Carter NP, Harrow J, Ning Z, Herrero J, Searle SM, Enright A, Geisler R, Plasterk RH, Lee C, Westerfield M, de Jong PJ, Zon LI, Postlethwait JH, Nüsslein-Volhard C, Hubbard TJ, Roest Crollius H, Rogers J, Stemple DL (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496(7446):498–503CrossRefGoogle Scholar
  85. International Agency for Research on Cancer (IARC) (1997) Monographs on the evaluation of carcinogenic risks to humans, vol 68. Silica, Some Silicates, Coal Dust and Para-Aramid Fibrils, Lyon, FranceGoogle Scholar
  86. Johnston BD, Scown TM, Moger J, Cumberland SA, Baalousha M, Linge K, van Aerle R, Jarvis K, Lead JR, Tyler CR (2010) Bioavailability of nanoscale metal oxides TiO2, CeO2, and ZnO to fish. Environ Sci Technol 44(3):1144–1151CrossRefGoogle Scholar
  87. Jones HR, Robb CT, Perretti M, Rossi AG (2016) The role of neutrophils in inflammation resolution. Semin Immunol 28(2):137–145CrossRefGoogle Scholar
  88. Jovanović B, Anastasova L, Rowe EW, Zhang Y, Clapp AR, Palić D (2011) Effects of nanosized titanium dioxide on innate immune system of fathead minnow (Pimephales promelas Rafinesque, 1820). Ecotoxicol Environ Saf 74(4):675–683CrossRefGoogle Scholar
  89. Kagan VE, Tyurina YY, Tyurin VA, Konduru NV, Potapovich AI, Osipov AN, Kisin ER, Schwegler-Berry D, Mercer R, Castranova V, Shvedova AA (2006) Direct and indirect effects of single walled carbon nanotubes on RAW 264.7 macrophages: role of iron. Toxicol Lett 165(1):88–100CrossRefGoogle Scholar
  90. Kanther M, Sun X, Mühlbauer M, Mackey LC, Flynn EJ 3rd, Bagnat M, Jobin C, Rawls JF (2011) Microbial colonization induces dynamic temporal and spatial patterns of NF-κB activation in the zebrafish digestive tract. Gastroenterology 141(1):197–207CrossRefGoogle Scholar
  91. Kermanizadeh A, Brown DM, Hutchison GR, Stone V (2013a) Engineered nanomaterial impact in the liver following exposure via an intravenous route–the role of polymorphonuclear leukocytes and gene expression in the organ. J Nanomed Nanotechol 4:157Google Scholar
  92. Kermanizadeh A, Pojana G, Gaiser BK, Birkedal R, Bilanicová D, Wallin H, Jensen KA, Sellergren B, Hutchison GR, Marcomini A, Stone V (2013b) In vitro assessment of engineered nanomaterials using a hepatocyte cell line: cytotoxicity, pro-inflammatory cytokines and functional markers. Nanotoxicology 7(3):301–313CrossRefGoogle Scholar
  93. Kermanizadeh A, Vranic S, Boland S, Moreau K, Baeza-Squiban A, Gaiser BK, Andrzejczuk LA, Stone V (2013c) An in vitro assessment of panel of engineered nanomaterials using a human renal cell line: cytotoxicity, pro-inflammatory response, oxidative stress and genotoxicity. BMC Nephrol 14:96CrossRefGoogle Scholar
  94. Kim YH, Boykin E, Stevens T, Lavrich K, Gilmour MI (2014) Comparative lung toxicity of engineered nanomaterials utilizing in vitro, ex vivo and in vivo approaches. J Nanobiotechnology 26(12):47CrossRefGoogle Scholar
  95. Knaapen AM, Güngör N, Schins RP, Borm PJ, Van Schooten FJ (2006) Neutrophils and respiratory tract DNA damage and mutagenesis: a review. Mutagenesis 21(4):225–236CrossRefGoogle Scholar
  96. Kong JS, Min KB, Min JY (2019) Temporary workers’ skipping of meals and eating alone in South Korea: the Korean national health and nutrition examination survey for 2013–2016. Int J Environ Res Public Health 16(13):pii: E2319.  https://doi.org/10.3390/ijerph16132319CrossRefGoogle Scholar
  97. Labib S, Williams A, Yauk CL, Nikota JK, Wallin H, Vogel U, Halappanavar S (2016) Nano-risk science: application of toxicogenomics in an adverse outcome pathway framework for risk assessment of multi-walled carbon nanotubes. Part Fibre Toxicol 13:15CrossRefGoogle Scholar
  98. Landsiedel R, Ma-Hock L, Hofmann T, Wiemann M, Strauss V, Treumann S, Wohlleben W, Gröters S, Wiench K, van Ravenzwaay B (2014a) Application of short-term inhalation studies to assess the inhalation toxicity of nanomaterials. Part Fibre Toxicol 11:16CrossRefGoogle Scholar
  99. Landsiedel R, Sauer UG, Ma-Hock L, Schnekenburger J, Wiemann M (2014b) Pulmonary toxicity of nanomaterials: a critical comparison of published in vitro assays and in vivo inhalation or instillation studies. Nanomedicine (Lond) 9(16):2557–2585CrossRefGoogle Scholar
  100. Lanone S, Rogerieux F, Geys J, Dupont A, Maillot-Marechal E, Boczkowski J, Lacroix G, Hoet P (2009) Comparative toxicity of 24 manufactured nanoparticles in human alveolar epithelial and macrophage cell lines. Part Fibre Toxicol 6:14CrossRefGoogle Scholar
  101. Lee KJ, Nallathamby PD, Browning LM, Osgood CJ, Xu XH (2007) In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano 1(2):133–143CrossRefGoogle Scholar
  102. Lee HM, Shin DM, Song HM, Yuk JM, Lee ZW, Lee SH, Hwang SM, Kim JM, Lee CS, Jo EK (2009) Nanoparticles up-regulate tumor necrosis factor-alpha and CXCL8 via reactive oxygen species and mitogen-activated protein kinase activation. Toxicol Appl Pharmacol 238(2):160–169CrossRefGoogle Scholar
  103. Lee KJ, Browning LM, Nallathamby PD, Desai T, Cherukuri PK, Xu XH (2012) In vivo quantitative study of sized-dependent transport and toxicity of single silver nanoparticles using zebrafish embryos. Chem Res Toxicol 25(5):1029–1046CrossRefGoogle Scholar
  104. Lee O, Green JM, Tyler CR (2015) Transgenic fish systems and their application in ecotoxicology. Crit Rev Toxicol 45:124–141CrossRefGoogle Scholar
  105. Levraud JP, Disson O, Kissa K, Bonne I, Cossart P, Herbomel P, Lecuit M (2009) Real-time observation of listeria monocytogenes-phagocyte interactions in living zebrafish larvae. Infect Immun 77(9):3651–3660CrossRefGoogle Scholar
  106. Li L, Zhang WQ, Yan B, Shi YQ, Wen ZL (2012) Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration. J Biol Chem 287(30):25353–25360CrossRefGoogle Scholar
  107. Lieschke GJ, Currie PD (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8(5):353–367CrossRefGoogle Scholar
  108. Lin A, Loughman JA, Zinselmeyer BH, Miller MJ, Caparon MG (2009) Streptolysin S inhibits neutrophil recruitment during the early stages of Streptococcus pyogenes infection. Infect Immun 77(11):5190–5201CrossRefGoogle Scholar
  109. Lin S, Zhao Y, Xia T, Meng H, Ji Z, Liu R, George S, Xiong S, Wang X, Zhang H, Pokhrel S, Mädler L, Damoiseaux R, Lin S, Nel AE (2011) High content screening in zebrafish speeds up hazard ranking of transition metal oxide nanoparticles. ACS Nano 5(9):7284–7295CrossRefGoogle Scholar
  110. Lin S, Zhao Y, Nel AE, Lin S (2013) Zebrafish: an in vivo model for nano EHS studies. Small 9(9–10):1608–1618CrossRefGoogle Scholar
  111. Liz R, Simard JC, Leonardi LB, Girard D (2015) Silver nanoparticles rapidly induce atypical human neutrophil cell death by a process involving inflammatory caspases and reactive oxygen species and induce neutrophil extracellular traps release upon cell adhesion. Int Immunopharmacol 28(1):616–625CrossRefGoogle Scholar
  112. Loynes CA, Martin JS, Robertson A, Trushell DM, Ingham PW, Whyte MK, Renshaw SA (2010) Pivotal advance: pharmacological manipulation of inflammation resolution during spontaneously resolving tissue neutrophilia in the zebrafish. J Leukoc Biol 87(2):203–212CrossRefGoogle Scholar
  113. Lucas CD, Allen KC, Dorward DA, Hoodless LJ, Melrose LA, Marwick JA, Tucker CS, Haslett C, Duffin R, Rossi AG (2013) Flavones induce neutrophil apoptosis by down-regulation of Mcl-1 via a proteasomal-dependent pathway. FASEB J 27(3):1084–1094CrossRefGoogle Scholar
  114. MacRae CA, Peterson RT (2015) Zebrafish as tools for drug discovery. Nat Rev Drug Discov 14(10):721–731CrossRefGoogle Scholar
  115. Ma-Hock L, Treumann S, Strauss V, Brill S, Luizi F, Mertler M, Wiench K, Gamer AO, van Ravenzwaay B, Landsiedel R (2009) Inhalation toxicity of multiwall carbon nanotubes in rats exposed for 3 months. Toxicol Sci 112(2):468–481CrossRefGoogle Scholar
  116. Marjoram L, Alvers A, Deerhake ME, Bagwell J, Mankiewicz J, Cocchiaro JL, Beerman RW, Willer J, Sumigray KD, Katsanis N, Tobin DM, Rawls JF, Goll MG, Bagnat M (2015) Epigenetic control of intestinal barrier function and inflammation in zebrafish. Proc Natl Acad Sci USA 112(9):2770–2775CrossRefGoogle Scholar
  117. Martin JS, Renshaw SA (2009) Using in vivo zebrafish models to understand the biochemical basis of neutrophilic respiratory disease. Biochem Soc Trans 37(Pt 4):830–837.  https://doi.org/10.1042/BST0370830.ReviewCrossRefGoogle Scholar
  118. Massarsky A, Dupuis L, Taylor J, Eisa-Beygi S, Strek L, Trudeau VL, Moon TW (2013) Assessment of nanosilver toxicity during zebrafish (Danio rerio) development. Chemosphere 92(1):59–66CrossRefGoogle Scholar
  119. Mathias JR, Walters KB, Huttenlocher A (2009) Neutrophil motility in vivo using zebrafish. Methods Mol Biol 571:151–166CrossRefGoogle Scholar
  120. Mathias JR, Saxena MT, Mumm JS (2012) Advances in zebrafish chemical screening technologies. Future Med Chem 4(14):1811–1822CrossRefGoogle Scholar
  121. Mayadas TN, Cullere X, Lowell CA (2014) The multifaceted functions of neutrophils. Annu Rev Pathol 9:181–218CrossRefGoogle Scholar
  122. Maynard AD, Aitken RJ, Butz T, Colvin V, Donaldson K, Oberdörster G, Philbert MA, Ryan J, Seaton A, Stone V, Tinkle SS, Tran L, Walker NJ, Warheit DB (2006) Safe handling of nanotechnology. Nature 444(7117):267–269CrossRefGoogle Scholar
  123. McLeish JA, Chico TJ, Taylor HB, Tucker C, Donaldson K, Brown SB (2010) Skin exposure to micro- and nano-particles can cause haemostasis in zebrafish larvae. Thromb Haemost 103(4):797–807CrossRefGoogle Scholar
  124. McWilliams A (2016) The maturing nanotechnology market: products and applications. BCC Research, Wellesley (Editor)Google Scholar
  125. Meeker ND, Trede NS (2008) Immunology and zebrafish: spawning new models of human disease. Dev Comp Immunol 32(7):745–757CrossRefGoogle Scholar
  126. Meijer AH (2016) Protection and pathology in TB: learning from the zebrafish model. Semin Immunopathol 38(2):261–273CrossRefGoogle Scholar
  127. Merrifield DL, Shaw BJ, Harper GM, Saoud IP, Davies SJ, Handy RD, Henry TB (2013) Ingestion of metal-nanoparticle contaminated food disrupts endogenous microbiota inzebrafish (Danio rerio). Environ Pollut 174:157–163CrossRefGoogle Scholar
  128. Mesens N, Crawford AD, Menke A, Hung PD, Van Goethem F, Nuyts R, Hansen E, Wolterbeek A, Van Gompel J, De Witte P, Esguerra CV (2015) Are zebrafish larvae suitable for assessing the hepatotoxicity potential of drug candidates? J Appl Toxicol 35(9):1017–1029CrossRefGoogle Scholar
  129. Mestas J, Hughes CC (2004) Of mice and not men: differences between mouse and human immunology. J Immunol 172(5):2731–2738CrossRefGoogle Scholar
  130. Mitrano DM, Nowack B (2017) The need for a life-cycle based aging paradigm for nanomaterials: importance of real-world test systems to identify realistic particle transformations. Nanotechnology 28(7):072001.  https://doi.org/10.1088/1361-6528/28/7/072001 (Epub 2017 Jan 11)CrossRefGoogle Scholar
  131. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB (2014) Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 20(7):1126–1167CrossRefGoogle Scholar
  132. Monteiller C, Tran L, MacNee W, Faux S, Jones A, Miller B, Donaldson K (2007) The pro-inflammatory effects of low-toxicity low-solubility particles, nanoparticles and fine particles, on epithelial cells in vitro: the role of surface area. Occup Environ Med 64(9):609–615 (Epub 2007 Apr 4)CrossRefGoogle Scholar
  133. Monteiro-Riviere NA, Inman AO, Wang YY, Nemanich RJ (2005) Surfactant effects on carbon nanotube interactions with human keratinocytes. Nanomedicine. 1(4):293–299CrossRefGoogle Scholar
  134. Mourabit N, Arakrak A, Bakkali M, Laglaoui A (2017) Nasal carriage of sequence type 22 MRSA and livestock-associated ST398 clones in Tangier, Morocco. J Infect Dev Ctries 11(7):536–542.  https://doi.org/10.3855/jidc.9235CrossRefGoogle Scholar
  135. Mugoni V, Camporeale A, Santoro MM (2014) Analysis of oxidative stress in zebrafish embryos. JoVE 89:51328Google Scholar
  136. Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6(3):173–182CrossRefGoogle Scholar
  137. Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311(5761):622–627CrossRefGoogle Scholar
  138. Nguyen KC, Richards L, Massarsky A, Moon TW, Tayabali AF (2016) Toxicological evaluation of representative silver nanoparticles in macrophages and epithelial cells. Toxicol In Vitro 33:163–173CrossRefGoogle Scholar
  139. Nguyen-Chi M, Phan QT, Gonzalez C, Dubremetz J-F, Levraud J-P, Lutfalla G (2014). Transient infection of the zebrafish notochord with E. coli induces chronic inflammation. Dis Model Mech 7(7):871–882CrossRefGoogle Scholar
  140. Niethammer P, Grabher C, Look AT, Mitchison TJ (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459(7249):996–999CrossRefGoogle Scholar
  141. Novoa B, Figueras A (2012) Zebrafish: model for the study of inflammation and the innate immune response to infectious diseases. Adv Exp Med Biol 946:253–275CrossRefGoogle Scholar
  142. Nowack B (2017) Evaluation of environmental exposure models for engineered nanomaterials in a regulatory context. NanoImpact 8:38–47.  https://doi.org/10.1016/j.impact.2017.06.005CrossRefGoogle Scholar
  143. Oberdörster G, Stone V, Donaldson K (2007) Toxicology of nanoparticles: a historical perspective. Nanotoxicology 1:2–25CrossRefGoogle Scholar
  144. Ogawara K, Yoshida M, Furumoto K, Takakura Y, Hashida M, Higaki K, Kimura T (1999) Uptake by hepatocytes and biliary excretion of intravenously administered polystyrene microspheres in rats. J Drug Target 7(3):213–221CrossRefGoogle Scholar
  145. Olsen H, Betton G, Robinson D, Thomas K, Monro A, Kolaja G, Lilly P, Sanders J, Sipes G, Bracken W, Dorato M, Van Deun K, Smith P, Berger B, Heller A (2000) Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul Toxicol Pharmacol 32:56–67CrossRefGoogle Scholar
  146. 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):1315–1324CrossRefGoogle Scholar
  147. Osborne OJ, Lin S, Chang CH, Ji Z, Yu X, Wang X, Lin S, Xia T, Nel AE (2015) Organ-specific and size-dependent Ag nanoparticle toxicity in gills and intestines of adult zebrafish. ACS Nano 9(10):9573–9584CrossRefGoogle Scholar
  148. Osborne OJ, Mukaigasa K, Nakajima H, Stolpe B, Romer I, Philips U, Lynch I, Mourabit S, Hirose S, Lead JR, Kobayashi M, Kudoh T, Tyler CR (2016) Sensory systems and ionocytes are targets for silver nanoparticle effects in fish. Nanotoxicology 10(9):1276–1286CrossRefGoogle Scholar
  149. Park EJ, Park K (2009) Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. Toxicol Lett 184(1):18–25CrossRefGoogle Scholar
  150. Pase L, Layton JE, Wittmann C, Ellett F, Nowell CJ, Reyes-Aldasoro CC, Varma S, Rogers KL, Hall CJ, Keightley MC, Crosier PS, Grabher C, Heath JK, Renshaw SA, Lieschke GJ (2012) Neutrophil-delivered myeloperoxidase dampens the hydrogen peroxide burst after tissue wounding in zebrafish. Curr Biol 22(19):1818–1824CrossRefGoogle Scholar
  151. Pati R, Das I, Mehta RK, Sahu R, Sonawane A (2016) Zinc-Oxide nanoparticles exhibit genotoxic, clastogenic, cytotoxic and actin depolymerization effects by inducing oxidative stress responses in macrophages and adult mice. Toxicol Sci 150(2):454–472CrossRefGoogle Scholar
  152. Poon IK, Lucas CD, Rossi AG, Ravichandran KS (2014) Apoptotic cell clearance: basic biology and therapeutic potential. Nat Rev Immunol 14(3):166–180CrossRefGoogle Scholar
  153. Progatzky F, Cook HT, Lamb JR, Bugeon L, Dallman MJ (2016) Mucosal inflammation at the respiratory interface: a zebrafish model. Am J Physiol Lung Cell Mol Physiol 310(6):L551–L561CrossRefGoogle Scholar
  154. Rauscher H, Rasmussen K, Sokull-Klüttgen B (2017) Regulatory aspects of nanomaterials in the EU. Chem Ing Tec 89:224–231CrossRefGoogle Scholar
  155. Renshaw SA, Loynes CA, Elworthy S, Ingham PW, Whyte MK (2007) Modeling inflammation in the zebrafish: how a fish can help us understand lung disease. Exp Lung Res 33(10):549–554CrossRefGoogle Scholar
  156. Rizzo LY, Golombek SK, Mertens ME, Pan Y, Laaf D, Broda J, Jayapaul J, Möckel D, Subr V, Hennink WE, Storm G, Simon U, Jahnen-Dechent W, Kiessling F, Lammers T (2013) In vivo nanotoxicity testing using the zebrafish embryo assay. J Mater Chem B Mater Biol Med.  https://doi.org/10.1039/C3TB20528BCrossRefGoogle Scholar
  157. Robb CT, Regan KH, Dorward DA, Rossi AG (2016) Key mechanisms governing resolution of lung inflammation. Semin Immunopathol 38(4):425–448CrossRefGoogle Scholar
  158. Roberts DJ (2013) Nuts and bolts of transfusion medicine: the supply of blood and quality of the products. Transfus Med 23(5):299–301.  https://doi.org/10.1111/tme.12080CrossRefGoogle Scholar
  159. Robertson AL, Ogryzko NV, Henry KM, Loynes CA, Foulkes MJ, Meloni MM, Wang X, Ford C, Jackson M, Ingham PW, Wilson HL, Farrow SN, Solari R, Flower RJ, Jones S, Whyte MK, Renshaw SA (2016) Identification of benzopyrone as a common structural feature in compounds with anti-inflammatory activity in a zebrafish phenotypic screen. Dis Model Mech 9(6):621–632CrossRefGoogle Scholar
  160. Rombough P (2002) Gills are needed for ionoregulation before they are needed for O(2) uptake in developing zebrafish Danio rerio. J Exp Biol 205(Pt 12):1787–1794Google Scholar
  161. Rovida C, Hartung T (2009) Re-evaluation of animal numbers and costs for in vivo tests to accomplish REACH legislation requirements for chemicals—a report by the transatlantic think tank for toxicology. Altex 26(3):187–208CrossRefGoogle Scholar
  162. Rushton EK, Jiang J, Leonard SS, Eberly S, Castranova V, Biswas P, Elder A, Han X, Gelein R, Finkelstein J, Oberdörster G (2010) Concept of assessing nanoparticle hazards considering nanoparticle dosemetric and chemical/biological response metrics. J Toxicol Environ Health A. 73(5):445–461CrossRefGoogle Scholar
  163. Russell WMS, Burch RL (1959) The principles of humane experimental technique. Universities Federation for Animal Welfare, Wheathampstead (UK). (as reprinted 1992)Google Scholar
  164. Sadauskas E, Wallin H, Stoltenberg M, Vogel U, Doering P, Larsen A, Danscher G (2007) Kupffer cells are central in the removal of nanoparticles from the organism. Part Fibre Toxicol 19(4):10CrossRefGoogle Scholar
  165. Sayes CM, Reed KL, Warheit DB (2007) Assessing toxicity of fine and nanoparticles: comparing in vitro measurements to invivo pulmonary toxicity profiles. Toxicol Sci 97(1):163–180CrossRefGoogle Scholar
  166. Scherbart AM, Langer J, Bushmelev A, van Berlo D, Haberzettl P, van Schooten FJ, Schmidt AM, Rose CR, Schins RP, Albrecht C (2011) Contrasting macrophage activation by fine and ultrafine titanium dioxide particles is associated with different uptake mechanisms. Part Fibre Toxicol 8:31CrossRefGoogle Scholar
  167. Schmidt K (2007) NanoFrontiers: visions for the future of nanotechnology. The Project on Emerging Nanotechnologies, Woodrow Wilson International Center for Scholars, Washington, DC. http://www.nanotechproject.org/process/assets/files/2704/181_pen6_nanofrontiers.pdf
  168. Schmidt CW (2009) Nanotechnology-related environment, health, and safety research examining the national strategy. Environ Health Persp 117:A158–A161Google Scholar
  169. Selck H, Handy RD, Fernandes TF, Klaine SJ, Petersen EJ (2016) Nanomaterials in the aquatic environment: a European Union-United States perspective on the status of ecotoxicity testing, research priorities, and challenges ahead. Environ Toxicol Chem 35(5):1055–1067CrossRefGoogle Scholar
  170. Semmler-Behnke M, Takenaka S, Fertsch S, Wenk A, Seitz J, Mayer P, Oberdörster G, Kreyling WG (2007) Efficient elimination of inhaled nanoparticles from the alveolar region: evidence for interstitial uptake and subsequent reentrainment onto airways epithelium. Environ Health Perspect 115(5):728–733 (Epub 2007 Feb 6)CrossRefGoogle Scholar
  171. Semmler-Behnke M, Kreyling WG, Lipka J, Fertsch S, Wenk A, Takenaka S, Schmid G, Brandau W. (2008) Biodistribution of 1.4- and 18-nm gold particles in rats. Small 4(12):2108–2111.  https://doi.org/10.1002/smll.200800922CrossRefGoogle Scholar
  172. Shi M, Kwon HS, Peng Z, Elder A, Yang H (2012) Effects of surface chemistry on the generation of reactive oxygen species by coppernanoparticles. ACS Nano 6(3):2157–2164CrossRefGoogle Scholar
  173. Shiau CE, Kaufman Z, Meireles AM, Talbot WS (2015) Differential requirement for irf8 in formation of embryonic and adult macrophages in zebrafish. PLoS ONE 10(1):e0117513CrossRefGoogle Scholar
  174. Sipes NS, Padilla S, Knudsen TB (2011) Zebrafish: as an integrative model for twenty-first century toxicity testing. Birth Defects Res C Embryo Today 93:256–267CrossRefGoogle Scholar
  175. Soares T, Ribeiro D, Proença C, Chisté RC, Fernandes E, Freitas M (2016) Size-dependent cytotoxicity of silver nanoparticles in human neutrophils assessed by multiple analytical approaches. Life Sci 145:247–254CrossRefGoogle Scholar
  176. Soehnlein O, Steffens S, Hidalgo A, Weber C (2017) Neutrophils as protagonists and targets in chronic inflammation. Nat Rev Immunol 17(4):248–261CrossRefGoogle Scholar
  177. Stone JA, Stejskal A, Howard L (1999) Absolute interferometry with a 670-nm external cavity diode laser. Appl Opt 38(28):5981–5994CrossRefGoogle Scholar
  178. Stone V, Tuinman M, Vamvakopoulos JE, Shaw J, Brown D, Petterson S, Faux SP, Borm P, MacNee W, Michaelangeli F, Donaldson K (2000) Increased calcium influx in a monocytic cell line on exposure to ultrafine carbon black. Eur Respir J 15(2):297–303CrossRefGoogle Scholar
  179. Stone V, Miller MR, Clift MJ, Elder A, Mills NL, Møller P, Schins RP, Vogel U, Kreyling WG, Jensen KA, Kuhlbusch TA, Schwarze PE, Hoet P, Pietroiusti A, De Vizcaya-Ruiz A, Baeza-Squiban A, Tran CL, Cassee FR (2016) Nanomaterials vs Ambient Ultrafine Particles: an opportunity to exchange toxicology knowledge. Environ Health Perspect. (Epub ahead of print)Google Scholar
  180. Strähle U, Scholz S, Geisler R, Greiner P, Hollert H, Rastegar S, Schumacher A, Selderslaghs I, Weiss C, Witters H, Braunbeck T (2012) Zebrafish embryos as an alternative to animal experiments—a commentary on the definition of the onset of protected life stages in animal welfare regulations. Reprod Toxicol 33(2):128–132CrossRefGoogle Scholar
  181. Streng A, Goettler D, Haerlein M, Lehmann L, Ulrich K, Prifert C, Krempl C, Weißbrich B, Liese JG (2019) Spread and clinical severity of respiratory syncytial virus a genotype ON1 in Germany, 2011–2017. BMC Infect Dis 19(1):613.  https://doi.org/10.1186/s12879-019-4266-yCrossRefGoogle Scholar
  182. Sukardi H, Chng HT, Chan EC, Gong Z, Lam SH (2011) Zebrafish for drug toxicity screening: bridging the in vitro cell-based models and in vivo mammalian models. Expert Opin Drug Metab Toxicol 7(5):579–89.  https://doi.org/10.1517/17425255.2011.562197 (Epub 2011 Feb 23. Review)CrossRefGoogle Scholar
  183. Susewind J, de Souza Carvalho-Wodarz C, Repnik U, Collnot EM, Schneider-Daum N, Griffiths GW, Lehr CM (2016) A 3D co-culture of three human cell lines to model the inflamed intestinal mucosa for safety testing of nanomaterials. Nanotoxicology 10(1):53–62Google Scholar
  184. Teeguarden JG, Mikheev VB, Minard KR, Forsythe WC, Wang W, Sharma G, Karin N, Tilton SC, Waters KM, Asgharian B, Price OR, Pounds JG, Thrall BD (2014) Comparative iron oxide nanoparticle cellular dosimetry and response in mice by the inhalation and liquid cell culture exposure routes. Part Fibre Toxicol 2014(11):46CrossRefGoogle Scholar
  185. Tian QE, Li HD, Yan M, Cai HL, Tan QY, Zhang WY (2012) Astragalus polysaccharides can regulate cytokine and P-glycoprotein expression in H22 tumor-bearing mice. World J Gastroenterol 18(47):7079–7086.  https://doi.org/10.3748/wjg.v18.i47.7079CrossRefGoogle Scholar
  186. Törnqvist E, Annas A, Granath B, Jalkesten E, Cotgreave I, Öberg M (2014) Strategic focus on 3R principles reveals major reductions in the use of animals in pharmaceutical toxicity testing. PLoS ONE 9(7):e101638CrossRefGoogle Scholar
  187. Torraca V, Masud S, Spaink HP, Meijer AH (2014) Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model. Dis Model Mech. 7(7):785–797CrossRefGoogle Scholar
  188. Traver D, Herbomel P, Patton EE, Murphey RD, Yoder JA, Litman GW, Catic A, Amemiya CT, Zon LI, Trede NS (2003) The zebrafish as a model organism to study development of the immune system. Adv Immunol 81:253–330Google Scholar
  189. Trede NS, Langenau DM, Traver D, Look AT, Zon LI (2004) The use of zebrafish to understand immunity. Immunity 20(4):367–379CrossRefGoogle Scholar
  190. Tuomela S, Autio R, Buerki-Thurnherr T, Arslan O, Kunzmann A, Andersson-Willman B, Wick P, Mathur S, Scheynius A, Krug HF, Fadeel B, Lahesmaa R (2013) Gene expression profiling of immune-competent human cells exposed to engineered zinc oxide or titanium dioxide nanoparticles. PLoS ONE 8(7):e68415CrossRefGoogle Scholar
  191. Usenko CY, Harper SL, Tanguay RL (2008) Fullerene C60 exposure elicits an oxidative stress response in embryonic zebrafish. Toxicol Appl Pharmacol 229(1):44–55CrossRefGoogle Scholar
  192. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1):44–84CrossRefGoogle Scholar
  193. van Aerle R, Lange A, Moorhouse A, Paszkiewicz K, Ball K, Johnston BD, de-Bastos E, de-Bastos E, Tyler CR, Santos EM (2013) Molecular mechanisms of toxicity of silver nanoparticles in zebrafish embryos. Environ Sci Technol 47(14):8005–8014CrossRefGoogle Scholar
  194. Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D, Hull MS (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer productsinventory. J Nanotechnol 6:1769–1780Google Scholar
  195. Vojtech LN, Sanders GE, Conway C, Ostland V, Hansen JD (2009) Host immune response and acute disease in a zebrafish model of Francisella pathogenesis. Infect Immun 77(2):914–925CrossRefGoogle Scholar
  196. Wagner JC, Sleggs CA, Marcgand P (1960) Diffuse pleural mesothelioma and asbestos exposure in the North Western Cape Province. Br J Ind Med 17:260–271Google Scholar
  197. Walker SL, Ariga J, Mathias JR, Coothankandaswamy V, Xie X, Distel M, Köster RW, Parsons MJ, Bhalla KN, Saxena MT, Mumm JS (2012) automated reporter quantification in vivo: high-throughput screening method for reporter-based assays in zebrafish. PLoS ONE 7(1):e29916CrossRefGoogle Scholar
  198. Wang J, Arase H (2014) Regulation of immune responses by neutrophils. Ann NY Acad Sci 1319:66–81CrossRefGoogle Scholar
  199. Warheit DB, Sayes CM, Reed KL (2009) Nanoscale and fine zinc oxide particles: can in vitro assays accurately forecast lung hazards following inhalation exposures? Environ Sci Technol 43(20):7939–7945CrossRefGoogle Scholar
  200. White RM, Sessa A, Burke C, Bowman T, LeBlanc J, Ceol C, Bourque C, Dovey M, Goessling W, Burns CE, Zon LI (2008) Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2(2):183–189CrossRefGoogle Scholar
  201. Wiemann M, Vennemann A, Sauer UG, Wiench K, Ma-Hock L, Landsiedel R (2016) An in vitro alveolar macrophage assay for predicting the short-term inhalation toxicity of nanomaterials. J Nanobiotechnology 14:16CrossRefGoogle Scholar
  202. Wilson MR, Lightbody JH, Donaldson K, Sales J, Stone V (2002) Interactions between ultrafine particles and transition metals in vivo and in vitro. Toxicol Appl Pharmacol 184(3):172–179CrossRefGoogle Scholar
  203. Wilson MR, Foucaud L, Barlow PG, Hutchison GR, Sales J, Simpson RJ, Stone V (2007) Nanoparticle interactions with zinc and iron: implications for toxicology and inflammation. Toxicol Appl Pharmacol 225(1):80–89CrossRefGoogle Scholar
  204. Witasp E, Shvedova AA, Kagan VE, Fadeel B (2009) Single-walled carbon nanotubes impair human macrophage engulfment of apoptotic cell corpses. Inhal Toxicol 21(Suppl 1):131–136CrossRefGoogle Scholar
  205. Xiong D, Fang T, Yu L, Sima X, Zhu W (2011) Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 409(8):1444–1452CrossRefGoogle Scholar
  206. Xu H, Dong X, Zhang Z, Yang M, Wu X, Liu H, Lao Q, Li C (2015) Assessment of immunotoxicity of dibutyl phthalate using live zebrafish embryos. Fish Shellfish Immunol 45(2):286–292CrossRefGoogle Scholar
  207. Yang L, Watts DJ (2005) Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicol Lett 158:122–132.  https://doi.org/10.1016/j.toxlet.2005.03.003CrossRefGoogle Scholar
  208. Zhang Y, Zhu L, Zhou Y, Chen J (2015) Accumulation and elimination of iron oxide nanomaterials in zebrafish (Danio rerio) upon chronic aqueous exposure. J Environ Sci (China) 30:223–230CrossRefGoogle Scholar
  209. Zhao X, Wang S, Wu Y, You H, Lv L (2013) Acute ZnO nanoparticles exposure induces developmental toxicity, oxidative stress and DNA damage in embryo-larval zebrafish. Aquat Toxicol 136–137:49–59CrossRefGoogle Scholar
  210. Zhu X, Tian S, Cai Z (2012) Toxicity assessment of iron oxide nanoparticles in zebrafish (Danio rerio) early life stages. PLoS ONE 7(9):e46286CrossRefGoogle Scholar
  211. Zon LI, Peterson RT (2005) In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 4(1):35–44CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Physical Chemistry and Nanoscience, Department of Chemistry, Faculty of ScienceAl Baha UniversityBaljurashiSaudi Arabia

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