Responses of oxidative stress, genotoxicity and immunotoxicity as biomarkers in Theba pisana snails dietary exposed to silver nanoparticles

References

• Chaloupka K, Malam Y, Seifalian AM. Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol. 2010;28:580–588.
   PubMed Web of Science ®Google Scholar
• Hardman R. Toxicologic review of quantum dots: toxicity depends on physicochemical and environmental factors. Environ Health Perspect. 2006;114:165–172.
   PubMed Web of Science ®Google Scholar
• Yu S, Liu J. Introduction. In: Liu J, Jiang G, editors. Silver nanoparticles in the environment. Berlin: Springer-Verlag; 2015. p. 1–8. Chapter 1.
   Google Scholar
• Klaine SJ, Alvarez PJJ, Batley GE, et al. Nanomaterials in the environment: Behavior, fate, bioavailability, and effects. Environ Toxicol Chem. 2008;27:1825–1851.
   PubMed Web of Science ®Google Scholar
• Wang P, Menzies NW, Dennis PG, et al. Silver nanoparticles entering soils via the wastewater–sludge–soil pathway pose low risk to plants but elevated Cl concentrations increase Ag bioavailability. Environ. Sci. Technol. 2016;50:8274–8281.
   PubMed Web of Science ®Google Scholar
• Oberdörster G, Oberdörster E, Oberdörster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect. 2005;113:823–839.
   PubMed Web of Science ®Google Scholar
• Lapresta-Fernández A, Fernández A, Blasco J. Nanoecotoxicity effects of engineered silver and gold nanoparticles in aquatic organisms. TrAC, Trends Anal Chem. 2012;32:40–59.
   Web of Science ®Google Scholar
• Garcia-Velasco N, Pena-Cearra A, Bilbao E, et al. Integrative assessment of the effects produced by Ag nanoparticles at different levels of biological complexity in Eisenia fetida maintained in two standard soils (OECD and LUFA 2.3). Chemosphere. 2017;181:747–758.
   PubMed Web of Science ®Google Scholar
• Galloway TS, Sanger RC, Smith KL, et al. Rapid assessment of marine pollution using multiple biomarkers and chemical immunoassays. Environ Sci Technol. 2002;36:2219–2226.
   PubMed Web of Science ®Google Scholar
• Crane M, Handy RD, Garrod J, et al. Ecotoxicity test methods and environmental hazard assessment for engineered nanoparticles. Ecotoxicology. 2008;17:421–437.
   PubMed Web of Science ®Google Scholar
• Galloway TS, Depledge MH. Immunotoxicity in invertebrates: measurement and ecotoxicological relevance. Ecotoxicology. 2001;10:5–23.
   PubMed Web of Science ®Google Scholar
• Wessel N, Rousseau S, Caisey X, et al. Investigating the relationship between embryotoxic and genotoxic effects of benzo[a]pyrene, 17 alpha-ethinylestradiol and endosulfan on Crassostrea gigas embryos. Aqua Toxicol. 2007;85:133–142.
   PubMed Web of Science ®Google Scholar
• Bologenesi C, Hayashi M. Micronucleus assay in aquatic animals. Mutagenesis. 2011;26:205–213.
   PubMed Web of Science ®Google Scholar
• Marins AT, Rodrigues CR, Real CC, et al. Integrated biomarkers response confirms the antioxidant role of diphenyl diselenide against atrazine. Ecotoxicol Environ Saf. 2018;151:192–198.
   Web of Science ®Google Scholar
• Cattaneo R, Moraes BS, Loro VL, et al. Tissue biochemical alterations of Cyprinus carpio exposed to commercial herbicide containing Clomazone under rice-field conditions. Arch Environ Contam Toxicol. 2012;62:97–106.
   PubMed Web of Science ®Google Scholar
• Canty MN, Hagger JA, Moore RTB, et al. Sublethal impact of short term exposure to the organophosphate pesticide azamethiphos in the marine mollusc Mytilus edulis. Mar Poll Bull. 2007;54:396–402.
   PubMed Web of Science ®Google Scholar
• De Vaufleury A, Coeurdassier M, Pandard P, et al. How terrestrial snails can be used in risk assessment of soils. Environ Toxicol Chem. 2006;25:797–806.
   PubMed Web of Science ®Google Scholar
• Radwan MA, El-Gendy KS, Gad AF. Biomarkers of oxidative stress in the land snail, Theba pisana for assessing ecotoxicological effects of urban metal pollution. Chemosphere. 2010;79:40–46.
   PubMed Web of Science ®Google Scholar
• Notten MJ, Oosthoek AJ, Rozema J, et al. Heavy metal concentrations in a soil-plant-snail food chain along a terrestrial soil pollution gradient. Environ Pollut. 2005;138:178–190.
   PubMed Web of Science ®Google Scholar
• Sidiropoulou E, Feidantsis K, Kalogiannis S, et al. Insights into the toxicity of iron oxides nanoparticles in land snails. Comp Biochem Physiol C. 2018;206-207:1–10.
   PubMed Web of Science ®Google Scholar
• Dwivedi AD, Gopal K. Biosynthesis of silver and gold nanoparticles using Chenopodium album leaf extract. Colloids Surf A. 2010;369:27–30.
   Web of Science ®Google Scholar
• Dubey SP, Lahtinen M, Sillanpaa M. Tansy fruit mediated greener synthesis of silver and gold nanoparticles. Proc Biochem. 2010;45:1065–1071.
   Web of Science ®Google Scholar
• El-Gendy KS, Radwan MA, Gad AF. Feeding and growth responses of the snail Theba pisana to dietary metal exposure. Arch Environ Contam Toxicol. 2011;60:272–280.
   PubMed Web of Science ®Google Scholar
• Nair V, Turner GE. The thiobarbituric acid test for lipid peroxidation: structure of the adduct with malondialdehyde. Lipids. 1984;19:804–805.
   Web of Science ®Google Scholar
• Owens WI, Belcher RV. A colorimetric micro-method for the determination of glutathione. Biochem J. 1965;94:705–711.
   PubMed Web of Science ®Google Scholar
• Beers RF J, Sizer IW. Spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952;195:133–140.
   PubMed Web of Science ®Google Scholar
• Vessey DA, Boyer TD. Differential activation and inhibition of different forms of rat liver glutathione S-transferase by the herbicides 2,4-dichloro phenoxy acetate (2,4-D) and 2,4,S trichloro phenoxy acetate (2,4, S-T). Toxicol Appl Pharmacol. 1984;73:492–499.
   PubMed Web of Science ®Google Scholar
• Villela IV, Oliveira IM, Silva J, et al. DNA damage and repair in haemolymph cells of golden mussel (Limnoperna fortune) exposed to environmental contaminants. Mutat Res. 2006;697:78–86.
   Web of Science ®Google Scholar
• Uliasz TF, Hewett SJ. A microtiter trypan blue absorbance assay for quantitative determination of excitoxic neuronal injury in cell culture. J Neurosci Methods. 2000;100:157–163.
   PubMed Web of Science ®Google Scholar
• Pipe RK, Coles JA, Farley SR. Assays for measuring immune response in the mussel Mytilus edulis. Tech Fish Immunol. 1995;4:93–100.
   Google Scholar
• Pipe RK, Coles JA, Carissan FMM, et al. Copper induced immunomodulation in the marine mussel Mytilus edulis. Aqua Toxicol. 1999;46:43–54.
   Web of Science ®Google Scholar
• Ratcliffe NA, Nigam Y, Mello CB, et al. Trypanosoma cruzi erythrocyte agglutinins: a comparative study of occurrence and properties in the gut and hemolymph of Rhodnius prolixus. Exp Parasitol. 1996;83:83–93.
   PubMed Web of Science ®Google Scholar
• Dyrynda EA, Pipe RK, Burt GR, et al. Modulations in the immune defences of mussels (Mytilus edulis) from contaminated sites in the UK. Aquat Toxicol. 1998;42:169–185.
   Web of Science ®Google Scholar
• Ashida M, Ohnishi E. Activation of pre-phenol oxidase in hemolymph of the silkworm. Archive Biochem Biophys. 1967; 122: 411–416.
   PubMed Web of Science ®Google Scholar
• Chance B, Maehly AC. Assay of catalases and peroxidases. Methods Enzymol. 1955;2:773–775.
   Web of Science ®Google Scholar
• Rahmankulova K. Kliniceskaja biohimija, Belarus kn. Minsks. 1976;7:218.
   Google Scholar
• Lowry OH, Rasebrough NJ, Farr AL, et al. Protein measurement with the folin phenol reagent. J Biol Chem. 1951;193:265–275.
   PubMed Web of Science ®Google Scholar
• CoStat program. Microcomputer program analysis, CoHort software, Version 2.6. Monterey, CA; 2002.
   Google Scholar
• Philip D. Green synthesis of gold and silver nanoparticles using Hibiscus rosa sinensis. Physica E. 2010;42:1417–1424.
   Google Scholar
• Maiti S, Krishnan D, Barman G, et al. Antimicrobial activities of silver nanoparticles synthesized from Lycopersicon esculentum extract. J Anal Sci Technol. 2014;5(40).doi.org/10.1186/s40543-014-0040-3
   Google Scholar
• Goudarzi M, Mir N, Mousavi-Kamazani M, et al. Biosynthesis and characterization of silver nanoparticles prepared from two novel natural precursors by facile thermal decomposition methods. Sci Rep. 2016;6(32539) doi: 10.1038/srep32539
   PubMed Web of Science ®Google Scholar
• Jeeva K, Thiyagarajan M, Elangovan V, et al. Caesalpinia coriaria leaf extracts mediated biosynthesis of metallic silver nanoparticles and their antibacterial activity against clinically isolated pathogens. Ind Crops Prod. 2014;52:714–720.
   Web of Science ®Google Scholar
• McCarthy JF, Shugart LR. Biological markers of environmental contamination. In: McCarthy JF, Shugart LR, editors. Biomarkers of environmental contamination. Boca Raton: Lewis Publishers; 1990. p. 3–16.
   Google Scholar
• Khalil AM. Physiological and genotoxic responses of the earthworm Aporrectodea caliginosa exposed to sublethal concentrations of AgNPs. J Basic Appl Zool. 2016;74:8–15.
   Google Scholar
• Yang X, Gondikas AP, Marinakos SM, et al. Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans. Environ Sci Technol. 2011;46:1119–1127.
   PubMed Web of Science ®Google Scholar
• Ringwood AH, Hameedi MJ, Lee RF, et al. Bivalve biomarker workshop: overview and discussion summaries. Biomarkers. 1999;4:391–399.
   PubMed Web of Science ®Google Scholar
• Ali D, Yadav PG, Kumar S, et al. Sensitivity of freshwater pulmonate snail Lymnaea luteola L., to silver nanoparticles. Chemosphere. 2014;104:134–140.
   PubMed Web of Science ®Google Scholar
• Gagné F, Auclair J, Turcotte P, et al. Sublethal effects of silver nanoparticles and dissolved silver in freshwater mussels. J Toxicol Environ Health A. 2013;76:479–490.
   PubMed Web of Science ®Google Scholar
• DeLeve LD, Kaplowitz N. Glutathione metabolism and its role in hepatotoxicity. Pharmacol Therap. 1991;52:287–305.
   PubMed Web of Science ®Google Scholar
• Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. Vol. 4. Oxford: Clarendon; 2007.
   Google Scholar
• Pen'a-Llopis S, Ferrando MD, Pena JB. Impaired glutathione redox status is associated with decreased survival in two organophosphate-poisoned marine bivalves. Chemosphere. 2002;47:485–497.
   PubMed Web of Science ®Google Scholar
• Canesi L, Fabbri R, Gallo G, et al. Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles (nano carbon black, C60 fullerene, nano-TiO2, nano-SiO2). Aquat Toxicol. 2010;100:168–177.
   PubMed Web of Science ®Google Scholar
• Ali D. Oxidative stress-mediated apoptosis and genotoxicity induced by silver nanoparticles in freshwater snail Lymnaea luteola L. Biol Trace Elem Res. 2014;162:333–341.
   PubMed Web of Science ®Google Scholar
• McCarthy MP, Carroll DL, Ringwood AH. Tissue specific responses of oysters, Crassostrea virginica to silver nanoparticles. Aquat Toxicol. 2013;138–139:123–128.
   PubMed Web of Science ®Google Scholar
• Gomes T, Pereira CG, Cardoso C, et al. Effects of silver nanoparticles exposure in the mussel Mytilus galloprovincialis. Mar Environ Res. 2014;101:208–214.
   PubMed Web of Science ®Google Scholar
• Mouneyrac C, Buffet PE, Poirier L, et al. Fate and effects of metal-based nanoparticles in two marine invertebrates, the bivalve mollusc Scrobicularia plana and the annelid polychaete Hediste diversicolor. Environ Sci Pollut Res. 2014;21:7899–7912.
   PubMed Web of Science ®Google Scholar
• Buffet PE, Zalouk-Vergnoux A, Châtel A, et al. A marine mesocosm study on the environmental fate of silver nanoparticles and toxicity effects on two endobenthic species: the ragworm Hediste diversicolor and the bivalve mollusc Scrobicularia plana. Sci Total Environ. 2014;470–471:1151–1159.
   PubMed Web of Science ®Google Scholar
• Fourie F, Reinecke SA, Reinecke AJ. The determination of earthworm species sensitivity differences to cadmium genotoxicity using the comet assay. Ecotoxicol Environ Saf. 2007;67:361–368.
   PubMed Web of Science ®Google Scholar
• Chakraborty S, Ray M, Ray S. Toxicity of sodium arsenite in the gill of an economically important mollusc of India. Fish Shellfish Immunol. 2010;29:136–148.
   PubMed Web of Science ®Google Scholar
• Gomes T, Araújo O, Pereira R, et al. Genotoxicity of copper oxide and silver nanoparticles in the mussel Mytilus galloprovincialis. Mar Environ Res. 2013;84:51–59.
   PubMed Web of Science ®Google Scholar
• Munari M, Sturve J, Frenzilli G, et al. Genotoxic effects of Ag2S and CdS nanoparticles in blue mussel (Mytilus edulis) haemocytes. Chem Ecol. 2014;30:719–725. doi: 10.1080/02757540.2014.894989
   Web of Science ®Google Scholar
• Calisi A, Lionetto MG, Giordano ME, et al. Morphometric alterations in Mytilus galloprovincialis granulocytes: a new biomarker. J Environ Toxicol Chem. 2008;27:1435–1441.
   PubMed Web of Science ®Google Scholar
• Matozzo V, Gagné F. Immunotoxicology approaches in ecotoxicology: lessons from mollusks. In: Ballarin L, Cammarata M, editors. Lessons in immunity: from single-cell organisms to mammals. 1st ed. Elsevier, Amsterdam: Academic Press; 2016. p. 29–51. Chapter 3.
   Google Scholar
• Hayashi Y, Heckmann LH, Simonsen V, et al. Time-course profiling of molecular stress responses to silver nanoparticles in the earthworm Eisenia fetida. Ecotoxicol Environ Saf. 2013;98:219–226.
   PubMed Web of Science ®Google Scholar
• Aits S, Jaattela M. Lysosomal cell death at a glance. J Cell Sci. 2013;126:1905–1912.
   PubMed Web of Science ®Google Scholar
• Black MC, Ferrell JR, Horning RC, et al. DNA strand breakage in freshwater mussels (Anodonta grandis) exposed to lead in the laboratory and field. J Environ Toxicol Chem. 1996;15:802–808.
   Web of Science ®Google Scholar
• Brousseau P, Pellerin J, Morin Y, et al. Flow cytometry as a tool to demonstrate the disturbance of phagocytosis in the clam Mya arenaria following in vitro exposure to heavy metals. Toxicology. 2000;142:145–156.
   PubMed Web of Science ®Google Scholar
• Pipe RK, Coles JA. Environmental contaminants influencing immune function in marine bivalve molluscs. Fish Shellfish Immunol. 1995;5:581–595.
   Web of Science ®Google Scholar
• Barmo C, Ciacci C, Canonico B, et al. In vivo effects of n-TiO2 on digestive gland and immune function of the marine bivalve Mytilus galloprovincialis. Aqua Toxicol. 2013;132–133:9–18.
   PubMed Web of Science ®Google Scholar
• Katsumiti A, Gilliland D, Arostegui I, et al. Mechanisms of toxicity of Ag nanoparticles in comparison to bulk and ionic Ag on mussel hemocytes and gill cells. PLoS One. 2015;10:1–30.
   Web of Science ®Google Scholar
• Regoli F. Lysosomal responses as a sensitive stress index in biomonitoring heavy metal pollution. Mar Ecol Prog Ser. 1992;84:63–69.
   Web of Science ®Google Scholar
• Cajaraville MP, Robledo Y, Etxeberria M, et al. Cellular biomarkers as useful tools in the biological monitoring of environmental pollution: molluscan digestive lysosomes. In: Cajaraville MP, editor. Cell biology in environmental Toxicology. Bilbo: University of the Basque Country Press Service; 1995. p. 29–55.
   Google Scholar
• Marigómez I, Soto M, Cajaraville MP, et al. Cellular and subcellular distribution of metals in molluscs. Microscope Res Technol. 2002;56:358–392.
   PubMed Web of Science ®Google Scholar
• Regoli F, Nigro M, Orlando E. Lysosomal and antioxidant responses to metals in the Antarctic scallops Adamussium colbecki. Aqua Toxicol. 1998;40:375–392.
   Web of Science ®Google Scholar
• Russo J, Lefeuvre-Orfila L, Lagadic L. Hemocyte-specific responses to the peroxidizing herbicide fomesafen in the pond snail Lymnaea stagnalis (Gastropoda. Pulmonata). Environ Pollut. 2007;146:420–427.
   PubMed Web of Science ®Google Scholar
• Tedesco S, Doyle H, Blasco J, et al. Oxidative stress and toxicity of gold nanoparticles in Mytilus edulis. Aquat Toxicol. 2010;100:178–186.
   PubMed Web of Science ®Google Scholar
• Auguste M, Ciacci C, Balbi T, et al. Effects of nanosilver on Mytilus galloprovincialis hemocytes and early embryo development. Aquat Toxicol. 2018;203:107–116.
   PubMed Web of Science ®Google Scholar
• Russo J, Madec L, Brehélin M. Effect of a toxicant on phagocytosis pathways in the freshwater snail Lymnaea stagnalis. Cell Tissue Res. 2008;333:147–158.
   PubMed Web of Science ®Google Scholar
• Rodriguez J, Le Moullac G. State of the art of immunological tools and health control of penaeid shrimp. Aquaculture. 2000;191:109–119.
   Web of Science ®Google Scholar
• Völker C, Kämpken I, Boedicker C, et al. Toxicity of silver nanoparticles and ionic silver: comparison of adverse effects and potential toxicity mechanisms in the freshwater clam Sphaerium corneum. Nanotoxicology. 2015;9:677–685.
   PubMed Web of Science ®Google Scholar
• Cheng W, Wang LU, Chen JC. Effect of water temperature on the immune response of white shrimp Litopenaeus vannamei to Vibrio alginolyticus. Aquaculture. 2005;250:592–601.
   Web of Science ®Google Scholar
• Lowe DM, Fossato VU. The influence of environmental contaminants on lysosomal activity in the digestive cells of mussels (Mytilus edulis) from the Venice Lagoon. Aquat Toxicol. 2000;48:75–85.
   PubMed Web of Science ®Google Scholar
• Suresh K, Mohandas A. Hemolymph acid phosphatase activity pattern in copper-stressed bivalves. J Invert Pathol. 1990;55:118–125.
   Web of Science ®Google Scholar
• Ciacci C, Canonico B, Bilanicov A, et al. Immunomodulation by different types of N-oxides in the hemocytes of the marine bivalve Mytilus galloprovincialis. PLoS One. 2012;7(5):e36937.
   PubMed Web of Science ®Google Scholar
• Burmester T. Evolutionary history and diversity of arthropod hemocyanins. Micron. 2004;35(1–2):121–122.
   PubMed Web of Science ®Google Scholar
• Bislimi K, Behluli A, Halili J, et al. Impact of pollution from Kosova’s power plant in obiliq on some biochemical parameters of the local population of garden snail (Helix pomatia L.). Resour Environ. 2013;3:15–19.
   Google Scholar