Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-25T03:42:56.128Z Has data issue: false hasContentIssue false

Liver Alterations in Two Freshwater Fish Species (Carassius auratus and Danio rerio) Following Exposure to Different TiO2 Nanoparticle Concentrations

Published online by Cambridge University Press:  09 August 2013

Mário S. Diniz*
Affiliation:
REQUIMTE, Departamento de Química, Faculdade de Ciências e Tecnologia, Centro de Química Fina e Biotecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal
António P. Alves de Matos
Affiliation:
Anatomia Patológica, Centro Hospitalar de Lisboa Central-HCC, Rua da Beneficência 8, 1069-166 Lisboa, Portugal; Centro de Estudos do Ambiente e do Mar (CESAM/FCUL)-Faculdade de Ciências da Universidade de Lisboa and Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Quinta da Granja, Monte de Caparica, 2829-511 Caparica, Portugal
Joana Lourenço
Affiliation:
REQUIMTE, Departamento de Química, Faculdade de Ciências e Tecnologia, Centro de Química Fina e Biotecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal
Luísa Castro
Affiliation:
IMAR-Instituto do Mar, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa – Departamento de Ciências e Engenharia do Ambiente. Quinta da Torre, 2829-516 Caparica, Portugal
Isabel Peres
Affiliation:
IMAR-Instituto do Mar, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa – Departamento de Ciências e Engenharia do Ambiente. Quinta da Torre, 2829-516 Caparica, Portugal
Elsa Mendonça
Affiliation:
LNEG, Estrada do Paço do Lumiar 22, 1649-038 Lisboa, Portugal
Ana Picado
Affiliation:
LNEG, Estrada do Paço do Lumiar 22, 1649-038 Lisboa, Portugal
*
*Corresponding author. E-mail: mesd@fct.unl.pt
Get access

Abstract

The toxicity of titanium dioxide nanoparticles (TIO2 NPs) and oxidative stress effects were studied in two freshwater fish species (Carassius auratus and Danio rerio) exposed for 21 days to different concentrations (0.01, 0.1, 1, 10, 100/mgL) of TiO2 NPs and to a control (tap water). Additional fish were transferred to clean water for 14 days to assess the ability to recover from exposure to TiO2 NPs. Activities of the enzyme glutathione-S-transferase (GST) and lipid peroxidation (LPO) (malondialdheyde) were measured as indicators of oxidative stress. Histological and ultra-structural changes in livers from bothspecies of fish were evaluated by light and electron microscopy. Results show a general GST activity increase according to TiO2 NPs concentrations, which is in agreement with data from LPO. After 21 days, GST activities decreased possibly caused by suppression of GST synthesis as a result of severe stress. Histological and ultra-structural analysis of livers from exposed fish show degeneration of the hepatic tissue and alterations in hepatocytes such as glycogen depletion and an increase in lipofucsin lysosome-like granules. After a depuration period a partial recovery for biochemical markers and cells was observed. The results suggest that TiO2 promotes alterations in hepatic tissues compatible with oxidative stress.

Type
Portuguese Society for Microscopy
Copyright
Copyright © Microscopy Society of America 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agius, C. & Roberts, R.J. (2003). Melano-macrophage centres and their role in fish pathology. J Fish Diseases 26, 499509.CrossRefGoogle ScholarPubMed
Bernet, D., Schmidt, H., Meier, W., Burkhardt-Holm, P. & Wahli, T. (1999). Histopathology in fish: A proposal for a protocol to assess aquatic pollution. J Fish Dis 22, 2534.CrossRefGoogle Scholar
Boyle, D., Al-Bairuty, G.A., Ramsden, C.S., Sloman, K.A., Henry, T.B. & Handy, R.D. (2013). Subtle alterations in swimming speed distributions of rainbow trout exposed to titanium dioxide nanoparticles are associated with gill rather than brain injury. Aquat Toxicol 126, 116127.Google Scholar
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248254.Google Scholar
Chen, J.Y., Dong, X., Xin, Y.Y. & Zhao, M.R. (2011a). Effects of titanium dioxide nanoparticles on growth and some histological parameters of zebrafish (Danio rerio) after a long-term exposure. Aquat Toxicol 101, 493499.Google Scholar
Chen, T.H., Lin, C.Y. & Tseng, M.C. (2011b). Behavioral effects of titanium dioxide nanoparticles on larval zebrafish (Danio rerio). Mar Poll Bull 63, 303308.Google Scholar
Chen, X. & Mao, S.S. (2007). Titanium dioxide nanomaterials: Synthesis, properties, modifications, and applications. Chem Rev 107(7), 28912959.CrossRefGoogle ScholarPubMed
Clemente, Z., Castro, V.L., Jonsson, C.M. & Fraceto, L.F. (2012). Ecotoxicology of nano-TiO2—An evaluation of its toxicity to organisms of aquatic ecosystems. Int J Environ Res 6(1), 3350.Google Scholar
Costa, P.M., Diniz, M.S., Caeiro, S., Lobo, J., Martins, M., Ferreira, A.M., Caetano, M., Vale, C., DelValls, T.Á. & Costa, M.H. (2009). Histological biomarkers in gills and liver of juvenile Solea senegalensis exposed to contaminated estuarine sediments: A weighted indices approach. Aquat Toxicol 92(3), 202212.Google Scholar
Dini, L., Lentini, A., Diez, G.D., Rocha, M., Falasca, L., Serafino, L. & Vidal-Vanaclocha, F. (1995). Phagocytosis of apoptotic bodies by liver endothelial cells. J Cell Sci 108, 967973.Google Scholar
Dodd, N.J.F. & Jha, A.N. (2009). Titanium dioxide induced cell damage: A proposed role of the carboxyl radical. Mutation Res 660, 7982.CrossRefGoogle Scholar
Duan, Y., Liu, J., Ma, L., Li, N., Liu, H., Wang, J., Zheng, L., Liu, C., Wang, X., Zhao, X., Yan, J., Wang, S., Wang, H., Zhang, X. & Hong, F. (2010). Toxicological characteristics of nanoparticulate anatase titanium dioxide in mice. Biomaterials 31, 894899.CrossRefGoogle ScholarPubMed
Fako, V. & Furgeson, D. (2009). Zebrafish as a correlative and predictive model for assessing biomaterial nanotoxicity. Adv Drug Deliver Rev 61, 478486.Google Scholar
Federici, G., Shaw, B.J. & Handy, R.D. (2007). Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): Gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84, 415430.Google Scholar
Gurr, J.R., Wang, A.S.S., Chen, C.H. & Jan, K.Y. (2005). Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicol 213, 6673.Google Scholar
Habig, W.H., Pabst, M.J. & Jakoby, W.B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 246, 71307139.Google Scholar
Hao, L., Wang, Z. & Xing, B. (2009). Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in Juvenile Carp (Cyprinus carpio). J Environ Sci 21, 14591466.Google Scholar
Hussain, S.M., Hess, K.L., Gearhart, J.M., Geiss, K.T. & Schlager, J.J. (2005). In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol In Vitro 19, 975983.Google Scholar
Johnston, B.D., Scown, T.M., Moger, J., Cumberland, S.A., Baalousha, M., Linge, K., van Aerle, R., Jarvis, K., Lead, J.R. & Tyler, C.R. (2010). Bioavailability of nanoscale metal oxides TiO2, CeO2, and ZnO to fish. Environ Sci Technol 44, 11441151.CrossRefGoogle ScholarPubMed
Jovanovic, B., Anastasova, L., Rowe, E.W., Zhang, Y., Clapp, A.R. & Palic, D. (2011). Effects of nanosized titanium dioxide on innate immune system of fathead minnow (Pimephales promelas Rafinesque, 1820). Ecotox Environ Safety 74, 675683.Google Scholar
Jovanovic, B. & Palic, D. (2012). Immunotoxicology of non-functionalized engineered nanoparticles in aquatic organisms with special emphasis on fish—Review of current knowledge, gap identification, and call for further research. Aquat Toxicol 118119, 141151.Google Scholar
Kaegi, R., Ulrich, A., Sinnet, B., Vonbank, R., Wichser, A., Zuleeg, S., Simmler, H., Brunner, S., Vonmont, H., Burkhardt, M. & Boller, M. (2008). Synthetic TiO2 nanoparticle emission from exterior facades into the aquatic environment. Environ Pollut 156, 233239.Google Scholar
Kahru, A. & Dubourguier, H-C. (2010). From ecotoxicology to nanoecotoxicology. Toxicology 269, 105119.Google Scholar
Kerr, J.F.R., Gobe, G.C., Winterford, C.M. & Harmon, B.V. (1995). Anatomical methods in cell death. In Methods Cell Biology, vol. 46, Schwartz, L.M. & Osborne, B.A. (Eds.), pp. 127. San Diego, CA: Academic Press.Google Scholar
Kiser, M.A., Westerhoff, P., Benn, T., Wang, Y., Pérez-Rivera, J. & Hristovski, K. (2009). Titanium nanomaterial removal and release from wastewater treatment plants. Environ Sci Technol 43, 67576763.Google Scholar
Klaine, S.J., Koelmans, A.A., Horne, N., Carley, S., Handy, R.D., Kapustka, L., Nowack, B. & von der Kammer, F. (2012). Paradigms to assess the environmental impact of manufactured nanomaterials. Environ Toxicol Chem 31, 314.Google Scholar
Lapresta-Fernandez, A., Fernandez, A. & Blasco, J. (2012). Nanoecotoxicity effects of engineered silver and gold nanoparticles in aquatic organisms. Trends Anal Chem 32, 4059.CrossRefGoogle Scholar
Lovern, S.B. & Klaper, R. (2006). Daphnia magna mortality when exposed to titanium dioxide and fullerene (C60) nanoparticles. Environ Toxicol Chem 25, 11321137.Google Scholar
Martoja, R. & Martoja-Pierson, M. (1967). Initiation aux Techniques de L'Histologie Animal. Paris: Masson.Google Scholar
Menard, A., Drobne, D. & Jemec, A. (2011). Ecotoxicity of nanosized TiO2. Review of in vivo data. Environ Poll 159, 677684.CrossRefGoogle ScholarPubMed
Meseguer, J., López-Ruiz, A. & Esteban, M.A. (1994). Melano-macrophages of the seawater teleosts, sea bass (Dicentrarchus labrax) and gilthead seabream (Sparus aurata): Morphology, formation and possible function. Cell Tissue Res 277, 110.Google Scholar
Moore, M.N. (2006). Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32, 967976.Google Scholar
Mylonas, C. & Kouretas, D. (1999). Lipid peroxidation and tissue damage. In Vivo 13(3), 295309.Google Scholar
Nowack, B. & Bucheli, T.D. (2007). Occurrence behavior and effects of nanoparticles in the environment. Environ Poll 150, 522.Google Scholar
Oberdorster, G., Oberdorster, E. & Oberdorster, J. (2005). Nanotoxicology: An emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113, 823839.Google Scholar
OECD (1992). Guideline for the Testing of Chemicals: Fish Acute Toxicity Test. Test No. 203, p. 10. Paris: OECD. Google Scholar
OECD (2009). Guideline for the Testing of Chemicals: A Short-Term Screening for Oestrogenic and Androgenic Activity, and Aromatase Inhibition. Test No. 230: 21-day Fish Assay, p. 38. Paris: OECD. Google Scholar
Ohkawa, H., Ohishi, N. & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2), 351358.Google Scholar
Palaniappan, P.L.R.M. & Pramod, K.S. (2011). Raman spectroscopic investigation on the microenvironment of the liver tissues of zebrafish (Danio rerio) due to titanium dioxide exposure. Vibrat Spectr 56, 146153.Google Scholar
Palsamy, P., Sivakumar, S. & Subramanian, S. (2010). Resveratrol attenuates hyperglycemia-mediated oxidative stress, proinflammatory cytokines and protects hepatocytes ultrastructure in streptozotocin–nicotinamide-induced experimental diabetic rats. Chemico-Biol Interac 186, 200210.Google Scholar
Paterson, G., Ataria, J.M., Hoque, M.E., Burns, D.C. & Metcalfe, C.D. (2011). The toxicity of titanium dioxide nanopowder to early life stages of the Japanese medaka (Oryzias latipes). Chemosphere 82, 10021009.Google Scholar
Peralta-Videa, J.R., Zhao, L., Lopez-Moreno, M.L., de la Rosa, G., Hong, J. & Gardea-Torresdeya, J.L. (2011). Nanomaterials and the environment: A review for the biennium 2008–2010. J Haz Mat 186, 115.CrossRefGoogle Scholar
Ramsden, C.S., Henry, T.B. & Handy, R.D. (2013). Sub-lethal effects of titanium dioxide nanoparticles on the physiology and reproduction of zebrafish. Aquat Toxicol 126, 404413.Google Scholar
Ramsden, C.S., Smith, T.J., Shaw, B.J. & Handy, R.D. (2009). Dietary exposure to titanium dioxide nanoparticles in rainbow trout (Oncorhynchus mykiss): No effect on growth, but subtle biochemical disturbances in the brain. Ecotoxicol 18, 939951.Google Scholar
Reeves, J.F., Davies, S.J., Dodd, N.J. & Jha, A.N. (2008). Hydroxyl radicals (•OH) are associated with titanium dioxide (TiO2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutation Res 640, 113122.Google Scholar
Reyes-Coronado, D., Rodríguez-Gattorno, G., Espinosa-Pesqueira, M.E., Cab, C., de Coss, R. & Oskam, G. (2008). Phase-pure TiO2 nanoparticles: Anatase, brookite and rutile. Nanotech 19, 1019.Google Scholar
Royal Society (2004). Nanoscience and Nanotechnologies: Opportunities and Uncertainties. Cardiff, UK: Clyvedon Press. Available at http://www.nanotec.org.uk/finalReport.htm.Google Scholar
Savolainen, K., Pylkkänen, L., Norppa, H., Falck, G., Lindberg, H., Tuomi, T., Vippola, M., Alenius, H., Hämeri, K., Koivisto, J., Brouwer, D., Mark, D., Bard, D., Berges, M., Jankowska, E., Posniak, M., Farmer, P., Singh, R., Krombach, F., Bihari, P., Kasper, G. & Seipenbusch, M. (2010). Nanotechnologies, engineered nanomaterials and occupational health and safety—A review. Safety Sci 48, 957963.Google Scholar
Scown, T.M., van Aerle, R., Johnston, B.D., Cumberland, S., Lead, J.R., Owen, R. & Tyler, C.R. (2009). High doses of intravenously administered titanium dioxide nanoparticles accumulate in the kidneys of rainbow trout but with no observable impairment of renal function. Toxicol Sci 109, 372380.Google Scholar
Shaw, B.J. & Handy, R.D. (2011). Physiological effects of nanoparticles on fish: A comparison of nanometals versus metal ions. Environ Int 37, 10831097.Google Scholar
Siddiqui, M.K.J., Mahboob, M., Anjum, F. & Mustafa, M. (1993). Alterations in extra hepatic glutathione S-transferase activity in pigeon exposed to dimethoate, piperonyl butoxide and DDT. Indian J Experim Biol 31, 278279.Google Scholar
StatSoft, Inc. (2007). STATISTICA (data analysis software system), version 8.0. Available at www.statsoft.com.Google Scholar
Takashima, F. & Hibiya, T. (1995). An Atlas of Fish Histology: Normal and Pathological Features, 2nd ed. Tokyo: Kodansha.Google Scholar
U.S. Environmental Protection Agency (1996). OPPTS 850.1075. Fish Acute Toxicity Test, Freshwater and Marine. EPA 712-C-96-118. Ecological Effects Test Guidelines. Washington, DC: U.S. Environmental Protection Agency.Google Scholar
Wang, J., Zhu, X., Zhang, X., Zhao, Z., Liu, H., George, R., Wilson-Rawls, J., Chang, Y. & Chen, Y. (2011). Disruption of zebrafish (Danio rerio) reproduction upon chronic exposure to TiO2 nanoparticles. Chemosphere 83, 461467.Google Scholar
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, 14441452.Google Scholar
Zhang, J.F., Liu, H., Sun, Y.Y., Wang, X.R., Wu, J.C. & Xuea, Y.Q. (2005). Responses of the antioxidant defenses of the Goldfish Carassius auratus, exposed to 2,4-dichlorophenol. Environ Toxicol Pharmacol 19, 185190.Google Scholar
Zhu, X., Wang, J., Zhang, X., Chang, Y. & Chen, Y. (2010). Trophic transfer of TiO2 anoparticles from daphnia to zebrafish in a simplified freshwater food chain. Chemosphere 79, 928933.CrossRefGoogle Scholar