najoNanosystems: Physics, Chemistry, MathematicsНаносистемы: физика, химия, математика2220-80542305-7971Университет ИТМО10.17586/2220-8054-2019-10-3-289-302najo-562Research ArticleCHEMISTRY AND MATERIAL SCIENCEХИМИЯ И МАТЕРИАЛОВЕДЕНИЕSynergetic action of ceria nanoparticles and doxorubicin on the early development of two fish species, Danio rerio and Puntius tetrazonaKrysanovE. Yu.

Moscow, 119071

krysanov@sevin.ruDemidovaT. B.

Moscow, 119071

IvanovaO. S.

Moscow, 119991 

OrdzhonikidzeK. G.

Moscow, 119991 

ShcherbakovA. B.

Kiev, D 03680

IvanovV. K.

Moscow, 119991

Tomsk, 634050

van@igic.ras.ruSevertsov Institute of Ecology and Evolution, Russian Academy of SciencesRussian FederationKurnakov Institute of General and Inorganic Chemistry, Russian Academy of SciencesRussian FederationVavilov Institute of General Genetics, Russian Academy of SciencesRussian FederationZabolotny Institute of Microbiology and Virology,NAS of UkraineUkraineKurnakov Institute of General and Inorganic Chemistry, Russian Academy of Sciences; National Research Tomsk State UniversityRussian Federation201907082025103289302Copyright © Krysanov E.Y., Demidova T.B., Ivanova O.S., Ordzhonikidze K.G., Shcherbakov A.B., Ivanov V.K., 20252025Krysanov E.Y., Demidova T.B., Ivanova O.S., Ordzhonikidze K.G., Shcherbakov A.B., Ivanov V.K.Krysanov E.Y., Demidova T.B., Ivanova O.S., Ordzhonikidze K.G., Shcherbakov A.B., Ivanov V.K.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://nanojournal.ifmo.ru/jour/article/view/562

The combined action of ceria nanoparticles and doxorubicin on the early stages of ontogenesis of Danio rerio and Puntius tetrazona was studied. Results obtained indicate that there is a synergetic effect of CeO2 nanoparticles and doxorubicin which is demonstrated by a high incidence of embryonic malformations in fish. This synergetic effect is more pronounced in tiger barbs than in zebrafish, and depends strongly on the synthetic route of ceria nanoparticles’ preparation, the most notable effects being registered for citrate-stabilized nanoparticles.

This work was partially supported by research grants of Russian foundation for Basic Research No. 18-29- 05023 mk.ReferencesAdachi G., Imanaka N., Kang Z.C. Binary Rare Earth Oxides. Kluwer Academic Publishers, Dordrecht, 2005, 133 p.Adachi G., Imanaka N., Kang Z.C. Binary Rare Earth Oxides. Kluwer Academic Publishers, Dordrecht, 2005, 133 p.Trovarelli A. Catalysis by Ceria and Related Materials. Imperial College Press, London, 2002, 58 p.Trovarelli A. Catalysis by Ceria and Related Materials. Imperial College Press, London, 2002, 58 p.Ivanov V.K., Shcherbakov A.B., Usatenko A.V. Structure-Sensitive Properties and Biomedical Applications of Nanodispersed Cerium Dioxide. Russ. Chem. Rev., 2009, 78 (9), P. 855–871.Ivanov V.K., Shcherbakov A.B., Usatenko A.V. Structure-Sensitive Properties and Biomedical Applications of Nanodispersed Cerium Dioxide. Russ. Chem. Rev., 2009, 78 (9), P. 855–871.Karakoti A., Singh S., et al. Redox-Active Radical Scavenging Nanomaterials. Chem. Soc. Rev., 2010, 39 (11), 4422.Karakoti A., Singh S., et al. Redox-Active Radical Scavenging Nanomaterials. Chem. Soc. Rev., 2010, 39 (11), 4422.Shcherbakov A.B., Ivanov V.K., et al. Nanocrystalline Ceria Based Materials – Perspectives for Biomedical Application. Biophysics (Oxf)., 2011, 56 (6), P. 987–1004.Shcherbakov A.B., Ivanov V.K., et al. Nanocrystalline Ceria Based Materials – Perspectives for Biomedical Application. Biophysics (Oxf)., 2011, 56 (6), P. 987–1004.Das S., Dowding J.M., et al. Cerium Oxide Nanoparticles: Applications and Prospects in Nanomedicine. Nanomedicine, 2013, 8 (9), P. 1483– 1508.Das S., Dowding J.M., et al. Cerium Oxide Nanoparticles: Applications and Prospects in Nanomedicine. Nanomedicine, 2013, 8 (9), P. 1483– 1508.Shcherbakov A.B., Zholobak N.M., Spivak N.Y., Ivanov V.K. Advances and Prospects of Using Nanocrystalline Ceria in Cancer Theranostics. Russ. J. Inorg. Chem., 2014, 59 (13), P. 1556–1575.Shcherbakov A.B., Zholobak N.M., Spivak N.Y., Ivanov V.K. Advances and Prospects of Using Nanocrystalline Ceria in Cancer Theranostics. Russ. J. Inorg. Chem., 2014, 59 (13), P. 1556–1575.Park E.-J., Choi J., Park Y.-K., Park K. Oxidative Stress Induced by Cerium Oxide Nanoparticles in Cultured BEAS-2B Cells. Toxicology, 2008, 245 (1–2), P. 90–100.Park E.-J., Choi J., Park Y.-K., Park K. Oxidative Stress Induced by Cerium Oxide Nanoparticles in Cultured BEAS-2B Cells. Toxicology, 2008, 245 (1–2), P. 90–100.Horie M., Nishio K., et al. Cellular Responses Induced by Cerium Oxide Nanoparticles: Induction of Intracellular Calcium Level and Oxidative Stress on Culture Cells. J. Biochem., 2011, 150 (4), P. 461–471.Horie M., Nishio K., et al. Cellular Responses Induced by Cerium Oxide Nanoparticles: Induction of Intracellular Calcium Level and Oxidative Stress on Culture Cells. J. Biochem., 2011, 150 (4), P. 461–471.Tseng M.T., Lu X., et al. Alteration of Hepatic Structure and Oxidative Stress Induced by Intravenous Nanoceria. Toxicol. Appl. Pharmacol., 2012, 260 (2), P. 173–182.Tseng M.T., Lu X., et al. Alteration of Hepatic Structure and Oxidative Stress Induced by Intravenous Nanoceria. Toxicol. Appl. Pharmacol., 2012, 260 (2), P. 173–182.Lee S.S., Song W., et al. Antioxidant Properties of Cerium Oxide Nanocrystals as a Function of Nanocrystal Diameter and Surface Coating. ACS Nano, 2013, 7 (11), P. 9693–9703.Lee S.S., Song W., et al. Antioxidant Properties of Cerium Oxide Nanocrystals as a Function of Nanocrystal Diameter and Surface Coating. ACS Nano, 2013, 7 (11), P. 9693–9703.Karakoti A.S., Monteiro-Riviere N.A., et al. Nanoceria as Antioxidant: Synthesis and Biomedical Applications. JOM, 2008, 60 (3), P. 33–37.Karakoti A.S., Monteiro-Riviere N.A., et al. Nanoceria as Antioxidant: Synthesis and Biomedical Applications. JOM, 2008, 60 (3), P. 33–37.Hirst S.M., Karakoti A., et al. Bio-Distribution and in Vivo Antioxidant Effects of Cerium Oxide Nanoparticles in Mice. Environ. Toxicol., 2013, 28 (2), P. 107–118.Hirst S.M., Karakoti A., et al. Bio-Distribution and in Vivo Antioxidant Effects of Cerium Oxide Nanoparticles in Mice. Environ. Toxicol., 2013, 28 (2), P. 107–118.Chigurupati S., Mughal M.R., et al. Effects of Cerium Oxide Nanoparticles on the Growth of Keratinocytes, Fibroblasts and Vascular Endothelial Cells in Cutaneous Wound Healing. Biomaterials, 2013, 34 (9), P. 2194–2201.Chigurupati S., Mughal M.R., et al. Effects of Cerium Oxide Nanoparticles on the Growth of Keratinocytes, Fibroblasts and Vascular Endothelial Cells in Cutaneous Wound Healing. Biomaterials, 2013, 34 (9), P. 2194–2201.Karakoti A.S., Munusamy P., et al. Preparation and Characterization Challenges to Understanding Environmental and Biological Impacts of Ceria Nanoparticles. Surf. Interface Anal., 2012, 44 (8), P. 882–889.Karakoti A.S., Munusamy P., et al. Preparation and Characterization Challenges to Understanding Environmental and Biological Impacts of Ceria Nanoparticles. Surf. Interface Anal., 2012, 44 (8), P. 882–889.Cassee F.R., van Balen E.C., et al. Exposure, Health and Ecological Effects Review of Engineered Nanoscale Cerium and Cerium Oxide Associated with Its Use as a Fuel Additive. Crit. Rev. Toxicol., 2011, 41 (3), P. 213–229.Cassee F.R., van Balen E.C., et al. Exposure, Health and Ecological Effects Review of Engineered Nanoscale Cerium and Cerium Oxide Associated with Its Use as a Fuel Additive. Crit. Rev. Toxicol., 2011, 41 (3), P. 213–229.Van Hoecke K., De Schamphelaere K.A.C., et al. Aggregation and Ecotoxicity of CeO2 Nanoparticles in Synthetic and Natural Waters with Variable PH, Organic Matter Concentration and Ionic Strength. Environ. Pollut., 2011, 159 (4), P. 970–976.Van Hoecke K., De Schamphelaere K.A.C., et al. Aggregation and Ecotoxicity of CeO2 Nanoparticles in Synthetic and Natural Waters with Variable PH, Organic Matter Concentration and Ionic Strength. Environ. Pollut., 2011, 159 (4), P. 970–976.Artells E., Issartel J., et al. Exposure to Cerium Dioxide Nanoparticles Differently Affect Swimming Performance and Survival in Two Daphnid Species. PLoS One, 2013, 8 (8), e71260.Artells E., Issartel J., et al. Exposure to Cerium Dioxide Nanoparticles Differently Affect Swimming Performance and Survival in Two Daphnid Species. PLoS One, 2013, 8 (8), e71260.Arnold M.C., Badireddy A.R., et al. Cerium Oxide Nanoparticles Are More Toxic than Equimolar Bulk Cerium Oxide in Caenorhabditis Elegans. Arch. Environ. Contam. Toxicol., 2013, 65 (2), P. 224–233.Arnold M.C., Badireddy A.R., et al. Cerium Oxide Nanoparticles Are More Toxic than Equimolar Bulk Cerium Oxide in Caenorhabditis Elegans. Arch. Environ. Contam. Toxicol., 2013, 65 (2), P. 224–233.Jemec A., Djinovic P., ´ Crnivec I.G.O., Pintar A. The Hazard Assessment of Nanostructured CeO ˇ 2-Based Mixed Oxides on the Zebrafish Danio Rerio under Environmentally Relevant UV-A Exposure. Sci. Total Environ., 2015, 506–507, P. 272–278.Jemec A., Djinovic P., ´ Crnivec I.G.O., Pintar A. The Hazard Assessment of Nanostructured CeO ˇ 2-Based Mixed Oxides on the Zebrafish Danio Rerio under Environmentally Relevant UV-A Exposure. Sci. Total Environ., 2015, 506–507, P. 272–278.O’Brien N., Cummins E. Nano-Scale Pollutants: Fate in Irish Surface and Drinking Water Regulatory Systems. Hum. Ecol. Risk Assess. An Int. J., 2010, 16 (4), P. 847–872.O’Brien N., Cummins E. Nano-Scale Pollutants: Fate in Irish Surface and Drinking Water Regulatory Systems. Hum. Ecol. Risk Assess. An Int. J., 2010, 16 (4), P. 847–872.Johnson A.C., Park B. Predicting Contamination by the Fuel Additive Cerium Oxide Engineered Nanoparticles within the United Kingdom and the Associated Risks. Environ. Toxicol. Chem., 2012, 31 (11), P. 2582–2587.Johnson A.C., Park B. Predicting Contamination by the Fuel Additive Cerium Oxide Engineered Nanoparticles within the United Kingdom and the Associated Risks. Environ. Toxicol. Chem., 2012, 31 (11), P. 2582–2587.Zhang P., He X., et al. Distribution and Bioavailability of Ceria Nanoparticles in an Aquatic Ecosystem Model. Chemosphere, 2012, 89 (5), P. 530–535.Zhang P., He X., et al. Distribution and Bioavailability of Ceria Nanoparticles in an Aquatic Ecosystem Model. Chemosphere, 2012, 89 (5), P. 530–535.Bottero J.-Y., Auffan M., et al. Manufactured Metal and Metal-Oxide Nanoparticles: Properties and Perturbing Mechanisms of Their Biological Activity in Ecosystems. Comptes Rendus Geosci., 2011, 343 (2–3), P. 168–176.Bottero J.-Y., Auffan M., et al. Manufactured Metal and Metal-Oxide Nanoparticles: Properties and Perturbing Mechanisms of Their Biological Activity in Ecosystems. Comptes Rendus Geosci., 2011, 343 (2–3), P. 168–176.Manier N., Garaud M., et al. Behaviour of Ceria Nanoparticles in Standardized Test Media – Influence on the Results of Ecotoxicological Tests. J. Phys. Conf. Ser., 2011, 304, 012058.Manier N., Garaud M., et al. Behaviour of Ceria Nanoparticles in Standardized Test Media – Influence on the Results of Ecotoxicological Tests. J. Phys. Conf. Ser., 2011, 304, 012058.Garc´ıa A., Espinosa R., et al. Acute Toxicity of Cerium Oxide, Titanium Oxide and Iron Oxide Nanoparticles Using Standardized Tests. Desalination, 2011, 269 (1–3), P. 136–141.Garc´ıa A., Espinosa R., et al. Acute Toxicity of Cerium Oxide, Titanium Oxide and Iron Oxide Nanoparticles Using Standardized Tests. Desalination, 2011, 269 (1–3), P. 136–141.Ould-Moussa N., Safi M., et al. In Vitro Toxicity of Nanoceria: Effect of Coating and Stability in Biofluids. Nanotoxicology, 2014, 8 (7), P. 799–811.Ould-Moussa N., Safi M., et al. In Vitro Toxicity of Nanoceria: Effect of Coating and Stability in Biofluids. Nanotoxicology, 2014, 8 (7), P. 799–811.Quik J.T.K., Lynch I., et al. Effect of Natural Organic Matter on Cerium Dioxide Nanoparticles Settling in Model Fresh Water. Chemosphere, 2010, 81 (6), P. 711–715.Quik J.T.K., Lynch I., et al. Effect of Natural Organic Matter on Cerium Dioxide Nanoparticles Settling in Model Fresh Water. Chemosphere, 2010, 81 (6), P. 711–715.Schwabe F., Schulin R., et al. Influence of Two Types of Organic Matter on Interaction of CeO2 Nanoparticles with Plants in Hydroponic Culture. Chemosphere, 2013, 91 (4), P. 512–520.Schwabe F., Schulin R., et al. Influence of Two Types of Organic Matter on Interaction of CeO2 Nanoparticles with Plants in Hydroponic Culture. Chemosphere, 2013, 91 (4), P. 512–520.Han Y., Zhang J., Qian J., Hu C. Cardiotoxicity Evaluation of Anthracyclines in Zebrafish ( Danio Rerio ). J. Appl. Toxicol., 2015, 35 (3), P. 241–252.Han Y., Zhang J., Qian J., Hu C. Cardiotoxicity Evaluation of Anthracyclines in Zebrafish ( Danio Rerio ). J. Appl. Toxicol., 2015, 35 (3), P. 241–252.Ivanov V.K., Polezhaeva O.S., et al. Microwave-Hydrothermal Synthesis of Stable Nanocrystalline Ceria Sols for Biomedical Uses. Russ. J. Inorg. Chem., 2010, 55 (1), P. 1–5.Ivanov V.K., Polezhaeva O.S., et al. Microwave-Hydrothermal Synthesis of Stable Nanocrystalline Ceria Sols for Biomedical Uses. Russ. J. Inorg. Chem., 2010, 55 (1), P. 1–5.Kimmel C.B., Ballard W.W., et al. Stages of Embryonic Development of the Zebrafish. Dev. Dyn., 1995, 203 (3), P. 253–310.Kimmel C.B., Ballard W.W., et al. Stages of Embryonic Development of the Zebrafish. Dev. Dyn., 1995, 203 (3), P. 253–310.Zhu X., Zhu L., et al. Comparative Toxicity of Several Metal Oxide Nanoparticle Aqueous Suspensions to Zebrafish (Danio Rerio) Early Developmental Stage. J. Environ. Sci. Heal. Part A, 2008, 43 (3), P. 278–284.Zhu X., Zhu L., et al. Comparative Toxicity of Several Metal Oxide Nanoparticle Aqueous Suspensions to Zebrafish (Danio Rerio) Early Developmental Stage. J. Environ. Sci. Heal. Part A, 2008, 43 (3), P. 278–284.Chen T.-H., Lin C.-Y., Tseng M.-C. Behavioral Effects of Titanium Dioxide Nanoparticles on Larval Zebrafish (Danio Rerio). Mar. Pollut. Bull., 2011, 63 (5–12), P. 303–308.Chen T.-H., Lin C.-Y., Tseng M.-C. Behavioral Effects of Titanium Dioxide Nanoparticles on Larval Zebrafish (Danio Rerio). Mar. Pollut. Bull., 2011, 63 (5–12), P. 303–308.Sun H., Zhang X., et al. Enhanced Accumulation of Arsenate in Carp in the Presence of Titanium Dioxide Nanoparticles. Water. Air. Soil Pollut., 2007, 178 (1–4), P. 245–254.Sun H., Zhang X., et al. Enhanced Accumulation of Arsenate in Carp in the Presence of Titanium Dioxide Nanoparticles. Water. Air. Soil Pollut., 2007, 178 (1–4), P. 245–254.Zhang X., Sun H., et al. Enhanced Bioaccumulation of Cadmium in Carp in the Presence of Titanium Dioxide Nanoparticles. Chemosphere, 2007, 67 (1), P. 160–166.Zhang X., Sun H., et al. Enhanced Bioaccumulation of Cadmium in Carp in the Presence of Titanium Dioxide Nanoparticles. Chemosphere, 2007, 67 (1), P. 160–166.Hu X., Chen Q., et al. Combined Effects of Titanium Dioxide and Humic Acid on the Bioaccumulation of Cadmium in Zebrafish. Environ. Pollut., 2011, 159 (5), P. 1151–1158.Hu X., Chen Q., et al. Combined Effects of Titanium Dioxide and Humic Acid on the Bioaccumulation of Cadmium in Zebrafish. Environ. Pollut., 2011, 159 (5), P. 1151–1158.Fan W., Cui M., et al. Nano-TiO2 Enhances the Toxicity of Copper in Natural Water to Daphnia Magna. Environ. Pollut., 2011, 159 (3), P. 729–734.Fan W., Cui M., et al. Nano-TiO2 Enhances the Toxicity of Copper in Natural Water to Daphnia Magna. Environ. Pollut., 2011, 159 (3), P. 729–734.Wang D., Hu J., Irons D.R., Wang J. Synergistic Toxic Effect of Nano-TiO2 and As(V) on Ceriodaphnia Dubia. Sci. Total Environ., 2011, 409 (7), P. 1351–1356.Wang D., Hu J., Irons D.R., Wang J. Synergistic Toxic Effect of Nano-TiO2 and As(V) on Ceriodaphnia Dubia. Sci. Total Environ., 2011, 409 (7), P. 1351–1356.Han Z., Li J., Bao W., Wang J. Enhanced Toxicity of Atrazine to Daphnia Magna in the Presence of Nano-CeO2. Chinese J. Geochemistry, 2012, 31 (3), P. 297–302.Han Z., Li J., Bao W., Wang J. Enhanced Toxicity of Atrazine to Daphnia Magna in the Presence of Nano-CeO2. Chinese J. Geochemistry, 2012, 31 (3), P. 297–302.Chang C., Wu S.L., et al. Developmental Toxicity of Doxorubicin Hydrochloride in Embryo-Larval Stages of Zebrafish. Biomed. Mater. Eng., 2014, 24 (1), P. 909–916.Chang C., Wu S.L., et al. Developmental Toxicity of Doxorubicin Hydrochloride in Embryo-Larval Stages of Zebrafish. Biomed. Mater. Eng., 2014, 24 (1), P. 909–916.Recillas S., Garca A., et al. Use of CeO2, TiO2 and Fe3O4 Nanoparticles for the Removal of Lead from Water. Desalination, 2011, 277 (1–3), P. 213–220.Recillas S., Garca A., et al. Use of CeO2, TiO2 and Fe3O4 Nanoparticles for the Removal of Lead from Water. Desalination, 2011, 277 (1–3), P. 213–220.Brigante M., Schulz P.C. Adsorption of the Antibiotic Minocycline on Cerium(IV) Oxide: Effect of PH, Ionic Strength and Temperature. Microporous Mesoporous Mater., 2012, 156, P. 138–144.Brigante M., Schulz P.C. Adsorption of the Antibiotic Minocycline on Cerium(IV) Oxide: Effect of PH, Ionic Strength and Temperature. Microporous Mesoporous Mater., 2012, 156, P. 138–144.Fent K., Weisbrod C.J., Wirth-Heller A., Pieles U. Assessment of Uptake and Toxicity of Fluorescent Silica Nanoparticles in Zebrafish (Danio Rerio) Early Life Stages. Aquat. Toxicol., 2010, 100 (2), P. 218–228.Fent K., Weisbrod C.J., Wirth-Heller A., Pieles U. Assessment of Uptake and Toxicity of Fluorescent Silica Nanoparticles in Zebrafish (Danio Rerio) Early Life Stages. Aquat. Toxicol., 2010, 100 (2), P. 218–228.Felix L.C., Ortega V.A., Ede J.D., Goss G.G. Physicochemical Characteristics of Polymer-Coated Metal-Oxide Nanoparticles and Their Toxicological Effects on Zebrafish (Danio Rerio) Development. Environ. Sci. Technol., 2013, 47 (12), P. 6589–6596.Felix L.C., Ortega V.A., Ede J.D., Goss G.G. Physicochemical Characteristics of Polymer-Coated Metal-Oxide Nanoparticles and Their Toxicological Effects on Zebrafish (Danio Rerio) Development. Environ. Sci. Technol., 2013, 47 (12), P. 6589–6596.Poudel L., Wen A.M., et al. Electronic Structure and Partial Charge Distribution of Doxorubicin in Different Molecular Environments. Chem. Phys. Chem., 2015, 16 (7), P. 1451–1460.Poudel L., Wen A.M., et al. Electronic Structure and Partial Charge Distribution of Doxorubicin in Different Molecular Environments. Chem. Phys. Chem., 2015, 16 (7), P. 1451–1460.Curry D., Cameron A., et al. Adsorption of Doxorubicin on Citrate-Capped Gold Nanoparticles: Insights into Engineering Potent Chemotherapeutic Delivery Systems. Nanoscale, 2015, 7 (46), P. 19611–19619.Curry D., Cameron A., et al. Adsorption of Doxorubicin on Citrate-Capped Gold Nanoparticles: Insights into Engineering Potent Chemotherapeutic Delivery Systems. Nanoscale, 2015, 7 (46), P. 19611–19619.Nawara K., Romiszewski J., et al. Adsorption of Doxorubicin onto Citrate-Stabilized Magnetic Nanoparticles. J. Phys. Chem. C, 2012, 116 (9), P. 5598–5609.Nawara K., Romiszewski J., et al. Adsorption of Doxorubicin onto Citrate-Stabilized Magnetic Nanoparticles. J. Phys. Chem. C, 2012, 116 (9), P. 5598–5609.Auffan M., Masion A., et al. Long-Term Aging of a CeO2 Based Nanocomposite Used for Wood Protection. Environ. Pollut., 2014, 188, P. 1–7.Auffan M., Masion A., et al. Long-Term Aging of a CeO2 Based Nanocomposite Used for Wood Protection. Environ. Pollut., 2014, 188, P. 1–7.

The authors declare that there are no conflicts of interest present.