Zinc Oxide Nanoparticles Induce DNA Damage in Sand Dollar Scaphechinus mirabilis Sperm
Abstract
:1. Introduction
2. Materials and Methods
2.1. Preparation of Working Solutions
2.2. Description of the Experiment
2.3. Comet Assay
2.4. Statistical Analysis
3. Results and Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Giese, B.; Klaessig, F.; Park, B.; Kaegi, R.; Steinfeldt, M.; Wigger, H.; von Gleich, A.; Gottschalk, F. Risks, release and concentrations of engineered nanomaterial in the environment. Sci. Rep. 2018, 8, 1565. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Latif, H.M.R.; Dawood, M.A.O.; Menanteau-Ledouble, S.; El-Matbouli, M. Environmental transformation of n-TiO 2 in the aquatic systems and their ecotoxicity in bivalve mollusks: A systematic review. Ecotoxicol. Environ. Saf. 2020, 200, 110776. [Google Scholar] [CrossRef] [PubMed]
- Ahamed, A.; Liang, L.; Lee, M.Y.; Bobacka, J.; Lisak, G. Too small to matter? Physicochemical transformation and toxicity of engineered nTiO 2, nSiO 2, nZnO, carbon nanotubes, and nAg. J. Hazard. Mater. 2021, 404 Pt A, 124107. [Google Scholar] [CrossRef]
- Mueller, N.; Nowack, B. Exposure modeling of engineered nanoparticles in the environment. Environ. Sci. Technol. 2008, 42, 4447–4453. [Google Scholar] [CrossRef]
- Garcia, C.V.; Shin, G.H.; Kim, J.T. Metal oxide-based nanocomposites in food packaging: Applications, migration, and regulations. Trends Food Sci. Technol. 2018, 82, 21–31. [Google Scholar] [CrossRef]
- Sruthi, S.; Ashtami, J.; Mohanan, P.V. Biomedical application and hidden toxicity of Zinc oxide nanoparticles. Mater. Today Chem. 2018, 10, 175–186. [Google Scholar] [CrossRef]
- Nel, A.; Xia, T.; Mädler, L.; Li, N. Toxic potential of materials at the nanolevel. Science 2006, 311, 622–627. [Google Scholar] [CrossRef] [Green Version]
- Suh, W.H.; Suslick, K.S.; Stucky, G.D.; Suh, Y.H. Nanotechnology, nanotoxicology, and neuroscience. Prog. Neurobiol. 2009, 87, 133–170. [Google Scholar] [CrossRef] [Green Version]
- Sawicki, K.; Czajka, M.; Matysiak-Kucharek, M.; Fal, B.; Drop, B.; Męczyńska-Wielgosz, S.; Sikorska, K.; Kruszewski, M.; Kapka-Skrzypczak, L. Toxicity of metallic nanoparticles in the central nervous system. Nanotechnol. Rev. 2019, 8, 175–200. [Google Scholar] [CrossRef] [Green Version]
- Bongaerts, E.; Nawrot, T.S.; van Pee, T.; Ameloot, M.; Bové, H. Translocation of (ultra)fine particles and nanoparticles across the placenta; a systematic review on the evidence of in vitro, ex vivo, and in vivo studies. Part. Fibre Toxicol. 2020, 17, 56. [Google Scholar] [CrossRef]
- Arora, S.; Rajwade, J.M.; Paknikar, K.M. Nanotoxicology and in vitro studies: The need of the hour. Toxicol. Appl. Pharmacol. 2012, 258, 151–165. [Google Scholar] [CrossRef] [PubMed]
- Bondarenko, O.; Juganson, K.; Ivask, A.; Kasemets, K.; Mortimer, M.; Kahru, A. Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: A critical review. Arch. Toxicol. 2013, 87, 1181–1200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeevanandam, J.; Barhoum, A.; Chan, Y.S.; Dufresne, A.; Danquah, M.K. Review on nanoparticles and nanostructured materials: History, sources, toxicity and regulations. Beilstein J. Nanotechnol. 2018, 9, 1050–1074. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moore, M.N. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ. Int. 2006, 32, 967–976. [Google Scholar] [CrossRef]
- Matranga, V.; Corsi, I. Toxic effects of engineered nanoparticles in the marine environment: Model organisms and molecular approaches. Mar. Environ. Res. 2012, 76, 32–40. [Google Scholar] [CrossRef]
- Keller, A.A.; Wang, H.; Zhou, D.; Lenihan, H.S.; Cherr, G.; Cardinale, B.J.; Miller, R.; Ji, Z. Stability and aggregation of metal oxide nanoparticles in natural aqueous matrices. Environ. Sci. Technol. 2010, 44, 1962–1967. [Google Scholar] [CrossRef]
- Canesi, L.; Ciacci, C.; Fabbri, R.; Marcomini, A.; Pojana, G.; Gallo, G. Bivalve mollusks as a unique target group for nanotoxity. Mar. Environ. Res. 2012, 76, 16–21. [Google Scholar] [CrossRef]
- Xu, L.; Wang, Z.; Zhao, J.; Lin, M.; Xing, B. Accumulation of metal-based nanoparticles in marine bivalve mollusks from offshore aquaculture as detected by single particle ICP-MS. Environ. Pollut. 2020, 260, 114043. [Google Scholar] [CrossRef]
- Paul, S.K.; Dutta, H.; Sarkar, S.; Sethi, L.N.; Ghosh, S.K. Nanosized zinc oxide: Super-functionalities, present scenario of application, safety issues, and future prospects in food processing and allied industries. Food Rev. Int. 2019, 35, 505–535. [Google Scholar] [CrossRef]
- Manzo, S.; Miglietta, M.; Rametta, G.; Buono, S.; Francia, G. Embryotoxicity and spermiotoxicity of nanosized ZnO for Mediterranean sea urchin Paracentrotus lividus. J. Hazard. Mater. 2013, 254, 1–9. [Google Scholar] [CrossRef]
- Trevisan, R.; Delapedra, G.; Mello, D.F.; Arl, M.; Schmidt, É.C.; Meder, F.; Monopoli, M.; Cargnin-Ferreira, E.; Bouzon, Z.L.; Fisher, A.S.; et al. Gills are an initial target of zinc oxide nanoparticles in oysters Crassostrea gigas, leading to mitochondrial disruption and oxidative stress. Aquat. Toxicol. 2014, 153, 27–38. [Google Scholar] [CrossRef] [PubMed]
- Prato, E.; Fabbrocini, A.; Libralato, G.; Migliore, L.; Parlapiano, I.; D’Adamo, R.; Rotini, A.; Manfra, L.; Lofrano, G.; Carraturo, F.; et al. Comparative toxicity of ionic and nanoparticulate zinc in the species Cymodoce truncata, Gammarus aequicauda and Paracentrotus lividus. Environ. Sci. Pollut. Res. Int. 2021, 28, 42891–42900. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.; Zhu, L.; Duan, Z. Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage. J. Environ. Sci. Health. A Tox. Hazard. Subst. Environ. Eng. 2008, 43, 278–284. [Google Scholar] [CrossRef] [PubMed]
- Minetto, D.; Ghirardini, A.V.; Libralato, G. Saltwater ecotoxicology of Ag, Au, CuO, TiO2, ZnO and C60 engineered nanoparticles: An overview. Environ. Int. 2016, 92–93, 189–201. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mazur, A.A.; Zhuravel, E.V.; Slobodskova, V.V.; Mazur, M.A. Assessment of the toxic effect of zinc ions and nano-sized zinc oxide on the early development of the sand dollar Scaphechinus mirabilis (Agassiz, 1864) (Echinodermata: Echinoidea). Russ. J. Mar. Bio. 2020, 46, 49–55. [Google Scholar] [CrossRef]
- Li, J.; Schiavo, S.; Xiangli, D.; Rametta, G.; Miglietta, M.L.; Oliviero, M.; Changwen, W.; Manzo, S. Early ecotoxic effects of ZnO nanoparticle chronic exposure in Mytilus galloprovincialis revealed by transcription of apoptosis and antioxidant-related genes. Ecotoxicology 2018, 27, 369–384. [Google Scholar] [CrossRef]
- Oliviero, M.; Schiavo, S.; Dumontet, S.; Manzo, S. DNA damages and offspring quality in sea urchin Paracentrotus lividus sperms exposed to ZnO nanoparticles. Sci. Total Environ. 2019, 651, 756–765. [Google Scholar] [CrossRef]
- Mazur, A.A.; Zhuravel, E.V.; Slobodskova, V.V.; Mazur, M.A.; Kukla, S.P.; Chelomin, V.P. Waterborne exposure of adult sand dollar, Scaphechinus mirabilis (Agassiz, 1864), to zinc ions and zinc oxide nanoparticles affects early development of its offspring. Water Air Soil Pollut. 2020, 231, 115. [Google Scholar] [CrossRef]
- Beiras, R.; Durán, I.; Bellas, J.; Sánchez-Marín, P. Biological Effects of Contaminants: Paracentrotus Lividus Sea Urchin Embryo Test with Marine Sediment Elutriates; International Council for the Exploration of the Sea (ICES): Copenhagen, Denmark, 2012; p. 13. [CrossRef]
- Nobre, C.R.; Santana, M.F.M.; Maluf, A.; Cortez, F.S.; Cesar, A.; Pereira, C.D.S.; Turra, A. Assessment of microplastic toxicity to embryonic development of the sea urchin Lytechinus variegatus (Echinodermata: Echinoidea). Mar. Pollut. Bull. 2015, 92, 99–104. [Google Scholar] [CrossRef]
- Lewis, C.; Galloway, T.S. Genotoxic damage in Polychaetes: A study of species and cell-type sensitivities. Mutat. Res. Genet. Toxicol. Environ. Mutat. 2008, 654, 69–75. [Google Scholar] [CrossRef] [Green Version]
- Lacaze, E.; Geffard, O.; Goyet, D.; Bony, S.; Devaux, A. Linking genotoxic responses in Gammarus fossarum germ cells with reproduction impairment, using the Comet assay. Environ. Res. 2011, 111, 626–634. [Google Scholar] [CrossRef] [PubMed]
- Lacaze, E.; Geffard, O.; Bony, S.; Devaux, A. Genotoxicity assessment in the amphipod Gammarus fossarum by use of the alkaline Comet assay. Mutat. Res. 2010, 700, 32–38. [Google Scholar] [CrossRef] [PubMed]
- Devaux, Y.; Zangrando, J.; Schroen, B.; Creemers, E.E.; Pedrazzini, T.; Chang, C.P.; Dorn, G.W.; Thum, T.; Heymans, S. Cardiolinc Network. Long noncoding RNAs in cardiac development and ageing. Nat. Rev. Cardiol. 2015, 12, 415–425. [Google Scholar] [CrossRef] [PubMed]
- Hamlin, H.J.; Marciano, K.; Downs, C.A. Migration of nonylphenol from food-grade plastic is toxic to the coralreef fish species Pseudochromis fridmani. Chemosphere 2015, 139, 223–228. [Google Scholar] [CrossRef]
- Messinetti, S.; Mercurio, S.; Parolini, M.; Sugni, M.; Pennati, R. Effects of polystyrene microplastics on early stages of two marine invertebrates with different feeding strategies. Environ. Pollut. 2018, 237, 1080–1087. [Google Scholar] [CrossRef]
- Balbi, T.; Camisassi, G.; Montagna, M.; Fabbri, R.; Franzellitti, S.; Carbone, C. Impact of cationic polystyrene nanoparticles (PS-NH2) on early embryo development of Mytilus galloprovincialis: Effects on shell formation. Chemosphere 2017, 186, 1–9. [Google Scholar] [CrossRef]
- Smith, M.A.; Fernandez-Triana, J.; Roughley, R.; Hebert, D.N. DNA barcode accumulation curves for understudied taxa and areas. Mol. Ecol. Resour. 2009, 9, 208–216. [Google Scholar] [CrossRef]
- Mahaye, N.; Thwala, M.; Cowan, D.A.; Musee, N. Genotoxicity of metal based engineered nanoparticles in aquatic organisms: A review. Mutat. Res. 2017, 773, 134–160. [Google Scholar] [CrossRef]
- Tang, Y.; Xin, H.; Yang, S.; Guo, M.; Malkoske, T.; Yin, D.; Xia, S. Environmental risks of ZnO nanoparticle exposure on Microcystis aeruginosa: Toxic effects and environmental feedback. Aquat. Toxicol. 2018, 204, 19–26. [Google Scholar] [CrossRef]
- Dinnel, P.A.; Stober, Q.J.; Crumley, S.C.; Nakatani, R.E. Development of a sperm cell toxicity test for marine water. Aquat. Toxicol. Haz. Asses. 1982, 1, 82–98. [Google Scholar] [CrossRef]
- Mitchelmore, C.L.; Birmelin, C.; Livingstone, D.R.; Chipman, J.K. Detection of DNA strand breaks in isolated mussels (Mytilus edulis) digestive gland cells using the “comet” assay. Ecotoxicol. Environ. Saf. 1998, 41, 51–58. [Google Scholar] [CrossRef] [PubMed]
- Gallo, A.; Boni, R.; Buttino, I.; Tosti, E. Spermiotoxicity of nickel nanoparticles in the marine invertebrate Ciona intestinalis (ascidians). Nanotoxicology 2016, 10, 1096–1104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Han, Y.; Shi, W.; Rong, J.; Zha, S.; Guan, X.; Sun, H.; Liu, G. Exposure to waterborne nTiO2 reduces fertilization success and increases polyspermy in a bivalve mollusc: A threat to population recruitment. Environ. Sci. Technol. 2019, 53, 12754–12763. [Google Scholar] [CrossRef] [PubMed]
- Devakumar, C.; Gopalakrishnan, H.; Chinnasamy, A.; Subramanian, B.; Durai, P. Toxicity of silver nanoparticles on fertilization success and early development of the marine polychaete Hydroides elegans (Haswell, 1883). J. Basic Appl. Zool. 2017, 78, 1. [Google Scholar] [CrossRef] [Green Version]
- Gallo, A.; Manfra, L.; Boni, R.; Rotini, A.; Migliore, L.; Tosti, E. Cytotoxicity and genotoxicity of CuO nanoparticles in sea urchin spermatozoa through oxidative stress. Environ. Int. 2018, 118, 325–333. [Google Scholar] [CrossRef] [PubMed]
- Hanna, S.K.; Miller, R.J.; Zhou, D.; Keller, A.A.; Lenihan, H.S. Accumulation and toxicity of metal oxide nanoparticles in a soft-sediment estuarine amphipod. Aquat. Toxicol. 2013, 142–143, 441–446. [Google Scholar] [CrossRef] [Green Version]
- Gambardella, C.; Morgana, S.; Bari, G.D.; Ramoino, P.; Bramini, M.; Diaspro, A.; Falugi, C.; Faimali, M. Multidisciplinary screening of toxicity induced by silica nanoparticles during sea urchin development. Chemosphere 2015, 139, 486–495. [Google Scholar] [CrossRef]
- Mwaanga, P.; Carraway, E.R.; van den Hurk, P. The induction of biochemical changes in Daphnia magna by CuO and ZnO nanoparticles. Aquat. Toxicol. 2014, 150, 201–209. [Google Scholar] [CrossRef]
- Rim, K.T.; Song, S.W.; Kim, H.Y. Oxidative DNA damage from nanoparticle exposure and its application to workers’ health: A literature review. Saf. Health Work 2013, 4, 177–186. [Google Scholar] [CrossRef] [Green Version]
- Huerta-García, E.; Márquez-Ramírez, S.G.; Ramos-Godinez, M.P.; López-Saavedra, A.; Herrera, L.A.; Parra, A.; Alfaro-Moreno, E.; Gómez, E.O.; López-Marure, R. Internalization of titanium dioxide nanoparticles by glial cells is given at short times and is mainly mediated by actin reorganization-dependent endocytosis. NeuroToxicology 2015, 51, 27–37. [Google Scholar] [CrossRef]
- Kazama, M.; Hino, A. Sea urchin spermatozoa generate at least two reactive oxygen species; the type of reactive oxygen species changes under different conditions. Mol. Reprod. Dev. 2012, 79, 283–295. [Google Scholar] [CrossRef] [PubMed]
- Kukla, S.; Slobodskova, V.; Mazur, A.; Chelomin, V.; Kamenev, Y. Genotoxic testing of titanium dioxide nanoparticles in Far Eastern mussels, Mytilus trossulus. Pollution 2021, 7, 129–140. [Google Scholar] [CrossRef]
- Akcha, F.; Spagnol, C.; Rouxel, J. Genotoxicity of diuron and glyphosate in oyster spermatozoa and embryos. Aquat. Toxicol. 2012, 106–107, 104–113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Devaux, A.; Fiat, L.; Gillet, C.; Bony, S. Reproduction impairment following paternal genotoxin exposure in brown trout (Salmo trutta) and Arctic charr (Salvelinus alpinus). Aquat. Toxicol. 2011, 101, 405–411. [Google Scholar] [CrossRef]
- Santos, R.; Palos-Ladeiro, M.; Besnard, A.; Porcher, J.M.; Bony, S.; Sanchez, W.; Devaux, A. Relationship between DNA damage in sperm after ex vivo exposure and abnormal embryo development in the progeny of the three-spined stickleback. Reprod. Toxicol. 2013, 36, 6–11. [Google Scholar] [CrossRef]
- Pérez-Cerezales, S.; Martínez-Páramo, S.; Beirão, J.; Herráez, M.P. Evaluation of DNA damage as a quality marker for rainbow trout sperm cryopreservation and use of LDL as cryoprotectant. Theriogenology 2010, 74, 282–289. [Google Scholar] [CrossRef]
Purity, % | Zeta Potential, mV | Particle Size, nm | Hydraulic Radius, nm | BET, m2/g |
---|---|---|---|---|
≥99.5 | −39.4 | 40–50 | 200 | 58 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kukla, S.P.; Chelomin, V.P.; Mazur, A.A.; Slobodskova, V.V. Zinc Oxide Nanoparticles Induce DNA Damage in Sand Dollar Scaphechinus mirabilis Sperm. Toxics 2022, 10, 348. https://doi.org/10.3390/toxics10070348
Kukla SP, Chelomin VP, Mazur AA, Slobodskova VV. Zinc Oxide Nanoparticles Induce DNA Damage in Sand Dollar Scaphechinus mirabilis Sperm. Toxics. 2022; 10(7):348. https://doi.org/10.3390/toxics10070348
Chicago/Turabian StyleKukla, Sergey Petrovich, Victor Pavlovich Chelomin, Andrey Alexandrovich Mazur, and Valentina Vladimirovna Slobodskova. 2022. "Zinc Oxide Nanoparticles Induce DNA Damage in Sand Dollar Scaphechinus mirabilis Sperm" Toxics 10, no. 7: 348. https://doi.org/10.3390/toxics10070348