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Articles

Responses to iron oxide and zinc oxide nanoparticles in echinoderm embryos and microalgae: uptake, growth, morphology, and transcriptomic analysis

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Pages 1342-1361 | Received 27 Oct 2019, Accepted 10 Sep 2020, Published online: 14 Oct 2020

References

  • Adeleye, A. S., J. R. Conway, K. Garner, Y. Huang, Y. Su, and A. A. Keller. 2016. “Engineered Nanomaterials for Water Treatment and Remediation: Costs, Benefits, and Applicability.” Chemical Engineering Journal 286: 640–662. doi:10.1016/j.cej.2015.10.105.
  • Akasaka, K., H. Uemoto, F. Wilt, K. Mitsunaga-Nakatsubo, and H. Shimada. 1997. “ Oral-Aboral Ectoderm Differentiation of Sea Urchin Embryos is Disrupted in Response to Calcium Ionophore.” Development, Growth & Differentiation 39 (3): 373–379. doi:10.1046/j.1440-169x.1997.t01-2-00013.x.
  • Al-Subiai, S. N., V. M. Arlt, P. E. Frickers, J. W. Readman, B. Stolpe, J. R. Lead, A. J. Moody, and A. N. Jha. 2012. “Merging Nano-genotoxicology with Eco-genotoxicology: An Integrated Approach to Determine Interactive Genotoxic and Sub-Lethal Toxic Effects of C(60) Fullerenes and Fluoranthene in Marine Mussels, Mytilus sp.” Mutation Research 745 (1-2): 92–103. doi:10.1016/j.mrgentox.2011.12.019.
  • Aruoja, V., H.-C. Dubourguier, K. Kasemets, and A. Kahru. 2009. “Toxicity of Nanoparticles of CuO, ZnO and TiO2 to Microalgae Pseudokirchneriella subcapitata.” The Science of the Total Environment 407 (4): 1461–1468. doi:10.1016/j.scitotenv.2008.10.053.
  • Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, et al. 2000. “Gene Ontology: Tool for the Unification of Biology. The Gene Ontology Consortium.” Nature Genetics 25 (1): 25–29. doi:10.1038/75556.
  • Bachelet-Violette, L., A. K. A. Silva, M. Maire, A. Michel, O. Brinza, P. Ou, V. Ollivier, et al. 2014. “Strong and Specific Interaction of Ultra Small Superparamagnetic Iron Oxide Nanoparticles and Human Activated Platelets Mediated by Fucoidan Coating.” RSC Advances 4 (10): 4864–4871. doi:10.1039/c3ra46757k.
  • Baker, T. J., C. R. Tyler, and T. S. Galloway. 2014. “Impacts of Metal and Metal Oxide Nanoparticles on Marine Organisms.” Environmental Pollution (Barking, Essex : 1987) 186: 257–271. doi:10.1016/j.envpol.2013.11.014.
  • Baltaci, A. K., and K. Yuce. 2018. “Zinc Transporter Proteins.” Neurochemical Research 43 (3): 517–530. doi:10.1007/s11064-017-2454-y.
  • Bardou, P., J. Mariette, F. Escudié, C. Djemiel, and C. Klopp. 2014. “Jvenn: An Interactive Venn Diagram Viewer.” BMC Bioinformatics 15: 293doi:10.1186/1471-2105-15-293.
  • Blinova, I., A. Ivask, M. Heinlaan, M. Mortimer, and A. Kahru. 2010. “Ecotoxicity of Nanoparticles of CuO and ZnO in Natural water.” Environ. Pollut 158 (1): 41–47. doi:10.1016/j.envpol.2009.08.017.
  • Bondarenko, O., K. Juganson, A. Ivask, K. Kasemets, M. Mortimer, and A. Kahru. 2013. “Toxicity of Ag, CuO and ZnO Nanoparticles to Selected Environmentally Relevant Test Organisms and Mammalian Cells In Vitro: A Critical Review.” Archives of Toxicology 87 (7): 1181–1200. doi:10.1007/s00204-013-1079-4.
  • Brayner, R., A. Couté, J. Livage, C. Perrette, and C. Sicard. 2011. “Micro-Algal Biosensors.” Analytical and Bioanalytical Chemistry 401 (2): 581–597. doi:10.1007/s00216-011-5107-z.
  • Bundschuh, M., J. Filser, S. Lüderwald, M. S. McKee, G. Metreveli, G. E. Schaumann, R. Schulz, and S. Wagner. 2018. “Nanoparticles in the Environment: Where Do we Come from, Where Do we Go to?” Environmental Sciences Europe 30 (1): 6. doi:10.1186/s12302-018-0132-6.
  • Canesi, L., and I. Corsi. 2016. “Effects of Nanomaterials on Marine Invertebrates.” The Science of the Total Environment 565: 933–940. doi:10.1016/j.scitotenv.2016.01.085.
  • Carballeira, C.,. J. Ramos-Gómez, L. Martín-Díaz, and T. A. DelValls. 2012. “Identification of Specific Malformations of Sea Urchin Larvae for Toxicity Assessment: Application to Marine Pisciculture Effluents.” Marine Environmental Research 77: 12–22. doi:10.1016/j.marenvres.2012.01.001.
  • Châtel, A., and C. Mouneyrac. 2017. “Signaling Pathways Involved in Metal-Based Nanomaterial Toxicity Towards Aquatic Organisms.” Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP 196: 61–70. doi:10.1016/j.cbpc.2017.03.014.
  • Chen, F., Z. Xiao, L. Yue, J. Wang, Y. Feng, X. Zhu, Z. Wang, and B. Xing. 2019. “Algae Response to Engineered Nanoparticles: Current Understanding, Mechanisms and Implications.” Environmental Science: Nano 6 (4): 1026–1042.
  • Chiu, M.-H., Z. A. Khan, S. G. Garcia, A. D. Le, A. Kagiri, J. Ramos, S.-M. Tsai, et al. 2017. “Effect of Engineered Nanoparticles on Exopolymeric Substances Release from Marine Phytoplankton.” Nanoscale Research Letters 12 (1): 620. doi:10.1186/s11671-017-2397-x.
  • Coffman, J. A., and E. H. Davidson. 2001. “ Oral-Aboral Axis Specification in the Sea Urchin Embryo. I. Axis Entrainment by Respiratory Asymmetry.” Dev. Biol 230 (1): 18–28. doi:10.1006/dbio.2000.9996.
  • Covian-Nares, J. F., R. M. Smith, and S. S. Vogel. 2008. “Two Independent Forms of Endocytosis Maintain Embryonic Cell Surface Homeostasis during Early Development.” Developmental Biology 316 (1): 135–148. doi:10.1016/j.ydbio.2008.01.017.
  • Crawford, B. J., and R. D. Burke. 2004. “TEM and SEM Methods.” In Methods in Cell Biology, 411–441. Academic Press.
  • Cuvelier, M. L., J. Guo, A. C. Ortiz, M. J. van Baren, M. A. Tariq, F. Partensky, and A. Z. Worden. 2017. “Responses of the Picoprasinophyte Micromonas Commoda to Light and Ultraviolet Stress.” PloS One 12 (3): e0172135doi:10.1371/journal.pone.0172135.
  • Derelle, E., C. Ferraz, M.-L. Escande, S. Eychenié, R. Cooke, G. Piganeau, Y. Desdevises, L. Bellec, H. Moreau, and N. Grimsley. 2008. “ Life-Cycle and Genome of OtV5, a Large DNA Virus of the Pelagic Marine Unicellular Green Alga Ostreococcus tauri.” PloS One 3 (5): e2250doi:10.1371/journal.pone.0002250.
  • Exbrayat, J.-M., E. N. Moudilou, and E. Lapied. 2015. “Harmful Effects of Nanoparticles on Animals [Online].” Journal of Nanotechnology 2015: 1–10. Available from: https://www.hindawi.com/journals/jnt/2015/861092/. [Accessed 12 Mar 2020]. doi:10.1155/2015/861092.
  • Fairbairn, E. A., A. A. Keller, L. Mädler, D. Zhou, S. Pokhrel, and G. N. Cherr. 2011. “Metal Oxide Nanomaterials in Seawater: Linking Physicochemical Characteristics with Biological Response in Sea Urchin Development.” J. Hazard. Mater 192 (3): 1565–1571. doi:10.1016/j.jhazmat.2011.06.080.
  • Franklin, N. M., N. J. Rogers, S. C. Apte, G. E. Batley, G. E. Gadd, and P. S. Casey. 2007. “Comparative Toxicity of Nanoparticulate ZnO, Bulk ZnO, and ZnCl2 to a Freshwater Microalga (Pseudokirchneriella subcapitata): the Importance of Particle Solubility.” Environmental Science & Technology 41 (24): 8484–8490. doi:10.1021/es071445r.
  • Gambardella, C., S. Ferrando, A. M. Gatti, E. Cataldi, P. Ramoino, M. G. Aluigi, M. Faimali, A. Diaspro, and C. Falugi. 2016. “Review: Morphofunctional and Biochemical Markers of Stress in Sea Urchin Life Stages Exposed to Engineered Nanoparticles.” Environmental Toxicology 31 (11): 1552–1562. doi:10.1002/tox.22159.
  • George, S., S. Pokhrel, T. Xia, B. Gilbert, Z. Ji, M. Schowalter, A. Rosenauer, et al. 2010. “Use of a Rapid Cytotoxicity Screening Approach to Engineer a Safer Zinc Oxide Nanoparticle through Iron Doping.” ACS Nano 4 (1): 15–29. doi:10.1021/nn901503q.
  • Gottschalk, F., C. Lassen, J. Kjoelholt, F. Christensen, and B. Nowack. 2015. “Modeling Flows and Concentrations of Nine Engineered Nanomaterials in the Danish Environment.” International Journal of Environmental Research and Public Health 12 (5): 5581–5602. doi:10.3390/ijerph120505581.
  • Gottschalk, F., T. Sun, and B. Nowack. 2013. “Environmental Concentrations of Engineered Nanomaterials: Review of Modeling and Analytical Studies.” Environmental Pollution (Barking, Essex : 1987), 181: 287–300. doi:10.1016/j.envpol.2013.06.003.
  • Guillard, R. R. L., and P. E. Hargraves. 1993. “Stichochrysis Immobilis is a Diatom, Not a Chrysophyte.” Phycologia 32 (3): 234–236. doi:10.2216/i0031-8884-32-3-234.1.
  • Hanssen, K. Ø., J. H. Andersen, T. Stiberg, R. A. Engh, J. Svenson, A.-M. Genevière, and E. Hansen. 2012. “Antitumoral and Mechanistic Studies of Ianthelline Isolated from the Arctic Sponge Stryphnus Fortis.” Anticancer Research 32 (10): 4287–4297.
  • Heinlaan, M., A. Ivask, I. Blinova, H.-C. Dubourguier, and A. Kahru. 2008. “Toxicity of Nanosized and Bulk ZnO, CuO and TiO2 to Bacteria Vibrio fischeri and Crustaceans Daphnia Magna and Thamnocephalus Platyurus.” Chemosphere 71 (7): 1308–1316. doi:10.1016/j.chemosphere.2007.11.047.
  • Hou, J., Y. Wu, X. Li, B. Wei, S. Li, and X. Wang. 2018. “Toxic Effects of Different Types of Zinc Oxide Nanoparticles on Algae, Plants, Invertebrates, Vertebrates and Microorganisms.” Chemosphere 193: 852–860. doi:10.1016/j.chemosphere.2017.11.077.
  • Huang, K., D. R. Diener, A. Mitchell, G. J. Pazour, G. B. Witman, and J. L. Rosenbaum. 2007. “Function and Dynamics of PKD2 in Chlamydomonas reinhardtii Flagella.” The Journal of Cell Biology 179 (3): 501–514. doi:10.1083/jcb.200704069.
  • Kadar, E., F. Simmance, O. Martin, N. Voulvoulis, S. Widdicombe, S. Mitov, J. R. Lead, and J. W. Readman. 2010. “The Influence of Engineered Fe(2)O(3) Nanoparticles and Soluble (FeCl(3)) Iron on the Developmental Toxicity Caused by CO(2)-Induced Seawater Acidification.” Environmental Pollution (Barking, Essex : 1987) 158 (12): 3490–3497. doi:10.1016/j.envpol.2010.03.025.
  • Kanehisa, M., M. Araki, S. Goto, M. Hattori, M. Hirakawa, M. Itoh, T. Katayama, et al. 2008. “KEGG for Linking Genomes to Life and the Environment.” Nucleic Acids Research 36 (Database issue): D480–484. doi:10.1093/nar/gkm882.
  • Kanehisa, M., S. Goto, M. Hattori, K. F. Aoki-Kinoshita, M. Itoh, S. Kawashima, T. Katayama, M. Araki, and M. Hirakawa. 2006. “From Genomics to Chemical Genomics: New Developments in KEGG.” Nucleic Acids Research 34 (Database issue): D354–357. doi:10.1093/nar/gkj102.
  • Keller, A. A., and A. Lazareva. 2014. “Predicted Releases of Engineered Nanomaterials: From Global to Regional to Local.” Environmental Science & Technology Letters 1 (1): 65–70. doi:10.1021/ez400106t.
  • Keller, A. A., H. Wang, D. Zhou, H. S. Lenihan, G. Cherr, B. J. Cardinale, R. Miller, and Z. Ji. 2010. “Stability and Aggregation of Metal Oxide Nanoparticles in Natural Aqueous Matrices.” Environmental Science & Technology 44 (6): 1962–1967. doi:10.1021/es902987d.
  • Kim, R.-O., J. S. Choi, B.-C. Kim, and W.-K. Kim. 2017. “Comparative Analysis of Transcriptional Profile Changes in Larval Zebrafish Exposed to Zinc Oxide Nanoparticles and Zinc Sulfate.” Bulletin of Environmental Contamination and Toxicology 98 (2): 183–189. doi:10.1007/s00128-016-1995-0.
  • Klimova, E. M., A. I. Bozhkov, E. A. Bychenko, E. V. Lavinskaya, N. M. Zholobak, and A. M. Korobov. 2019. “Characteristics of the Response of the Microalga (Dunaliella Viridis) to Cerium Compounds in Culture.” Biosystems Diversity 27 (2): 142–147. doi:10.15421/011919.
  • Landa, P., R. Vankova, J. Andrlova, J. Hodek, P. Marsik, H. Storchova, J. C. White, and T. Vanek. 2012. “Nanoparticle-Specific Changes in Arabidopsis thaliana Gene Expression after Exposure to ZnO, TiO2, and Fullerene Soot.” Journal of Hazardous Materials 241-242: 55–62. doi:10.1016/j.jhazmat.2012.08.059.
  • Lead, J. R., G. E. Batley, P. J. J. Alvarez, M.-N. Croteau, R. D. Handy, M. J. McLaughlin, J. D. Judy, and K. Schirmer. 2018. “Nanomaterials in the Environment: Behavior, Fate, Bioavailability, and Effects – An Updated Review.” Environmental Toxicology and Chemistry 37 (8): 2029–2063. doi:10.1002/etc.4147.
  • Levy, M., N. Luciani, D. Alloyeau, D. Elgrabli, V. Deveaux, C. Pechoux, S. Chat, et al. 2011. “Long Term in Vivo Biotransformation of Iron Oxide Nanoparticles.” Biomaterials 32 (16): 3988–3999. doi:10.1016/j.biomaterials.2011.02.031.
  • Lewinski, N., V. Colvin, and R. Drezek. 2008. “Cytotoxicity of Nanoparticles.” Small (Weinheim an Der Bergstrasse, Germany) 4 (1): 26–49. doi:10.1002/smll.200700595.
  • Ma, H., P. M. Bertsch, T. C. Glenn, N. J. Kabengi, and P. L. Williams. 2009. “Toxicity of Manufactured Zinc Oxide Nanoparticles in the Nematode Caenorhabditis elegans.” Environmental Toxicology and Chemistry 28 (6): 1324–1330. doi:10.1897/08-262.1.
  • Ma, H., P. L. Williams, and S. A. Diamond. 2013. “Ecotoxicity of Manufactured ZnO Nanoparticles – A Review.” Environmental Pollution (Barking, Essex: 1987) 172: 76–85. doi:10.1016/j.envpol.2012.08.011.
  • Magro, M.,. G. Sinigaglia, L. Nodari, J. Tucek, K. Polakova, Z. Marusak, S. Cardillo, et al. 2012. “Charge Binding of Rhodamine Derivative to OH-Stabilized Nanomaghemite: Universal Nanocarrier for Construction of Magnetofluorescent Biosensors.” Acta Biomaterialia 8 (6): 2068–2076. doi:10.1016/j.actbio.2012.02.005.
  • Majedi, S. M., H. K. Lee, and B. C. Kelly. 2012. “Chemometric Analytical Approach for the Cloud Point Extraction and Inductively Coupled Plasma Mass Spectrometric Determination of Zinc Oxide Nanoparticles in Water Samples.” Analytical Chemistry 84 (15): 6546–6552. doi:10.1021/ac300833t.
  • Manzo, S., M. L. Miglietta, G. Rametta, S. Buono, and G. Di Francia. 2013. “Embryotoxicity and Spermiotoxicity of Nanosized ZnO for Mediterranean Sea Urchin Paracentrotus Lividus.” Journal of Hazardous Materials 254-255: 1–9. doi:10.1016/j.jhazmat.2013.03.027.
  • Marcus, M.,. M. Karni, K. Baranes, I. Levy, N. Alon, S. Margel, and O. Shefi. 2016. “Iron Oxide Nanoparticles for Neuronal Cell Applications: Uptake Study and Magnetic Manipulations.” Journal of Nanobiotechnology 14 (1):37. doi:10.1186/s12951-016-0190-0.
  • Marisa, I., V. Matozzo, M. Munari, A. Binelli, M. Parolini, A. Martucci, E. Franceschinis, N. Brianese, and M. G. Marin. 2016. “In Vivo Exposure of the Marine Clam Ruditapes Philippinarum to Zinc Oxide Nanoparticles: responses in Gills, Digestive Gland and Haemolymph.” Environmental Science and Pollution Research International 23 (15): 15275–15293. doi:10.1007/s11356-016-6690-5.
  • Marrone, V., M. Piscopo, G. Romano, A. Ianora, A. Palumbo, and M. Costantini. 2012. “Defensome against Toxic Diatom Aldehydes in the Sea Urchin Paracentrotus Lividus.” PloS One 7 (2): e31750doi:10.1371/journal.pone.0031750.
  • Massart, R. 1981. “Preparation of Aqueous Magnetic Liquids in Alkaline and Acidic Media.” IEEE Transactions on Magnetics 17 (2): 1247–1248. doi:10.1109/TMAG.1981.1061188.
  • Migliaccio, O., I. Castellano, G. Romano, and A. Palumbo. 2014. “Stress Response to Cadmium and Manganese in Paracentrotus Lividus Developing Embryos is Mediated by Nitric Oxide.” Aquat. Toxicol 156: 125–134. doi:10.1016/j.aquatox.2014.08.007.
  • Miller, R. J., H. S. Lenihan, E. B. Muller, N. Tseng, S. K. Hanna, and A. A. Keller. 2010. “Impacts of Metal Oxide Nanoparticles on Marine Phytoplankton.” Environmental Science & Technology 44 (19): 7329–7334. doi:10.1021/es100247x.
  • Mitchell, D. R. 2007. “The Evolution of Eukaryotic Cilia and Flagella as Motile and Sensory Organelles.” Advances in Experimental Medicine and Biology 607: 130–140. doi:10.1007/978-0-387-74021-8_11.
  • Montané, M.-H., and K. Kloppstech. 2000. “The Family of Light-Harvesting-Related Proteins (LHCs, ELIPs, HLIPs): Was the Harvesting of Light Their Primary Function?.” Gene 258 (1-2): 1–8. doi:10.1016/S0378-1119(00)00413-3.
  • Montané, M.-H., B. Petzold, and K. Kloppstech. 1999. “Formation of Early-Light-Inducible-Protein Complexes and Status of Xanthophyll Levels under High Light and Cold Stress in Barley (Hordeum Vulgare L.).” Planta 208 (4): 519–527. doi:10.1007/s004250050589.
  • von Moos, N., and V. I. Slaveykova. 2014. “Oxidative Stress Induced by Inorganic Nanoparticles in Bacteria and Aquatic Microalgae-State of the Art and Knowledge Gaps.” Nanotoxicology 8 (6): 605–630. doi:10.3109/17435390.2013.809810.
  • Morelli, E., E. Gabellieri, A. Bonomini, D. Tognotti, G. Grassi, and I. Corsi. 2018. “TiO2 Nanoparticles in Seawater: Aggregation and Interactions with the Green Alga Dunaliella tertiolecta.” Ecotoxicology and Environmental Safety 148: 184–193. doi:10.1016/j.ecoenv.2017.10.024.
  • Mukherjee, K., and K. Acharya. 2018. “Toxicological Effect of Metal Oxide Nanoparticles on Soil and Aquatic Habitats.” Archives of Environmental Contamination and Toxicology 75 (2): 175–186. doi:10.1007/s00244-018-0519-9.
  • Oliviero, M., S. Schiavo, G. Rametta, M. L. Miglietta, and S. Manzo. 2017. “Different Sizes of ZnO Diversely Affected the Cytogenesis of the Sea Urchin Paracentrotus Lividus.” The Science of the Total Environment 607-608: 176–183. doi:10.1016/j.scitotenv.2017.07.038.
  • Park, H.-G., and M.-K. Yeo. 2015. “Comparison of Gene Expression Patterns from Zebrafish Embryos between Pure Silver Nanomaterial and Mixed Silver Nanomaterial Containing Cells of Hydra Magnipapillata.” Molecular & Cellular Toxicology 11 (3): 307–314. doi:10.1007/s13273-015-0030-6.
  • Piticharoenphun, S., L. Šiller, M.-L. Lemloh, M. Salome, M. Cotte, B. Kaulich, A. Gianoncelli, et al. 2012. “Agglomeration of Silver Nanoparticles in Sea Urchin.” International Journal of Environmental Pollution and Remediation 1(1): 46–52 doi:10.11159/ijepr.2012.007.
  • Polak, N., D. S. Read, K. Jurkschat, M. Matzke, F. J. Kelly, D. J. Spurgeon, and S. R. Stürzenbaum. 2014. “Metalloproteins and Phytochelatin Synthase May Confer Protection against Zinc Oxide Nanoparticle Induced Toxicity in Caenorhabditis elegans.” Comparative Biochemistry and Physiology. Toxicology & Pharmacology : CBP 160: 75–85. doi:10.1016/j.cbpc.2013.12.001.
  • Qian, H., K. Zhu, H. Lu, M. Lavoie, S. Chen, Z. Zhou, Z. Deng, J. Chen, and Z. Fu. 2016. “Contrasting Silver Nanoparticle Toxicity and Detoxification Strategies in Microcystis aeruginosa and Chlorella Vulgaris: New Insights from Proteomic and Physiological Analyses.” The Science of the Total Environment 572: 1213–1221. doi:10.1016/j.scitotenv.2016.08.039.
  • Quigg, A., W.-C. Chin, C.-S. Chen, S. Zhang, Y. Jiang, A.-J. Miao, K. A. Schwehr, C. Xu, and P. H. Santschi. 2013. “Direct and Indirect Toxic Effects of Engineered Nanoparticles on Algae: Role of Natural Organic Matter.” ACS Sustainable Chemistry & Engineering 1 (7): 686–702. doi:10.1021/sc400103x.
  • Ragusa, M. A., S. Costa, A. Cuttitta, F. Gianguzza, and A. Nicosia. 2017. “Coexposure to Sulfamethoxazole and Cadmium Impairs Development and Attenuates Transcriptional Response in Sea Urchin Embryo.” Chemosphere 180: 275–284. doi:10.1016/j.chemosphere.2017.04.030.
  • Robinson, M. D., D. J. McCarthy, and G. K. Smyth. 2010. “edgeR: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data.” Bioinformatics (Oxford, England) 26 (1): 139–140. doi:10.1093/bioinformatics/btp616.
  • Roccheri, M. C., M. Agnello, R. Bonaventura, and V. Matranga. 2004. “Cadmium Induces the Expression of Specific Stress Proteins in Sea Urchin Embryos.” Biochemical and Biophysical Research Communications 321 (1): 80–87. doi:10.1016/j.bbrc.2004.06.108.
  • Rocha, T. L., T. Gomes, V. S. Sousa, N. C. Mestre, and M. J. Bebianno. 2015. “Ecotoxicological Impact of Engineered Nanomaterials in Bivalve Molluscs: An Overview.” Marine Environmental Research 111: 74–88. doi:10.1016/j.marenvres.2015.06.013.
  • Roger, J., J. N. Pons, R. Massart, A. Halbreich, and J. C. Bacri. 1999. “Some Biomedical Applications of Ferrofluids.” The European Physical Journal Applied Physics 5 (3): 321–325. doi:10.1051/epjap:1999144.
  • Russo, R.,. R. Bonaventura, and V. Matranga. 2014. “Time- and Dose-Dependent Gene Expression in Sea Urchin Embryos Exposed to UVB.” Marine Environmental Research 93: 85–92. doi:10.1016/j.marenvres.2013.08.006.
  • Satori, C. P., V. Kostal, and E. A. Arriaga. 2011. “Individual Organelle pH Determinations of Magnetically Enriched Endocytic Organelles via Laser-Induced Fluorescence Detection .” Analytical Chemistry 83 (19): 7331–7339. doi:10.1021/ac201196n.
  • Scheibe, R. 2004. “Malate Valves to Balance Cellular Energy Supply.” Physiologia Plantarum 120 (1): 21–26. doi:10.1111/j.0031-9317.2004.0222.x.
  • da Silva B. F., S. Pérez, P. Gardinalli, R. K. Singhal, A. A. Mozeto. and D. Barceló 2011. “Analytical Chemistry of Metallic Nanoparticles in Natural Environments.” TrAC Trends in Analytical Chemistry 30 (3): 528–540. doi:10.1016/j.trac.2011.01.008.
  • Singhal, R. K., J. Preetha, R. Karpe, K. Tirumalesh, S. C. Kumar, and A. G. Hegde. 2006. “The Use of Ultra Filtration in Trace Metal Speciation Studies in Sea Water.” Environment International 32 (2): 224–228. doi:10.1016/j.envint.2005.08.015.
  • Su, G., X. Zhang, J. P. Giesy, J. Musarrat, Q. Saquib, A. A. Alkhedhairy, and H. Yu. 2015. “Comparison on the Molecular Response Profiles between Nano Zinc Oxide (ZnO) Particles and Free Zinc Ion Using a Genome-Wide Toxicogenomics Approach.” Environmental Science and Pollution Research 22 (22): 17434–17442. doi:10.1007/s11356-015-4507-6.
  • Sun, Z., and C. A. Ettensohn. 2017. “TGF-β Sensu Stricto Signaling Regulates Skeletal Morphogenesis in the Sea Urchin Embryo.” Developmental Biology 421 (2): 149–160. doi:10.1016/j.ydbio.2016.12.007.
  • Torres-Duarte, C., A. S. Adeleye, S. Pokhrel, L. Mädler, A. A. Keller, and G. N. Cherr. 2016. “Developmental Effects of Two Different Copper Oxide Nanomaterials in Sea Urchin (Lytechinus Pictus) Embryos.” Nanotoxicology 10 (6): 671–679. doi:10.3109/17435390.2015.1107145.
  • Torres-Duarte, C., K. M. Ramos-Torres, R. Rahimoff, and G. N. Cherr. 2017. “Stage Specific Effects of Soluble Copper and Copper Oxide Nanoparticles during Sea Urchin Embryo Development and Their Relation to Intracellular Copper Uptake.” Aquatic Toxicology (Amsterdam, Netherlands) 189: 134–141. doi:10.1016/j.aquatox.2017.05.008.
  • Trask, B. J., G. J. van den Engh, and J. H. Elgershuizen. 1982. “Analysis of Phytoplankton by Flow Cytometry.” Cytometry 2 (4): 258–264. doi:10.1002/cyto.990020410.
  • Tsiokas, L. 2009. “Function and Regulation of TRPP2 at the Plasma Membrane.” American Journal of Physiology. Renal Physiology 297 (1): F1–9. doi:10.1152/ajprenal.90277.2008.
  • Tualla, I. P. B., and J. G. Bitacura. 2016. “Effects of Cadmium and Zinc on the Gamete Viability, Fertilization, and Embryonic Development of Tripneustes Gratilla (Linnaeus).” Scientifica 2016: 8175213doi:10.1155/2016/8175213.
  • Valdiglesias, V.,. N. Fernández-Bertólez, G. Kiliç, C. Costa, S. Costa, S. Fraga, M. J. Bessa, E. Pásaro, J. P. Teixeira, and B. Laffon. 2016. “Are Iron Oxide Nanoparticles Safe? Current Knowledge and Future Perspectives.” Journal of Trace Elements in Medicine and Biology 38: 53–63. doi:10.1016/j.jtemb.2016.03.017.
  • Wong, S. W. Y., P. T. Y. Leung, A. B. Djurišić, and K. M. Y. Leung. 2010. “Toxicities of Nano Zinc Oxide to Five Marine Organisms: Influences of Aggregate Size and Ion Solubility.” Analytical and Bioanalytical Chemistry 396 (2): 609–618. doi:10.1007/s00216-009-3249-z.
  • Worden, A. Z., J.-H. Lee, T. Mock, P. Rouzé, M. P. Simmons, A. L. Aerts, A. E. Allen, et al. 2009. “Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas.” Science (New York, N.Y.) 324 (5924): 268–272. doi:10.1126/science.1167222.
  • Wu, B., C. Torres-Duarte, B. J. Cole, and G. N. Cherr. 2015. “Copper Oxide and Zinc Oxide Nanomaterials Act as Inhibitors of Multidrug Resistance Transport in Sea Urchin Embryos: their Role as Chemosensitizers.” Environmental Science & Technology 49 (9): 5760–5770. doi:10.1021/acs.est.5b00345.
  • Xia, T., M. Kovochich, M. Liong, L. Mädler, B. Gilbert, H. Shi, J. I. Yeh, J. I. Zink, and A. E. Nel. 2008. “Comparison of the Mechanism of Toxicity of Zinc Oxide and Cerium Oxide Nanoparticles Based on Dissolution and Oxidative Stress Properties.” ACS Nano 2 (10): 2121–2134. doi:10.1021/nn800511k.
  • Yung, M. M. N., S. W. Y. Wong, K. W. H. Kwok, F. Z. Liu, Y. H. Leung, W. T. Chan, X. Y. Li, A. B. Djurišić, and K. M. Y. Leung. 2015. “Salinity-Dependent Toxicities of Zinc Oxide Nanoparticles to the Marine Diatom Thalassiosira Pseudonana.” Aquatic Toxicology (Amsterdam, Netherlands) 165: 31–40. doi:10.1016/j.aquatox.2015.05.015.
  • Zhao, X., S. Wang, Y. Wu, H. You, and L. Lv. 2013. “Acute ZnO Nanoparticles Exposure Induces Developmental Toxicity, Oxidative Stress and DNA Damage in Embryo-Larval Zebrafish.” Aquatic Toxicology (Amsterdam, Netherlands) 136-137: 49–59. doi:10.1016/j.aquatox.2013.03.019.
  • Zhou, C., Y. Carotenuto, V. Vitiello, C. Wu, J. Zhang, and I. Buttino. 2018. “De Novo Transcriptome Assembly and Differential Gene Expression Analysis of the Calanoid Copepod Acartia Tonsa Exposed to Nickel Nanoparticles.” Chemosphere 209: 163–172. doi:10.1016/j.chemosphere.2018.06.096.

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