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Article

Gold nanoparticles ingested by oyster larvae are internalized by cells through an alimentary endocytic pathway

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Pages 901-913 | Received 03 May 2018, Accepted 07 Jun 2018, Published online: 11 Jul 2018

References

  • Albanese, A., P. S. Tang, and W. C. W. Chan. 2012. “The Effect of Nanoparticle Size, Shape, and Surface Chemistry on Biological Systems.” Annual Review of Biomedical Engineering 14 (1): 1–16. doi:10.1146/annurev-bioeng-071811-150124.
  • Ambrosone, A., V. Marchesano, V. Mazzarella, and C. Tortiglione. 2014. “Nanotoxicology Using the Sea Anemone Nematostella vectensis: From Developmental Toxicity to Genotoxicology.” Nanotoxicology 8 (5): 508–520. doi:10.3109/17435390.2013.802386.
  • Baalousha, M., G. Cornelis, T.A.J. Kuhlbusch, I. Lynch, C. Nickel, W. Peijnenburg, and N. W. Van Den Brink. 2016. “Modeling Nanomaterial Fate and Uptake in the Environment: Current Knowledge and Future Trends.” Environmental Science: Nano 3 (2): 323–345. doi:10.1039/C5EN00207A.
  • Baker, T. J., C. R. Tyler, and T. S. Galloway. 2014. “Impacts of Metal and Metal Oxide Nanoparticles on Marine Organisms.” Environmental Pollution 186: 257–271. doi:10.1016/j.envpol.2013.11.014.
  • Bayne, B. L. 2017. “Reproduction.” Chap. 9 in Biology of Oysters, edited by B. Bayne, 565–701. San Diego, CA: Elsevier.
  • Canton, I., and G. Battaglia. 2012. “Endocytosis at the Nanoscale.” Chemical Society Reviews 41 (7): 2718–2739.
  • Domouhtsidou, G. P., and V. K. Dimitriadis. 2000. “Ultrastructural Localization of Heavy Metals (Hg, Ag, Pb, and Cu) in Gills and Digestive Gland of Mussels, Mytilus galloprovincialis (L.).” Archives of Environmental Contamination and Toxicology 38 (4): 472–478. doi:10.1039/c2cs15309b.
  • Douillet, P. 1993. “Bacterivory in Pacific oyster Crassostrea gigas larvae”. Marine Ecology Progress Series 98: 123–134.
  • Elston, R. 1980a. “Functional Anatomy, Histology and Ultrastructure of the Soft Tissues of the Larval American Oyster, Crassostrea virginica.” Proceedings of the National Shellfisheries Association 70: 65–93.
  • Elston, R. 1980b. “Functional Morphology of the Coelomocytes of the Larval Oysters (Crassostrea virginica and Crassostrea gigas).” Journal of the Marine Biological Association of the United Kingdom 60: 947–957. doi:10.1017/S0025315400042004.
  • Etxeberria, M., M. P. Cajaraville, and I. Marigomez. 1995. “Changes in Digestive Cell Lysosomal Structure in Mussels as Biomarkers of Environmental Stress in the Urdaibai Estuary (Biscay Coast, Iberian Peninsula).” Marine Pollution Bulletin 30 (9): 599–603. doi:10.1016/0025-326X(94)00248-8.
  • Gallager, S. M. 1988. “Visual Observations of Particle Manipulation during Feeding in Larvae of a Bivalve Mollusc.” Bulletin of Marine Science 43: 344–365.
  • Galtsoff, P. 1964. “Larval Development and Metamorphosis.” Chap. 16 in The American oyster, Crassostrea virginica Gmelin, 355–380. Washington, USA: Fishery Bulletin of the U.S. Fish Wildlife Service–4.
  • Hou, W.-C., P. Westerhoff, and J. D. Posner. 2013. “Biological Accumulation of Engineered Nanomaterials: A Review of Current Knowledge.” Environmental Science: Processes and Impacts 15 (1): 103–122. doi:10.1039/C2EM30686G.
  • Hull, M. S., P. Chaurand, J. Rose, M. Auffan, J.-Y. Bottero, J. C. Jones, I. R. Schultz, and P. J. Vikesland. 2011. “Filter-Feeding Bivalves Store and Biodeposit Colloidally Stable Gold Nanoparticles.” Environmental Science & Technology 45 (15): 6592–6599. doi:10.1021/es200809c.
  • Joubert, Y., J.-F. Pan, P.-E. Buffet, P. Pilet, D. Gilliland, E. Valsami-Jones, C. Mouneyrac, and C. Amiard-Triquet. 2013. “Subcellular Localization of Gold Nanoparticles in the Estuarine Bivalve Scrobicularia plana after Exposure through the Water.” Gold Bulletin 46 (1): 47–56.
  • Kadar, E., F. Simmance, O. Martin, N. Voulvoulis, S. Widdicombe, S. Mitov, J. R. Lead, and J. W. Readman. 2010. “The Influence of Engineered Fe2O3 Nanoparticles and Soluble (FeCl3) Iron on the Developmental Toxicity Caused by CO2-Induced Seawater Acidification.” Environmental Pollution 158 (12): 3490–3497. doi:10.1016/j.envpol.2010.03.025.
  • Kettler, K., K. Veltman, D. Van De Meent, A. Van Wezel, and A. J. Hendriks. 2014. “Cellular Uptake of Nanoparticles as Determined by Particle Properties, Experimental Conditions, and Cell Type.” Environmental Toxicology and Chemistry 33 (3): 481–492. doi:10.1002/etc.2470.
  • Koehler, A., U. Marx, K. Broeg, S. Bahns, and J. Bressling. 2008. “Effects of Nanoparticles in Mytilus edulis Gills and Hepatopancreas – A New Threat to Marine Life?” Marine Environmental Research 66 (1): 12–14. doi:10.1016/j.marenvres.2008.02.009.
  • Kwok, K. W. H., M. Auffan, A. R. Badireddy, C. M. Nelson, M. R. Wiesner, A. Chilkoti, J. Liu, S. M. Marinakos, and D. E. Hinton. 2012. “Uptake of Silver Nanoparticles and Toxicity to Early Life Stages of Japanese Medaka (Oryzias latipes): Effect of Coating Materials.” Aquatic Toxicology 120–121: 59–66. doi:10.1016/j.aquatox.2012.04.012.
  • Leverett D, T. J. 2013. “Oyster Embryo-Larval Bioassay (Revised).” ICES Techniques in Marine Environmental Sciences No (54): 34.
  • Ma, S., and D. Lin. 2013. “The Biophysicochemical Interactions at the Interfaces between Nanoparticles and Aquatic Organisms: Adsorption and Internalization.” Environmental Science: Processes and Impacts 15 (1): 145–160. doi:10.1039/C2EM30637A.
  • Magesky, A., CaO. Ribeiro, and É. Pelletier. 2016. “Physiological Effects and Cellular Responses of Metamorphic Larvae and Juveniles of Sea Urchin Exposed to Ionic and Nanoparticulate Silver.” Aquatic Toxicology (Amsterdam, Netherlands) 174: 208–227. doi:10.1016/j.aquatox.2016.02.018.
  • Marchesano, V., Y. Hernandez, W. Salvenmoser, A. Ambrosone, A. Tino, B. Hobmayer, J. M De La Fuente, and C. Tortiglione. 2013. “Imaging Inward and Outward Trafficking of Gold Nanoparticles in Whole Animals.” ACS Nano 7 (3): 2431–2442. doi:10.1021/nn305747e.
  • Marigómez, I., A. Orbea, I. Olabarrieta, M. Etxeberria, and M. P. Cajaraville. 1996. “Structural Changes in the Digestive Lysosomal System of Sentinel Mussels as Biomarkers of Environmental Stress in Mussel-Watch Programmes.” Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 113 (2): 291–297. doi:10.1016/0742-8413(95)02100-0.
  • Meyer, J. N., C. A. Lord, X. Y. Yang, E. A. Turner, A. R. Badireddy, S. M. Marinakos, A. Chilkoti, M. R. Wiesner, and M. Auffan. 2010. “Intracellular Uptake and Associated Toxicity of Silver Nanoparticles in Caenorhabditis elegans.” Aquatic Toxicology 100 (2): 140–150. doi:10.1016/j.aquatox.2010.07.016.
  • Millar, R. H. 1955. “Notes on the Mechanism of Food Movement in the Gut of the Larval Oyster, Ostrea edulis.” Quarterly Journal of Microscopical Science 96: 539–544.
  • Moore, M. N., A. Viarengo, P. Donkin, and A. J. S. Hawkins. 2007. “Autophagic and Lysosomal Reactions to Stress in the Hepatopancreas of Blue Mussels.” Aquatic Toxicology 84 (1): 80–91. doi:10.1016/j.aquatox.2007.06.007.
  • Noventa, S., C. Hacker, D. Rowe, C. Elgy, and T. Galloway. 2018a. “Dissolution and Bandgap Paradigms for Predicting the Toxicity of Metal Oxide Nanoparticles in the Marine Environment: An in Vivo Study with Oyster Embryos.” Nanotoxicology 12 (1): 63–78.
  • Noventa, S., D. Rowe, and T. Galloway. 2018b. “Mitigating Effect of Organic Matter on the in vivo Toxicity of Metal Oxide Nanoparticles in the Marine Environment.” Environmental Science: Nano. doi:10.1039/C8EN00175H.
  • Nowack, B. 2017. “Evaluation of Environmental Exposure Models for Engineered Nanomaterials in a Regulatory Context.” NanoImpact 8: 38–47.
  • Owen, G. 1970. “The Fine Structure of the Digestive Tubules of the Marine Bivalve Cardium edule.” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 258 (822): 245–260.
  • Owen, G. 1972. “Lysosomes, Peroxisomes and Bivalves.” Science Progress 60 (239): 299–318.
  • Peijnenburg, W. J. G. M., M. Baalousha, J. Chen, Q. Chaudry, F. Von Der Kammer, T.A.J. Kuhlbusch, J. Lead, et al. 2015. “A Review of the Properties and Processes Determining the Fate of Engineered Nanomaterials in the Aquatic Environment.” Critical Reviews in Environmental Science and Technology 45 (19): 2084–2134.
  • Renault, S., M. Baudrimont, N. Mesmer-Dudons, P. Gonzalez, S. Mornet, and A. Brisson. 2008. “Impacts of Gold Nanoparticle Exposure on Two Freshwater Species: A Phytoplanktonic Alga (Scenedesmus subspicatus) and a Benthic Bivalve (Corbicula fluminea).” Gold Bulletin 41 (2): 116–126.
  • Ringwood, A. H., N. Levi-Polyachenko, and D. L. Carroll. 2009. “Fullerene Exposures with Oysters: Embryonic, Adult, and Cellular Responses.” Environmental Science and Technology 43 (18): 7136–7141.
  • Ringwood, A. H., M. Mccarthy, T. C. Bates, and D. L. Carroll. 2010. “The Effects of Silver Nanoparticles on Oyster Embryos.” Marine Environmental Research 69: S49–S51.
  • Rocha, T. L., S. M. T. Sabóia-Morais, and M. J. Bebianno. 2016. “Histopathological Assessment and Inflammatory Response in the Digestive Gland of Marine Mussel Mytilus galloprovincialis Exposed to Cadmium-Based Quantum Dots.” Aquatic Toxicology 177: 306–315.
  • Schultz, C., K. Powell, A. Crossley, K. Jurkschat, P. Kille, A. J. Morgan, D. Read, et al. 2015. “Analytical Approaches to Support Current Understanding of Exposure, Uptake and Distributions of Engineered Nanoparticles by Aquatic and Terrestrial Organisms.” Ecotoxicology 24 (2): 239–261.
  • Selck, H., R. D. Handy, T. F. Fernandes, S. J. Klaine, and E. J. Petersen. 2016. “Nanomaterials in the Aquatic Environment: An EU-USA Perspective on the Status of Ecotoxicity Testing, Research Priorities and Challenges Ahead.” Environmental Toxicology and Chemistry 35 (5): 1055–1067.
  • Unrine, J. M., O. V. Tsyusko, S. E. Hunyadi, J. D. Judy, and P. M. Bertsch. 2010. “Effects of Particle Size on Chemical Speciation and Bioavailability of Copper to Earthworms (Eisenia fetida) Exposed to Copper Nanoparticles.” Journal of Environmental Quality 39: 1942–1953.
  • Waller, T. R. 1981. “Functional Morphology and Development of Veliger Larvae of the European Oyster, Ostrea edulis Linné.” Washington, USA: Smithsonian Institution Press.
  • Wikfors, G. H., and R. M. Smolowitz. 1995. “Experimental and Histological Studies of Four Life-History Stages of the Eastern Oyster, Crassostrea virginica, Exposed to a Cultured Strain of the Dinoflagellate Prorocentrum minimum.” The Biological Bulletin 188 (3): 313–328.
  • Wray, A. T., and S. J. Klaine. 2015. “Modeling the Influence of Physicochemical Properties on Gold Nanoparticle Uptake and Elimination by Daphnia magna.” Environmental Toxicology and Chemistry 34 (4): 860–872.
  • Yonge, C. M. 1926a. “XV.—the Digestive Diverticula in the Lamellibranchs.” Transactions of the Royal Society of Edinburgh 54 (03): 703–718.
  • Yonge, C. M. 1926b. “Structure and Physiology of the Organs of Feeding and Digestion in Ostrea edulis.” Journal of the Marine Biological Association of the United Kingdom 14 (02): 295–386.
  • Yonge, C. M. 1931. “Digestive Processes in Marine Invertebrates and Fishes.” J. du Conseil Internat. pour L'Explor. de La Mer 6 (2): 175–212.
  • Zhang, S., H. Gao, and G. Bao. 2015. “Physical Principles of Nanoparticle Cellular Endocytosis.” ACS Nano 9 (9): 8655–8671.