Polystyrene nanoplastics exposure caused defective neural tube morphogenesis through caveolae-mediated endocytosis and faulty apoptosis

References

• Andrady, A. L. 2011. “Microplastics in the Marine Environment.” Marine Pollution Bulletin 62: 1596–1605. doi:10.1016/j.marpolbul.2011.05.030.
   PubMed Web of Science ®Google Scholar
• Browne, M. A., T. Galloway, and R. Thompson. 2007. “Microplastic–An Emerging Contaminant of Potential Concern?” Integrated Environmental Assessment and Management 3: 559–561. doi:10.1002/ieam.5630030412.
   PubMed Web of Science ®Google Scholar
• Burek, M. J., and R. W. Oppenheim. 1999. “Cellular Interactions that Regulate Programmed Cell Death in the Developing Vertebrate Nervous System.” In Cell Death and Diseases of the Nervous System, 145–179. Springer.
   Google Scholar
• Carbery, M., W. O’Connor, and T. Palanisami. 2018. “Trophic Transfer of Microplastics and Mixed Contaminants in the Marine Food Web and Implications for Human Health.” Environment International 115: 400–409. doi:10.1016/j.envint.2018.03.007.
   PubMed Web of Science ®Google Scholar
• Cartwright, L., M. S. Poulsen, H. M. Nielsen, G. Pojana, L. E. Knudsen, M. Saunders, and E. Rytting. 2012. “In Vitro Placental Model Optimization for Nanoparticle Transport Studies.” International Journal of Nanomedicine 7: 497–510.
   PubMed Web of Science ®Google Scholar
• Cecconi, F., M. Piacentini, and G. Fimia. 2008. “The Involvement of Cell Death and Survival in Neural Tube Defects: A Distinct Role for Apoptosis and Autophagy?” Cell Death & Differentiation 15: 1170–1177. doi:10.1038/cdd.2008.64.
   PubMed Web of Science ®Google Scholar
• Celá, P., B. Veselá, E. Matalová, Z. Večeřa, and M. Buchtová. 2014. “Embryonic Toxicity of Nanoparticles.” Cells Tissues Organs 199: 1–23. doi:10.1159/000362163.
   PubMed Web of Science ®Google Scholar
• Chae, Y., and Y.-J. An. 2017. “Effects of Micro- and Nanoplastics on Aquatic Ecosystems: Current Research Trends and Perspectives.” Marine Pollution Bulletin 124: 624–632. doi:10.1016/j.marpolbul.2017.01.070.
   PubMed Web of Science ®Google Scholar
• Chapman, S. C., J. Collignon, G. C. Schoenwolf, and A. Lumsden. 2001. “Improved Method for Chick Whole-Embryo Culture Using a Filter Paper Carrier. Developmental Dynamics.” Developmental Dynamics 220 (3): 284–289. doi:10.1002/1097-0177(20010301)220:3<284::AID-DVDY1102>3.0.CO;2-5.
   PubMedGoogle Scholar
• Cheng, X., G. Wang, Z. L. Ma, Y. Y. Chen, J. J. Fan, Z. L. Zhang, K. K. Lee, H. M. Luo, and X. Yang. 2012. “Exposure to 2,5-Hexanedione can Induce Neural Malformations in Chick Embryos.” Neurotoxicology 33: 1239–1247. doi:10.1016/j.neuro.2012.07.005.
   PubMed Web of Science ®Google Scholar
• Chi, H., M. R. Sarkisian, P. Rakic, and R. A. Flavell. 2005. “Loss of Mitogen-activated Protein Kinase Kinase Kinase 4 (MEKK4) Results in Enhanced Apoptosis and Defective Neural Tube Development.” Proceedings of the National Academy of Sciences 102: 3846–3851. doi:10.1073/pnas.0500026102.
   PubMed Web of Science ®Google Scholar
• Cole, M., P. Lindeque, E. Fileman, C. Halsband, and T. S. Galloway. 2015. “The Impact of Polystyrene Microplastics on Feeding, Function and Fecundity in the Marine Copepod Calanus Helgolandicus.” Environmental Science & Technology 49 (2): 1130–1137. doi:10.1021/es504525u.
   PubMed Web of Science ®Google Scholar
• Danopoulos, E., L. C. Jenner, M. Twiddy, and J. M. Rotchell. 2020. “Microplastic Contamination of Seafood Intended for Human Consumption: A Systematic Review and Meta-Analysis.” Environmental Health Perspectives 128 (12): 126002. doi:10.1289/EHP7171.
   PubMed Web of Science ®Google Scholar
• Dawson, A. L., S. Kawaguchi, C. K. King, K. A. Townsend, R. King, W. M. Huston, and S. M. Bengtson Nash. 2018. “Turning Microplastics into Nanoplastics through Digestive Fragmentation by Antarctic Krill.” Nature Communications 9 (1): 1001. doi:10.1038/s41467-018-03465-9.
   PubMedGoogle Scholar
• De Laurenzi, V., C. Di Ilio, V. Graziano, N. Allocati, and B. Favaloro. 2012. “Role of Apoptosis in Disease.” Aging 4: 330–349. doi:10.18632/aging.100459.
   PubMedGoogle Scholar
• De Zio, D., L. Giunta, M. Corvaro, E. Ferraro, and F. Cecconi. 2005. “Expanding Roles of Programmed Cell Death in Mammalian Neurodevelopment.” Seminars in Cell & Developmental Biology 16 (2): 281–294. Elsevier, doi:10.1016/j.semcdb.2004.12.003.
   PubMed Web of Science ®Google Scholar
• Deng, Y., Y. Zhang, B. Lemos, and H. Ren. 2017. “Tissue Accumulation of Microplastics in Mice and Biomarker Responses Suggest Widespread Health Risks of Exposure.” Scientific Reports. 7: 46687. doi:10.1038/srep46687.
   PubMed Web of Science ®Google Scholar
• Diamanti-Kandarakis, E., J.-P. Bourguignon, L. C. Giudice, R. Hauser, G. S. Prins, A. M. Soto, R. T. Zoeller, and A. C. Gore. 2009. “Endocrine-disrupting Chemicals: An Endocrine Society Scientific Statement.” Endocrine Reviews 30: 293–342. doi:10.1210/er.2009-0002.
   PubMed Web of Science ®Google Scholar
• Donnelly-Greenan, E. L., J. T. Harvey, H. M. Nevins, M. M. Hester, and W. A. Walker. 2014. “Prey and Plastic Ingestion of Pacific Northern Fulmars (Fulmarus Glacialis Rogersii) from Monterey Bay, California.” Marine Pollution Bulletin 85: 214–224. doi:10.1016/j.marpolbul.2014.05.046.
   PubMed Web of Science ®Google Scholar
• Eggenschwiler, J. T., and K. V. Anderson. 2000. “Dorsal and Lateral Fates in the Mouse Neural Tube Require the Cell-Autonomous Activity of the Open Brain Gene.” Developmental Biology 227 (2): 648–660. doi:10.1006/dbio.2000.9918.
   PubMed Web of Science ®Google Scholar
• Foroozandeh, P., and A. A. Aziz. 2018. “Insight into Cellular Uptake and Intracellular Trafficking of Nanoparticles.” Nanoscale Research Letters 13: 339. doi:10.1186/s11671-018-2728-6.
   PubMed Web of Science ®Google Scholar
• Fournier, S. B., J. N. D’Errico, D. S. Adler, S. Kollontzi, M. J. Goedken, L. Fabris, E. J. Yurkow, and P. A. Stapleton. 2020. “Nanopolystyrene Translocation and Fetal Deposition after Acute Lung Exposure during Late-Stage Pregnancy.” Particle and Fibre Toxicology 17: 55. doi:10.1186/s12989-020-00385-9.
   PubMed Web of Science ®Google Scholar
• Hamburger, V., and H. L. Hamilton. 1951. “A Series of Normal Stages in the Development of the Chick Embryo.” Journal of Morphology 88: 49–92. doi:10.1002/jmor.1050880104.
   PubMed Web of Science ®Google Scholar
• Hamburger, V., and H. L. Hamilton. 1992. “A Series of Normal Stages in the Development of the Chick Embryo.” Developmental Dynamics 195: 231–272. doi:10.1002/aja.1001950404.
   PubMed Web of Science ®Google Scholar
• Hasanzadeh Kafshgari, M., F. J Harding, and N. H Voelcker. 2015. “Insights into Cellular Uptake of Nanoparticles.” Current Drug Delivery 12: 63–77. doi:10.2174/1567201811666140821110631.
   PubMed Web of Science ®Google Scholar
• Hayat, M. 2017. Autophagy: Cancer, Other Pathologies, Inflammation, Immunity, Infection, and Aging. Vol. 12. Academic Press.
   Google Scholar
• Heerema-McKenney, A. 2018. “Defense and Infection of the Human Placenta.” APMIS: Acta Pathologica, Microbiologica, et Immunologica Scandinavica 126: 570–588. doi:10.1111/apm.12847.
   PubMed Web of Science ®Google Scholar
• Hillaireau, H., and P. Couvreur. 2009. “Nanocarriers’ Entry into the Cell: Relevance to Drug Delivery.” Cellular and Molecular Life Sciences 66: 2873–2896. doi:10.1007/s00018-009-0053-z.
   PubMed Web of Science ®Google Scholar
• Huang, J. P., P. C. Hsieh, C. Y. Chen, T. Y. Wang, P. C. Chen, C. C. Liu, C. C. Chen, and C. P. Chen. 2015. “Nanoparticles Can Cross Mouse Placenta and Induce Trophoblast Apoptosis.” Placenta 36: 1433–1441. doi:10.1016/j.placenta.2015.10.007.
   PubMed Web of Science ®Google Scholar
• Issac, M. N., and B. Kandasubramanian. 2021. “Effect of Microplastics in Water and Aquatic Systems.” Environmental Science and Pollution Research 28 (16): 19544–19562. doi:10.1007/s11356-021-13184-2.
   PubMed Web of Science ®Google Scholar
• Jani, P., G. W. Halbert, J. Langridge, and A. T. Florence. 1990. “Nanoparticle Uptake by the Rat Gastrointestinal Mucosa: Quantitation and Particle Size Dependency.” Journal of Pharmacy and Pharmacology 42: 821–826. doi:10.1111/j.2042-7158.1990.tb07033.x.
   PubMed Web of Science ®Google Scholar
• Jin, Y., J. Xia, Z. Pan, J. Yang, W. Wang, and Z. Fu. 2018. “Polystyrene Microplastics Induce Microbiota Dysbiosis and Inflammation in the Gut of Adult Zebrafish.” Environmental Pollution 235: 322–329. doi:10.1016/j.envpol.2017.12.088.
   PubMed Web of Science ®Google Scholar
• Kaga, S., N. P. Truong, L. Esser, D. Senyschyn, A. Sanyal, R. Sanyal, J. F. Quinn, T. P. Davis, L. M. Kaminskas, and M. R. Whittaker. 2017. “Influence of Size and Shape on the Biodistribution of Nanoparticles Prepared by Polymerization-induced Self-assembly.” Biomacromolecules 18: 3963–3970. doi:10.1021/acs.biomac.7b00995.
   PubMed Web of Science ®Google Scholar
• Karfunkel, P. 1974. “The Mechanisms of Neural Tube Formation.” International Review of Cytology 38: 245–271. doi:10.1016/S0074-7696(08)60927-4.
   Google Scholar
• Keelan, J. A. 2011. “Nanotoxicology: Nanoparticles versus the Placenta.” Nature Nanotechnology 6: 263. doi:10.1038/nnano.2011.65.
   PubMed Web of Science ®Google Scholar
• Knight, R., and G. Melino. 2011. “Cell Death in Disease: From 2010 Onwards.” Cell Death & Disease 2: e202. doi:10.1038/cddis.2011.89.
   PubMed Web of Science ®Google Scholar
• Koelmans, A. A., E. Besseling, and W. J. Shim. 2015. “Nanoplastics in the Aquatic Environment. Critical Review.” In Marine Anthropogenic Litter, edited by M. Bergmann, L. Gutow and M. Klages, 325–340. Cham: Springer International Publishing.
   Google Scholar
• Le, P. U., G. Guay, Y. Altschuler, and I. R. Nabi. 2002. “Caveolin-1 is a Negative Regulator of Caveolae-mediated Endocytosis to the Endoplasmic Reticulum.” Journal of Biological Chemistry 277 (5): 3371–3379. doi:10.1074/jbc.M111240200.
   PubMed Web of Science ®Google Scholar
• Lehner, R., C. Weder, A. Petri-Fink, and B. Rothen-Rutishauser. 2019. “Emergence of Nanoplastic in the Environment and Possible Impact on Human Health.” Environmental Science & Technology 53 (4): 1748–1765. doi:10.1021/acs.est.8b05512.
   PubMed Web of Science ®Google Scholar
• Lei, L., M. Liu, S. Yang, S. Lu, J. Hu, C. Cao, B. Xie, H. Shi, and D. H. J. E. S. Nano. 2018. “Polystyrene (Nano)Microplastics Cause Size-dependent Neurotoxicity, Oxidative Damage and Other Adverse Effects in Caenorhabditis elegans.” Environmental Science-Nano 5 (8): 2009–2020. doi:10.1039.C1038EN00412A.
   Google Scholar
• Li, D., K. Herault, K. Silm, A. Evrard, S. Wojcik, M. Oheim, E. Herzog, and N. Ropert. 2013. “Lack of Evidence for Vesicular Glutamate Transporter Expression in Mouse Astrocytes.” The Journal of Neuroscience 33: 4434–4455. doi:10.1523/JNEUROSCI.3667-12.2013.
   PubMed Web of Science ®Google Scholar
• Li, S., H. Li, D. Yang, X. Yu, D. M. Irwin, G. Niu, and H. Tan. 2017. “Excessive Autophagy Activation and Increased Apoptosis are Associated with Palmitic Acid-Induced Cardiomyocyte Insulin Resistance.” Journal of Diabetes Research 2017. doi:10.1155/2017/2376893.
   Web of Science ®Google Scholar
• Livak, K. J., and T. D. Schmittgen. 2001. “Analysis of Relative Gene Expression Data Using Real-time Quantitative PCR and the 2(-Delta Delta C(T)) Method.” Methods 25: 402–408. doi:10.1006/meth.2001.1262.
   PubMed Web of Science ®Google Scholar
• Lu, Y., Y. Zhang, Y. Deng, W. Jiang, Y. Zhao, J. Geng, L. Ding, and H. Ren. 2016. “Uptake and Accumulation of Polystyrene Microplastics in Zebrafish (Danio rerio) and Toxic Effects in Liver.” Environmental Science & Technology 50: 4054–4060. doi:10.1021/acs.est.6b00183.
   PubMed Web of Science ®Google Scholar
• Mattsson, K., E. V. Johnson, A. Malmendal, S. Linse, L.-A. Hansson, and T. Cedervall. 2017. “Brain Damage and Behavioural Disorders in Fish Induced by Plastic Nanoparticles Delivered through the Food Chain.” Scientific Reports 7 (1): 1–7. doi:10.1038/s41598-017-10813-0.
   PubMedGoogle Scholar
• Nijhawan, D., N. Honarpour, and X. Wang. 2000. “Apoptosis in Neural Development and Disease.” Annual Review of Neuroscience 23: 73–87. doi:10.1146/annurev.neuro.23.1.73.
   PubMed Web of Science ®Google Scholar
• North, E. J., and R. U. Halden. 2013. “Plastics and Environmental Health: The Road Ahead.” Reviews on Environmental Health 28: 1–8. doi:10.1515/reveh-2012-0030.
   PubMedGoogle Scholar
• Oh, P., P. Borgström, H. Witkiewicz, Y. Li, B. J. Borgström, A. Chrastina, K. Iwata, K. R. Zinn, R. Baldwin, and J. E. Testa. 2007. “Live Dynamic Imaging of Caveolae Pumping Targeted Antibody Rapidly and Specifically across Endothelium in the Lung.” Nature Biotechnology 25: 327–337. doi:10.1038/nbt1292.
   PubMed Web of Science ®Google Scholar
• Oppenheim, R. W. 1981. “Cell Death of Motoneurons in the Chick Embryo Spinal Cord.” The Journal of Neuroscience 1: 141–151. doi:10.1523/JNEUROSCI.01-02-00141.1981.
   PubMedGoogle Scholar
• Panariti, A., G. Miserocchi, and I. Rivolta. 2012. “The Effect of Nanoparticle Uptake on Cellular Behavior: Disrupting or Enabling Functions?” Nanotechnology, Science and Applications 5: 87.
   PubMedGoogle Scholar
• Pham, H. Q., K. Yoshioka, H. Mohri, H. Nakata, S. Aki, K. Ishimaru, N. Takuwa, and Y. Takuwa. 2018. “MTMR4, a Phosphoinositide-Specific 3'-Phosphatase, Regulates TFEB Activity and the Endocytic and Autophagic Pathways.” Genes to Cells 23 (8): 670–687. doi:10.1111/gtc.12609.
   Web of Science ®Google Scholar
• Plastic-Europe, A. 2006. Analysis of Plastics Production, Demand and Recovery in Europe. Brussels: Association of Plastic Manufacturers.
   Google Scholar
• Purves, D. 1985. Principles of Neural Development. Sinauer Associates Incorporated.
   Google Scholar
• Rafiee, M., L. Dargahi, A. Eslami, E. Beirami, M. Jahangiri-Rad, S. Sabour, and F. Amereh. 2018. “Neurobehavioral Assessment of Rats Exposed to Pristine Polystyrene Nanoplastics upon Oral Exposure.” Chemosphere 193: 745–753. doi:10.1016/j.chemosphere.2017.11.076.
   PubMed Web of Science ®Google Scholar
• Ragusa, A., A. Svelato, C. Santacroce, P. Catalano, V. Notarstefano, O. Carnevali, F. Papa, et al. 2021. “Plasticenta: First Evidence of Microplastics in Human Placenta.” Environment International 146: 106274. doi:10.1016/j.envint.2020.106274.
   PubMed Web of Science ®Google Scholar
• Rejman, J., M. Conese, and D. Hoekstra. 2006. “Gene Transfer by means of Lipo-and Polyplexes: Role of Clathrin and Caveolae-Mediated Endocytosis.” Journal of Liposome Research 16: 237–247. doi:10.1080/08982100600848819.
   PubMed Web of Science ®Google Scholar
• Richter, C. A., L. S. Birnbaum, F. Farabollini, R. R. Newbold, B. S. Rubin, C. E. Talsness, J. G. Vandenbergh, D. R. Walser-Kuntz, and F. S. Vom Saal. 2007. “In Vivo Effects of Bisphenol a in Laboratory Rodent Studies.” Reproductive Toxicology 24: 199–224. doi:10.1016/j.reprotox.2007.06.004.
   PubMed Web of Science ®Google Scholar
• Sabapathy, K., W. Jochum, K. Hochedlinger, L. Chang, M. Karin, and E. F. Wagner. 1999. “Defective Neural Tube Morphogenesis and Altered Apoptosis in the Absence of Both JNK1 and JNK2.” Mechanisms of Development 89: 115–124. doi:10.1016/S0925-4773(99)00213-0.
   PubMed Web of Science ®Google Scholar
• Sanes, D. H., T. A. Reh, and W. A. Harris. 2011. Development of the Nervous System. Academic Press.
   Google Scholar
• Sendra, M., E. Sparaventi, J. Blasco, I. Moreno-Garrido, and C. V. Araujo. 2020. “Ingestion and Bioaccumulation of Polystyrene Nanoplastics and Their Effects on the Microalgal Feeding of Artemia Franciscana.” Ecotoxicology and Environmental Safety 188: 109853. doi:10.1016/j.ecoenv.2019.109853.
   PubMed Web of Science ®Google Scholar
• Sendra, M., E. Staffieri, M. P. Yeste, I. Moreno-Garrido, J. M. Gatica, I. Corsi, and J. Blasco. 2019. “Are the Primary Characteristics of Polystyrene Nanoplastics Responsible for Toxicity and Ad/Absorption in the Marine Diatom Phaeodactylum Tricornutum?” Environmental Pollution 249: 610–619. doi:10.1016/j.envpol.2019.03.047.
   PubMed Web of Science ®Google Scholar
• Smith, J. L., and G. C. Schoenwolf. 1997. “Neurulation: coming to Closure.” Trends in Neurosciences 20 (11): 510–517. doi:10.1016/S0166-2236(97)01121-1.
   PubMed Web of Science ®Google Scholar
• Sun, S. W., X. Y. Zu, Q. H. Tuo, L. X. Chen, X. Y. Lei, K. Li, C. K. Tang, and D. F. Liao. 2010. “Caveolae and Caveolin-1 Mediate Endocytosis and Transcytosis of Oxidized Low Density Lipoprotein in Endothelial Cells.” Acta Pharmacologica Sinica 31 (10): 1336–1342. doi:10.1038/aps.2010.87.
   PubMed Web of Science ®Google Scholar
• Tanabe, Y., and T. M. Jessell. 1996. “Diversity and Pattern in the Developing Spinal Cord.” Science 274: 1115–1123. doi:10.1126/science.274.5290.1115.
   PubMed Web of Science ®Google Scholar
• Thompson, R. C., C. J. Moore, F. S. Vom Saal, and S. H. Swan. 2009. “Plastics, the Environment and Human Health: Current Consensus and Future Trends.” Philosophical Transactions of the Royal Society B: Biological Sciences 364 (1526): 2153–2166. doi:10.1098/rstb.2009.0053.
   PubMed Web of Science ®Google Scholar
• Vandenberg, L. N., R. Hauser, M. Marcus, N. Olea, and W. V. Welshons. 2007. “Human Exposure to Bisphenol A (BPA).” Reproductive Toxicology 24: 139–177. doi:10.1016/j.reprotox.2007.07.010.
   PubMed Web of Science ®Google Scholar
• Walczak, A. P., E. Kramer, P. J. Hendriksen, R. Helsdingen, M. van der Zande, I. M. Rietjens, and H. Bouwmeester. 2015. “In Vitro Gastrointestinal Digestion Increases the Translocation of Polystyrene Nanoparticles in an in Vitro Intestinal co-Culture Model.” Nanotoxicology 9: 886–894. doi:10.3109/17435390.2014.988664.
   PubMed Web of Science ®Google Scholar
• Wu, M., C. Yang, C. Du, and H. Liu. 2020. “Microplastics in Waters and Soils: Occurrence, Analytical Methods and Ecotoxicological Effects.” Ecotoxicology and Environment Safety 202: 110910. doi:10.1016/j.ecoenv.2020.110910.
   PubMed Web of Science ®Google Scholar
• Xu, L., G. Li, J. Wang, Y. Fan, Z. Wan, S. Zhang, S. Shaheen, et al. 2014. “Through an ITIM-Independent Mechanism the FcgammaRIIB Blocks B Cell Activation by Disrupting the Colocalized Microclustering of the B Cell Receptor and CD19.” Journal of Immunology 192: 5179–5191. doi:10.4049/jimmunol.1400101.
   PubMed Web of Science ®Google Scholar
• Yonekawa, T., and A. Thorburn. 2013. “Autophagy and Cell Death.” Essays in Biochemistry 55: 105–117. doi:10.1042/bse0550105.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., J. Wang, W. Huang, J. Cai, J. Ba, Y. Wang, Q. Ke, et al. 2018. “Nuclear Nestin Deficiency Drives Tumor Senescence via Lamin a/C-Dependent Nuclear Deformation.” Nature Communications 9: 3613. doi:10.1038/s41467-018-05808-y.
   PubMed Web of Science ®Google Scholar
• Zhao, J., and M. H. Stenzel. 2018. “Entry of Nanoparticles into Cells: The Importance of Nanoparticle Properties.” Polymer Chemistry 9 (3): 259–272. doi:10.1039/C7PY01603D.
   Web of Science ®Google Scholar