Maternal exposure to polystyrene microplastics alters placental metabolism in mice
Tóm tắt
The rapid growth in the worldwide use of plastics has resulted in a vast accumulation of microplastics in the air, soil and water. The impact of these microplastics on pregnancy and fetal development remains largely unknown. In pregnant mice, we recently demonstrated that exposure to micro- and nanoplastics throughout gestation resulted in significant fetal growth restriction. One possible explanation for reduced fetal growth is abnormal placental metabolism. To evaluate the effect of maternal exposure to microplastics on placental metabolism. In the present study, CD-1 pregnant mice were exposed to 5 μm polystyrene microplastics in filtered drinking water at one of four concentrations (0 ng/L (controls), 102 ng/L, 104 ng/L, 106 ng/L) throughout gestation (n = 7–11/group). At embryonic day 17.5, placental tissue samples were collected (n = 28–44/group). Metabolite profiles were determined using 1 H high-resolution magic angle spinning magnetic resonance spectroscopy. The relative concentration of lysine (p = 0.003) and glucose (p < 0.0001) in the placenta were found to decrease with increasing microplastic concentrations, with a significant reduction at the highest exposure concentration. Multivariate analysis identified shifts in the metabolic profile with MP exposure and pathway analysis identified perturbations in the biotin metabolism, lysine degradation, and glycolysis/gluconeogenesis pathways. Maternal exposure to microplastics resulted in significant alterations in placental metabolism. This study highlights the potential impact of microplastic exposure on pregnancy outcomes and that efforts should be made to minimize exposure to plastics, particularly during pregnancy.
Tài liệu tham khảo
Aghaei, Z., Sled, J. G., Kingdom, J. C., Baschat, A. A., Helm, P. A., Jobst, K. J., & Cahill, L. S. (2022). Maternal Exposure to Polystyrene Micro-and Nanoplastics Causes Fetal Growth Restriction in Mice. Environmental Science & Technology Letters, 9(5), 426-430. https://doi.org/10.1021/acs.estlett.2c00186
Barker, D. J. P. (1995). Fetal origins of coronary heart disease. Bmj, 311(6998), 171–174. https://doi.org/10.1136/bmj.311.6998.171.
Barker, D. J. P. (2006). Adult consequences of fetal growth restriction. Clinical Obstetrics and Gynecology, 49(2), 270–283. https://doi.org/10.1097/00003081-200606000-00009.
Baschat, A. (2004). Fetal responses to placental insufficiency: an update. Bjog, 111, 1031–1041. https://doi.org/10.1111/j.1471-0528.2004.00273.x.
Beckonert, O., Coen, M., Keun, H. C., Wang, Y., Ebbels, T. M. D., Holmes, E., Lindon, J. C., & Nicholson, J. K. (2010). High-resolution magic-angle-spinning NMR spectroscopy for metabolic profiling of intact tissues. Nature Protocols, 5(6), 1019–1032. https://doi.org/10.1038/nprot.2010.45.
Botterell, Z. L. R., Beaumont, N., Dorrington, T., Steinke, M., Thompson, R. C., & Lindeque, P. K. (2019). Bioavailability and effects of microplastics on marine zooplankton: a review. Environmental Pollution, 245, 98–110. https://doi.org/10.1016/j.envpol.2018.10.065.
Campanale, C., Massarelli, C., Savino, I., Locaputo, V., & Uricchio, V. F. (2020). A detailed review study on potential effects of microplastics and additives of concern on human health. International Journal of Environmental Research and Public Health, 17(4), 1212. https://doi.org/10.3390/ijerph17041212.
Caruso, A., Paradisi, G., Ferrazzani, S., Lucchese, A., Moretti, S., & Fulghesu, A. M. (1998). Effect of maternal carbohydrate metabolism on fetal growth. Obstetrics and Gynecology, 92(1), 8–12. https://doi.org/10.1016/s0029-7844(98)00138-0.
Cetin, I., Marconi, A. M., Bozzetti, P., Sereni, L. P., Corbetta, C., Pardi, G., & Battaglia, F. C. (1988). Umbilical amino acid concentrations in appropriate and small for gestational age infants: a biochemical difference present in utero. American Journal of Obstetrics and Gynecology, 158(1), 120–126. https://doi.org/10.1016/0002-9378(88)90792-2.
de Rooij, S. R., Painter, R. C., Holleman, F., Bossuyt, P. M. M., & Roseboom, T. J. (2007). The metabolic syndrome in adults prenatally exposed to the dutch famine. The American Journal of Clinical Nutrition, 86(4), 1219–1224. https://doi.org/10.1093/ajcn/86.4.1219.
Deng, Y., Zhang, Y., Lemos, B., & Ren, H. (2017). Tissue accumulation of microplastics in mice and biomarker responses suggest widespread health risks of exposure. Scientific Reports, 7(1), 1–10. https://doi.org/10.1038/srep46687.
Dessì, A., Ottonello, G., & Fanos, V. (2012). Physiopathology of intrauterine growth retardation: from classic data to metabolomics. The Journal of Maternal-Fetal & Neonatal Medicine, 25(sup5), 13–18. https://doi.org/10.3109/14767058.2012.714639.
Economides, D. L., Nicolaides, K. H., Gahl, W. A., Bernardini, I., & Evans, M. I. (1989). Plasma amino acids in appropriate-and small-for-gestational-age fetuses. American Journal of Obstetrics and Gynecology, 161(5), 1219–1227. https://doi.org/10.1016/0002-9378(89)90670-4.
Eerkes-Medrano, D., Thompson, R. C., & Aldridge, D. C. (2015). Microplastics in freshwater systems: a review of the emerging threats, identification of knowledge gaps and prioritisation of research needs. Water Research, 75, 63–82. https://doi.org/10.1016/j.watres.2015.02.012.
Frias, J. P. G. L., & Nash, R. (2019). Microplastics: finding a consensus on the definition. Marine Pollution Bulletin, 138, 145–147. https://doi.org/10.1016/j.marpolbul.2018.11.022.
Govindaraju, V., Young, K., & Maudsley, A. A. (2000). Proton NMR chemical shifts and coupling constants for brain metabolites. NMR in Biomedicine, 13(3), 129–153. https://doi.org/10.1002/1099-1492(200005)13:3<129::aid-nbm619>3.0.co;2-v.
Haave, M., Gomiero, A., Schönheit, J., Nilsen, H., & Olsen, A. B. (2021). Documentation of microplastics in tissues of wild coastal animals. Frontiers in Environmental Science, 9, 31. https://doi.org/10.3389/fenvs.2021.575058.
Hay, W. W. Jr. (2006). Placental-fetal glucose exchange and fetal glucose metabolism. Transactions of the American Clinical and Climatological Association, 117, 321.
Kaur, K., Lesseur, C., Deyssenroth, M. A., Kloog, I., Schwartz, J. D., Marsit, C. J., & Chen, J. (2022). PM2.5 exposure during pregnancy is associated with altered placental expression of lipid metabolic genes in a US birth cohort. Environmental Research, 211, 113066. https://doi.org/10.1016/j.envres.2022.113066.
Koelmans, A. A., Nor, N. H. M., Hermsen, E., Kooi, M., Mintenig, S. M., & De France, J. (2019). Microplastics in freshwaters and drinking water: critical review and assessment of data quality. Water Research, 155, 410–422. https://doi.org/10.1016/j.watres.2019.02.054.
Lambert, S., & Wagner, M. (2018). Microplastics are contaminants of emerging concern in freshwater environments: an overview. In: M. Wagner, S. Lambert (Eds), Freshwater Microplastics. The Handbook of Environmental Chemistry (vol 58, pp.1–23). Springer. https://doi.org/10.1007/978-3-319-61615-5_1
Luo, J., Turk, E. A., Gagoski, B., Copeland, N., Zhou, I. Y., Young, V., Bibbo, C., Robinson, J. N., Zera, C., Barth, W. H. Jr., Roberts, D. J., Sun, P. Z., & Grant, P. E. (2019). Preliminary evidence of dynamic glucose enhanced MRI of the human placenta during glucose tolerance test. Quantitative Imaging in Medicine and Surgery, 9(10), 1619–1627. https://doi.org/10.21037/qims.2019.09.16.
Marconi, A. M., Paolini, C., Buscaglia, M., Zerbe, G., Battaglia, F. C., & Pardi, G. (1996). The impact of gestational age and fetal growth on the maternal-fetal glucose concentration difference. Obstetrics & Gynecology, 87(6), 937–942. https://doi.org/10.1016/0029-7844(96)00048-8.
Michelsen, T. M., Holme, A. M., Holm, M. B., Roland, M. C., Haugen, G., Powell, T. L., Jansson, R., & Henriksen, T. (2019). Uteroplacental glucose uptake and fetal glucose consumption: a quantitative study in human pregnancies. The Journal of Clinical Endocrinology & Metabolism, 104(3), 873–882. https://doi.org/10.1210/jc.2018-01154.
Nicolini, U., Hubinont, C., Santolaya, J., Fisk, N. M., Coe, A. M., & Rodeck, C. H. (1989). Maternal-fetal glucose gradient in normal pregnancies and in pregnancies complicated by alloimmunization and fetal growth retardation. American Journal of Obstetrics and Gynecology, 161(4), 924–927. https://doi.org/10.1016/0002-9378(89)90753-9.
Pang, Z., Chong, J., Zhou, G., Morais, D., Chang, L., Barrette, M., Gauthier, C., Jacques, P. E., Li, S., & Xia, J. (2021). MetaboAnalyst 5.0: narrowing the gap between raw spectra and functional insights. Nucleic Acids Research, 49(W1), W388–W396. https://doi.org/10.1093/nar/gkab382.
Ragusa, A., Svelato, A., Santacroce, C., Catalano, P., Notarstefano, V., Carnevali, O., Papa, F., Rongioletti, M. C. A., Baiocco, F., Draghi, S., Amore, E., Rinaldo, D., Matta, M., & Giorgini, E. (2021). Plasticenta: first evidence of microplastics in human placenta. Environment International, 146, 106274. https://doi.org/10.1016/j.envint.2020.106274.
Schenetti, L., Mucci, A., Parenti, F., Cagnoli, R., Righi, V., Tosi, M. R., & Tugnoli, V. (2006). HR-MAS NMR spectroscopy in the characterization of human tissues: application to healthy gastric mucosa. Concepts in Magnetic Resonance Part A: An Educational Journal, 28(6), 430–443. https://doi.org/10.1002/cmr.a.20068.
Schenker, S., Hu, Z. Q., Johnson, R. F., Yang, Y., Frosto, T., Elliott, B. D., Henderson, G. I., & Mock, D. M. (1993). Human placental biotin transport: normal characteristics and effect of ethanol. Alcoholism Clinical and Experimental Research, 17(3), 566–575. https://doi.org/10.1111/j.1530-0277.1993.tb00801.x.
Schneider, C. M., Steeves, K. L., Mercer, G. V., George, H., Paranavitana, L., Simpson, M. J., Simpson, A. J., & Cahill, L. S. (2022). Placental metabolite profiles in late gestation for healthy mice. Metabolomics, 18(1), 10. https://doi.org/10.1007/s11306-021-01868-2.
Scholl, T. O., Sowers, M., Chen, X., & Lenders, C. (2001). Maternal glucose concentration influences fetal growth, gestation, and pregnancy complications. American Journal of Epidemiology, 154(6), 514–520. https://doi.org/10.1093/aje/154.6.514.
von Moos, N., Burkhardt-Holm, P., & Köhler, A. (2012). Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L after an experimental exposure. Environmental Science and Technology, 46, 11327–11335.
Waters, N. J., Garrod, S., Farrant, R. D., Haselden, J. N., Connor, S. C., Connelly, J., Lindon, J. C., Holmes, E., & Nicolson, J. K. (2000). High-resolution magic angle spinning 1H NMR spectroscopy of intact liver and kidney: optimization of sample preparation procedures and biochemical stability of tissue during spectral acquisition. Analytical Biochemistry, 282(1), 16–23. https://doi.org/10.1006/abio.2000.4574.
Wright, S. L., & Kelly, F. J. (2017). Plastic and human health: a micro issue? Environmental Science and Technology, 51(12), 6634–6647. https://doi.org/10.1021/acs.est.7b00423.
Wu, D., Xu, J., Lei, J., Mclane, M., van Zijl, P. C., & Burd, I. (2018). Dynamic glucose enhanced MRI of the placenta in a mouse model of intrauterine inflammation. Placenta, 69, 86–91. https://doi.org/10.1016/j.placenta.2018.07.012.
Yin, K., Wang, Y., Zhao, H., Wang, D., Guo, M., Mu, M., Liu, Y., Nie, X., Li, B., Li, J., & Xing, M. (2021). A comparative review of microplastics and nanoplastics: toxicity hazards on digestive, reproductive and nervous system. Science of The Total Environment, 774, 145758. https://doi.org/10.1016/j.scitotenv.2021.145758.
Zamudio, S., Torricos, T., Fik, E., Oyala, M., Echalar, L., Pullockaran, J., Tutino, E., Martin, B., Belliappa, S., Balanza, E., & Illsley, N. P. (2010). Hypoglycemia and the origin of hypoxia-induced reduction in human fetal growth. PloS one, 5(1), e8551. https://doi.org/10.1371/journal.pone.0008551.
Zhang, Q., Xu, E. G., Li, J., Chen, Q., Ma, L., Zeng, E. Y., & Shi, H. (2020). A review of microplastics in table salt, drinking water, and air: direct human exposure. Environmental Science and Technology, 54(7), 3740–3751. https://doi.org/10.1021/acs.est.9b04535.