Early Low-Level Arsenic Exposure Impacts Post-Synaptic Hippocampal Function in Juvenile Mice
Abstract
:1. Introduction
2. Materials and Methods
2.1. Arsenic Exposure
2.2. Electrophysiology
2.3. Analysis
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Santucci, D.; Rankin, J.; Laviola, G.; Aloe, L.; Alleva, E. Early exposure to aluminium affects eight-arm maze performance and hippocampal nerve growth factor levels in adult mice. Neurosci. Lett. 1994, 166, 89–92. [Google Scholar] [CrossRef]
- Liu, J.; Liu, X.; Wang, W.; McCauley, L.; Pinto-Martin, J.; Wang, Y.; Li, L.; Yan, C.; Rogan, W.J. Blood lead concentrations and children’s behavioral and emotional problems: A cohort study. JAMA Pediatr. 2014, 168, 737–745. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cory-Slechta, D.A.; Allen, J.L.; Conrad, K.; Marvin, E.; Sobolewski, M. Developmental exposure to low level ambient ultrafine particle air pollution and cognitive dysfunction. Neurotoxicology 2018, 69, 217–231. [Google Scholar] [CrossRef] [PubMed]
- Naujokas, M.F.; Anderson, B.; Ahsan, H.; Aposhian, H.V.; Graziano, J.H.; Thompson, C.; Suk, W.A. The broad scope of health effects from chronic arsenic exposure: Update on a worldwide public health problem. Environ. Health Perspect. 2013, 121, 295–302. [Google Scholar] [CrossRef]
- DeSimone, L.A.; McMahon, P.B.; Rosen, M.R. The Quality of Our Nation’s Waters: Water Quality in Principal Aquifers of the United States, 1991–2010; US Geological Survey: Reston, VA, USA, 2015; pp. 2330–5703.
- Guo, X.; Chen, X.; Wang, J.; Liu, Z.; Gaile, D.; Wu, H.; Yu, G.; Mao, G.; Yang, Z.; Di, Z.; et al. Multi-generational impacts of arsenic exposure on genome-wide DNA methylation and the implications for arsenic-induced skin lesions. Environ. Int. 2018, 119, 250–263. [Google Scholar] [CrossRef]
- Biswas, S.; Banna, H.U.; Jahan, M.; Anjum, A.; Siddique, A.E.; Roy, A.; Nikkon, F.; Salam, K.A.; Haque, A.; Himeno, S.; et al. In vivo evaluation of arsenic-associated behavioral and biochemical alterations in F0 and F1 mice. Chemosphere 2020, 245, 125619. [Google Scholar] [CrossRef]
- Htway, S.M.; Suzuki, T.; Kyaw, S.; Nohara, K.; Win-Shwe, T.T. Effects of maternal exposure to arsenic on social behavior and related gene expression in F2 male mice. Environ. Health Prev. Med. 2021, 26, 34. [Google Scholar] [CrossRef] [PubMed]
- Environmental Protection Agency. National primary drinking water regulations: Arsenic and clarifications to compliance and new source contaminants monitoring. Fed. Regist. 2001, 66, 69–76. [Google Scholar]
- NRC. Arsenic in Drinking Water; National Academy Press: Washington, DC, USA, 1999. [Google Scholar]
- Tolins, M.; Ruchirawat, M.; Landrigan, P. The developmental neurotoxicity of arsenic: Cognitive and behavioral consequences of early life exposure. Ann. Glob. Health 2014, 80, 303–314. [Google Scholar] [CrossRef]
- Tyler, C.R.; Allan, A.M. The Effects of Arsenic Exposure on Neurological and Cognitive Dysfunction in Human and Rodent Studies: A Review. Curr. Environ. Health Rep. 2014, 1, 132–147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- O’Bryant, S.E.; Edwards, M.; Menon, C.V.; Gong, G.; Barber, R. Long-term low-level arsenic exposure is associated with poorer neuropsychological functioning: A Project FRONTIER study. Int J. Environ. Res. Public Health 2011, 8, 861–874. [Google Scholar] [CrossRef]
- Rosado, J.L.; Ronquillo, D.; Kordas, K.; Rojas, O.; Alatorre, J.; Lopez, P.; Garcia-Vargas, G.; Del Carmen Caamano, M.; Cebrian, M.E.; Stoltzfus, R.J. Arsenic exposure and cognitive performance in Mexican schoolchildren. Environ. Health Perspect. 2007, 115, 1371–1375. [Google Scholar] [CrossRef] [Green Version]
- Wasserman, G.A.; Liu, X.; Parvez, F.; Ahsan, H.; Factor-Litvak, P.; van Geen, A.; Slavkovich, V.; LoIacono, N.J.; Cheng, Z.; Hussain, I.; et al. Water arsenic exposure and children’s intellectual function in Araihazar, Bangladesh. Environ. Health Perspect. 2004, 112, 1329–1333. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Calderon, J.; Navarro, M.E.; Jimenez-Capdeville, M.E.; Santos-Diaz, M.A.; Golden, A.; Rodriguez-Leyva, I.; Borja-Aburto, V.; Diaz-Barriga, F. Exposure to arsenic and lead and neuropsychological development in Mexican children. Environ. Res. 2001, 85, 69–76. [Google Scholar] [CrossRef]
- Wang, X.; Huang, X.; Zhou, L.; Chen, J.; Zhang, X.; Xu, K.; Huang, Z.; He, M.; Shen, M.; Chen, X.; et al. Association of arsenic exposure and cognitive impairment: A population-based cross-sectional study in China. Neurotoxicology 2020, 82, 100–107. [Google Scholar] [CrossRef]
- Tsai, S.-Y.; Chou, H.-Y.; The, H.-W.; Chen, C.-M.; Chen, C.-J. The Effects of Chronic Arsenic Exposure from Drinking Water on the Neurobehavioral Development in Adolescence. NeuroToxicology 2003, 24, 747–753. [Google Scholar] [CrossRef]
- Nigra, A.E.; Chen, Q.; Chillrud, S.N.; Wang, L.; Harvey, D.; Mailloux, B.; Factor-Litvak, P.; Navas-Acien, A. Inequalities in Public Water Arsenic Concentrations in Counties and Community Water Systems across the United States, 2006–2011. Environ. Health Perspect. 2020, 128, 127001. [Google Scholar] [CrossRef] [PubMed]
- Nelson-Mora, J.; Escobar, M.L.; Rodriguez-Duran, L.; Massieu, L.; Montiel, T.; Rodriguez, V.M.; Hernandez-Mercado, K.; Gonsebatt, M.E. Gestational exposure to inorganic arsenic (iAs3+) alters glutamate disposition in the mouse hippocampus and ionotropic glutamate receptor expression leading to memory impairment. Arch. Toxicol. 2018, 92, 1037–1048. [Google Scholar] [CrossRef]
- Siddoway, B.H.H.; Xia, H. Glutamatergic Synapses: Molecular Organisation. eLS 2011. Available online: https://doi.org/10.1002/9780470015902.a0000235.pub2 (accessed on 1 June 2021).
- Luo, J.H.; Qiu, Z.Q.; Shu, W.Q.; Zhang, Y.Y.; Zhang, L.; Chen, J.A. Effects of arsenic exposure from drinking water on spatial memory, ultra-structures and NMDAR gene expression of hippocampus in rats. Toxicol. Lett. 2009, 184, 121–125. [Google Scholar] [CrossRef]
- Zhang, C.; Li, S.; Sun, Y.; Dong, W.; Piao, F.; Piao, Y.; Liu, S.; Guan, H.; Yu, S. Arsenic downregulates gene expression at the postsynaptic density in mouse cerebellum, including genes responsible for long-term potentiation and depression. Toxicol. Lett. 2014, 228, 260–269. [Google Scholar] [CrossRef] [PubMed]
- Luo, J.H.; Qiu, Z.Q.; Zhang, L.; Shu, W.Q. Arsenite exposure altered the expression of NMDA receptor and postsynaptic signaling proteins in rat hippocampus. Toxicol. Lett. 2012, 211, 39–44. [Google Scholar] [CrossRef] [PubMed]
- Tyler, C.R.; Allan, A.M. Adult hippocampal neurogenesis and mRNA expression are altered by perinatal arsenic exposure in mice and restored by brief exposure to enrichment. PLoS ONE 2013, 8, e73720. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Htway, S.M.; Sein, M.T.; Nohara, K.; Win-Shwe, T.T. Effects of Developmental Arsenic Exposure on the Social Behavior and Related Gene Expression in C3H Adult Male Mice. Int. J. Environ. Res. Public Health 2019, 16, 174. [Google Scholar] [CrossRef] [Green Version]
- Kruger, K.; Binding, N.; Straub, H.; Musshoff, U. Effects of arsenite on long-term potentiation in hippocampal slices from young and adult rats. Toxicol. Lett. 2006, 165, 167–173. [Google Scholar] [CrossRef] [PubMed]
- Kruger, K.; Repges, H.; Hippler, J.; Hartmann, L.M.; Hirner, A.V.; Straub, H.; Binding, N.; Musshoff, U. Effects of dimethylarsinic and dimethylarsinous acid on evoked synaptic potentials in hippocampal slices of young and adult rats. Toxicol. Appl. Pharm. 2007, 225, 40–46. [Google Scholar] [CrossRef]
- Concha, G.; Vogler, G.; Lezcano, D.; Nermell, B.; Vahter, M. Exposure to Inorganic Arsenic Metabolites during Early Human Development. Toxicol. Sci. 1998, 44, 185–190. [Google Scholar] [CrossRef]
- Kruger, K.; Straub, H.; Hirner, A.V.; Hippler, J.; Binding, N.; Musshoff, U. Effects of monomethylarsonic and monomethylarsonous acid on evoked synaptic potentials in hippocampal slices of adult and young rats. Toxicol. Appl. Pharm. 2009, 236, 115–123. [Google Scholar] [CrossRef] [PubMed]
- Frankel, S.; Concannon, J.; Brusky, K.; Pietrowicz, E.; Giorgianni, S.; Thompson, W.D.; Currie, D.A. Arsenic exposure disrupts neurite growth and complexity in vitro. Neurotoxicology 2009, 30, 529–537. [Google Scholar] [CrossRef]
- Zhao, F.; Liao, Y.; Tang, H.; Piao, J.; Wang, G.; Jin, Y. Effects of developmental arsenite exposure on hippocampal synapses in mouse offspring. Metallomics 2017, 9, 1394–1412. [Google Scholar] [CrossRef]
- Jing, J.; Zheng, G.; Liu, M.; Shen, X.; Zhao, F.; Wang, J.; Zhang, J.; Huang, G.; Dai, P.; Chen, Y.; et al. Changes in the synaptic structure of hippocampal neurons and impairment of spatial memory in a rat model caused by chronic arsenite exposure. Neurotoxicology 2012, 33, 1230–1238. [Google Scholar] [CrossRef]
- Barnes, C.A. Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. J. Comp. Physiol Psychol 1979, 93, 74–104. [Google Scholar] [CrossRef]
- Rinaldi, T.; Kulangara, K.; Antoniello, K.; Markram, H. Elevated NMDA receptor levels and enhanced postsynaptic long-term potentiation induced by prenatal exposure to valproic acid. Proc. Natl. Acad. Sci. USA 2007, 104, 13501–13506. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Markram, K.; Rinaldi, T.; La Mendola, D.; Sandi, C.; Markram, H. Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 2008, 33, 901–912. [Google Scholar] [CrossRef]
- Schneider, T.; Przewlocki, R. Behavioral alterations in rats prenatally exposed to valproic acid: Animal model of autism. Neuropsychopharmacology 2005, 30, 80–89. [Google Scholar] [CrossRef] [PubMed]
- Engert, F.; Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399, 66–70. [Google Scholar] [CrossRef]
- Hofer, S.B.; Bonhoeffer, T. Dendritic spines: The stuff that memories are made of? Curr. Biol. 2010, 20, R157–R159. [Google Scholar] [CrossRef] [Green Version]
- Yuste, R.; Bonhoeffer, T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 2001, 24, 1071–1089. [Google Scholar] [CrossRef] [Green Version]
- Foley, K.; McKee, C.; Nairn, A.C.; Xia, H. Regulation of Synaptic Transmission and Plasticity by Protein Phosphatase 1. J. Neurosci. 2021, 41, 3040–3050. [Google Scholar] [CrossRef] [PubMed]
- Gao, J.; Hu, X.D.; Yang, H.; Xia, H. Distinct Roles of Protein Phosphatase 1 Bound on Neurabin and Spinophilin and Its Regulation in AMPA Receptor Trafficking and LTD Induction. Mol. Neurobiol. 2018, 55, 7179–7186. [Google Scholar] [CrossRef] [PubMed]
- Martinez, L.; Jimenez, V.; Garcia-Sepulveda, C.; Ceballos, F.; Delgado, J.M.; Nino-Moreno, P.; Doniz, L.; Saavedra-Alanis, V.; Castillo, C.G.; Santoyo, M.E.; et al. Impact of early developmental arsenic exposure on promotor CpG-island methylation of genes involved in neuronal plasticity. Neurochem. Int. 2011, 58, 574–581. [Google Scholar] [CrossRef] [PubMed]
- Carignan, C.C.; Cottingham, K.L.; Jackson, B.P.; Farzan, S.F.; Gandolfi, A.J.; Punshon, T.; Folt, C.L.; Karagas, M.R. Estimated exposure to arsenic in breastfed and formula-fed infants in a United States cohort. Environ. Health Perspect. 2015, 123, 500–506. [Google Scholar] [CrossRef] [PubMed]
- Thomas, D.J. Arsenic methylation—Lessons from three decades of research. Toxicology 2021, 457, 152800. [Google Scholar] [CrossRef]
- Watanabe, T.; Hirano, S. Metabolism of arsenic and its toxicological relevance. Arch. Toxicol. 2013, 87, 969–979. [Google Scholar] [CrossRef]
- Hall, M.; Gamble, M.; Slavkovich, V.; Liu, X.; Levy, D.; Cheng, Z.; van Geen, A.; Yunus, M.; Rahman, M.; Pilsner, J.R.; et al. Determinants of arsenic metabolism: Blood arsenic metabolites, plasma folate, cobalamin, and homocysteine concentrations in maternal-newborn pairs. Environ. Health Perspect. 2007, 115, 1503–1509. [Google Scholar] [CrossRef] [Green Version]
- Jin, Y.; Xi, S.; Li, X.; Lu, C.; Li, G.; Xu, Y.; Qu, C.; Niu, Y.; Sun, G. Arsenic speciation transported through the placenta from mother mice to their newborn pups. Environ. Res. 2006, 101, 349–355. [Google Scholar] [CrossRef]
- Odanaka, Y.; Matano, O.; Goto, S. Biomethylation of Inorganic Arsenic by the Rat and Some Laboratory-Animals. Bull. Environ. Contam Tox. 1980, 24, 452–459. [Google Scholar] [CrossRef]
- Vahter, M. Species-Differences in the Metabolism of Arsenic Compounds. Appl. Organomet. Chem. 1994, 8, 175–182. [Google Scholar] [CrossRef]
- Kruger, K.; Gruner, J.; Madeja, M.; Hartmann, L.M.; Hirner, A.V.; Binding, N.; Musshoff, U. Blockade and enhancement of glutamate receptor responses in Xenopus oocytes by methylated arsenicals. Arch. Toxicol. 2006, 80, 492–501. [Google Scholar] [CrossRef]
- Wilson, D. Arsenic Consumption in the United States. J. Environ. Health 2015, 78, 8–14. [Google Scholar]
Study | Exposure Type * | Age of Rodents Tested † | Exposure Onset | Exposure End |
---|---|---|---|---|
Nelson-Mora et al. (2018) | In vivo | Adult | Gestation | Adulthood |
Current Study | In vivo | Juvenile | Gestation | Early development |
Kruger et al. (2006) | Ex vivo | Juvenile/Adult | Following brain slice preparation | NA |
Kruger et al. (2007) | Ex vivo | Juvenile/Adult | ||
Kruger et al. (2009) | Ex vivo | Juvenile/Adult |
Study | Exposure Level | Basal Transmission | Paired-Pulse Facilitation (PPF) | Long-Term Potentiation (LTP) |
---|---|---|---|---|
In vivo exposure | ||||
Nelson-Mora et al. (2018) | 20 ppm | Decrease | Decrease * | Decrease |
Current Study | 36 ppm | Decrease | Decrease | Increase |
Current study | 50 ppb | Decrease | No change | No change † |
Acute, ex vivo exposure: Juvenile rodents | ||||
Kruger et al. (2006) | 1–100 μM | Decrease ‡ | Not tested | No change |
Kruger et al. (2007) | 1–100 μM | Decrease | Not tested | Decrease ‡ |
Kruger et al. (2009) | 1–100 μM | Decrease ‡ | Not tested | Increase ‡ |
Acute, ex vivo exposure: Adult rodents | ||||
Kruger et al. (2006) | 0.1–100 μM | Decrease ‡ | No change | Decrease |
Kruger et al. (2007) | 1–100 μM | Decrease | Not tested | Decrease ‡ |
Kruger et al. (2009) | 10–100 μM | Decrease ‡ | No change | Decrease |
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Foley, K.F.W.; Barnett, D.; Cory-Slechta, D.A.; Xia, H. Early Low-Level Arsenic Exposure Impacts Post-Synaptic Hippocampal Function in Juvenile Mice. Toxics 2021, 9, 206. https://doi.org/10.3390/toxics9090206
Foley KFW, Barnett D, Cory-Slechta DA, Xia H. Early Low-Level Arsenic Exposure Impacts Post-Synaptic Hippocampal Function in Juvenile Mice. Toxics. 2021; 9(9):206. https://doi.org/10.3390/toxics9090206
Chicago/Turabian StyleFoley, Karl F. W., Daniel Barnett, Deborah A. Cory-Slechta, and Houhui Xia. 2021. "Early Low-Level Arsenic Exposure Impacts Post-Synaptic Hippocampal Function in Juvenile Mice" Toxics 9, no. 9: 206. https://doi.org/10.3390/toxics9090206
APA StyleFoley, K. F. W., Barnett, D., Cory-Slechta, D. A., & Xia, H. (2021). Early Low-Level Arsenic Exposure Impacts Post-Synaptic Hippocampal Function in Juvenile Mice. Toxics, 9(9), 206. https://doi.org/10.3390/toxics9090206