Acknowledgement
We thank Dr. Timothy Ryan (ER-GCaMP6-150), Franck Polleux (mito-GCaMP5G, vGlut1-GCaMP5G), Karel Svoboda (PSD95-GCaMP2), and Doug Golenbock (eGFP) for providing plasmids.
References
- Amiri, A. and Turner-Henson, A. (2017) The roles of formaldehyde exposure and oxidative stress in fetal growth in the second trimester. J. Obstet. Gynecol. Neonatal. Nurs. 46, 51-62. https://doi.org/10.1016/j.jogn.2016.08.007
- Berkefeld, H., Sailer, C. A., Bildl, W., Rohde, V., Thumfart, J. O., Eble, S., Klugbauer, N., Reisinger, E., Bischofberger, J., Oliver, D., Knaus, H. G., Schulte, U. and Fakler, B. (2006) BKCa-Cav channel complexes mediate rapid and localized Ca2+-activated K+ signaling. Science 314, 615-620. https://doi.org/10.1126/science.1132915
- Borgert, C. J., Fuentes, C. and Burgoon, L. D. (2021) Principles of dose-setting in toxicology studies: the importance of kinetics for ensuring human safety. Arch. Toxicol. 95, 3651-3664. https://doi.org/10.1007/s00204-021-03155-4
- Catterall, W. A. (2011) Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 3, a003947.
- Chameau, P., Lucas, P., Melliti, K., Bournaud, R. and Shimahara, T. (1999) Development of multiple calcium channel types in cultured mouse hippocampal neurons. Neuroscience 90, 383-388. https://doi.org/10.1016/S0306-4522(98)00457-6
- Chang, M., Lee, D., Park, H., Ha, M., Hong, Y. C., Kim, Y., Kim, B. N., Kim, Y., Lim, Y. H. and Ha, E. H. (2018) Prenatal TVOCs exposure negatively influences postnatal neurobehavioral development. Sci. Total Environ. 618, 977-981. https://doi.org/10.1016/j.scitotenv.2017.09.046
- Chang, M., Park, H., Ha, M., Hong, Y. C., Lim, Y. H., Kim, Y., Kim, Y. J., Lee, D. and Ha, E. H. (2017) The effect of prenatal TVOC exposure on birth and infantile weight: the Mothers and Children's Environmental Health study. Pediatr. Res. 82, 423-428. https://doi.org/10.1038/pr.2017.55
- Citri, A. and Malenka, R. C. (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33, 18-41. https://doi.org/10.1038/sj.npp.1301559
- Condie, L. W., Hill, J. R. and Borzelleca, J. F. (1988) Oral toxicology studies with xylene isomers and mixed xylenes. Drug Chem. Toxicol. 11, 329-354. https://doi.org/10.3109/01480548809018107
- de Juan-Sanz, J., Holt, G. T., Schreiter, E. R., de Juan, F., Kim, D. S. and Ryan, T. A. (2017) Axonal endoplasmic reticulum Ca(2+) content controls release probability in CNS nerve terminals. Neuron 93, 867-881.e866. https://doi.org/10.1016/j.neuron.2017.01.010
- Fang, Z. X., Sonner, J., Laster, M. J., Ionescu, P., Kandel, L., Koblin, D. D., Eger, E. I. and Halsey, M. J. (1996) Anesthetic and convulsant properties of aromatic compounds and cycloalkanes: Implications for mechanisms of narcosis. Anesth. Analg. 83, 1097-1104. https://doi.org/10.1213/00000539-199611000-00035
- Giansante, G., Marte, A., Romei, A., Prestigio, C., Onofri, F., Benfenati, F., Baldelli, P. and Valente, P. (2020) Presynaptic L-type Ca(2+) channels increase glutamate release probability and excitatory strength in the hippocampus during chronic neuroinflammation. J. Neurosci. 40, 6825-6841. https://doi.org/10.1523/JNEUROSCI.2981-19.2020
- Grossman, A. W., Elisseou, N. M., McKinney, B. C. and Greenough, W. T. (2006) Hippocampal pyramidal cells in adult Fmr1 knockout mice exhibit an immature-appearing profile of dendritic spines. Brain Res. 1084, 158-164. https://doi.org/10.1016/j.brainres.2006.02.044
- Guo, H., Lee, S. C., Chan, L. Y. and Li, W. M. (2004) Risk assessment of exposure to volatile organic compounds in different indoor environments. Environ. Res. 94, 57-66. https://doi.org/10.1016/S0013-9351(03)00035-5
- Honma, T., Sudo, A., Miyagawa, M., Sato, M. and Hasegawa, H. (1983) Significant changes in the amounts of neurotransmitter and related substances in rat brain induced by subacute exposure to low levels of toluene and xylene. Ind. Health 21, 143-151. https://doi.org/10.2486/indhealth.21.143
- Ishikawa, T., Kaneko, M., Shin, H.S. and Takahashi, T. (2005) Presynaptic N-type and P/Q-type Ca2+ channels mediating synaptic transmission at the calyx of Held of mice. J. Physiol. 568, 199-209. https://doi.org/10.1113/jphysiol.2005.089912
- Kandyala, R., Raghavendra, S. P. and Rajasekharan, S. T. (2010) Xylene: an overview of its health hazards and preventive measures. J. Oral Maxillofac. Pathol. 14, 1-5.
- Kessi, M., Chen, B., Peng, J., Yan, F., Yang, L. and Yin, F. (2021) Calcium channelopathies and intellectual disability: a systematic review. Orphanet. J. Rare Dis. 16, 219.
- Kim, S. R., Eom, Y. and Lee, S. H. (2023a) Comprehensive analysis of sex differences in the function and ultrastructure of hippocampal presynaptic terminals. Neurochem. Int. 169, 105570.
- Kim, Y. K., Eom, Y., Yoon, H., Lee, Y. and Lee, S. H. (2023b) Benzo[a]pyrene represses synaptic vesicle exocytosis by inhibiting P/Q-type calcium channels in hippocampal neurons. Ecotox. Environ. Safe 263, 115301.
- Kishi, R., Harabuchi, I., Katakura, Y., Ikeda, T. and Miyake, H. (1993) Neurobehavioral effects of chronic occupational exposure to organic-solvents among Japanese industrial painters. Environ. Res. 62, 303-313. https://doi.org/10.1006/enrs.1993.1115
- Klingauf, J., Kavalali, E. T. and Tsien, R. W. (1998) Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394, 581-585. https://doi.org/10.1038/29079
- Kononenko, N. L. and Haucke, V. (2015) Molecular mechanisms of presynaptic membrane retrieval and synaptic vesicle reformation. Neuron 85, 484-496. https://doi.org/10.1016/j.neuron.2014.12.016
- Kwon, S. K., Sando, R., Lewis, T. L., Hirabayashi, Y., Maximov, A. and Polleux, F. (2016) LKB1 regulates mitochondria-dependent presynaptic calcium clearance and neurotransmitter release properties at excitatory synapses along cortical axons. PLoS Biol. 14, e1002516.
- Langman, J. M. (1994) Xylene - its toxicity, measurement of exposure levels, absorption, metabolism and clearance. Pathology 26, 301-309. https://doi.org/10.1080/00313029400169711
- Laslo-Baker, D., Barrera, M., Knittel-Keren, D., Kozer, E., Wolpin, J., Khattak, S., Hackman, R., Rovet, J. and Koren, G. (2004) Child neurodevelopmental outcome and maternal occupational exposure to solvents. Arch. Pediat. Adol. Med. 158, 956-961. https://doi.org/10.1001/archpedi.158.10.956
- Li, Z. Y., Burrone, J., Tyler, W. J., Hartman, K. N., Albeanu, D. F. and Murthy, V. N. (2005) Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc. Natl. Acad. Sci. U. S. A. 102, 6131-6136. https://doi.org/10.1073/pnas.0501145102
- Luhmann, H. J., Sinning, A., Yang, J. W., Reyes-Puerta, V., Stüttgen, M. C., Kirischuk, S. and Kilb, W. (2016) Spontaneous neuronal activity in developing neocortical networks: from single cells to large-scale interactions. Front. Neural. Circuit. 10, 40.
- Macholz, R. M. (1982) The Handbook of Environmental Chemistry. Wiley., New York.
- Mao, T., O'Connor, D. H., Scheuss, V., Nakai, J. and Svoboda, K. (2008) Characterization and subcellular targeting of GCaMP-type genetically-encoded calcium indicators. PLoS One 3, e1796.
- Mark, M. D., Maejima, T., Kuckelsberg, D., Yoo, J. W., Hyde, R. A., Shah, V., Gutierrez, D., Moreno, R. L., Kruse, W., Noebels, J. L. and Herlitze, S. (2011) Delayed postnatal loss of P/Q-type calcium channels recapitulates the absence epilepsy, dyskinesia, and ataxia phenotypes of genomic mutations. J. Neurosci. 31, 4311-4326. https://doi.org/10.1523/JNEUROSCI.5342-10.2011
- McKinney, A. A., Petrova, R. and Panagiotakos, G. (2022) Calcium and activity-dependent signaling in the developing cerebral cortex. Development 149, dev198853.
- Nakamura, Y., Harada, H., Kamasawa, N., Matsui, K., Rothman, J. S., Shigemoto, R., Silver, R. A., DiGregorio, D. A. and Takahashi, T. (2015) Nanoscale distribution of presynaptic Ca(2+) channels and its impact on vesicular release during development. Neuron 85, 145-158. https://doi.org/10.1016/j.neuron.2014.11.019
- Nakaoka, H., Hisada, A., Matsuzawa, D., Yamamoto, M., Mori, C.; Japan Environment and Children's Study (JECS) Group; Kamijima, M., Yamazaki, S., Ohya, Y., Kishi, R., Yaegashi, N., Hashimoto, K., Mori, C., Ito, S., Yamagata, Z., Inadera, H., Nakayama, T., Iso, H., Shima, M., Kurozawa, Y., Suganuma, N., Kusuhara, K. and Katoh, T. (2021) Associations between prenatal exposure to volatile organic compounds and neurodevelopment in 12-month-old children: The Japan Environment and Children's Study (JECS). Sci. Total Environ. 794, 148643.
- Nanou, E. and Catterall, W. A. (2018) Calcium channels, synaptic plasticity, and neuropsychiatric disease. Neuron 98, 466-481. https://doi.org/10.1016/j.neuron.2018.03.017
- Nethery, E., Brauer, M. and Janssen, P. (2009) Time-activity patterns of pregnant women and changes during the course of pregnancy. J. Expo. Sci. Environ. Epidemiol. 19, 317-324. https://doi.org/10.1038/jes.2008.24
- Niaz, K., Bahadar, H., Maqbool, F. and Abdollahi, M. (2015) A review of environmental and occupational exposure to xylene and its health concerns. EXCLI J. 14, 1167-1186.
- Nimmervoll, B., Flucher, B. E. and Obermair, G. J. (2013) Dominance of P/Q-type calcium channels in depolarization-induced presynaptic FM dye release in cultured hippocampal neurons. Neuroscience 253, 330-340. https://doi.org/10.1016/j.neuroscience.2013.08.052
- Panda, S., Behera, S., Alam, M. F. and Syed, G. H. (2021) Endoplasmic reticulum & mitochondrial calcium homeostasis: the interplay with viruses. Mitochondrion 58, 227-242. https://doi.org/10.1016/j.mito.2021.03.008
- Pelé, F., Muckle, G., Costet, N., Garlantézec, R., Monfort, C., Multigner, L., Rouget, F. and Cordier, S. (2013) Occupational solvent exposure during pregnancy and child behaviour at age 2. Occup. Environ. Med. 70, 114-119. https://doi.org/10.1136/oemed-2012-100892
- Recchia, G., Perbellini, L., Prati, G. F., Dean, P. and Ancona, G. (1985) Coma caused by probably accidental ingestion of xylene: treatment with hemoperfusion using activated charcoal. Med. Lav. 76, 67-73.
- Rosenberg, S. S. and Spitzer, N. C. (2011) Calcium signaling in neuronal development. Cold Spring Harb. Perspect. Biol. 3, a004259.
- Savolainen, H. and Pfaffli, P. (1980) Dose-dependent neurochemical changes during short-term inhalation exposure to m-xylene. Arch. Toxicol. 45, 117-122. https://doi.org/10.1007/BF01270909
- Schneggenburger, R. and Neher, E. (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406, 889-893. https://doi.org/10.1038/35022702
- Tang, D. and Xu, L. (2005) Study on lipid peroxidation in workers exposed to benzene, toluene and xylene. Chinese Occup. Med. 2, 016.
- Taskinen, H., Kyyronen, P., Hemminki, K., Hoikkala, M., Lajunen, K. and Lindbohm, M. L. (1994) Laboratory work and pregnancy outcome. J. Occup. Med. 36, 311-319. https://doi.org/10.1097/00043764-199403000-00008
- Till, C., Koren, G. and Rovet, J. F. (2001) Prenatal exposure to organic solvents and child neurobehavioral performance. Neurotoxicol. Teratol. 23, 235-245. https://doi.org/10.1016/S0892-0362(01)00141-6
- Uchida, Y., Nakatsuka, H., Ukai, H., Watanabe, T., Liu, Y. T., Huang, M. Y., Wang, Y. L., Zhu, F. Z., Yin, H. and Ikeda, M. (1993) Symptoms and signs in workers exposed predominantly to xylenes. Int. Arch. Occup. Environ. Health 64, 597-605. https://doi.org/10.1007/BF00517707
- Ullman, J. C., Yang, J., Sullivan, M., Bendor, J., Levy, J., Pham, E., Silm, K., Seifikar, H., Sohal, V. S., Nicoll, R. A. and Edwards, R. H. (2018) A mouse model of autism implicates endosome pH in the regulation of presynaptic calcium entry. Nat. Commun. 9, 330.
- United States. Agency for Toxic Substances and Disease Registry, Research Triangle Institute, and Sciences International Inc. (1995) Toxicological profile for xylene. U.S. Dept. of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry, Atlanta, Ga. xvii, 270, 276, 273 p.
- Wang, S. B., Ang, H. M. and Tade, M. O. (2007) Volatile organic compounds in indoor environment and photocatalytic oxidation: State of the art. Environ Int. 33, 694-705. https://doi.org/10.1016/j.envint.2007.02.011
- Wang, X. L., Jin, X. P., Fu, H., Chen, Z. Q., Da, C. D., Huang, X. F. and Ding, B. Q. (1999) Xylene-induced effects on brain neurotransmitters, behavior and fos protein in rats. Biomed. Environ. Sci. 12, 116-124.
- Womack, M. D. and Khodakhah, K. (2004) Dendritic control of spontaneous bursting in cerebellar Purkinje cells. J. Neurosci. 24, 3511-3521. https://doi.org/10.1523/JNEUROSCI.0290-04.2004
- Wu, L. G., Westenbroek, R. E., Borst, J. G. G., Catterall, W. A. and Sakmann, B. (1999) Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J. Neurosci. 19, 726-736. https://doi.org/10.1523/JNEUROSCI.19-02-00726.1999
- Xue, L., Zhang, Z., McNeil, B. D., Luo, F., Wu, X. S., Sheng, J., Shin, W. and Wu, L. G. (2012) Voltage-dependent calcium channels at the plasma membrane, but not vesicular channels, couple exocytosis to endocytosis. Cell Rep. 1, 632-638. https://doi.org/10.1016/j.celrep.2012.04.011
- Yu, I. T. S., Lee, N. L., Zhang, X. H., Chen, W. O., Lam, Y. T. and Wong, T. W. (2004) Occupational exposure to mixtures of organic solvents increases the risk of neurological symptoms among printing workers in Hong Kong. J. Occup. Environ. Med. 46, 323-330. https://doi.org/10.1097/01.jom.0000121367.69269.07