Perfluorooctane Sulfonate Induces Apoptosis of Cerebellar Granule Cells via a ROS-dependent Protein Kinase C Signaling Pathway
Abstract
Perfluorinated chemicals (PFCs) have been widely used in a variety of industry and consumer products. Perfluorooctane sulfonate (PFOS), a prominent member of perfluoroalkyls, is known as a neurotoxicant in developing brain and affects behavior and motor activity. However, mechanism of neurotoxicity still remains unknown. In this study, we attempted to analyze apoptotic effects of PFOS on developing neuron. Cerebellar granule cells derived from 7-day old SD rats and grown in culture for additional 7 days were used to mimic postnatal day (PND)-14 conditions. PFOS exposure increased ROS production, which was blocked by ROS inhibitor, N-acetylcysteine (NAC). PFOS selectively induced dose-dependent translocations of PKC-α, -βII and -ɛ among PKC isozymes tested. The translocation of these specific PKC isozymes was blocked by NAC. A panel of different approaches was utilized to detect apoptotic effects. PFOS induced caspase-3 activity and nucleosomal DNA fragmentation in a dose-dependent manner, which were blocked by pretreatment of NAC. These apoptotic effects were further confirmed by TUNEL staining. Increases of caspase-3 activity and nucleosomal DNA fragmentation were dampened by the inhibition of PKC isozymes using siRNA technique. Taken together, our results suggest that PFOS may induce apoptosis of cerebellar granule cells via a ROS-mediated PKC signaling pathway. PKC signal transduction pathway is pivotal in learning and memory and apoptosis of neuronal cells is a critical event in neurotoxicity. Thus, this study may contribute to understand a new mechanistic aspect of PFOS-induced neurotoxicities.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Although actin filament remodeling has only been demonstrated in response to PFOS exposure, several other in vitro studies have demonstrated the ability of PFOS, PFOA, and PFOSA to generate reactive oxygen species in neurons and astrocytes.
“Whereas this actin filament remodeling has only been demonstrated in response to PFOS exposure, several other in vitro studies have also demonstrated the ability of PFOS, PFOA, and PFOSA, to generate ROS in neurons and astrocytes (Lee et al., 2012; Reistad et al., 2013; Chen et al., 2014; Li Z. et al., 2017).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Lee et al., 2012
Cites
Perfluoroalkyl Acids: A Review of Monitoring and Toxicological Findings
Lau, C., Anitole, K., Hodes, C., Lai, D., Pfahles-Hutchens, A., & Seed, J. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfm128 · Cited by 2,620 · see citing works
Peer Reviewed: Perfluorochemical Surfactants in the Environment
Giesy, J. P., & Kannan, K. (2002) · Environmental Science & Technology · doi:10.1021/es022253t · Cited by 1,103 · see citing works
Effects of perfluorooctanoic acid exposure during pregnancy in the mouse.
Lau, C., Thibodeaux, J. R., Hanson, R., Narotsky, M., Rogers, J. M., Lindstrom, A., & Strynar, M. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfj105 · Cited by 547 · see citing works
The Protein Kinase C Family for Neuronal Signaling
Tanaka, C., & Nishizuka, Y. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.003003 · Cited by 543 · see citing works
Perfluorinated compounds in aquatic organisms at various trophic levels in a Great Lakes food chain
Kannan, K., Tao, L., Sinclair, E., Pastva, S. D., Jude, D. J., & Giesy, J. P. (2005) · Archives of Environmental Contamination and Toxicology · doi:10.1007/s00244-004-0133-x · Cited by 530 · see citing works
Protein Phosphorylation and Neuronal Function
Browning, M. D., Huganir, R. L., & Greengard, P. (1985) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1985.tb05468.x · Cited by 528 · see citing works
Johansson, N., Fredriksson, A., & Eriksson, P. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2007.10.008 · Cited by 463 · see citing works
Chen, C., Kano, M., Abeliovich, A., Chen, L., Bao, S., Kim, J. J., Hashimoto, K., Thompson, R. F., & Tonegawa, S. (1995) · Cell · doi:10.1016/0092-8674(95)90148-5 · Cited by 385 · see citing works
Liu, C., YU, K., SHI, X., Wang, J., Lam, P. K. S., Wu, R. S. S., & Zhou, B. S. (2007) · Aquatic Toxicology · doi:10.1016/j.aquatox.2007.02.006 · Cited by 367 · see citing works
Johansson, N., Eriksson, P., & Viberg, H. (2009) · Toxicological Sciences · doi:10.1093/toxsci/kfp029 · Cited by 284 · see citing works
Developmental Neurotoxicity of Perfluorinated Chemicals Modeled <i>in Vitro</i>
Slotkin, T. A., MacKillop, E. A., Melnick, R. L., Thayer, K. A., & Seidler, F. J. (2008) · Environmental Health Perspectives · doi:10.1289/ehp.11253 · Cited by 225 · see citing works
Eriksen, K. T., Raaschou‐Nielsen, O., Sørensen, M., Roursgaard, M., Loft, S. H., & Möller, P. (2010) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2010.04.024 · Cited by 192 · see citing works
New Insights and New Issues in Developmental Neurotoxicology
Olney, J. W. (2002) · NeuroToxicology · doi:10.1016/s0161-813x(01)00092-4 · Cited by 191 · see citing works
Qian, Y., Ducatman, A., Ward, R., Leonard, S., Bukowski, V., Lan Guo, N., Shi, X., Vallyathan, V., & Castranova, V. (2010) · Journal of Toxicology and Environmental Health, Part A · doi:10.1080/15287391003689317 · Cited by 191 · see citing works
Lithium Decreases Membrane‐Associated Protein Kinase C in Hippocampus: Selectivity for the α Isozyme
Manji, H. K., Etcheberrigaray, R., Chen, G., & Olds, J. L. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb07474.x · Cited by 161 · see citing works
Redox Regulation of the Intrinsic Pathway in Neuronal Apoptosis
Franklin, J. L. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3596 · Cited by 151 · see citing works
Protein phosphorylation and neuronal function.
Walaas, S. I., & Greengard, P. (1991) · Pharmacological Reviews · doi:10.1016/s0031-6997(25)06666-9 · Cited by 137 · see citing works
Mariussen, E., Myhre, O., Reistad, T., & Fonnum, F. (2002) · Toxicology and Applied Pharmacology · doi:10.1006/taap.2002.9353 · Cited by 133 · see citing works
Viberg, H., Mundy, W. R., & Eriksson, P. (2007) · NeuroToxicology · doi:10.1016/j.neuro.2007.10.007 · Cited by 131 · see citing works
Protein kinase C: a physiological mediator of enhanced transmitter output
Majewski, H., & Iannazzo, L. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00017-3 · Cited by 116 · see citing works
Harada, K. H., Yang, H.-R., Moon, C.-S., Hung, N. N., Hitomi, T., Inoue, K., Niisoe, T., Watanabe, T., Kamiyama, S., Takenaka, K., et al. (2010) · Chemosphere · doi:10.1016/j.chemosphere.2010.01.027 · Cited by 102 · see citing works
Matsushima, H., Shimohama, S., Chachin, M., Taniguchi, T., & Kimura, J. (1996) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1996.67010317.x · Cited by 95 · see citing works
Kodavanti, P. R. S., Ward, T. R., Ludewig, G., Robertson, L. W., & Birnbaum, L. S. (2005) · Toxicological Sciences · doi:10.1093/toxsci/kfi289 · Cited by 95 · see citing works
Wang, X., Li, B., Zhao, W., Liu, Y., Shang, D., Fang, W., & Chen, Y. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.05.128 · Cited by 88 · see citing works
Morikawa, A., Kamei, N., Harada, K. H., Inoue, K., Yoshinaga, T., Saito, N., & Koizumi, A. (2005) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2005.03.007 · Cited by 81 · see citing works
Neurotoxicity of perfluorooctane sulfonate (PFOS) in rats and mice after single oral exposure
Sato, I., Kawamoto, K., Nishikawa, Y., Tsuda, S., Yoshida, M., Yaegashi, K., Saito, N., Liu, W., & Jin, Y. (2009) · The Journal of Toxicological Sciences · doi:10.2131/jts.34.569 · Cited by 62 · see citing works
How is protein kinase C activated in CNS
Huang, K., & Huang, F. L. (1993) · Neurochemistry International · doi:10.1016/0197-0186(93)90037-6 · Cited by 57 · see citing works
Possible Molecular Targets of Halogenated Aromatic Hydrocarbons in Neuronal Cells
Yang, J., & Kodavanti, P. R. S. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.4283 · Cited by 51 · see citing works
Neurobehavioral Teratogenicity of Perfluorinated Alkyls in an Avian Model
Pinkas, A., Slotkin, T. A., Brick-Turin, Y., Van der Zee, E. A., & Yanai, J. (2010) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2009.11.004 · Cited by 48 · see citing works
Son, H., Madelian, V., & Carpenter, D. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00836-0 · Cited by 33 · see citing works
Beer, A., Slotkin, T. A., Seidler, F. J., Aldridge, J. E., & Yanai, J. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300582 · Cited by 31 · see citing works
Perfluorooctane Sulfonate Induces Apoptosis in N9 Microglial Cell Line
Zhang, L., Li, Y., Zeng, H., Li, M., Wan, Y., Schluesener, H. J., Zhang, Z., & Xu, S. (2010) · International Journal of Toxicology · doi:10.1177/1091581810387832 · Cited by 28 · see citing works
2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptosis of articular chondrocytes in culture
Yang, J., & Lee, H.-G. (2010) · Chemosphere · doi:10.1016/j.chemosphere.2010.01.040 · Cited by 25 · see citing works
Protein kinase C expression and activity in the human brain after ischaemic stroke
Krupiński, J., Kumar, M., Gaffney, J. J., & Kałuza, J. (1998) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-1998-1254 · Cited by 20 · see citing works
Reversal of heroin neurobehavioral teratogenicity by grafting of neural progenitors
Katz, S., Ben‐Hur, T., Ben-Shaanan, T. L., & Yanai, J. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05004.x · Cited by 18 · see citing works
Second messenger systems in brains of patients with Parkinson's or Huntington's disease.
Tanaka, C., Nishino, N., Hashimoto, T., Kitamura, N., Yoshihara, C., & Saito, N. (1993) · PubMed · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Environmental pollution, a hidden culprit for health issues
Xu, H., Yang, J., Sun, Z., Su, J., Liu, Q. S., Zhou, Q., & Jiang, G. (2022) · Eco-Environment & Health · doi:10.1016/j.eehl.2022.04.003 · Cited by 334 · see citing works
Lopez-Suarez, L., Awabdh, S. A., Coumoul, X., & Chauvet, C. (2022) · NeuroToxicology · doi:10.1016/j.neuro.2022.07.008 · Cited by 248 · see citing works
Starnes, H. M., Rock, K. D., Jackson, T. W., & Belcher, S. M. (2022) · Frontiers in Toxicology · doi:10.3389/ftox.2022.881584 · Cited by 166 · see citing works
Neurotoxicity of Perfluorooctane Sulfonate to Hippocampal Cells in Adult Mice
Long, Y., Wang, Y., Ji, G., Yan, L., Hu, F., & Gu, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054176 · Cited by 106 · see citing works
Chen, N., Li, J., Li, D., Yang, Y., & He, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113453 · Cited by 105 · see citing works
Di Nisio, A., Pannella, M., Vogiatzis, S., Sut, S., Dall'Acqua, S., Rocca, M. S., Antonini, A., Porzionato, A., De Caro, R., Bortolozzi, M., et al. (2022) · Environment International · doi:10.1016/j.envint.2021.106982 · Cited by 103 · see citing works
Han, R., Hu, M., Zhong, Q., Wan, C., Liu, L., Li, F., Zhang, F., & Ding, W. (2017) · Chemosphere · doi:10.1016/j.chemosphere.2017.08.070 · Cited by 97 · see citing works
Tukker, A. M., Bouwman, L. M. S., van Kleef, R. G. D. M., Hendriks, H. S., Legler, J., & Westerink, R. H. S. (2020) · Scientific Reports · doi:10.1038/s41598-020-62152-2 · Cited by 92 · see citing works
Fetal Exposure to Perfluorinated Compounds and Attention Deficit Hyperactivity Disorder in Childhood
Ode, A., Källén, K., Gustafsson, P., Rylander, L., Jönsson, B., Olofsson, P., Ivarsson, S. A., Lindh, C. H., & Rignell‐Hydbom, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0095891 · Cited by 82 · see citing works
Perfluoroalkyl Chemicals in Neurological Health and Disease: Human Concerns and Animal Models
Piekarski, D., Diaz, K., & McNerney, M. (2020) · NeuroToxicology · doi:10.1016/j.neuro.2020.01.001 · Cited by 76 · see citing works
Perfluorooctane sulfonate effects on the reproductive axis in adult male rats
López-Doval, S., Salgado, R., Pereiro, N., Moyano, R., & Lafuente, A. (2014) · Environmental Research · doi:10.1016/j.envres.2014.07.006 · Cited by 76 · see citing works
Cranberries (Oxycoccus quadripetalus) inhibit adipogenesis and lipogenesis in 3T3-L1 cells
Kowalska, K., Olejnik, A. M., Rychlik, J., & Grajek, W. (2013) · Food Chemistry · doi:10.1016/j.foodchem.2013.10.032 · Cited by 66 · see citing works
Li, Z., Liu, Q., Liu, C., Li, C., Li, Y., Li, S., Liu, X., & Shao, J. (2016) · Toxicology in Vitro · doi:10.1016/j.tiv.2016.11.002 · Cited by 63 · see citing works
Yuan, Z., Shao, X., Miao, Z., Zhao, B., Zheng, Z., & Zhang, J. (2018) · Chemosphere · doi:10.1016/j.chemosphere.2018.05.011 · Cited by 64 · see citing works
Su, P., Zhang, J., Wang, S., Aschner, M., Cao, Z., Zhao, F., Wang, D., Chen, J., & Luo, W. (2016) · NeuroToxicology · doi:10.1016/j.neuro.2015.12.019 · Cited by 64 · see citing works
Guo, J., Wu, P., Cao, J., Luo, Y., Chen, J., Wang, G., Guo, W., Wang, T., & He, X. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.05.018 · Cited by 63 · see citing works
Goodman, C. V., Till, C., Green, R. R., El-Sabbagh, J., Arbuckle, T. E., Hornung, R., Lanphear, B. P., Séguin, J. R., Booij, L., Fisher, M. M., et al. (2023) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2023.107181 · Cited by 63 · see citing works
XIAO, W., Jiang, Y., Men, Q., Yuan, L., Huang, Z., Liu, T., Li, W., & LIU, X. (2014) · International Journal of Oncology · doi:10.3892/ijo.2014.2735 · Cited by 62 · see citing works
Neurotoxic effects of perfluoroalkyl acids: Neurobehavioral deficit and its molecular mechanism
Wang, Y., Wang, L., Chang, W., Zhang, Y., Zhang, Y., & Liu, W. (2019) · Toxicology Letters · doi:10.1016/j.toxlet.2019.01.012 · Cited by 60 · see citing works
Salgado, R., López-Doval, S., Pereiro, N., & Lafuente, A. (2016) · Toxicology Letters · doi:10.1016/j.toxlet.2015.10.023 · Cited by 58 · see citing works
Perfluorooctane sulfonate (PFOS) induced embryotoxicity and disruption of cardiogenesis
Cheng, W., Yu, Z., Feng, L., & Wang, Y. (2013) · Toxicology in Vitro · doi:10.1016/j.tiv.2013.03.014 · Cited by 58 · see citing works
Li, Y., Men, B., He, Y., Xu, H., Liu, M., & Wang, D. (2017) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2017.06.140 · Cited by 57 · see citing works
Çelık, A., Eke, D., Ekinci, S. Y., & Yıldırım, S. (2012) · Food and Chemical Toxicology · doi:10.1016/j.fct.2012.11.054 · Cited by 55 · see citing works
Zhang, Q., Liu, W., Niu, Q. L., Wang, Y., Zhao, H., Zhang, H., Song, J., Tsuda, S., & Saito, N. (2016) · Toxicology Research · doi:10.1039/c5tx00184f · Cited by 55 · see citing works
Li, S., Qin, S., Zeng, H., Chou, W., Oudin, A., Kanninen, K. M., Jalava, P., Dong, G., & Zeng, X. (2024) · Eco-Environment & Health · doi:10.1016/j.eehl.2024.08.002 · Cited by 54 · see citing works
Wang, C., Nie, X., Zhang, Y., Li, T., Mao, J., Liu, X., Gu, Y., Shi, J., Xiao, J., Wan, C., et al. (2015) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2015.06.012 · Cited by 50 · see citing works
Lee, Y. J., Lee, H.-G., & Yang, J. (2012) · Chemosphere · doi:10.1016/j.chemosphere.2012.08.033 · Cited by 49 · see citing works
Berntsen, H. F., Bjørklund, C. G., Audinot, J., Hofer, T., Verhaegen, S., Lentzen, E., Gutleb, A. C., & Ropstad, E. (2017) · NeuroToxicology · doi:10.1016/j.neuro.2017.09.005 · Cited by 48 · see citing works
Khezri, A., Fraser, T., Nourizadeh-Lillabadi, R., Kamstra, J., Berg, V., Zimmer, K., & Ropstad, E. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18020291 · Cited by 47 · see citing works
Yao, X., Cao, J., Xu, L., Sun, X., Kang, J., Yang, G., Jiang, L., Geng, C., Gao, C., Zhong, L., et al. (2014) · Food and Chemical Toxicology · doi:10.1016/j.fct.2014.02.017 · Cited by 47 · see citing works
Zhang, H., Yolton, K. A., Webster, G. M., Ye, X., Calafat, A. M., Dietrich, K. N., Xu, Y. Y., Xie, C., Braun, J. M., Lanphear, B. P., et al. (2017) · Environment International · doi:10.1016/j.envint.2017.11.031 · Cited by 47 · see citing works
ROS-mediated apoptosis of HAPI microglia through p53 signaling following PFOS exposure
Ge, J., Wang, C., Nie, X., Yang, J., Lu, H., Song, X., Su, K., Li, T., Han, J., Zhang, Y., et al. (2016) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2016.06.025 · Cited by 47 · see citing works
NMDA receptor-mediated ERK 1/2 pathway is involved in PFHxS-induced apoptosis of PC12 cells
Lee, Y. J., Choi, S.-Y., & Yang, J. (2014) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2014.01.114 · Cited by 45 · see citing works
Pereiro, N., Moyano, R., Blanco, A., & Lafuente, A. (2014) · Toxicology Letters · doi:10.1016/j.toxlet.2014.01.003 · Cited by 42 · see citing works
Fede, C., Selvestrel, F., Compagnin, C., Mognato, M., Mancin, F., Reddi, E., & Celotti, L. (2012) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-012-6246-6 · Cited by 43 · see citing works
Lucas, J. H., Wang, Q., & Rahman, I. (2022) · Toxicological Sciences · doi:10.1093/toxsci/kfac096 · Cited by 40 · see citing works
ROS‐Triggered Autophagy Is Involved in PFOS‐Induced Apoptosis of Human Embryo Liver L‐02 Cells
Zeng, H., Zhu, B., Wang, Y.-Q., & He, Q. (2021) · BioMed Research International · doi:10.1155/2021/6625952 · Cited by 39 · see citing works
ROS-mediated JNK pathway critically contributes to PFOS-triggered apoptosis in SH-SY5Y cells
Sun, P., Gu, L., Luo, J., Qin, Y., Sun, L., & Jiang, S. (2019) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2019.106821 · Cited by 39 · see citing works
Alharthy, S. A., & Hardej, D. (2021) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2021.103652 · Cited by 38 · see citing works
Kim, J. H., Park, H. Y., Jeon, J. D., Kho, Y., Kim, S., Park, M.-S., & Hong, Y. (2015) · European Journal of Nutrition · doi:10.1007/s00394-015-0915-0 · Cited by 38 · see citing works
PFHxS induces apoptosis of neuronal cells via ERK1/2-mediated pathway
Lee, Y. J., Choi, S.-Y., & Yang, J. (2013) · Chemosphere · doi:10.1016/j.chemosphere.2013.09.059 · Cited by 37 · see citing works
Perfluorooctane sulfonate mediates secretion of IL-1β through PI3K/AKT NF-кB pathway in astrocytes
Chen, X., Nie, X., Mao, J., Zhang, Y., Yin, K., Sun, P., Luo, J., Liu, Y., Jiang, S., & Sun, L. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2018.03.004 · Cited by 37 · see citing works
Connexin 43 mediates PFOS-induced apoptosis in astrocytes
Dong, L., Yang, X., Gu, W., Zhao, K., Ge, H., Zhou, J., & Bai, X. (2015) · Chemosphere · doi:10.1016/j.chemosphere.2015.02.041 · Cited by 36 · see citing works
Perfluoroalkyl substances, thyroid hormones, and neuropsychological status in older adults
Shrestha, S., Bloom, M. S., Yucel, R. M., Seegal, R. F., Rej, R., McCaffrey, R. J., Wu, Q., Kannan, K., & Fitzgerald, E. F. (2016) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2016.12.013 · Cited by 35 · see citing works
Yao, X., Sha, S., Wang, Y., Sun, X., Cao, J., Kang, J., Jiang, L., Chen, M., & Ma, Y. (2016) · Toxicological Sciences · doi:10.1093/toxsci/kfw118 · Cited by 34 · see citing works
Eke, D., Çelık, A., Yılmaz, M. B., Aras, N., Sel, S. K., & Alptekın, D. (2017) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2017.06.075 · Cited by 31 · see citing works
Berntsen, H. F., Bjørklund, C. G., Strandabø, R. A. U., Haug, T. M., Moldes‐Anaya, A., Fuentes-Lazaro, J., Verhaegen, S., Paulsen, R. E., Tasker, R. A., & Ropstad, E. (2018) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2018.08.015 · Cited by 30 · see citing works
Bi, C., Junaid, M., Liu, Y., Guo, W., Jiang, X., Pan, B., Li, Z., & Xu, N. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.134242 · Cited by 29 · see citing works
Zhang, H., Zhang, C., Xu, D., Wang, Q., & Xu, D. (2023) · Environmental Pollution · doi:10.1016/j.envpol.2023.121650 · Cited by 29 · see citing works
Triningsih, D., Yang, J., Sim, K. H., Lee, C., & Lee, Y. J. (2021) · Toxicology in Vitro · doi:10.1016/j.tiv.2021.105105 · Cited by 27 · see citing works
Zhuchen, H.-Y., Wang, J., Liu, X., & Shi, Y. (2023) · Toxics · doi:10.3390/toxics11070571 · Cited by 28 · see citing works
Associations between the serum levels of PFOS/PFOA and IgG N-glycosylation in adult or children
Liu, J., Liu, S., Huang, Z., Fu, Y., Fei, J., Liu, X., & He, Z. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.114285 · Cited by 26 · see citing works
Wen, L., Chen, Y., Lee, Y.-C. G., Ko, T.-L., Chou, H., & Juan, S. (2021) · PLoS ONE · doi:10.1371/journal.pone.0245442 · Cited by 23 · see citing works
Huang, Q., Zhang, J., Peng, S., Du, M., Ow, S. Y., Pu, H., Pan, C., & Shen, H. (2013) · Journal of Applied Toxicology · doi:10.1002/jat.2963 · Cited by 23 · see citing works
Berntsen, H. F., Duale, N., Bjørklund, C. G., Rangel-Huerta, Ó. D., Dyrberg, K., Hofer, T., Rakkestad, K. E., Østby, G. C., Halsne, R., Boge, G. S., et al. (2020) · Environment International · doi:10.1016/j.envint.2020.106240 · Cited by 23 · see citing works
Choi, S., Kim, J., Park, J., Lee, K., Kim, E., & Jeon, W. B. (2013) · Food and Chemical Toxicology · doi:10.1016/j.fct.2013.07.070 · Cited by 21 · see citing works
Bull, S., Burnett, K., Vassaux, K., Ashdown, L., Brown, T., & Rushton, L. (2014) · EFSA Supporting Publications · doi:10.2903/sp.efsa.2014.en-572 · Cited by 20 · see citing works
Xu, T., Li, P., Wu, S., Li, D., Wu, J., Raley‐Susman, K. M., & He, D. (2016) · Bulletin of Environmental Contamination and Toxicology · doi:10.1007/s00128-016-1808-5 · Cited by 19 · see citing works
Perfluorooctane Sulfonate Disturbs Nanog Expression through miR-490-3p in Mouse Embryonic Stem Cells
Xu, B., Chen, X., Mao, Z., Chen, M., Han, X., Du, G., Ji, X., Chang, C., Rehan, V. K., Wang, X., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074968 · Cited by 19 · see citing works
Patel, R., Bradner, J. M., Stout, K. A., & Caudle, W. M. (2016) · Medical Sciences · doi:10.3390/medsci4030013 · Cited by 19 · see citing works
Yadav, A., Verhaegen, S., Verbruggen, E., Kerhoas, M., Huiberts, E. H. W., Hadera, M. G., Berntsen, H. F., Zimmer, K. E., Ropstad, E., & Paulsen, R. E. (2021) · Reproductive Toxicology · doi:10.1016/j.reprotox.2021.01.008 · Cited by 18 · see citing works
Park, S.-J., Sim, K. H., Shrestha, P., Yang, J., & Lee, Y. J. (2021) · Food and Chemical Toxicology · doi:10.1016/j.fct.2021.112478 · Cited by 17 · see citing works
Eke, D., & Çelık, A. (2015) · Drug and Chemical Toxicology · doi:10.3109/01480545.2015.1041601 · Cited by 18 · see citing works
Astrocytes Prevent Ethanol Induced Apoptosis of Nrf2 Depleted Neurons by Maintaining GSH Homeostasis
Narasimhan, M., Rathinam, M., Patel, D., Henderson, G. I., & Mahimainathan, L. (2012) · Open Journal of Apoptosis · doi:10.4236/ojapo.2012.12002 · Cited by 17 · see citing works
Mayilswami, S., Krishnan, K., Megharaj, M., & Naidu, R. (2014) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2014.09.017 · Cited by 17 · see citing works
Wang, Y., Zhao, H., Zhang, Q., Liu, W., & Quan, X. (2015) · Toxicology Research · doi:10.1039/c4tx00177j · Cited by 17 · see citing works
A subcellular study on reactive oxygen species generation by PFAS in HepG2 cells
Amstutz, V. H., Mircheva, A., Cengo, A., Dubois, L. J., Sijm, D. T. H. M., & Vrolijk, M. F. (2025) · Scientific Reports · doi:10.1038/s41598-025-07503-7 · Cited by 17 · see citing works
Sim, K. H., & Lee, Y. J. (2021) · Chemosphere · doi:10.1016/j.chemosphere.2021.132503 · Cited by 15 · see citing works
Mousavi, S. E., Yu, Q., & Shin, H. (2025) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2025.178972 · Cited by 13 · see citing works
Fang, X., Zhang, X., & Li, H. (2020) · Toxicology and Industrial Health · doi:10.1177/0748233720957534 · Cited by 13 · see citing works
Potential health effects of emerging environmental contaminants perfluoroalkyl compounds
Lee, Y. J. (2018) · Journal of Yeungnam Medical Science · doi:10.12701/yujm.2018.35.2.156 · Cited by 12 · see citing works
Wu, K., Tang, A., Zhang, X., Zhou, S., Wu, N., Tao, J., Chen, Y., Yang, G., Zhou, H., & You, M. (2025) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2025.118519 · Cited by 9 · see citing works
Hossain, M. M., Nawaz, M. Z., Dar, M. A., Geng, A., Alghamdi, H. A., Han, S. Y., & Zhu, D. (2024) · Journal of Hazardous Materials Advances · doi:10.1016/j.hazadv.2024.100579 · Cited by 9 · see citing works
Oxidative damage mechanism in Saccharomyces cerevisiae cells exposed to tetrachlorobisphenol A
Zhang, X., Zhang, Y., Ji, Z., Wang, F., Zhang, L., Song, M., & Li, H. (2020) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2020.103507 · Cited by 8 · see citing works
de Macedo, G. T., Claro, M. T., Ferreira, S. A., Loreto, J. S., Ajayi, B. O., Prestes, A. D. S., Adedara, I. A., Müller, T. E., dos Santos, M. M., & Barbosa, N. V. (2025) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2025.179972 · Cited by 7 · see citing works
Multiple toxicity evaluations of perfluorooctane sulfonate on intact planarian Dugesia japonica
Sun, J., Shao, X., Huang, J., Gong, M., Zhang, J., & Yuan, Z. (2023) · Environmental Science and Pollution Research · doi:10.1007/s11356-023-26842-4 · Cited by 7 · see citing works
Wu, P., Ding, C., Yan, M., Qian, B., Wang, W., Sun, P., & Zhao, J. (2019) · The Journal of Toxicological Sciences · doi:10.2131/jts.44.657 · Cited by 6 · see citing works
Viberg, H., & Mariussen, E. (2015) · Molecular and integrative toxicology · doi:10.1007/978-3-319-15518-0_9 · Cited by 5 · see citing works
Neurochemical mechanisms of perfluoroalkyl substances (PFAS) neurotoxic action
Brown-Leung, J. M., & Cannon, J. R. (2023) · Advances in neurotoxicology · doi:10.1016/bs.ant.2023.08.002 · Cited by 5 · see citing works
Sachdeva, S., Chatterjee, S., & Flora, S. J. S. (2020) · Medicine in Drug Discovery · doi:10.1016/j.medidd.2020.100045 · Cited by 4 · see citing works
Gonella, A., Giacomello, M., Finos, L., & Peruffo, A. (2025) · Research in Veterinary Science · doi:10.1016/j.rvsc.2025.105585 · Cited by 3 · see citing works
Importance of post-translational protein modifications in PFAS toxicity
Safreena, N., Chandra, G., Thirumalaikumar, V. P., & Cannon, J. R. (2025) · Toxicology · doi:10.1016/j.tox.2025.154260 · Cited by 4 · see citing works
Protein kinase cα is involved in impaired perinatal hypothyroid rat brain development
Zhang, H.-M., Lin, N., Dong, Y., Su, Q., & Luo, M. (2013) · Journal of Neuroscience Research · doi:10.1002/jnr.23125 · Cited by 2 · see citing works
Xie, C., Li, X., Wu, X., Zhang, S., Zhang, P., Vijver, M. G., Peijnenburg, W. J. G. M., Pang, Q., Lynch, I., & Guo, Z. (2025) · Environmental Research · doi:10.1016/j.envres.2025.122787 · Cited by 2 · see citing works
Ren, Z., Wang, X., Meng, L., Ren, D., Sun, J., Cai, Y., Duan, Y., Ning, X., Ku, T., & Sang, N. (2026) · Environment & Health · doi:10.1021/envhealth.5c00628 · Cited by 2 · see citing works
Toxicity assessment of perfluorooctane sulfonate on regenerating planarian Dugesia japonica
Sun, J., Huang, J., Gong, M., Shao, X., Zhang, J., & Yuan, Z. (2024) · Chemistry and Ecology · doi:10.1080/02757540.2024.2334464 · Cited by 1 · see citing works
Lorentzen, K. (2013) · BIBSYS Brage (BIBSYS (Norway)) · Cited by 1 · see citing works
Toxicología del sulfonato de perfluorooctano (PFOS) como modelo de compuesto orgánico fluorado
Pereiro, N., & Lafuente, A. (2012) · Redalyc (Universidad Autónoma del Estado de México)
Yao, X., & Ma, Y. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802936-7.00009-x
LI, D., Sun, L., Yuan, T., & Liang, X. (2017) · DEStech Transactions on Environment Energy and Earth Science · doi:10.12783/dteees/edep2017/15561
Fetal Exposure to Perfluorinated Compounds and Attention Deficit Hyperactivity Disorder in Childhood
Rignell‐Hydbom, A., Ode, A., Källén, K., Gustafsson, P., Rylander, L., Jönsson, B., Olofsson, P., Ivarsson, S. A., & Lindh, C. H. (2014) · ISEE Conference Abstracts · doi:10.1289/isee.2014.o-180
A review of cytotoxic effects of food additives on brain tissue
Karimi, F., Sadri, F., Soleimani, A., Azhdari, S., Karbasi, S., & Hosseini, S. F. (2025) · Nutritional Neuroscience · doi:10.1080/1028415x.2025.2573225
Moyano, P. M., Flores, A. N., Sanjuan, J., Plaza, J. C., Guerra-Menéndez, L., Naval, M. V., Abascal, L., Sierra, O. M., & del Pino, J. (2026) · Pharmaceutics · doi:10.3390/pharmaceutics18030292
Madorran, E., & Murua, A. (2026) · Environmental Science and Pollution Research · doi:10.1007/s11356-026-38056-5
- Authors
- Lee, H.-G., Lee, Y. J., & Yang, J.-H.
- Affiliations
- Daegu Catholic University (KR)
- Corresponding author
- Yang, Jae-Ho
- Venue
- NeuroToxicology
- Publisher
- Elsevier BV
- Published
- 2012-06
- Volume
- 33
- Issue
- 3
- Pages
- 314-320
- ISSN
- 0161-813X (ISSN-L)
- OpenAlex
- W2063924260
- Cited by
- 97
- References
- 36
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 3 · 2023: 5 · 2022: 5 · 2021: 8 · 2020: 7 · 2019: 4 · 2018: 4 · 2017: 8 · 2016: 9 · 2015: 8 · 2014: 11 · 2013: 8 · 2012: 6
- FWCI
- 8.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroToxicology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Land, Transport and Maritime Affairs
- Topics
- Physical Sciences › Environmental Science › Environmental Chemistry › Per- and polyfluoroalkyl substances research
- Life Sciences › Neuroscience › Developmental Neuroscience › Anesthesia and Neurotoxicity Research
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmaceutical Science › Fluorine in Organic Chemistry
- Keywords
- PFOS, neurotoxicity, apoptosis, cerebellar granule cells, reactive oxygen species, protein kinase C, PKC isoforms, caspase-3, N-acetylcysteine, postnatal development
- MeSH terms
- Animals, Antioxidants, Cell Survival, Cells, Cultured, Cerebellum, Dose-Response Relationship, Drug, Enzyme Activation, Fluorocarbons, Isoenzymes, Neurons, Protein Kinase C, Transfection, Signal Transduction, Rats, Sprague-Dawley, Apoptosis, Reactive Oxygen Species, Alkanesulfonic Acids, Oxidative Stress, Neurotoxicity Syndromes, In Situ Nick-End Labeling, Protein Transport, RNA Interference, Rats, Caspase 3, DNA Fragmentation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review