New perspective on the regulation of acetylcholinesterase via the aryl hydrocarbon receptor.
acetylcholinesterase
aryl hydrocarbon receptor
dioxin
dioxin-response element
microRNA
neurodevelopment
Journal
Journal of neurochemistry
ISSN: 1471-4159
Titre abrégé: J Neurochem
Pays: England
ID NLM: 2985190R
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
revised:
24
11
2020
received:
30
09
2020
accepted:
30
11
2020
pubmed:
6
12
2020
medline:
18
11
2021
entrez:
5
12
2020
Statut:
ppublish
Résumé
Acetylcholinesterase (AChE, EC 3.1.1.7) plays important roles in cholinergic neurotransmission and has been widely recognized as a biomarker for monitoring pollution by organophosphate (OP) and carbamate pesticides. Dioxin is an emerging environmental AChE disruptor and is a typical persistent organic pollutant with multiple toxic effects on the nervous system. Growing evidence has shown that there is a significant link between dioxin exposure and neurodegenerative diseases and neurodevelopmental disorders, most of which involve AChE and cholinergic dysfunctions. Therefore, an in-depth understanding of the effects of dioxin on AChE and the related mechanisms of action might help to shed light on the molecular bases of dioxin impacts on the nervous system. In the past decade, the effects of dioxins on AChE have been revealed in cultured cells of different origins and in rodent animal models. Unlike OP and carbamate pesticides, dioxin-induced AChE disturbance is not due to direct inhibition of enzymatic activity; instead, dioxin causes alterations of AChE expression in certain models. As a widely accepted mechanism for most dioxin effects, the aryl hydrocarbon receptor (AhR)-dependent pathway has become a research focus in studies on the mechanism of action of dioxin-induced AChE dysregulation. In this mini-review, the effects of dioxin on AChE and the diverse roles of the AhR pathway in AChE regulation are summarized. Additionally, the involvement of AhR in AChE regulation during different neurodevelopmental processes is discussed. These AhR-related findings might also provide new insight into AChE regulation triggered by diverse xenobiotics capable of interacting with AhR.
Substances chimiques
Dioxins
0
Receptors, Aryl Hydrocarbon
0
Acetylcholinesterase
EC 3.1.1.7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1254-1262Informations de copyright
© 2020 International Society for Neurochemistry.
Références
Abou-Donia, M. B., Siracuse, B., Gupta, N., & Sobel Sokol, A. (2016). Sarin (GB, O-isopropyl methylphosphonofluoridate) neurotoxicity: Critical review. Critical Reviews in Toxicology, 46, 845-875. https://doi.org/10.1080/10408444.2016.1220916
Agency U. E. P. (2000) Exposure and human health reassessment of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds. US Environmental Protection Agency, Office of Research and Development….
Ahmed, R. G. (2011). Perinatal TCDD exposure alters developmental neuroendocrine system. Food and Chemical Toxicology, 49, 1276-1284. https://doi.org/10.1016/j.fct.2011.03.008
Barron, M. G., & Woodburn, K. B. (1995). Ecotoxicology of chlorpyrifos. Reviews of Environmental Contamination and Toxicology, 144, 1-93.
Benazizaloya, R., Seidman, S., Timberg, R., Sternfeld, M., Zakut, H., & Soreq, H. (1993). Expression of a human acetylcholinesterase promoter reporter construct in developing neuromuscular-junctions of xenopus embryos. Proceedings of the National Academy of Sciences of the United States of America, 90, 2471-2475. https://doi.org/10.1073/pnas.90.6.2471
Bouchard, M. F., Oulhote, Y., Sagiv, S. K., Saint-Amour, D., & Weuve, J. (2014). Polychlorinated biphenyl exposures and cognition in older US adults: NHANES (1999-2002). Environmental Health Perspectives, 122, 73-78. https://doi.org/10.1289/ehp.1306532
Butcher, L. L. (1995). Cholinergic neurons and networks. The Rat Nervous System, 1003-1015.
Cajaraville, M. P., Bebianno, M. J., Blasco, J., Porte, C., Sarasquete, C., & Viarengo, A. (2000). The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: A practical approach. Science of the Total Environment, 247, 295-311. https://doi.org/10.1016/S0048-9697(99)00499-4
Chatonnet, F., Boudinot, E., Chatonnet, A., Taysse, L., Daulon, S., Champagnat, J., & Foutz, A. S. (2003). Respiratory survival mechanisms in acetylcholinesterase knockout mouse. European Journal of Neuroscience, 18, 1419-1427. https://doi.org/10.1046/j.1460-9568.2003.02867.x
Chobtang, J., de Boer, I. J., Hoogenboom, R. L., Haasnoot, W., Kijlstra, A., & Meerburg, B. G. (2011). The need and potential of biosensors to detect dioxins and dioxin-like polychlorinated biphenyls along the milk, eggs and meat food chain. Sensors (Basel), 11, 11692-11716. https://doi.org/10.3390/s111211692
Colović, M. B., Krstić, D. Z., Lazarević-Pašti, T. D., Bondžić, A. M., & Vasić, V. M. (2013). Acetylcholinesterase inhibitors: Pharmacology and toxicology. Current Neuropharmacology, 11, 315-335.
Cowley, S., Paterson, H., Kemp, P., & Marshall, C. J. (1994). Activation of map kinase kinase is necessary and sufficient for pc12 differentiation and for transformation of nih 3t3 cells. Cell, 77, 841-852.
Denison, M. S., & Nagy, S. R. (2003). Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annual Review of Pharmacology and Toxicology, 43, 309-334.
Denison, M. S., Soshilov, A. A., He, G. C., DeGroot, D. E., & Zhao, B. (2011). Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (Dioxin) receptor. Toxicological Sciences, 124, 1-22.
Elyakim, E., Sitbon, E., Faerman, A., Tabak, S., Montia, E., Belanis, L., Dov, A., Marcusson, E. G., Bennett, C. F., Chajut, A., & Cohen, D. (2010). hsa-miR-191 is a candidate oncogene target for hepatocellular carcinoma therapy. Cancer Research, 70, 8077-8087.
Endo, T., Kakeyama, M., Uemura, Y., Haijima, A., Okuno, H., Bito, H., & Tohyama, C. (2012). Executive function deficits and social-behavioral abnormality in mice exposed to a low dose of dioxin in utero and via lactation. PLoS One, 7, e50741.
EPA (2003). Exposure and Human Health Reassessment of 2,3,7,8-Tetrachlorodibenzo-p-Dioxin (TCDD) and Related Compounds. Environmental Protection Agency.
Eskenazi, B., Warner, M., Brambilla, P., Signorini, S., Ames, J., & Mocarelli, P. (2018). The Seveso accident: A look at 40 years of health research and beyond. Environment International, 121, 71-84.
Ferrario, J. B., Byrne, C. J., & Cleverly, D. H. (2000a). 2,3,7,8-Dibenzo-p-dioxins in Mined Clat products from the United States: Evidence for possible. Environmental Science and Technology, 34, 4524-4532.
Ferrario, J. B., Byrne, C. J., & Cleverly, D. H. (2000b). 2,3,7,8-Dibenzo-p-dioxins in Mined Clay products from the United States: Evidence for possible natural origin. Environmental Science and Technology, 34, 4524-4532.
Getman, D. K., Mutero, A., Inoue, K., & Taylor, P. (1995). Transcription factor repression and activation of the human acetylcholinesterase gene. The Journal of Biological Chemistry, 270, 23511-23519. https://doi.org/10.1074/jbc.270.40.23511
Gu, Y. Z., Hogenesch, J. B., & Bradfield, C. A. (2000). The PAS superfamily: Sensors of environmental and developmental signals. Annual Review of Pharmacology and Toxicology, 40, 519-561. https://doi.org/10.1146/annurev.pharmtox.40.1.519
Hanieh, H. (2015). Aryl hydrocarbon receptor-microRNA-212/132 axis in human breast cancer suppresses metastasis by targeting SOX4. Molecular Cancer, 14(1), 1-3.
Hanieh, H., & Alzahrani, A. (2013). MicroRNA-132 suppresses autoimmune encephalomyelitis by inducing cholinergic anti-inflammation: A new Ahr-based exploration. European Journal of Immunology, 43, 2771-2782. https://doi.org/10.1002/eji.201343486
Hanin, G., Shenhar-Tsarfaty, S., Yayon, N., Yau, Y. H., Bennett, E. R., Sklan, E. H., Rao, D. C., Rankinen, T., Bouchard, C., Geifman-Shochat, S., Shifman, S., Greenberg, D. S., & Soreq, H. (2014). Competing targets of microRNA-608 affect anxiety and hypertension. Human Molecular Genetics, 23, 4569-4580. https://doi.org/10.1093/hmg/ddu170
Hanin, G., & Soreq, H. (2011). Cholinesterase-targeting microRNAs identified in silico affect specific biological processes. Frontiers in Molecular Neuroscience, 4. https://doi.org/10.3389/fnmol.2011.00028
Hossain, S. M., Luckham, R. E., McFadden, M. J., & Brennan, J. D. (2009). Reagentless bidirectional lateral flow bioactive paper sensors for detection of pesticides in beverage and food samples. Analytical Chemistry, 81, 9055-9064. https://doi.org/10.1021/ac901714h
Jalady, A. M., & Dorandeu, F. (2013). Interest of the cholinesterase assay during organophosphate poisonings. Annales Francaises D'anesthesie Et De Reanimation, 32, 856-862.
Jiang, J. X. S., Choi, R. C. Y., Siow, N. L., Lee, H. H. C., Wan, D. C. C., & Tsim, K. W. K. (2003). Muscle induces neuronal expression of acetylcholinesterase in neuron-muscle co-culture - Transcriptional regulation mediated by camp-dependent signaling. The Journal of Biological Chemistry, 278, 45435-45444. https://doi.org/10.1074/jbc.M306320200
Kakeyama, M., Endo, T., Zhang, Y., Miyazaki, W., & Tohyama, C. (2014). Disruption of paired-associate learning in rat offspring perinatally exposed to dioxins. Archives of Toxicology, 88, 789-798.
Katase, N., Terada, K., Suzuki, T., Nishimatsu, S., & Nohno, T. (2015). miR-487b, miR-3963 and miR-6412 delay myogenic differentiation in mouse myoblast-derived C2C12 cells. BMC Cell Biology, 16, 13. https://doi.org/10.1186/s12860-015-0061-9
Kim, S. H., Henry, E. C., Kim, D. K., Kim, Y. H., Shin, K. J., Han, M. S., Lee, T. G., Kang, J. K., Gasiewicz, T. A., Ryu, S. H., & Suh, P. G.. (2006). Novel compound 2-methyl-2H-pyrazole-3-carboxylic acid (2-methyl-4-o-tolylazo-phenyl)-amide (CH-223191) prevents 2,3,7,8-TCDD-induced toxicity by antagonizing the aryl hydrocarbon receptor. Molecular Pharmacology, 69, 1871-1878.
Kimura, E., & Tohyama, C. (2018). Vocalization as a novel endpoint of atypical attachment behavior in 2,3,7,8-tetrachlorodibenzo-p-dioxin-exposed infant mice. Archives of Toxicology, 92, 1741-1749. https://doi.org/10.1007/s00204-018-2176-1
Kishi, R., Araki, A., Minatoya, M., Hanaoka, T., Miyashita, C., Itoh, S., Kobayashi, S., Ait Bamai, Y. U., Yamazaki, K., Miura, R., Tamura, N., Ito, K., & Goudarzi, H. (2017). The Hokkaido Birth Cohort Study on Environment and Children's Health: Cohort profile-updated 2017. Environmental Health and Preventive Medicine, 22, 46. https://doi.org/10.1186/s12199-017-0654-3
Krishnan, D., Cromwell, H. C., & Meserve, L. (2014). Effects of polychlorinated biphenyl (PCB) exposure on response perseveration and ultrasonic vocalization emission in rat during development. Endocrine Disruptors, 2, e969608. https://doi.org/10.4161/23273739.2014.969608
Larsson, M., van den Berg, M., Brenerová, P., van Duursen, M. B., van Ede, K. I., Lohr, C., Luecke-Johansson, S., Machala, M., Neser, S., Pěnčíková, K., & Poellinger, L.. (2015). Consensus toxicity factors for polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls combining in silico models and extensive in vitro screening of AhR-mediated effects in human and rodent cells. Chemical Research in Toxicology, 28, 641-650.
Li, S., Pei, X., Zhang, W., Xie, H. Q., & Zhao, B. (2014). Functional analysis of the dioxin response elements (DREs) of the murine CYP1A1 gene promoter: Beyond the core DRE sequence. International Journal of Molecular Sciences, 15, 6475-6487. https://doi.org/10.3390/ijms15046475
Lionetto, M. G., Caricato, R., Calisi, A., Giordano, M. E., & Schettino, T. (2013). Acetylcholinesterase as a biomarker in environmental and occupational medicine: New insights and future perspectives. BioMed Research International, 2013, 321213. https://doi.org/10.1155/2013/321213
Loeb, D. M., & Greene, L. A. (1993). Transfection with trk restores slow ngf binding, efficient ngf uptake, and multiple ngf responses to ngf-nonresponsive pc12 cell mutants. Journal of Neuroscience, 13, 2919-2929. https://doi.org/10.1523/JNEUROSCI.13-07-02919.1993
Luo, Y., Xie, H. Q., Chen, Y., Xia, Y., Sha, R., Liu, Y., Ma, Y., Xu, T., Xu, L. I., Wah-Keung Tsim, K., & Zhao, B. (2019). Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on acetylcholinesterase during myogenic differentiation of contractile rat primary skeletal muscle cells. Chemico-Biological Interactions, 308, 164-169. https://doi.org/10.1016/j.cbi.2019.05.018
Marsillach, J., Costa, L. G., & Furlong, C. E. (2013). Protein adducts as biomarkers of exposure to organophosphorus compounds. Toxicology, 307, 46-54. https://doi.org/10.1016/j.tox.2012.12.007
Massoulié, J. (2002). The origin of the molecular diversity and functional anchoring of cholinesterases. Neurosignals, 11, 130-143. https://doi.org/10.1159/000065054
Mitro, S. D., Birnbaum, L. S., Needham, B. L., & Zota, A. R. (2016). Cross-sectional Associations between exposure to persistent organic pollutants and leukocyte telomere length among U.S. adults in NHANES, 2001-2002. Environmental Health Perspectives, 124, 651-658. https://doi.org/10.1289/ehp.1510187
Moabbi, A. M., Agarwal, N., El Kaderi, B., & Ansari, A. (2012). Role for gene looping in intron-mediated enhancement of transcription. Proceedings of the National Academy of Sciences of the United States of America, 109, 8505-8510. https://doi.org/10.1073/pnas.1112400109
Mutero, A., Camp, S., & Taylor, P. (1995). Promoter elements of the mouse acetylcholinesterase gene - transcriptional regulation during muscle differentiation. Journal of Biological Chemistry, 270, 1866-1872. https://doi.org/10.1074/jbc.270.4.1866
Neugebauer, J., Wittsiepe, J., Kasper-Sonnenberg, M., Schoneck, N., Scholmerich, A., & Wilhelm, M. (2015). The influence of low level pre- and perinatal exposure to PCDD/Fs, PCBs, and lead on attention performance and attention-related behavior among German school-aged children: Results from the Duisburg Birth Cohort Study. International Journal of Hygiene and Environmental Health, 218, 153-162. https://doi.org/10.1016/j.ijheh.2014.09.005
Nguyen, A. H., Huang, Y., & Rao, B. D. (2013). Optimized Quantized Feedback in a Multiuser System Employing CDF Based Scheduling. In: 2013 IEEE 78th Vehicular Technology Conference (VTC Fall), pp. 1-5.
Nukaya, M., Moran, S., & Bradfield, C. A. (2009). The role of the dioxin-responsive element cluster between the Cyp1a1 and Cyp1a2 loci in aryl hydrocarbon receptor biology. Proceedings of the National Academy of Sciences of the United States of America, 106, 4923-4928. https://doi.org/10.1073/pnas.0809613106
Perrier, A. L., Massoulié, J., & Krejci, E. (2002). PRiMA: The membrane anchor of acetylcholinesterase in the brain. Neuron, 33, 275-285. https://doi.org/10.1016/S0896-6273(01)00584-0
Sarkar, A., Ray, D., Shrivastava, A. N., & Sarker, S. (2006). Molecular Biomarkers: Their significance and application in marine pollution monitoring. Ecotoxicology, 15, 333-340. https://doi.org/10.1007/s10646-006-0069-1
Schecter, A., Birnbaum, L., Ryan, J. J., & Constable, J. D. (2006). Dioxins: An overview. Environmental Research, 101, 419-428. https://doi.org/10.1016/j.envres.2005.12.003
Sha, R., Chen, Y., Luo, Y., Liu, Y., Xu, L., Xie, H. Q., & Zhao, B. (2019). Effects of astrocyte conditioned medium on neuronal AChE expression upon 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. Chemico-Biological Interactions, 309, 108686. https://doi.org/10.1016/j.cbi.2019.05.052
Sha, R., Chen, Y., Wang, Y., Luo, Y., Liu, Y., Ma, Y., Li, Y., Xu, L., Xie, H. Q., & Zhao, B. (2020). Gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin in mice: Neurobehavioral effects on female offspring. Science of the Total Environment, 752, 141784.
Shibamoto, T., Yasuhara, A., & Katami, T. (2007). Dioxin formation from waste incineration. Reviews of Environmental Contamination and Toxicology, 190, 1-41.
Siow, N. L., Choi, R. C., Cheng, A. W., Jiang, J. X., Wan, D. C., Zhu, S. Q., & Tsim, K. W. (2002a). A cyclic AMP-dependent pathway regulates the expression of acetylcholinesterase during myogenic differentiation of C2C12 cells. The Journal of Biological Chemistry, 277, 36129-36136. https://doi.org/10.1074/jbc.M206498200
Startin, J. R., & Rose, M. D. (2005) Dioxins and Dioxinlike PCBs in Food. In: Dioxins and Health, pp. 89-136.
Sun, Y. V., Boverhof, D. R., Burgoon, L. D., Fielden, M. R., & Zacharewski, T. R. (2004). Comparative analysis of dioxin response elements in human, mouse and rat genomic sequences. Nucleic Acids Research, 32, 4512-4523. https://doi.org/10.1093/nar/gkh782
Tai, P. T., Nishijo, M., Anh, N. T. N., Maruzeni, S., Nakagawa, H., Luong, H. V., Anh, T. H., Honda, R., Kido, T., & Nishijo, H. (2013). Dioxin exposure in breast milk and infant neurodevelopment in Vietnam. Occupational and Environmental Medicine, 70, 656-662. https://doi.org/10.1136/oemed-2012-101021
ten Tusscher, G. W., Leijs, M. M., de Boer, L., Legler, J., Olie, K., Spekreijse, H., van Dijk, B. W., Vulsma, T., Briët, J., Ilsen, A., & Koppe, J. G. (2014). Neurodevelopmental retardation, as assessed clinically and with magnetoencephalography and electroencephalography, associated with perinatal dioxin exposure. Science of the Total Environment, 491, 235-239. https://doi.org/10.1016/j.scitotenv.2014.02.100
Tijet, N., Boutros, P. C., Moffat, I. D., Okey, A. B., Tuomisto, J., & Pohjanvirta, R. (2006). Aryl hydrocarbon receptor regulates distinct dioxin-dependent and dioxin-independent gene batteries. Molecular Pharmacology, 69, 140-153. https://doi.org/10.1124/mol.105.018705
Tran, N. N., Pham, T. T., Ozawa, K., Nishijo, M., Nguyen, A. T. N., Tran, T. Q., Hoang, L. V., Tran, A. H., Phan, V. H. A., Nakai, A., Nishino, Y., & Nishijo, H. (2016). Impacts of perinatal dioxin exposure on motor coordination and higher cognitive development in Vietnamese Preschool children: A five-year follow-up. PLoS One, 11, e0147655. https://doi.org/10.1371/journal.pone.0147655
Van den Berg, M., Birnbaum, L. S., Denison, M., De Vito, M., Farland, W., Feeley, M., Fiedler, H., Hakansson, H., Hanberg, A., Haws, L., Rose, M., Safe, S., Schrenk, D., Tohyama, C., Tritscher, A., Tuomisto, J., Tysklind, M., Walker, N., & Peterson, R. E. (2006). The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicological Sciences, 93, 223-241. https://doi.org/10.1093/toxsci/kfl055
Van Dyk, J. S., & Pletschke, B. (2011). Review on the use of enzymes for the detection of organochlorine, organophosphate and carbamate pesticides in the environment. Chemosphere, 82, 291-307. https://doi.org/10.1016/j.chemosphere.2010.10.033
Xie, H. Q., Choi, R. C. Y., Leung, K. W., Chen, V. P., Chu, G. K. Y., & Tsim, K. W. K. (2009). Transcriptional regulation of proline-rich membrane anchor (PRiMA) of globular form acetylcholinesterase in neuron: An inductive effect of neuron differentiation. Brain Research, 1265, 13-23. https://doi.org/10.1016/j.brainres.2009.01.065
Xie, H. Q., Leung, K. W., Chen, V. P., Chan, G. K. L., Xu, S. L., Guo, A. J. Y., Zhu, K. Y., Zheng, K. Y. Z., Bi, C. W., Zhan, J. Y. X., Chan, W. K. P., Choi, R. C. Y., & Tsim, K. W. K. (2010). PRiMA directs a restricted localization of tetrameric AChE at synapses. Chemico-Biological Interactions, 187, 78-83. https://doi.org/10.1016/j.cbi.2010.02.018
Xie, H. Q., Xia, Y., Xu, T., Chen, Y., Fu, H., Li, Y., Luo, Y., Xu, L. I., Tsim, K. W. K., & Zhao, B. (2018). 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces alterations in myogenic differentiation of C2C12 cells. Environmental Pollution, 235, 965-973. https://doi.org/10.1016/j.envpol.2017.12.016
Xie, H. Q., Xu, H. M., Fu, H. L., Hu, Q., Tian, W. J., Pei, X. H., & Zhao, B. (2013). AhR-mediated effects of dioxin on neuronal acetylcholinesterase expression in vitro. Environmental Health Perspectives, 121, 613-618.
Xie, H. Q., Xu, T., Chen, Y. S., Li, Y. P., Xia, Y. J., Xu, S. L., Wang, L. Y., Tsim, K. W. K., & Zhao, B. (2016). New perspectives for multi-level regulations of neuronal acetylcholinesterase by dioxins. Chemico-Biological Interactions, 259, 286-290. https://doi.org/10.1016/j.cbi.2016.06.030
Xu, H. M., Xie, H. Q., Tao, W. Q., Zhou, Z. G., Li, S. Z., & Zhao, B. (2014). Dioxin and dioxin-like compounds suppress acetylcholinesterase activity via transcriptional downregulations in vitro. Journal of Molecular Neuroscience, 53, 417-423. https://doi.org/10.1007/s12031-013-0167-5
Xu, L., Chen, Y., Xie, H. Q. H., Xu, T., Fu, H., Zhang, S., Tsim, K. W. K., Bi, C. W. C., & Zhao, B. (2016). 2,3,7,8-Tetrachlorodibenzo-p-dioxin suppress AChE activity in NGF treated PC12 cells. Chemico-Biological Interactions, 259, 282-285. https://doi.org/10.1016/j.cbi.2016.08.003
Xu, T., Xie, H. D. Q., Li, Y. P., Xia, Y. J., Chen, Y. S., Xu, L., Wang, L. Y., & Zhao, B. (2017). CDC42 expression is altered by dioxin exposure and mediated by multilevel regulations via AhR in human neuroblastoma cells. Scientific Reports, 7(1), 1-10.
Xu, T., Xie, H. D. Q., Li, Y. P., Xia, Y. J., Sha, R., Wang, L. Y., Chen, Y. S., Xu, L., & Zhao, B. (2018). Dioxin induces expression of hsa-miR-146b-5p in human neuroblastoma cells. Journal of Environmental Sciences, 63, 260-267. https://doi.org/10.1016/j.jes.2017.06.038
Yamada, T., Hirata, A., Sasabe, E., Yoshimura, T., Ohno, S., Kitamura, N., & Yamamoto, T. (2014). TCDD disrupts posterior palatogenesis and causes cleft palate. Journal of Cranio-Maxillo-Facial Surgery, 42, 1-6. https://doi.org/10.1016/j.jcms.2013.01.024
Yi, S. W., Hong, J. S., Ohrr, H., & Yi, J. J. (2014). Agent Orange exposure and disease prevalence in Korean Vietnam veterans: The Korean veterans health study. Environmental Research, 133, 56-65. https://doi.org/10.1016/j.envres.2014.04.027
Zhang, S., Kim, K., Jin, U. H., Pfent, C., Cao, H. J., Amendt, B., Liu, X. Y., Wilson-Robles, H., & Safe, S. (2012). Aryl hydrocarbon receptor agonists induce MicroRNA-335 expression and inhibit lung metastasis of estrogen receptor negative breast cancer cells. Molecular Cancer Therapeutics, 11, 108-118. https://doi.org/10.1158/1535-7163.MCT-11-0548
Zhao, B., DeGroot, D. E., Hayashi, A., He, G. C., & Denison, M. S. (2010). CH223191 is a ligand-selective antagonist of the Ah (Dioxin) receptor. Toxicological Sciences, 117, 393-403. https://doi.org/10.1093/toxsci/kfq217
Zhao, F., Wan, Y., Zhao, H., Hu, W., Mu, D., Webster, T. F., & Hu, J. (2016). Levels of blood organophosphorus flame retardants and association with changes in human sphingolipid homeostasis. Environmental Science and Technology, 50, 8896-8903. https://doi.org/10.1021/acs.est.6b02474