Atrazine and mancozeb induce excitotoxicity and cytotoxicity in primary cultures of mouse cerebellar cortex

References

• Axelstad, M., J. Boberg, C. Nellemann, M. Kiersgaard, P.R. Jacobsen, S. Christiansen, K.S. Hougaard, and U. Hass. 2011. “Exposure to the Widely Used Fungicide Mancozeb Causes Thyroid Hormone Disruption in Rat Dams but no Behavioral Effects in the Offspring.” Toxicological Science 20: 439–446.
   Web of Science ®Google Scholar
• Baltazar, M.T., R.J. Dinis-Oliveira, M. de Lourdes Bastos, A.M. Tsatsakis, J.A. Duarte, and F. Carvalho. 2014. “Pesticides Exposure as Etiological Factors of Parkinson's Disease and Other Neurodegenerative Diseases – A Mechanistic Approach.” Toxicology Letters 230: 85–103.
   PubMed Web of Science ®Google Scholar
• Bardullas, U., M. Giordano, and V. Rodríguez. 2011. “Chronic Atrazine Exposure Causes Disruption of the Spontaneous Locomotor Activity and Alters the Striatal Dopaminergic System of the Male Sprague-Dawley Rat.” Neurotoxicology and Teratology 33: 263–272.
   PubMed Web of Science ®Google Scholar
• Bartley, A.F., E.K. Lucas, L.J. Brady, Q. Li, J.J. Hablitz, R.M. Cowell, and L.E. Dobrunz. 2015. “Interneuron Transcriptional Dysregulation Causes Frequency-dependent Alterations in the Balance of Inhibition and Excitation in Hippocampus.” The Journal of Neuroscience, 18 November 35: 15276–15290
   PubMed Web of Science ®Google Scholar
• Bhattarai, J.P., S.J. Park, S.W. Chun, D.H. Cho, and S.K. Han. 2015. “Activation of Synaptic and Extrasynaptic Glycine Receptors by Taurine in Preoptic Hypothalamic Neurons.” Neuroscience Letters 608: 51–56.
   PubMed Web of Science ®Google Scholar
• Blahová, J., L. Plhalová, M. Hostovský, L. Divišová, R. Dobšíková, I. Mikulíková, S. Stěpánová, and Z. Svobodová. 2013. “Oxidative Stress Responses in Zebrafish Danio Rerio After Subchronic Exposure to Atrazine.” Food and Chemical Toxicology 61: 82–85.
   PubMed Web of Science ®Google Scholar
• Benítez-Díaz, P., L. Miranda-Contreras, Z. Peña-Contreras, D. Dávila-Vera, R.V. Mendoza-Briceño, and E. Palacios-Prü. 2006. “Histotypic Mouse Parietal Cortex Cultures: Excitation/inhibition Ratio and Ultrastructural Analysis.” Journal of Neuroscience Methods 156: 64–70.
   PubMed Web of Science ®Google Scholar
• Chan, C.Y., H.S. Sun, S.M. Shah, M.S. Agovic, I. Ho, E. Friedman, and S.P. Banerjee. 2013. “Direct Interaction of Taurine with the NMDA Glutamate Receptor Subtype via Multiple Mechanisms.” Advances in Experimental Medicine and Biology 775: 45–52.
   PubMed Web of Science ®Google Scholar
• Chen, J.Y., Y. Song, and L.S. Zhang. 2013. “Immunotoxicity of Atrazine in Balb/c Mice.” Journal of Environmental Science and Health. Part B. 48: 637–645.
   PubMed Web of Science ®Google Scholar
• Domico, L.M., G.D. Zeevalk, L.P. Bernard, and K.R. Cooper. 2006. “Acute Neurotoxic Effects of Mancozeb and Maneb in Mesencephalic Neuronal Cultures are Associated with Mitochondrial Dysfunction.” Neurotoxicology 27: 816–825.
   PubMed Web of Science ®Google Scholar
• Domico, L.M., K.R. Cooper, L.P. Bernard, and G.D. Zeevalk. 2007. “Reactive Oxygen Species Generation by the Ethylene-bis-dithiocarbamate (EBDC) Fungicide Mancozeb and its Contribution to Neuronal Toxicity in Mesencephalic Cells.” Neurotoxicology 28: 1079–1091.
   PubMed Web of Science ®Google Scholar
• Foradori, C.D., A.D. Zimmerman, L.R. Hinds, K.L. Zuloaga, C.B. Breckenridge, and R.J. Handa. 2013. “Atrazine Inhibits Pulsatile Gonadotropin-releasing Hormone (GnRH) Release Without Altering GnRH Messenger RNA or Protein Levels in the Female Rat.” Biology of Reproduction 88: 1–9.
   PubMed Web of Science ®Google Scholar
• Fujikawa, D.G. 2015. “The Role of Excitotoxic Programmed Necrosis in Acute Brain Injury.” Computational and Structural Biotechnology Journal 13: 212–231.
   PubMed Web of Science ®Google Scholar
• García, M., M. Santaeufemia, and M.J. Melgar. 2012. “Triazine Residues in Raw Milk and Infant Formulas from Spanish Northwest by a Diphasic Dialysis Extraction.” Food and Chemical Toxicology 50: 503–510.
   PubMed Web of Science ®Google Scholar
• Goldner, W.S., D.P. Sandler, F. Yu, J.A. Hoppin, F. Kamel, and T.D. Levan. 2010. “Pesticide Use and Thyroid Disease Among Women in the Agricultural Health Study.” American Journal of Epidemiology 171: 455–464.
   PubMed Web of Science ®Google Scholar
• Gut, I.M., P.H. Beske, K.S. Hubbard, M.E. Lyman, T.A. Hamilton, and P.M. McNutt. 2013. “Novel Application of Stem Cell-derived Neurons to Evaluate the Time- and Dose-dependent Progression of Excitotoxic Injury.” PloS One 8: e64423.
   PubMed Web of Science ®Google Scholar
• Harrison Brody, A., E. Chou, J.M. Gray, N.J. Pokyrwka, and K.M. Raley-Susman. 2013. “Mancozeb-induced Behavioral Deficits Precede Structural Neural Degeneration.” Neurotoxicology 34: 74–81.
   PubMed Web of Science ®Google Scholar
• Hayes, T.B., L.L. Anderson, V.R. Beasley, S.R. de Solla, T. Iguchi, H. Ingraham, P. Kestemont, et al. 2011. “Demasculinization and Feminization of Male Gonads by Atrazine: Consistent Effects Across Vertebrate Classes.” The Journal of Steroid Biochemistry and Molecular Biology 127: 64–73.
   PubMed Web of Science ®Google Scholar
• Heusinkveld, H.J., M. van den Berg, and R.H. Westerink. 2014. “In Vitro Dopaminergic Neurotoxicity of Pesticides: A Link with Neurodegeneration?” The Veterinary Quarterly 34: 120–131.
   PubMed Web of Science ®Google Scholar
• Jablonowski, N.D., A. Schäffer, and P. Burauel. 2011. “Still Present After All These Years: Persistence Plus Potential Toxicity Raise Questions About the Use of Atrazine.” Environmental Science and Pollution Research International 18: 328–331.
   PubMed Web of Science ®Google Scholar
• Keane, P.C., M. Kurzawa, P.G. Blain, and C.M. Morris. 2011. “Mitochondrial Dysfunction in Parkinson's Disease.” Parkinson's Disease 15: 1–18.
   Web of Science ®Google Scholar
• Leon, R., H. Wu, Y. Jin, J. Wei, C. Buddhala, H. Prentice, and J.Y. Wu. 2009. “Protective Function of Taurine in Glutamate-induced Apoptosis in Cultured Neurons.” Journal of Neuroscience Research 87: 1185–1194.
   PubMed Web of Science ®Google Scholar
• Li, Y., Y. Sun, J. Yang, Y. Wu, J. Yu, and B. Li. 2014. “Age-dependent Dopaminergic Dysfunction Following Fetal Exposure to Atrazine in SD Rats.” Environmental Toxicology and Pharmacology 37: 1275–1282.
   PubMed Web of Science ®Google Scholar
• Lim, S., S.Y. Ahn, I.C. Song, M.H. Chung, H.C. Jang, K.S. Park, K.U. Lee, Y.K. Pak, and H.K. Lee. 2009. “Chronic Exposure to the Herbicide Atrazine Causes Mitochondrial Dysfunction and Insulin Resistance.” PloS one 4: e5186.
   PubMed Web of Science ®Google Scholar
• Lin, Z., C.A. Dodd, and N.M. Filipov. 2013. “Short-term Atrazine Exposure Causes Behavioral Deficits and Disrupts Monoaminergic Systems in Male C57BL/6 Mice.” Neurotoxicology and Teratology 39: 26–35.
   PubMed Web of Science ®Google Scholar
• Malagarriga, D., A.E. Villa, J. Garcia-Ojalvo, and A.J. Pons. 2015. “Mesoscopic Segregation of Excitation and Inhibition in a Brain Network Model.” PLoS Computational Biology 11: e1004007.
   PubMed Web of Science ®Google Scholar
• Mehta, A., M. Prabhakar, P. Kumar, R. Deshmukh, and P.L. Sharma. 2013. “Excitotoxicity: Bridge to Various Triggers in Neurodegenerative Disorders.” European Journal of Pharmacology 698: 6–18.
   PubMed Web of Science ®Google Scholar
• Miranda-Contreras, L., P.R. Benítez-Díaz, R.V. Mendoza-Briceño, M.C. Delgado-Sáez, and E.L. Palacios-Prü. 1999. “Levels of Amino Acid Neurotransmitters During Mouse Cerebellar Neurogenesis and in Histotypic Cerebellar Cultures.” Developmental Neuroscience 21: 147–158.
   PubMed Web of Science ®Google Scholar
• Miranda-Contreras, L., R. Dávila-Ovalles, P. Benítez-Díaz, Z. Peña-Contreras, and E. Palacios-Prü. 2005. “Effects of Prenatal Paraquat and Mancozeb Exposure on Amino Acid Synaptic Transmission in Developing Mouse Cerebellar Cortex.” Developmental Brain Research 160: 19–27.
   PubMedGoogle Scholar
• Negga, R., J.A. Stuart, M.L. Machen, J. Salva, A.J. Lizek, S.J. Richardson, A.S. Osborne, O. Mirallas, K.A. McVey, and V.A. Fitsanakis. 2012. “Exposure to Glyphosate- and/or Mn/Zn-ethylene-bis-dithiocarbamate-Containing Pesticides Leads to Degeneration of γ-aminobutyric Acid and Dopamine Neurons in Caenorhabditis elegans.” Neurotoxicity Research 21: 281–290.
   PubMed Web of Science ®Google Scholar
• Nelson, S.B., and V. Valakh. 2015. “Excitatory/Inhibitory Balance and Circuit Homeostasis in Autism Spectrum Disorders.” Neuron 87: 684–698.
   PubMed Web of Science ®Google Scholar
• Nödler, K., T. Licha, and D. Voutsa. 2013. “Twenty Years Later Atrazine Concentrations in Selected Coastal Waters of the Mediterranean and the Baltic Sea.” Marine Pollution Bulletin 70: 112–118.
   PubMed Web of Science ®Google Scholar
• Nordby, K.C., A. Andersen, L.M. Irgens, and P. Kristensen. 2005. “Indicators of Mancozeb Exposure in Relation to Thyroid Cancer and Neural Tube Defects In Farmers' Families.” Scandinavian Journal of Work, Environment & Health 31: 89–96.
   PubMed Web of Science ®Google Scholar
• Oray, B., H.S. Lu, and R.W. Gracy. 1983. “High Performance Liquid Chromatographic Separation of Dns-amino acid Derivatives and Applications to Peptide and Protein Structural Studies.” Journal of Chromatography 270: 253–266.
   Web of Science ®Google Scholar
• Panganiban, N., C. Cortes-Maramba, M.L. Dioquino, H. Suplido, A. Ho, A. Francisco-Rivera, and Y. Manglicmot. 2004. “Correlation Between Blood Ethylenethiourea and Thyroid Gland Disorders Among Banana Plantation Workers in the Philippines.” Environmental Health Perspectives 112: 42–45.
   PubMed Web of Science ®Google Scholar
• Peighambarzadeh, S., S. Safi, S. Shahtaheri, M. Javanbakht, and A. Rahimi Forushani. 2011. “Presence of Atrazine in the Biological Samples of Cattle and its Consequence Adversity in Human Health.” Iranian Journal of Public Health 40: 112–121.
   PubMed Web of Science ®Google Scholar
• Pekny, M., and M. Nilsson. 2005. “Astrocyte Activation and Reactive Gliosis.” Glia 50: 427–434.
   PubMed Web of Science ®Google Scholar
• Peña-Contreras, Z., D. Dávila-Vera, E. Labarca-Villasmil, L. Miranda-Contreras, and R.V. Mendoza Briceño. 2011. “Efectos de la Atrazina en Cultivos Primarios de Corteza Cerebelosa de Ratón Utilizando el Método de Golgi Modificado.” Acta Microscopica 20: 112–119.
   Google Scholar
• Pezzoli, G., and E. Cereda. 2013. “Exposure to Pesticides or Solvents and Risk of Parkinson's Disease.” Neurology 80: 2035–2041.
   PubMed Web of Science ®Google Scholar
• Purkayastha, P., A. Malapati, P. Yogeeswari, and D. Sriram. 2015. “A Review on GABA/glutamate Pathway for Therapeutic Intervention of ASD and ADHD.” Current Medicinal Chemistry 22: 1850–1859.
   PubMed Web of Science ®Google Scholar
• Shelton, J.F., E.M. Geraghty, D.J. Tancredi, L.D. Delwiche, R.J. Schmidt, B. Ritz, R.L. Hansen, and I. Hertz-Picciotto. 2014. “Neurodevelopmental Disorders and Prenatal Residential Proximity to Agricultural Pesticides: The CHARGE Study.” Environmental Health Perspectives 122: 1103–1109.
   PubMed Web of Science ®Google Scholar
• Song, X.Y., J.N. Li, Y.P. Wu, B. Zhang, and B.X. Li. 2015. “Atrazine Causes Autophagy- and Apoptosis-related Neurodegenerative Effects in Dopaminergic Neurons in the Rat Nigrostriatal Dopaminergic System. 2015.” International Journal of Molecular Science. 16: 13490–13506.
   PubMed Web of Science ®Google Scholar
• Srivastava, A.K., W. Ali, R. Singh, K. Bhui, S. Tyagi, A.A. Al-Khedhairy, P.K. Srivastava, J. Musarrat, and Y. Shukla. 2012. “Mancozeb-induced Genotoxicity and Apoptosis in Cultured Human Lymphocytes.” Life Sciences 90: 815–824.
   PubMed Web of Science ®Google Scholar
• Stoker, T.E., D.L. Guidici, S.C. Laws, and R.L. Cooper. 2002. “The Effects of Atrazine Metabolites on Puberty and Thyroid Function in the Male Wistar Rat.” Toxicological Sciences 67: 198–206.
   PubMed Web of Science ®Google Scholar
• Stoscheck, C.M. 1990. “Quantitation of Protein.” In Methods in Enzymology, edited by M.P. Deutscher, vol. 182, 50–68. New York: Academic Press.
   Google Scholar
• Tao, H.W., Y.T. Li, and L.I. Zhang. 2014. “Formation of Excitation-inhibition Balance: Inhibition Listens and Changes its Tune.” Trends in Neurosciences 37: 528–530.
   PubMed Web of Science ®Google Scholar
• Virág, L., A.L. Salzman, and C. Szabó. 1998. “Poly(ADP-ribose) Synthetase Activation Mediates Mitochondrial Injury During Oxidant-induced Cell Death.” Journal of Immunology 161: 3753–3759.
   PubMed Web of Science ®Google Scholar
• Viviani, B., M. Boraso, N. Marchetti, and M. Marinovich. 2014. “Perspectives on Neuroinflammation and Excitotoxicity: A Neurotoxic Conspiracy?” Neurotoxicology 43: 10–20.
   PubMed Web of Science ®Google Scholar
• Williams, C.J., and D.T. Dexter. 2014. “Neuroprotective and Symptomatic Effects of Targeting Group III mGlu Receptors in Neurodegenerative Disease.” Journal of Neurochemistry 129: 4–20.
   PubMed Web of Science ®Google Scholar
• Woodman, R.C., P.E. Newburger, P. Anklesaria, R.W. Erickson, J. Rae, M.S. Cohen, and J.T. Curnutte. 1995. “A New X-linked Variant of Chronic Granulomatous Disease Characterized by the Existence of a Normal Clone of Respiratory Burst-competent Phagocytic Cells.” Blood 85: 231–241.
   PubMed Web of Science ®Google Scholar
• Wu, J.Y., and H. Prentice. 2010. “Role of Taurine in the Central Nervous System.” Journal of Biomedical Science 17 (Suppl 1): S1.
   PubMed Web of Science ®Google Scholar
• Yizhar, O., L.E. Fenno, M. Prigge, F. Schneider, T.J. Davidson, D.J. O'Shea, V.S. Sohal, et al. 2011. “Neocortical Excitation/inhibition Balance in Information Processing and Social Dysfunction.” Nature 477: 171–178.
   PubMed Web of Science ®Google Scholar
• Zhang, Z., and Q.Q. Sun. 2011. “The Balance Between Excitation and Inhibition and Functional Sensory Processing in the Somatosensory Cortex.” International Review of Neurobiology 97: 305–333.
   PubMed Web of Science ®Google Scholar
• Zhao, S., J. Liu, F. Zhao, W. Liu, N. Li, Q. Suo, J. Zhao, and L. Zhao. 2013. “Sub-acute Exposure to the Herbicide Atrazine Suppresses Cell Immune Functions in Adolescent Mice.” Bioscience Trends 7: 193–201.
   PubMed Web of Science ®Google Scholar