Exposure to a glyphosate-based herbicide during pregnancy and lactation induces neurobehavioral alterations in rat offspring

Aguilar, 2003, Fearfulness and sex in F2 Roman rats: males display more fear though both sexes share the same fearfulness traits, Physiol. Behav., 78, 723, 10.1016/S0031-9384(03)00043-X Anadón, 2008, Neurotoxicological effects of the herbicide glyphosate, Toxicol. Lett., S164, 10.1016/j.toxlet.2008.06.255 Antonelli, 2014, Behavioral disorders in Parkinson's disease: the role of dopamine, Parkinsonism Relat. Disord., 20, S10, 10.1016/S1353-8020(13)70005-1 Astiz, 2009, Effect of pesticides on cell survival in liver and brain rat tissues, Ecotoxicol. Environ. Saf., 72, 2025, 10.1016/j.ecoenv.2009.05.001 Bano, 2014, Anxiolytic and hyperlocomotive effects of aqueous extract of Nigella sativa L. seeds in rats, Pak. J. Pharm. Sci., 27, 1547 Barbosa, 2001, Parkinsonism after glycine-derivate exposure, Mov. Disord., 16, 565, 10.1002/mds.1105 Beuret, 2005, Effect of the herbicide glyphosate on liver lipoperoxidation in pregnant rats and their fetuses, Reprod. Toxicol., 19, 501, 10.1016/j.reprotox.2004.09.009 Bohn, 2014, Compositional differences in soybeans on the market: glyphosate accumulates in Roundup Ready GM soybeans, Food. Chem., 153, 207, 10.1016/j.foodchem.2013.12.054 Cannizzaro, 2001, Long-lasting handling affects behavioural reactivity in adult rats of both sexes prenatally exposed to diazepam, Brain Res., 904, 225, 10.1016/S0006-8993(01)02462-3 Cattani, 2014, Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: involvement of glutamate excitotoxicity, Toxicology, 320, 34, 10.1016/j.tox.2014.03.001 Courvoisier, 1996, Behavioral and neuroendocrine reactivity to stress in the WKHA/WKY inbred rat strains: a multifactorial and genetic analysis, Brain Res., 743, 77, 10.1016/S0006-8993(96)01023-2 Culbreth, 2012, Comparison of chemical-induced changes in proliferation and apoptosis in human and mouse neuroprogenitor cells, Neurotoxicology, 33, 1499, 10.1016/j.neuro.2012.05.012 Cummings, 2010, Mother counts: how effects of environmental contaminants on maternal care could affect the offspring and future generations, Front. Neuroendocrinol., 31, 440, 10.1016/j.yfrne.2010.05.004 Choleris, 2001, A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field, Neurosci. Biobehav. Rev., 25, 235, 10.1016/S0149-7634(01)00011-2 Chong, 2005, Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease, Prog. Neurobiol., 75, 207, 10.1016/j.pneurobio.2005.02.004 Chopin, 1987, Animal models of anxiety: the effect of compounds that modify 5-HT neurotransmission, Trends Pharmacol. Sci., 8, 383, 10.1016/0165-6147(87)90101-5 Chorfa, 2013, Specific pesticide-dependent increases in alpha-synuclein levels in human neuroblastoma (SH-SY5Y) and melanoma (SK-MEL-2) cell lines, Toxicol. Sci., 133, 289, 10.1093/toxsci/kft076 Daruich, 2001, Effect of the herbicide glyphosate on enzymatic activity in pregnant rats and their fetuses, Environ. Res., 85, 226, 10.1006/enrs.2000.4229 Denenberg, 1969, Open-field bheavior in the rat: what does it mean?, Ann. N. Y. Acad. Sci., 159, 852, 10.1111/j.1749-6632.1969.tb12983.x El-Shenawy, 2009, Oxidative stress responses of rats exposed to Roundup and its active ingredient glyphosate, Environ. Toxicol. Pharmacol., 28, 379, 10.1016/j.etap.2009.06.001 Fox, 1965, Reflex-ontogeny and behavioural development of the mouse, Anim. Behav., 13, 234, 10.1016/0003-3472(65)90041-2 Gad, 1988 Gallo, 2015, Upregulation of dopamine D2 receptors in the nucleus accumbens indirect pathway increases locomotion but does not reduce alcohol consumption, Neuropsychopharmacology, 40, 1609, 10.1038/npp.2015.11 Garber, 2011 Giannakopoulou, 2010, Modulation of the basal ganglia dopaminergic system in a transgenic mouse exhibiting dystonia-like features, J. Neural. Transm., 117, 1401, 10.1007/s00702-010-0521-5 GRAIN, 2009, Twelve years of GM soya in Argentina – a disaster for people and the environment, Seedling, 16 Gray, 1971, Sex differences in emotional behaviour in mammals including man: endocrine bases, Acta Psychol. (Amst), 35, 29, 10.1016/0001-6918(71)90029-1 Gray, 1984, Behavioural studies of the role of GABA in anxiolytic drug action, Neuropharmacology, 23, 827, 10.1016/0028-3908(84)90267-3 Hernández-Plata, 2015, The herbicide glyphosate causes behavioral changes and alterations in dopaminergic markers in male Sprague–Dawley rat, Neurotoxicology, 46, 79, 10.1016/j.neuro.2014.12.001 Hübler, 2005, Functional observational battery and motor activity in rats after single administration of two NHE 1 inhibitors, Toxicol. Appl. Pharmacol., 208, 266, 10.1016/j.taap.2005.02.017 Iezhitsa, 2001, Effects of bromantan on offspring maturation and development of reflexes, Neurotoxicol. Teratol., 23, 213, 10.1016/S0892-0362(01)00119-2 Joyce, 2007, Dopamine D3 receptor agonists for protection and repair in Parkinson's disease, Curr. Opin. Pharmacol., 7, 100, 10.1016/j.coph.2006.11.004 Kim, 2013, Repeated heat exposure impairs nigrostriatal dopaminergic neurons in mice, Biol. Pharm. Bull., 36, 1556, 10.1248/bpb.b13-00268 Larsen, 2012, Effects of sub-lethal exposure of rats to the herbicide glyphosate in drinking water: glutathione transferase enzyme activities, levels of reduced glutathione and lipid peroxidation in liver, kidneys and small intestine, Environ. Toxicol. Pharmacol., 34, 811, 10.1016/j.etap.2012.09.005 Le Couteur, 1999, Pesticides and Parkinson's disease, Biomed. Pharmacother., 53, 122, 10.1016/S0753-3322(99)80077-8 Liu, 2013, Changes in 5-HT1A receptor expression in the oculomotor nucleus in a rat model of post-traumatic stress disorder, J. Mol. Neurosci., 49, 360, 10.1007/s12031-012-9874-6 Liu, 2015, GABA and 5-HT systems are implicated in the anxiolytic-like effect of spinosin in mice, Pharmacol. Biochem. Behav., 128, 41, 10.1016/j.pbb.2014.11.003 Menendez-Helman, 2012, Glyphosate as an acetylcholinesterase inhibitor in Cnesterodon decemmaculatus, Bull. Environ. Contam. Toxicol., 88, 6, 10.1007/s00128-011-0423-8 Mercurio, 2014, Glyphosate persistence in seawater, Mar. Pollut. Bull., 85, 385, 10.1016/j.marpolbul.2014.01.021 Mesnage, 2013, Ethoxylated adjuvants of glyphosate-based herbicides are active principles of human cell toxicity, Toxicology, 313, 122, 10.1016/j.tox.2012.09.006 Michel, 2013, Specific needs of dopamine neurons for stimulation in order to survive: implication for Parkinson disease, FASEB J., 27, 3414, 10.1096/fj.12-220418 Modesto, 2010, Roundup causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus, Chemosphere, 78, 294, 10.1016/j.chemosphere.2009.10.047 Molina, 1987, Sensorimotor maturation and alcohol responsiveness in rats prenatally exposed to alcohol during gestational day 8, Neurotoxicol. Teratol., 9, 121, 10.1016/0892-0362(87)90088-2 Mose, 2008, Placental passage of benzoic acid, caffeine, and glyphosate in an ex vivo human perfusion system, J. Toxicol. Environ. Health A, 71, 984, 10.1080/01932690801934513 Mugford, 1998, Sex-dependent metabolism of xenobiotics, Drug Metab. Rev., 30, 441, 10.3109/03602539808996322 Näslund, 2015, Differences in anxiety-like behavior within a batch of Wistar rats are associated with differences in serotonergic transmission enhanced by acute SRI administration, and abolished by serotonin depletion, Int. J. Neuropsychopharmacol., 18 Negga, 2012, Exposure to glyphosate- and/or Mn/Zn-ethylene-bis-dithiocarbamate-containing pesticides leads to degeneration of gamma-aminobutyric acid and dopamine neurons in Caenorhabditis elegans, Neurotox. Res., 21, 281, 10.1007/s12640-011-9274-7 Olivier, 2013, The role of the serotonergic and GABA system in translational approaches in drug discovery for anxiety disorders, Front. Pharmacol., 4, 74, 10.3389/fphar.2013.00074 Pellow, 1985, Validation of op closed arm entries in an elevated plus-maze as a measure of anxiety in the rat, Neurosci. J. Methods, 14, 149, 10.1016/0165-0270(85)90031-7 Peruzzo, 2008, Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina, Environ. Pollut., 156, 61, 10.1016/j.envpol.2008.01.015 Poulsen, 2009, Modeling placental transport: correlation of in vitro BeWo cell permeability and ex vivo human placental perfusion, Toxicol. In Vitro, 23, 1380, 10.1016/j.tiv.2009.07.028 Prut, 2003, The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review, Eur. J. Pharmacol., 463, 3, 10.1016/S0014-2999(03)01272-X Ricceri, 2006, Developmental neurotoxicity of organophosphorous pesticides: fetal and neonatal exposure to chlorpyrifos alters sex-specific behaviors at adulthood in mice, Toxicol. Sci., 93, 105, 10.1093/toxsci/kfl032 Richardson, 2014, Elevated serum pesticide levels and risk for Alzheimer disease, JAMA Neurol., 71, 284, 10.1001/jamaneurol.2013.6030 Samanta, 2014, Biochemical effects of glyphosate based herbicide, Excel Mera 71 on enzyme activities of acetylcholinesterase (AChE), lipid peroxidation (LPO), catalase (CAT), glutathione-S-transferase (GST) and protein content on teleostean fishes, Ecotoxicol. Environ. Saf., 107, 120, 10.1016/j.ecoenv.2014.05.025 Sandrini, 2013, Effects of glyphosate on cholinesterase activity of the mussel Perna perna and the fish Danio rerio and Jenynsia multidentata: in vitro studies, Aquat. Toxicol., 130–131, 171, 10.1016/j.aquatox.2013.01.006 Steimer, 1997, Brain metabolism of progesterone, coping behaviour and emotional reactivity in male rats from two psychogenetically selected lines, J. Neuroendocrinol., 9, 169, 10.1046/j.1365-2826.1997.t01-1-00571.x Tamburella, 2012, The selective norepinephrine reuptake inhibitor atomoxetine counteracts behavioral impairments in trimethyltin-intoxicated rats, Eur. J. Pharmacol., 683, 148, 10.1016/j.ejphar.2012.02.045 Teubal, 2009, Expansión del modelo sojero en la Argentina. De la producción de alimentos a los commodities, 161 Teubal, 2005, Transformaciones agrarias en la Argentina. Agricultura industrial y sistema agroalimentario, 37 Treit, 1993, Anxiolytic effects of serotonergic interventions in the shock-probe burying test and the elevated plus-maze test, Behav. Brain Res., 54, 23, 10.1016/0166-4328(93)90045-R Trigo, 2011 US-EPA, 2011 Van Stempvoort, 2014, Residues of the herbicide glyphosate in riparian groundwater in urban catchments, Chemosphere, 95, 455, 10.1016/j.chemosphere.2013.09.095 Vaz, 2015, Cardiovascular and behavioral effects produced by administration of liposome-entrapped GABA into the rat central nervous system, Neuroscience, 285, 60, 10.1016/j.neuroscience.2014.10.067 Walsh, 1976, The open-field test: a critical review, Psychol. Bull., 83, 482, 10.1037/0033-2909.83.3.482 Wang, 2011, Parkinsonism after chronic occupational exposure to glyphosate, Parkinsonism Relat. Disord., 17, 486, 10.1016/j.parkreldis.2011.02.003 Williams, 2000, Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate, for humans, Regul. Toxicol. Pharmacol., 31, 117, 10.1006/rtph.1999.1371