Glyphosate Induces Metaphase II Oocyte Deterioration and Embryo Damage by Zinc Depletion and Overproduction of Reactive Oxygen Species

Abarikwu, 2015, Combined effects of repeated administration of Bretmont Wipeout (glyphosate) and Ultrazin (atrazine) on testosterone, oxidative stress and sperm quality of Wistar rats, Toxicol Mech Methods, 25, 70, 10.3109/15376516.2014.989349 Agarwal, 2012, The effects of oxidative stress on female reproduction: a review, Reprod Biol Endocrinol, 10, 49, 10.1186/1477-7827-10-49 Alarcon, 2019, Neonatal exposure to a glyphosate-based herbicide alters the histofunctional differentiation of the ovaries and uterus in lambs, Mol Cell Endocrinol, 482, 45, 10.1016/j.mce.2018.12.007 Aldhaheri, 2017, Dimercapto-1-propanesulfonic acid (DMPS) induces metaphase II mouse oocyte deterioration, Free Radic Biol Med, 112, 445, 10.1016/j.freeradbiomed.2017.08.015 Bain, 2011, The early embryo response to intracellular reactive oxygen species is developmentally regulated, Reprod Fertil Dev, 23, 561, 10.1071/RD10148 Banerjee, 2012, Melatonin prevents hypochlorous acid-induced alterations in microtubule and chromosomal structure in metaphase-II mouse oocytes, J Pineal Res, 53, 122, 10.1111/j.1600-079X.2012.00977.x Banerjee, 2013, Peroxynitrite affects the cumulus cell defense of metaphase II mouse oocytes leading to disruption of the spindle structure in vitro, Fertil Steril, 100, 10.1016/j.fertnstert.2013.04.030 Banerjee, 2012, IL-6 and mouse oocyte spindle, PLoS One, 7, 10.1371/annotation/947afede-1969-4061-a535-164655e9de72 Benachour, 2009, Glyphosate formulations induce apoptosis and necrosis in human umbilical, embryonic, and placental cells, Chem Res Toxicol, 22, 97, 10.1021/tx800218n Benbrook, 2016, Trends in glyphosate herbicide use in the United States and globally, Environ Sci Eur, 28, 3, 10.1186/s12302-016-0070-0 Bernhardt, 2011, Zinc requirement during meiosis I-meiosis II transition in mouse oocytes is independent of the MOS-MAPK pathway, Biol Reprod, 84, 526, 10.1095/biolreprod.110.086488 Boocock, 1983, Kinetics of 5-enolpyruvylshikimate-3-phosphate synthase inhibition by glyphosate, FEBS Lett, 154, 127, 10.1016/0014-5793(83)80888-6 Brändli, 2012, Herbicides found in Human Urine, Ithaka Journal, 270 Caetano, 2012, Understanding the inactivation process of organophosphorus herbicides: A DFT study of glyphosate metallic complexes with Zn2+, Ca2+, Mg2+, Cu2+, Co3+, Fe3+, Cr3+, and Al3+, International Journal of Quantum Chemistry, 112, 2752, 10.1002/qua.23222 Chan, 1992, NTP technical report on the toxicity studies of Glyphosate (CAS No. 1071-83-6) Administered In Dosed Feed To F344/N Rats And B6C3F1 Mice, Toxic Rep Ser, 16 Chang, 2011, Occurrence and fate of the herbicide glyphosate and its degradate aminomethylphosphonic acid in the atmosphere, Environ Toxicol Chem, 30, 548, 10.1002/etc.431 Choi, 2007, Oxidative stress and tumor necrosis factor-alpha-induced alterations in metaphase II mouse oocyte spindle structure, Fertil Steril, 88, 1220, 10.1016/j.fertnstert.2007.02.067 Dictenberg, 1998, Pericentrin and gamma-tubulin form a protein complex and are organized into a novel lattice at the centrosome, J Cell Biol, 141, 163, 10.1083/jcb.141.1.163 Doxsey, 1994, Pericentrin, a highly conserved centrosome protein involved in microtubule organization, Cell, 76, 639, 10.1016/0092-8674(94)90504-5 Duke, 2008, Glyphosate: a once-in-a-century herbicide, Pest Manag Sci, 64, 319, 10.1002/ps.1518 Duncan, 2016, The zinc spark is an inorganic signature of human egg activation, Sci Rep, 6, 24737, 10.1038/srep24737 Eide, 2011, The oxidative stress of zinc deficiency, Metallomics, 3, 1124, 10.1039/c1mt00064k Eroglu, 1998, Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes, Fertil Steril, 69, 944, 10.1016/S0015-0282(98)00030-2 Falchuk, 2001, Zinc physiology and biochemistry in oocytes and embryos, Biometals, 14, 385, 10.1023/A:1012994427351 Falchuk, 1995, Zinc uptake and distribution in Xenopus laevis oocytes and embryos, Biochemistry, 34, 16524, 10.1021/bi00050a037 Fiorino, 2018, Effects of glyphosate on early life stages: comparison between Cyprinus carpio and Danio rerio, Environ Sci Pollut Res Int, 25, 8542, 10.1007/s11356-017-1141-5 Flora, 2010, Chelation in metal intoxication, Int J Environ Res Public Health, 7, 2745, 10.3390/ijerph7072745 Franz, 1997, Glyphosate: A Unique Global Herbicide, 90 Gasnier, 2009, Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines, Toxicology, 262, 184, 10.1016/j.tox.2009.06.006 George, 2013, Emptying of Intracellular Calcium Pool and Oxidative Stress Imbalance Are Associated with the Glyphosate-Induced Proliferation in Human Skin Keratinocytes HaCaT Cells, ISRN Dermatol, 2013, 10.1155/2013/825180 Gillezeau, 2019, The evidence of human exposure to glyphosate: a review, Environ Health, 18, 2, 10.1186/s12940-018-0435-5 Goud, 2005, Nitric oxide delays oocyte aging, Biochemistry, 44, 11361, 10.1021/bi050711f Goud, 2006, Activation of the cGMP signaling pathway is essential in delaying oocyte aging in diabetes mellitus, Biochemistry, 45, 11366, 10.1021/bi060910e Goud, 2008, Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid, Free Radic Biol Med, 44, 1295, 10.1016/j.freeradbiomed.2007.11.014 Goud, 2014, Dynamics of nitric oxide, altered follicular microenvironment, and oocyte quality in women with endometriosis, Fertil Steril, 102, 10.1016/j.fertnstert.2014.03.053 Greim, 2015, Evaluation of carcinogenic potential of the herbicide glyphosate, drawing on tumor incidence data from fourteen chronic/carcinogenicity rodent studies, Crit Rev Toxicol, 45, 185, 10.3109/10408444.2014.1003423 Griffith, 2008, Mutations in pericentrin cause Seckel syndrome with defective ATR- dependent DNA damage signaling, Nat Genet, 40, 232, 10.1038/ng.2007.80 Gros, 2019, Influence of metal ions on glyphosate detection by FMOC-Cl, Environ Monit Assess, 191, 244, 10.1007/s10661-019-7387-2 Guerrero Schimpf, 2017, Neonatal exposure to a glyphosate based herbicide alters the development of the rat uterus, Toxicology, 376, 2, 10.1016/j.tox.2016.06.004 Hanna, 2003, Zinc influences the in vitro development of peri-implantation mouse embryos, Birth Defects Res A Clin Mol Teratol, 67, 414, 10.1002/bdra.10046 Hokanson, 2007, Alteration of estrogen-regulated gene expression in human cells induced by the agricultural and horticultural herbicide glyphosate, Hum Exp Toxicol, 26, 747, 10.1177/0960327107083453 Hu, 2001, Effects of low O2 and ageing on spindles and chromosomes in mouse oocytes from pre-antral follicle culture, Hum Reprod, 16, 737, 10.1093/humrep/16.4.737 Jayasumana, 2014, Glyphosate, hard water and nephrotoxic metals: are they the culprits behind the epidemic of chronic kidney disease of unknown etiology in Sri Lanka?, Int J Environ Res Public Health, 11, 2125, 10.3390/ijerph110202125 Jayasumana, 2015, Drinking well water and occupational exposure to Herbicides is associated with chronic kidney disease, in Padavi-Sripura, Sri Lanka, Environ Health, 14, 6, 10.1186/1476-069X-14-6 Jeelani, 2018, Acrolein, a commonly found environmental toxin, causes oocyte mitochondrial dysfunction and negatively affects embryo development, Free Radic Res, 52, 929, 10.1080/10715762.2018.1487559 Jeelani, 2017, Cyclophosphamide and acrolein induced oxidative stress leading to deterioration of metaphase II mouse oocyte quality, Free Radic Biol Med, 110, 11, 10.1016/j.freeradbiomed.2017.05.006 Jeon, 2015, Effect of zinc on in vitro development of porcine embryos, Theriogenology, 84, 531, 10.1016/j.theriogenology.2015.04.006 Jiang, 2014, A microtubule-associated zinc finger protein, BuGZ, regulates mitotic chromosome alignment by ensuring Bub3 stability and kinetochore targeting, Dev Cell, 28, 268, 10.1016/j.devcel.2013.12.013 Khan, 2015, Diffused Intra-Oocyte Hydrogen Peroxide Activates Myeloperoxidase and Deteriorates Oocyte Quality, PLoS One, 10, 10.1371/journal.pone.0132388 Khan, 2016, Peroxynitrite deteriorates oocyte quality through disassembly of microtubule organizing centers, Free Radic Biol Med, 91, 275, 10.1016/j.freeradbiomed.2015.12.033 Kim, 2011, Zinc sparks are triggered by fertilization and facilitate cell cycle resumption in mammalian eggs, ACS Chem Biol, 6, 716, 10.1021/cb200084y Kim, 2010, Zinc availability regulates exit from meiosis in maturing mammalian oocytes, Nat Chem Biol, 6, 674, 10.1038/nchembio.419 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 Lee, 2018, Critical Role of Zinc as Either an Antioxidant or a Prooxidant in Cellular Systems, Oxid Med Cell Longev, 2018, 10.1155/2018/9156285 Li, 2018, Zinc deficiency causes neural tube defects through attenuation of p53 ubiquitylation, Development, 145 Lindley, 2001, Cryopreservation of human cumulus cells for co-cultures and assessment of DNA damage after thawing using the comet assay, J Assist Reprod Genet, 18, 534, 10.1023/A:1011991806423 Madsen, 1978, Stability Constants of Copper(II), Zinc, Manganese(II), Calcium, and Magnesium Complexes of N-(Phosphonomethyl)glycine (Glyphosate), Acta Chemica Scandinavica, 32a, 79, 10.3891/acta.chem.scand.32a-0079 Menezo, 2011, Zinc concentrations in serum and follicular fluid during ovarian stimulation and expression of Zn2+ transporters in human oocytes and cumulus cells, Reprod Biomed Online, 22, 647, 10.1016/j.rbmo.2011.03.015 Mertens, 2018, Glyphosate, a chelating agent-relevant for ecological risk assessment?, Environ Sci Pollut Res Int, 25, 5298, 10.1007/s11356-017-1080-1 Mesnage, 2015, Transcriptome profile analysis reflects rat liver and kidney damage following chronic ultra-low dose Roundup exposure, Environ Health, 14, 70, 10.1186/s12940-015-0056-1 Mesnage, 2015, Potential toxic effects of glyphosate and its commercial formulations below regulatory limits, Food Chem Toxicol, 84, 133, 10.1016/j.fct.2015.08.012 Mesnage, 2017, Evaluation of estrogen receptor alpha activation by glyphosate-based herbicide constituents, Food Chem Toxicol, 108, 30, 10.1016/j.fct.2017.07.025 Miyoshi, 2004, DISC1 localizes to the centrosome by binding to kendrin, Biochem Biophys Res Commun, 317, 1195, 10.1016/j.bbrc.2004.03.163 Myers, 2016, Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement, Environ Health, 15, 19, 10.1186/s12940-016-0117-0 Paganelli, 2010, Glyphosate-based herbicides produce teratogenic effects on vertebrates by impairing retinoic acid signaling, Chem Res Toxicol, 23, 1586, 10.1021/tx1001749 Pannu, 2012, Induction of robust de novo centrosome amplification, high-grade spindle multipolarity and metaphase catastrophe: a novel chemotherapeutic approach, Cell Death Dis, 3, e346, 10.1038/cddis.2012.82 Paumgartten, 2017, Glyphosate exposure, cardiovascular diseases and cancer risks, J Public Health Emerg, 1, 15, 10.21037/jphe.2016.12.17 Perego, 2017, Evidence for direct effects of glyphosate on ovarian function: glyphosate influences steroidogenesis and proliferation of bovine granulosa but not theca cells in vitro, J Appl Toxicol, 37, 692, 10.1002/jat.3417 Prasad, 2007, Zinc supplementation decreases incidence of infections in the elderly: effect of zinc on generation of cytokines and oxidative stress, Am J Clin Nutr, 85, 837, 10.1093/ajcn/85.3.837 Roberts, 2010, A prospective observational study of the clinical toxicology of glyphosate-containing herbicides in adults with acute self-poisoning, Clin Toxicol (Phila), 48, 129, 10.3109/15563650903476491 Rong-Mullins, 2017, Genetic variation in Dip5, an amino acid permease, and Pdr5, a multiple drug transporter, regulates glyphosate resistance in S. cerevisiae, PLoS One, 12, 10.1371/journal.pone.0187522 Roy, 2016, Glyphosate induces neurotoxicity in zebrafish, Environ Toxicol Pharmacol, 42, 45, 10.1016/j.etap.2016.01.003 Samsel, 2013, Glyphosate’s Suppression of Cytochrome P450 Enzymes and Amino Acid Biosynthesis by the Gut Microbiome: Pathways to Modern Diseases, Entropy, 15, 1416, 10.3390/e15041416 Samsel, 2013, Glyphosate, pathways to modern diseases II: Celiac sprue and gluten intolerance, Interdiscip Toxicol, 6, 159, 10.2478/intox-2013-0026 Samsel, 2015, Glyphosate, pathways to modern diseases III: Manganese, neurological diseases, and associated pathologies, Surg Neurol Int, 6, 45, 10.4103/2152-7806.153876 Scribner, 2003 Shaeib, 2013, Impact of hydrogen peroxide-driven Fenton reaction on mouse oocyte quality, Free Radic Biol Med, 58, 154, 10.1016/j.freeradbiomed.2012.12.007 Sharma, 2013, Spindle and chromosomal alterations in metaphase II oocytes, Reprod Sci, 20, 1293, 10.1177/1933719113483018 Song, 2009, Dietary zinc restriction and repletion affects DNA integrity in healthy men, Am J Clin Nutr, 90, 321, 10.3945/ajcn.2008.27300 Soubry, 2010, The transcriptional repressor Kaiso localizes at the mitotic spindle and is a constituent of the pericentriolar material, PLoS One, 5, e9203, 10.1371/journal.pone.0009203 Stefanidou, 2006, Zinc: a multipurpose trace element, Arch Toxicol, 80, 1, 10.1007/s00204-005-0009-5 Sun, 2016, Construction of a Dual-Fluorescence Reporter System to Monitor the Dynamic Progression of Pluripotent Cell Differentiation, Stem Cells Int, 2016, 10.1155/2016/1390284 Takagi, 2014, Micromechanics of the vertebrate meiotic spindle examined by stretching along the pole-to-pole axis, Biophys J, 106, 735, 10.1016/j.bpj.2013.12.033 Talbot, 1991, Acute poisoning with a glyphosate-surfactant herbicide (’Roundup’): a review of 93 cases, Hum Exp Toxicol, 10, 1, 10.1177/096032719101000101 Tibelius, 2009, Microcephalin and pericentrin regulate mitotic entry via centrosome- associated Chk1, J Cell Biol, 185, 1149, 10.1083/jcb.200810159 Tizhe, 2014, Serum biochemical assessment of hepatic and renal functions of rats during oral exposure to glyphosate with zinc, Comp Clin Path, 23, 1043, 10.1007/s00580-013-1740-6 Tizhe, 2014, Influence of zinc supplementation on histopathological changes in the stomach, liver, kidney, brain, pancreas and spleen during subchronic exposure of Wistar rats to glyphosate, Comp Clin Path, 23, 1535, 10.1007/s00580-013-1818-1 Van Bruggen, 2018, Environmental and health effects of the herbicide glyphosate, Sci Total Environ, 616-617, 255, 10.1016/j.scitotenv.2017.10.309 Verit, 2017, Cardiovascular risk may be increased in women with unexplained infertility, Clin Exp Reprod Med, 44, 28, 10.5653/cerm.2017.44.1.28 WHO, 2017, 321 Wicke, 2019, Identification of the first glyphosate transporter by genomic adaptation, Environ Microbiol, 21, 1287, 10.1111/1462-2920.14534 Williams, 2012, Developmental and reproductive outcomes in humans and animals after glyphosate exposure: a critical analysis, J Toxicol Environ Health B Crit Rev, 15, 39, 10.1080/10937404.2012.632361 Wozniak, 2018, The mechanism of DNA damage induced by Roundup 360 PLUS, glyphosate and AMPA in human peripheral blood mononuclear cells - genotoxic risk assessement, Food Chem Toxicol, 120, 510, 10.1016/j.fct.2018.07.035 Xiang, 2005, Expression of a wheat cytochrome P450 monooxygenase in yeast and its inhibition by glyphosate, Pest Manag Sci, 61, 402, 10.1002/ps.969 Xu, 2016, The role of L-type amino acid transporters in the uptake of glyphosate across mammalian epithelial tissues, Chemosphere, 145, 487, 10.1016/j.chemosphere.2015.11.062 Zdziarski, 2014, GM crops and the rat digestive tract: a critical review, Environ Int, 73, 423, 10.1016/j.envint.2014.08.018 Zhang, 2019, The toxic effects and possible mechanisms of glyphosate on mouse oocytes, Chemosphere, 237, 124435, 10.1016/j.chemosphere.2019.124435 Zhang, 2016, The fertilization-induced zinc spark is a novel biomarker of mouse embryo quality and early development, Sci Rep, 6, 22772, 10.1038/srep22772 Zhang, 2017, Biological impacts of glyphosate on morphology, embryo biomechanics and larval behavior in zebrafish (Danio rerio), Chemosphere, 181, 270, 10.1016/j.chemosphere.2017.04.094 Zimmerman, 2004, Mitosis-specific anchoring of gamma tubulin complexes by pericentrin controls spindle organization and mitotic entry, Mol Biol Cell, 15, 3642, 10.1091/mbc.e03-11-0796 Zouaoui, 2013, Determination of glyphosate and AMPA in blood and urine from humans: about 13 cases of acute intoxication, Forensic Sci Int, 226, e20, 10.1016/j.forsciint.2012.12.010