Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: Involvement of glutamate excitotoxicity

Toxicology

Volumn 320, Issue 1, 2014, Pages 34-45

  Cattani, Daiane ^a   de Liz Oliveira Cavalli, Vera Lúcia ^a   Heinz Rieg, Carla Elise ^a   Domingues, Juliana Tonietto ^a   Dal Cim, Tharine ^a   Tasca, Carla Inês ^a   Mena Barreto Silva, Fátima Regina ^a   Zamoner, Ariane ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Calcium; Glutamatergic excitotoxicity; Glyphosate; Kinase pathways; Oxidative stress

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 AMINO 5 PHOSPHONOVALERIC ACID; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; ALANINE AMINOTRANSFERASE; ALPHA METHYL 4 CARBOXYPHENYLGLYCINE; ALPHA METHYLAMINOISOBUTYRIC ACID; ASPARTATE AMINOTRANSFERASE; CALCIUM 45; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CARBON 14; DIZOCILPINE; GAMMA GLUTAMYLTRANSFERASE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTAMATE AMMONIA LIGASE; GLUTAMIC ACID; GLUTAMINE; GLUTATHIONE; GLYPHOSATE; HERBICIDE; ISOBUTYRIC ACID; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; NIFEDIPINE; ROUNDUP; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM TRANSPORT; CELL VIABILITY; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; EXCITOTOXICITY; EXTRACELLULAR CALCIUM; FLUID INTAKE; HIPPOCAMPUS; IMMATURITY; INCUBATION TIME; LACTATION; LIPID PEROXIDATION; LONG TERM EXPOSURE; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NEUROTOXICITY; NEUROTRANSMITTER UPTAKE; NONHUMAN; OXIDATIVE STRESS; PREGNANCY; PRIORITY JOURNAL; PROGENY; RAT; SIGNAL TRANSDUCTION; SYNAPTOGENESIS; WEIGHT GAIN;

EID: 84896918766     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2014.03.001     Document Type: Article

References (53)

1. Almeida R.D., Manadas B.J., Melo C.V., Gomes J.R., Mendes C.S., Grãos M.M., Carvalho R.F., Carvalho A.P., Duarte C.B. Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ. 2005, 12:1329-1343.
2. Alvestad S., Hammer J., Qu H., Håberg A., Ottersen O.P., Sonnewald U. Reduced astrocytic contribution to the turnover of glutamate, glutamine, and GABA characterizes the latent phase in the kainate model of temporal lobe epilepsy. J. Cereb. Blood Flow Metab. 2011, 31:1675-1686.
3. Astiz M., de Alaniz M.J., Marra C.A. The oxidative damage and inflammation caused by pesticides are reverted by lipoic acid in rat brain. Neurochem. Int. 2012, 61:1231-1241.
4. Barbosa E.R., Leiros da Costa M.D., Bacheschi L.A., Scaff M., Leite C.C. Parkinsonism after glycine-derivate exposure. Move. Disord. 2001, 16:565-568.
5. Barlow B.K., Lee D.W., Cory-Slechta D.A., Opanashuk L.A. Moduation of antioxidant defence systems by the environmental pesticide Maneb in dopaminergic cells. Neurotoxicology 2005, 26:63-75.
6. Benachour N., Séralini G.-E. Glyphosate formulations induce apoptosis and necrosis in human umbilical, embryonic, and placental cells. Chem. Res. Toxicol. 2009, 22:97-105.
7. Bird R.P., Draper A.H. Comparative studies on different methods of malondyhaldehydedetermination. Methods Enzymol. 1984, 90:105-110.
8. Brent R.L. Environmental causes of human congenital malformations: the pediatrician's role in dealing with these complex clinical problems caused by a multiplicity of environmental and genetic factors. Pediatrics 2004, 113:957-968.
9. Cattani D., Goulart P.B., Cavalli V.L., Winkelmann-Duarte E., Dos Santos A.Q., Pierozan P., de Souza D.F., Woehl V.M., Fernandes M.C., Silva F.R., Gonçalves C.A., Pessoa-Pureur R., Zamoner A. Congenital hypothyroidism alters the oxidative status, enzyme activities and morphological parameters in the hippocampus of developing rats. Mol. Cell. Endocrinol. 2013, 375:14-26.
10. Choe E.S., Wang J.Q. CaMKII regulates amphetamine-induced ERK1/2 phosphorylation in striatal neurons. NeuroReport 2002, 13:1013-1016.
11. Chong Z.Z., Li F., Maiese K. Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease. Prog. Neurobiol. 2005, 75:207-246.
12. Chorfa A., Bétemps D., Morignat E., Lazizzera C., Hogeveen K., Andrieu T., Baron T. Specific pesticide-dependent increases in α-synuclein levels in human neuroblastoma (SH-SY5Y) and melanoma (SK-MEL-2) cell lines. Toxicol. Sci. 2013, 133:289-297.
13. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65:1-105.
14. Dang T.N., Arseneault M., Ramassamy C. Regulation of redox-sensitive signaling pathways in rat primary astrocytes following acrolein exposure. J. Alzheimers Dis. 2011, 25:263-277.
15. de Liz Oliveira Cavalli V.L., Cattani D., Heinz Rieg C.E., Pierozan P., Zanatta L., Benedetti Parisotto E., Wilhelm Filho D., Mena Barreto Silva F.R., Pessoa-Pureur R., Zamoner A. Roundup disrupts male reproductive functions by triggering calcium-mediated cell death in rat testis and Sertoli cells. Free Radic. Biol. Med. 2013, 65C:335-346.
16. El-Shenawy N.S. Oxidative stress responses of rats exposed to Roundup and its active ingredient glyphosate. Environ. Toxicol. Pharmacol. 2009, 28:379-385.
17. Gomes J.R., Costa J.T., Melo C.V., Felizzi F., Monteiro P., Pinto M.J., Inácio A.R., Wieloch T., Almeida R.D., Grãos M., Duarte C.B. Excitotoxicity downregulates TrkB.FL signaling and upregulates the neuroprotective truncated TrkB receptors in cultured hippocampal and striatal neurons. J. Neurosci. 2012, 32:4610-4622.
18. Gui Y.X., Fan X.N., Wang H.M., Wang G., Chen S.D. Glyphosate induced cell death through apoptotic and autophagic mechanisms. Neurotoxicol. Teratol. 2012, 34:344-349.
19. Hayden K.M., Norton M.C., Darcey D., Ostbye T., Zandi P.P., Breitner J.C., Welsh-Bohmer K.A. Occupational exposure to pesticides increases the risk of incident AD: the Cache County study. Neurology 2010, 74:1524-1530. Cache County Study Investigators.
20. Jenstad M., Quazi A.Z., Zilberter M., Haglerød C., Berghuis P., Saddique N., Goiny M., Buntup D., Davanger S.S., Haug F.M., Barnes C.A., McNaughton B.L., Ottersen O.P., Storm-Mathisen J., Harkany T., Chaudhry F.A. System A transporter SAT2 mediates replenishment of dendritic glutamate pools controlling retrograde signaling by glutamate. Cereb. Cortex 2009, 19:1092-1106.
21. Ji R.R., Woolf C.J. Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol. Dis. 2001, 8:1-10.
22. Kanamori K., Ross B.D. Quantitative determination of extracellular glutamine concentration in rat brain, and its elevation in vivo by system A transport inhibitor, alpha-(methylamino)isobutyrate. J. Neurochem. 2004, 90:203-210.
23. Kirby M.L., Barlow R.L., Bloomquit J.R. Neurotoxicity of the organochlorine insecticide hepatochlor to murine striatal dopaminergic pathways. Toxicol. Sci. 2001, 61:100-106.
24. Le Couteur D.G., Mc Lean A.J., Taylor M.C., Woodham B.L., Board P.G. Pesticides and Parkinson's disease. Biomed. Pharmacother. 1999, 53:122-130.
25. Lee D.H., Blomhoff R., Jacobs D.R. Is serum gamma glutamyltransferase a marker of oxidative stress?. Free Radic. Res. 2004, 38:535-539.
26. Londres F. Agrotóxicos no Brasil: um guia para ação em defesa da vida. Rio de Janeiro: AS-PTA - Assessoria e Serviços a Projetos em Agricultura Alternativa 2011.
27. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-267.
28. Marc J., Mulner-Lorillon O., Boulben S., Hureau D., Durand G., Bellé R. Pesticide Roundup provokes cell division dysfunction at the level of CDK1/cyclin B activation. Chem. Res. Toxicol. 2002, 15:326-331.
29. Morken T.S., Brekke E., Håberg A., Widerøe M., Brubakk A.M., Sonnewald U. Neuron-astrocyte interactions, pyruvate carboxylation and the pentose phosphate pathway in the neonatal rat brain. Neurochem. Res. 2013.
30. Negga R., Stuart J.A., Machen M.L., Salva J., Lizek A.J., Richardson S.J., Osborne A.S., Mirallas O., McVey K.A., Fitsanakis V.A. 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. Neurotox. Res. 2012, 21(3):281-290.
31. Negga R., Rudd D.A., Davis N.S., Justice A.N., Hatfield H.E., Valente A.L., Fields A.S., Fitsanakis V.A. Exposure to Mn/Zn ethylene-bis-dithiocarbamate and glyphosate pesticides leads to neurodegeneration in Caenorhabditis elegans. Neurotoxicology 2011, 32:331-341.
32. Negga R., Stuart J.A., Machen M.L., Salva J., Lizek A.J., Richardson S.J., Osborne A.S., Mirallas O., McVey K.A., Fitsanakis V.A. 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. Neurotox. Res. 2012, 21:281-290.
33. 2+ions across mitochondrial coupling membrane by N-(phosphonomethyl)glycine. Toxicology 1990, 61:205-209.
34. Orlowsky M., Meister A. Gamma-glutamyl-p-nitroanilide: a new convenient substrate for determination and study of l- and d-gamma-glutamyltranspeptidase activities. Biochim. Biophys. Acta 1963, 73:679-681.
35. Paganelli A., Gnazzo V., Acosta H., López S.L., Carrasco A.E. Glyphosate-based herbicides produce teratogenic effects on vertebrates by impairing retinoic acid signaling. Chem. Res. Toxicol. 2010, 23:1586-1595.
36. Patel S., Singh V., Kumar A., Gupta Y.K., Singh M.P. Status of antioxidant defence system and expression of toxicant responsive genes in striatum of maneb- and paraquat-induced Parkinson's disease phenotype in mouse: mechanism of neurodegeneration. Brain Res. 2006, 1081:9-18.
37. Peng J., Peng L., Stevenson F.F., Doctrow S., Andersen J.K. Iron and Paraquat as synergistic environmental risk factors in sporadic Parkinson's disease accelerate age-related neurodegeneration. J. Neurosci. 2007, 27:6914-6922.
38. Pérez-De La Cruz V., Konigsberg M., Pedraza-Chaverri J., Herrera-Mundo N., Díaz-Muñoz M., Morán J., Fortoul-van der Goes T., Rondán-Zárate A., Maldonado P.D., Ali S.F., Santamaría A. Cytoplasmic calcium mediates oxidative damage in an excitotoxic/energetic deficit synergic model in rats. Eur. J. Neurosci. 2008, 27:1075-1085.
39. Pessoa-Pureur R., Wajner M. Cytoskeleton as a potential target in the neuropathology of maple syrup urine disease: insight from animal studies. J. Inherit. Metab. Dis. 2007, 30:664-672.
40. Rami A., Ferger D., Krieglstein J. Blockade of calpain proteolytic activity rescues neurons from glutamate excitotoxicity. Neurosci. Res. 1997, 27:93-97.
41. Reitman S., Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am. J. Clin. Pathol. 1957, 28:56-63.
42. Richard S., Moslemi S., Sipahutar H., Benachour N., Séralini G.E. Differential effects of glyphosate and roundup on human placental cells and aromatase. Environ. Health Perspect. 2005, 113:716-720.
43. Silva F.R., Leite L.D., Barreto K.P., D'Agostini C., Zamoner A. Effect of 3,5,3'-triiodo-l-thyronine on amino acid accumulation and membrane potential in Sertoli cells of the rat testis. Life Sci. 2001, 69:977-986.
44. Sutor B., Luhmann H.J. Development of excitatory and inhibitory postsynaptic potentials in the rat neocortex. Perspect. Dev. Neurobiol. 1995, 2:409-419.
45. Torres F.V., Hansen F., Doridio Locks-Coelho L., Souza D.O. Increase of extracellular glutamate concentration increases its oxidation and diminishes glucose oxidation in isolated mouse hippocampus: reversible by TFB-TBOA. J. Neurosci. Res. 2013, 10.1002/jnr.23187.
46. Tsui M.T., Chu L.M. Aquatic toxicity of glyphosatebased formulations: comparison between different organisms and the effects of environmental factors. Chemosphere 2003, 52:1189-1197.
47. Wang G., Fan X.N., Tan Y.Y., Cheng Q., Chen S.D. Parkinsonism after chronic occupational exposure to glyphosate. Parkinsonism Relat. Disord. 2011, 17:486-487.
48. Wang X.F., Li S., Chou A.P., Bronstein J.M. Inhibitory effects of pesticides on proteasome activity: implication in Parkinson's disease. Neurobiol. Dis. 2006, 2:198-205.
49. Williams G.M., Kroes R., Munro I.C. Safety evaluation and risk assessment of the herbicide roundup and its active ingredient, glyphosate, for human. Regul. Toxicol. Pharmacol. 2000, 31:117-165.
50. Zamoner A., Heimfarth L., Oliveira Loureiro S., Royer C., Mena Barreto Silva F.R., Pessoa-Pureur R. Nongenomic actions of thyroxine modulate intermediate filament phosphorylation in cerebral cortex of rats. Neuroscience 2008, 156:640-652.
51. 2+uptake in cerebral cortex from young rats. Neurosci. Res. 2007, 57:98-103.
52. Zhang X., Daugherty S.L., de Groat W.C. Activation of CaMKII and ERK1/2 contributes to the time-dependent potentiation of Ca2+ response elicited by repeated application of capsaicin in rat DRG neurons. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R644-R654.
53. Zhao G., Zhao Y., Wang X., Xu Y. Knockdown of glucose-6-phosphate dehydrogenase (G6PD) following cerebral ischemic reperfusion: the pros and cons. Neurochem. Int. 2012, 61:146-155.