Maternal exposure to glyphosate-based herbicide causes long-term changes in vascular relaxation from offspring adult rats
DOI:
https://doi.org/10.33448/rsd-v10i16.23505Keywords:
Glyphosate; Vascular reactivity; Oxidative stress; Fetal Programming.Abstract
This study aimed to investigate whether exposure to glyphosate-based herbicide during the gestational phase promotes long-term effects on the vasomotor function of the thoracic aorta and the possible involvement of oxidative stress and cyclooxygenase II in these alterations. For this, in a isolated organ bath, the endothelium-dependent and independent relaxation of aortic rings of rats from mothers treated with glyphosate in the maternal phase (O-GHB) and tap water the control group (O-CON) were evaluated. Pharmacological tools such as L-NAME, TEMPOL and Indomethacin were used for investigate possible mechanisms. As a result, an impairment in vascular relaxation related to an endothelial dysfunction in O-GHB rats was observed. This endothelial dysfunction was reversed when the aortic rings were in the presence of superoxide dismutase and COX-2 mimetic, supporting the hypothesis that adverse effects during the intrauterine phase, such as oxidative stress caused by glyphosate, can lead to late changes in the function of some organs, in the case studied here, in vascular reactivity in the aorta.
References
Ait-Bali, Y., Ba-M’hamed, S., Gambarotta, G., Sassoè-Pognetto, M., Giustetto, M., & Bennis, M. (2020). Pre- and postnatal exposure to glyphosate-based herbicide causes behavioral and cognitive impairments in adult mice: evidence of cortical ad hippocampal dysfunction. Archives of Toxicology, 94(5), 1703–1723. https://doi.org/10.1007/s00204-020-02677-7
Anadón, A., Martínez-Larrañaga, M. R., Martínez, M. A., Castellano, V. J., Martínez, M., Martin, M. T., Nozal, M. J., & Bernal, J. L. (2009). Toxicokinetics of glyphosate and its metabolite aminomethyl phosphonic acid in rats. Toxicology Letters, 190(1), 91–95. https://doi.org/10.1016/J.TOXLET.2009.07.008
ANVISA. (2012). Relatório: Vigilância em Saúde de Populações Expostas a Agrotóxicos no Estado do Espírito Santo.
Baldi, I., Gruber, A., Rondeau, V., Lebailly, P., Brochard, P., & Fabrigoule, C. (2011). Neurobehavioral effects of long-term exposure to pesticides: results from the 4-year follow-up of the PHYTONER study. Occupational and Environmental Medicine, 68(2), 108–115. https://doi.org/10.1136/OEM.2009.047811
Beuret, C. J., Zirulnik, F., & Giménez, M. S. (2005). Effect of the herbicide glyphosate on liver lipoperoxidation in pregnant rats and their fetuses. In Reproductive Toxicology (Vol. 19, Issue 4, pp. 501–504). https://doi.org/10.1016/j.reprotox.2004.09.009
Casares, F. M., & Mantione, K. J. (2006). Pesticides may be altering constitutive nitric oxide release, thereby compromising health. Medical Science Monitor : International Medical Journal of Experimental and Clinical Research, 12(10). https://pubmed.ncbi.nlm.nih.gov/17006416/
Cattani, D., Cesconetto, P. A., Tavares, M. K., Parisotto, E. B., de Oliveira, P. A., Rieg, C. E. H., Leite, M. C., Prediger, R. D. S., Wendt, N. C., Razzera, G., Filho, D. W., & Zamoner, A. (2017). Developmental exposure to glyphosate-based herbicide and depressive-like behavior in adult offspring: Implication of glutamate excitotoxicity and oxidative stress. Toxicology, 387(February), 67–80. https://doi.org/10.1016/j.tox.2017.06.001
Chan, Y. C., Chang, S. C., Hsuan, S. L., Chien, M. S., Lee, W. C., Kang, J. J., Wang, S. C., & Liao, J. W. (2007). Cardiovascular effects of herbicides and formulated adjuvants on isolated rat aorta and heart. Toxicology in Vitro, 21(4), 595–603. https://doi.org/10.1016/J.TIV.2006.12.007
Daruich, J., Zirulnik, F., & Sofía Gimenez, M. (2001). Effect of the herbicide glyphosate on enzymatic activity in pregnant rats and their fetuses. Environmental Research, 85(3), 226–231. https://doi.org/10.1006/enrs.2000.4229
de Amarante Junior, O. P., dos Santos, T. C. R., Brito, N. M., & Ribeiro, M. L. (2002). Glyphosate: properties, toxicity, use and legislation. Química Nova, 25(4), 589–593. https://doi.org/10.1590/S0100-40422002000400014
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. (2013). Roundup disrupts male reproductive functions by triggering calcium-mediated cell death in rat testis and Sertoli cells. Free Radical Biology & Medicine, 65, 335–346. https://doi.org/10.1016/J.FREERADBIOMED.2013.06.043
Gallegos, C. E., Bartos, M., Bras, C., Gumilar, F., Antonelli, M. C., & Minetti, A. (2016). Exposure to a glyphosate-based herbicide during pregnancy and lactation induces neurobehavioral alterations in rat offspring. NeuroToxicology, 53, 20–28. https://doi.org/10.1016/j.neuro.2015.11.015
Gilden, R. C., Huffling, K., & Sattler, B. (2010). Pesticides and health risks. Journal of Obstetric, Gynecologic, and Neonatal Nursing: JOGNN, 39(1), 103–110. https://doi.org/10.1111/J.1552-6909.2009.01092.X
Gimbrone, M. A., & García-Cardeña, G. (2016). Endothelial Cell Dysfunction and the Pathobiology of Atherosclerosis. Circulation Research, 118(4), 620–636. https://doi.org/10.1161/CIRCRESAHA.115.306301
Gress, S., Lemoine, S., Séralini, G. E., & Puddu, P. E. (2015). Glyphosate-Based Herbicides Potently Affect Cardiovascular System in Mammals: Review of the Literature. Cardiovascular Toxicology, 15(2), 117–126. https://doi.org/10.1007/s12012-014-9282-y
Guzik, T. J., & Touyz, R. M. (2017). Oxidative Stress, Inflammation, and Vascular Aging in Hypertension. Hypertension (Dallas, Tex. : 1979), 70(4), 660–667. https://doi.org/10.1161/HYPERTENSIONAHA.117.07802
Hass, U., Boberg, J., Christiansen, S., Jacobsen, P. R., Vinggaard, A. M., Taxvig, C., Poulsen, M. E., Herrmann, S. S., Jensen, B. H., Petersen, A., Clemmensen, L. H., & Axelstad, M. (2012). Adverse effects on sexual development in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reproductive Toxicology, 34(2), 261–274. https://doi.org/10.1016/j.reprotox.2012.05.090
IBAMA. (2016). Relatórios de comercialização de agrotóxicos. http://www.ibama.gov.br/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos#sobreosrelatorios
K, W., G, G., Z, E., P, P., JE, G., MS, R., NA, B., & X, L. (2014). Use of a glyphosate-based herbicide-induced nephrotoxicity model to investigate a panel of kidney injury biomarkers. Toxicology Letters, 225(1), 192–200. https://doi.org/10.1016/J.TOXLET.2013.12.009
Kim, K. H., Kabir, E., & Jahan, S. A. (2017). Exposure to pesticides and the associated human health effects. The Science of the Total Environment, 575, 525–535. https://doi.org/10.1016/J.SCITOTENV.2016.09.009
Kimmel, G. L., Kimmel, C. A., Williams, A. L., & Desesso, J. M. (2013). Evaluation of developmental toxicity studies of glyphosate with attention to cardiovascular development. Critical Reviews in Toxicology, 43(2), 79–95. https://doi.org/10.3109/10408444.2012.749834
Langley-Evans, S. C., Gardner, D. S., & Welham, S. J. M. (1998). Intrauterine programming of cardiovascular disease by maternal nutritional status. Nutrition (Burbank, Los Angeles County, Calif.), 14(1), 39–47. https://doi.org/10.1016/S0899-9007(97)00391-2
Larsen, K., Najle, R., Lifschitz, A., Maté, M. L., Lanusse, C., & Virkel, G. L. (2014). Effects of sublethal exposure to a glyphosate-based herbicide formulation on metabolic activities of different xenobiotic-metabolizing enzymes in rats. International Journal of Toxicology, 33(4), 307–318. https://doi.org/10.1177/1091581814540481
Larsen, K., Najle, R., Lifschitz, A., & Virkel, G. (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. Environmental Toxicology and Pharmacology, 34(3), 811–818. https://doi.org/10.1016/j.etap.2012.09.005
Marc, J., Mulner-Lorillon, O., & Bellé, R. (2004). Glyphosate-based pesticides affect cell cycle regulation. Biology of the Cell, 96(3), 245–249. https://doi.org/10.1016/J.BIOLCEL.2003.11.010
Mesnage, R., Clair, E., Gress, S., Then, C., Székács, A., & Séralini, G. E. (2013). Cytotoxicity on human cells of Cry1Ab and Cry1Ac Bt insecticidal toxins alone or with a glyphosate-based herbicide. Journal of Applied Toxicology : JAT, 33(7), 695–699. https://doi.org/10.1002/JAT.2712
Milić, M., Žunec, S., Micek, V., Kašuba, V., Mikolić, A., Lovaković, B. T., Semren, T. Ž., Pavičić, I., Čermak, A. M. M., Pizent, A., Vrdoljak, A. L., Valencia-Quintana, R., Sánchez-Alarcón, J., & Želježić, D. (2018). Oxidative stress, cholinesterase activity, and DNA damage in the liver, whole blood, and plasma of Wistar rats following a 28-day exposure to glyphosate. Arhiv Za Higijenu Rada i Toksikologiju, 69(2), 154–168. https://doi.org/10.2478/AIHT-2018-69-3114
Pan, L., Xu, M., Yang, D., Wang, B., Zhao, Q., Ding, E.-M., & Zhu, B. (2017). The association between coronary artery disease and glyphosate exposure found in pesticide factory workers. Journal of Public Health and Emergency, 1(June 2016), 4–4. https://doi.org/10.21037/jphe.2016.12.04
Pereira, J. L., Pereira, R. R., Resende-Silva, G. A., Jakelaitis, A., Silva, A. A., & Picanço, M. C. (2020). Glyphosate impact on arthropods associated to roundup ready and conventional soybean (Glycine max l.). Planta Daninha, 38, 1–11. https://doi.org/10.1590/S0100-83582020380100047
Pu, Y., Yang, J., Chang, L., Qu, Y., Wang, S., Zhang, K., Xiong, Z., Zhang, J., Tan, Y., Wang, X., Fujita, Y., Ishima, T., Wang, D., Hwang, S. H., Hammock, B. D., & Hashimoto, K. (2020). Maternal glyphosate exposure causes autism-like behaviors in offspring through increased expression of soluble epoxide hydrolase. Proceedings of the National Academy of Sciences of the United States of America, 117(21). https://doi.org/10.1073/pnas.1922287117
Relyea, R. A. (2005). The lethal impacts of Roundup and predatory stress on six species of North American tadpoles. Archives of Environmental Contamination and Toxicology, 48(3), 351–357. https://doi.org/10.1007/S00244-004-0086-0
Vieira, L. D., Farias, J. S., de Queiroz, D. B., Cabral, E. v., Lima-Filho, M. M., Sant’Helena, B. R. M., Aires, R. S., Ribeiro, V. S., Santos-Rocha, J., Xavier, F. E., & Paixão, A. D. (2018). Oxidative stress induced by prenatal LPS leads to endothelial dysfunction and renal haemodynamic changes through angiotensin II/NADPH oxidase pathway: Prevention by early treatment with α-tocopherol. Biochimica et Biophysica Acta - Molecular Basis of Disease, 1864(12), 3577–3587. https://doi.org/10.1016/j.bbadis.2018.09.019
Wang, G., Fan, X. N., Tan, Y. Y., Cheng, Q., & Chen, S. di. (2011). Parkinsonism after chronic occupational exposure to glyphosate. Parkinsonism & Related Disorders, 17(6), 486–487. https://doi.org/10.1016/J.PARKRELDIS.2011.02.003
Warembourg, C., Basagaña, X., Seminati, C., de Bont, J., Granum, B., Lyon-Caen, S., Manzano-Salgado, C. B., Pin, I., Sakhi, A. K., Siroux, V., Slama, R., Urquiza, J., Vrijheid, M., Thomsen, C., & Casas, M. (2019). Exposure to phthalate metabolites, phenols and organophosphate pesticide metabolites and blood pressure during pregnancy. International Journal of Hygiene and Environmental Health, 222(3), 446–454. https://doi.org/10.1016/J.IJHEH.2018.12.011
WHO. (1990). Public Health Impact of Pesticides Used in Agriculture. Geneva, Switzerland. https://apps.who.int/iris/bitstream/handle/10665/39772/9241561394.pdf?sequence=1&isAllowed=y
Wickerham, E. L., Lozoff, B., Shao, J., Kaciroti, N., Xia, Y., & Meeker, J. D. (2012). Reduced birth weight in relation to pesticide mixtures detected in cord blood of full-term infants. Environment International, 47, 80–85. https://doi.org/10.1016/J.ENVINT.2012.06.007
Yavuz, T., Delibas, N., Yildirim, B., Altuntas, I., Candir, O., Cora, A., Karahan, N., Ibrisim, E., & Kutsal, A. (2005). Vascular wall damage in rats induced by organophosphorus insecticide methidathion. Toxicology Letters, 155(1), 59–64. https://doi.org/10.1016/J.TOXLET.2004.08.012
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Copyright (c) 2021 Mariana Luiza Rodrigues de Marins; Jeniffer Ailane Nunes Torres; Vivian Giselly da Silva Moraes; Rebeca Gonçalves Leite; Nâmora Carvalho Nascimento; Luciano Augusto de Araújo Ribeiro Ribeiro; Marcos Verissimo de Oliveira Cardoso; Fabrício Souza Silva; Diego Barbosa de Queiroz
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