Glyphosate-based herbicide worsens alterations induced by cafeteria diet on rat uterus

in Journal of Endocrinology
Authors:
María Victoria Zanardi Instituto de Salud y Ambiente del Litoral (ISAL), Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Santa Fe, Argentina
Cátedra de Fisiología Humana, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Santa Fe, Argentina
Faculty of Biology, Institute of Zoology, Technische Universität Dresden, Dresden, Germany

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https://orcid.org/0000-0002-2014-172X
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María Paula Gastiazoro Instituto de Salud y Ambiente del Litoral (ISAL), Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Santa Fe, Argentina
Cátedra de Fisiología Humana, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Santa Fe, Argentina

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María Florencia Rossetti Instituto de Salud y Ambiente del Litoral (ISAL), Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Santa Fe, Argentina
Departamento de Bioquímica Clínica y Cuantitativa, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Santa Fe, Argentina

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Florencia Doná Instituto de Salud y Ambiente del Litoral (ISAL), Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Santa Fe, Argentina

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Gisela Paola Lazzarino Instituto de Salud y Ambiente del Litoral (ISAL), Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Santa Fe, Argentina
Departamento de Bioquímica Clínica y Cuantitativa, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Santa Fe, Argentina

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Oliver Zierau Faculty of Biology, Institute of Zoology, Technische Universität Dresden, Dresden, Germany

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Jorgelina Varayoud Instituto de Salud y Ambiente del Litoral (ISAL), Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Santa Fe, Argentina
Cátedra de Fisiología Humana, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Santa Fe, Argentina

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Milena Durando Instituto de Salud y Ambiente del Litoral (ISAL), Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Santa Fe, Argentina
Cátedra de Fisiología Humana, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Santa Fe, Argentina

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Correspondence should be addressed to M V Zanardi: zanardimvictoria@gmail.com
DOI:
https://doi.org/10.1530/JOE-24-0071
Volume/Issue:
Volume 261: Issue 3
Article Type:
Research Article
Article ID:
e240071
Online Publication Date:
02 May 2024
Copyright:
© the author(s) 2024
Restricted access
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Exposure to glyphosate-based herbicides (GBH) and consumption of cafeteria (CAF) diet, which are widespread in Western society, seem to be associated with endometrial hyperplasia (EH). Here, we aimed to evaluate the effects of a subchronic low dose of GBH added to the CAF diet on the rat uterus. Female Wistar rats were fed from postnatal day (PND)21 until PND240 with chow (control) or CAF diet. Since PND140, rats also received GBH (2 mg of glyphosate/kg/day) or water through food, yielding four experimental groups: control, CAF, GBH, and CAF+GBH. On PND240, CAF and CAF+GBH animals showed an increased adiposity index. With respect to the control group, no changes in the serum levels of 17β-estradiol and progesterone were found. However, progesterone levels were higher in the CAF+GBH group than in the CAF and GBH groups. In the uterus, both studied factors alone and in combination induced morphological and molecular changes associated with EH. Furthermore, the addition of GBH provoked an increased thickness of subepithelial stroma in rats fed with the CAF diet. As a consequence of GBH exposure, CAF+GBH rats exhibited an increased density of abnormal gland area, considered preneoplastic lesions, as well as a reduced PTEN and p27 expression, both tumor suppressor molecules that inhibit cell proliferation, with respect to control rats. These results indicate that the addition of GBH exacerbates the CAF effects on uterine lesions and that the PTEN/p27 signaling pathway seems to be involved. Further studies focusing on the interaction between unhealthy diets and environmental chemicals should be encouraged to better understand uterine pathologies.

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Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© the author(s) 2024
Article ID:
e240071
Article Type:
Research Article
Received Date:
16 Mar 2024
Accepted Date:
05 Apr 2024
Print Publication Date:
01 Jun 2024
Online Publication Date:
02 May 2024
Keywords:
endometrial hyperplasia; p27; phosphatase and tensin homolog; uterine glands

  • An HJ, Lee YH, Cho NH, Shim JY, Kim JY, Lee C & & Kim SJ 2002 Alteration of PTEN expression in endometrial carcinoma is associated with down-regulation of cyclin-dependent kinase inhibitor, p27. Histopathology 41 437–445. (https://doi.org/10.1046/j.1365-2559.2002.01455.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Barnett JA & & Gibson DL 2020 Separating the empirical wheat from the pseudoscientific chaff: A critical review of the literature surrounding glyphosate, dysbiosis and wheat-sensitivity. Frontiers in Microbiology 11 556729. (https://doi.org/10.3389/fmicb.2020.556729)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Benbrook CM 2016 Trends in glyphosate herbicide use in the United States and globally. Environmental Sciences Europe 28 3. (https://doi.org/10.1186/s12302-016-0070-0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Beuret CJ, Zirulnik F & & Giménez MS 2005 Effect of the herbicide glyphosate on liver lipoperoxidation in pregnant rats and their fetuses. Reproductive Toxicology 19 501–504. (https://doi.org/10.1016/j.reprotox.2004.09.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bosquiazzo VL, Vigezzi L, Muñoz-de-Toro M & & Luque EH 2013 Perinatal exposure to diethylstilbestrol alters the functional differentiation of the adult rat uterus. Journal of Steroid Biochemistry and Molecular Biology 138 1–9. (https://doi.org/10.1016/j.jsbmb.2013.02.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chandra V, Kim JJ, Benbrook DM, Dwivedi A & & Rai R 2015 Therapeutic options for management of endometrial hyperplasia. Journal of Gynecologic Oncology 27 e8. (https://doi.org/10.3802/jgo.2016.27.e8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Davis JF, Tracy AL, Schurdak JD, Tschöp MH, Lipton JW, Clegg DJ & & Benoit SC 2008 Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behavioral Neuroscience 122 1257–1263. (https://doi.org/10.1037/a0013111)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dixon D, Alison R, Bach U, Colman K, Foley GL, Harleman JH, Haworth R, Herbert R, Heuser A & Long G et al.2014 Nonproliferative and proliferative lesions of the rat and mouse female reproductive system. Journal of Toxicologic Pathology 27 1S–107S. (https://doi.org/10.1293/tox.27.1S)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dunneram Y, Greenwood DC & & Cade JE 2019 Diet, menopause and the risk of ovarian, endometrial and breast cancer. Proceedings of the Nutrition Society 78 438–448. (https://doi.org/10.1017/S0029665118002884)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Erkanli S, Kayaselcuk F, Kuscu E, Bagis T, Bolat F, Haberal A & & Demirhan B 2006 Expression of survivin, PTEN and p27 in normal, hyperplastic, and carcinomatous endometrium. International Journal of Gynecological Cancer 16 1412–1418. (https://doi.org/10.1111/j.1525-1438.2006.00541.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • European Food Safety Authority 2015 Peer review of the pesticide risk assessment of the potential endocrine disrupting properties of glyphosate. EFSA Journal 15 e04979. (https://doi.org/10.2903/j.efsa.2017.4979)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • European Food Safety Authority 2021 Setting of an import tolerance for glyphosate in soyabeans. EFSA Journal 19 e06880 (https://doi.org/10.2903/j.efsa.2021.6880)

  • Gastiazoro MP, Guerrero-Schimpf M, Durando M, Lazzarino GP, Andreoli MF, Zierau O, Luque EH, Ramos JG & & Varayoud J 2018 Induction of uterine hyperplasia after cafeteria diet exposure. Molecular and Cellular Endocrinology 477 112–120. (https://doi.org/10.1016/j.mce.2018.06.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gastiazoro MP, Rossetti MF, Schumacher R, Stoker C, Durando M, Zierau O, Ramos JG & & Varayoud J 2022 Epigenetic disruption of placental genes by chronic maternal cafeteria diet in rats. Journal of Nutritional Biochemistry 106 109015. (https://doi.org/10.1016/j.jnutbio.2022.109015)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gillezeau C, van Gerwen M, Shaffer RM, Rana I, Zhang L, Sheppard L & & Taioli E 2019 The evidence of human exposure to glyphosate: a review. Environmental Health 18 2. (https://doi.org/10.1186/s12940-018-0435-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bracho GS, Acosta MV, Altamirano GA, Tschopp MV, Luque EH, Kass L & & Bosquiazzo VL 2020 Androgen receptor and uterine histoarchitecture in a PCOS rat model. Molecular and Cellular Endocrinology 518 110973. (https://doi.org/10.1016/j.mce.2020.110973)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Guerrero Schimpf M, Milesi MM, Ingaramo PI, Luque EH & & Varayoud J 2017 Neonatal exposure to a glyphosate based herbicide alters the development of the rat uterus. Toxicology 376 2–14. (https://doi.org/10.1016/j.tox.2016.06.004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Guerrero Schimpf M, Milesi MM, Luque EH & & Varayoud J 2018 Glyphosate-based herbicide enhances the uterine sensitivity to estradiol in rats. Journal of Endocrinology 239 197–213. (https://doi.org/10.1530/JOE-18-0207)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Guerrero Schimpf M, Milesi MM, Zanardi MV & & Varayoud J 2022 Disruption of developmental programming with long-term consequences after exposure to a glyphosate-based herbicide in a rat model. Food and Chemical Toxicology 159 112695. (https://doi.org/10.1016/j.fct.2021.112695)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gunin AG, Mashin IN & & Zakharov DA 2001 Proliferation, mitosis orientation and morphogenetic changes in the uterus of mice following chronic treatment with both estrogen and glucocorticoid hormones. Journal of Endocrinology 169 23–31. (https://doi.org/10.1677/joe.0.1690023)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kubsad D, Nilsson EE, King SE, Sadler-Riggleman I, Beck D & & Skinner MK 2019 Assessment of glyphosate induced epigenetic transgenerational inheritance of pathologies and sperm epimutations: generational toxicology. Scientific Reports 9 6372. (https://doi.org/10.1038/s41598-019-42860-0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kuhn TM, Dhanani S & & Ahmad S 2023 An overview of endometrial cancer with novel therapeutic strategies. Current Oncology 30 7904–7919. (https://doi.org/10.3390/curroncol30090574)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lalanza JF & & Snoeren EMS 2021 The cafeteria diet: a standardized protocol and its effects on behavior. Neuroscience and Biobehavioral Reviews 122 92–119. (https://doi.org/10.1016/j.neubiorev.2020.11.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lazzarino GP, Acutain MF, Canesini G, Andreoli MF & & Ramos JG 2019 Cafeteria diet induces progressive changes in hypothalamic mechanisms involved in food intake control at different feeding periods in female rats. Molecular and Cellular Endocrinology 498 110542. (https://doi.org/10.1016/j.mce.2019.110542)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lazzarino GP, Andreoli MF, Rossetti MF, Stoker C, Tschopp MV, Luque EH & & Ramos JG 2017 Cafeteria diet differentially alters the expression of feeding-related genes through DNA methylation mechanisms in individual hypothalamic nuclei. Molecular and Cellular Endocrinology 450 113–125. (https://doi.org/10.1016/j.mce.2017.05.005)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Li Y, Dong Z, Liu S, Gao F, Zhang J, Peng Z, Wang L & & Pan X 2022 Astaxanthin improves the development of the follicles and oocytes through alleviating oxidative stress induced by BPA in cultured follicles. Scientific Reports 12 7853. (https://doi.org/10.1038/s41598-022-11566-1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mac Loughlin TM, Peluso ML & & Marino DJG 2022 Evaluation of pesticide pollution in the Gualeguay Basin: an extensive agriculture area in Argentina. Science of the Total Environment 851 158142. (https://doi.org/10.1016/j.scitotenv.2022.158142)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Manservisi F, Falcioni L, Bua L, Menghetti I, Mandrioli D, Galeati G, Spinaci M, Tamanini C & & Belpoggi F 2018 Control Data on endocrine sensitive endpoints for untreated Sprague-Dawley rats from the Ramazzini Institute colony. European Journal of Oncology 23 80–85.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Meftaul IM, Venkateswarlu K, Dharmarajan R, Annamalai P, Asaduzzaman M, Parven A & & Megharaj M 2020 Controversies over human health and ecological impacts of glyphosate: is it to be banned in modern agriculture? Environmental Pollution 263 114372. (https://doi.org/10.1016/j.envpol.2020.114372)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Michalczyk K, Niklas N, Rychlicka M & & Cymbaluk-Płoska A 2021 The influence of biologically active substances secreted by the adipose tissue on endometrial cancer. Diagnostics 11 494. (https://doi.org/10.3390/diagnostics11030494)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Milesi MM, Lorenz V, Durando M, Rossetti MF & & Varayoud J 2021 Glyphosate herbicide: reproductive outcomes and multigenerational effects. Frontiers in Endocrinology 12 672532. (https://doi.org/10.3389/fendo.2021.672532)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Milesi MM, Lorenz V, Pacini G, Repetti MR, Demonte LD, Varayoud J & & Luque EH 2018 Perinatal exposure to a glyphosate-based herbicide impairs female reproductive outcomes and induces second-generation adverse effects in Wistar rats. Archives of Toxicology 92 2629–2643. (https://doi.org/10.1007/s00204-018-2236-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Moore K & & Brewer MA 2017 Endometrial cancer: is this a new disease?. American Society of Clinical Oncology Educational Book 37 435–442. (https://doi.org/10.1200/EDBK_175666)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mutter GL 2000 Histopathology of genetically defined endometrial precancers. International Journal of Gynecological Pathology 19 301–309. (https://doi.org/10.1097/00004347-200010000-00002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nakai M, Cook L, Pyter LM, Black M, Sibona J, Turner RT, Jeffery EH & & Bahr JM 2005 Dietary soy protein and isoflavones have no significant effect on bone and a potentially negative effect on the uterus of sexually mature intact Sprague-Dawley female rats. Menopause 12 291–298. (https://doi.org/10.1097/01.GME.0000146109.50235.DO)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Özkara SK & & Corakci A 2004 Significantly decreased P27 expression in endometrial carcinoma compared to complex hyperplasia with atypia (correlation with p53 expression). Pathology Oncology Research 10 89–97. (https://doi.org/10.1007/BF02893462)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Palframan KM & & Myers KP 2016 Modern ‘junk food’ and minimally-processed ‘natural food’ cafeteria diets alter the response to sweet taste but do not impair flavor-nutrient learning in rats. Physiology and Behavior 157 146–157. (https://doi.org/10.1016/j.physbeh.2016.01.010)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Petridou E, Belechri M, Dessypris N, Koukoulomatis P, Diakomanolis E, Spanos E & & Trichopoulos D 2002 Leptin and body mass index in relation to endometrial cancer risk. Annals of Nutrition and Metabolism 46 147–151. (https://doi.org/10.1159/000063081)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Prat J, Gallardo A, Cuatrecasas M & & Catasús L 2007 Endometrial carcinoma: pathology and genetics. Pathology 39 72–87. (https://doi.org/10.1080/00313020601136153)

  • Ramos JG, Varayoud J, Bosquiazzo VL, Luque EH & & Muñoz-de-Toro M 2002 Cellular turnover in the rat uterine cervix and its relationship to estrogen and progesterone receptor dynamics. Biology of Reproduction 67 735–742. (https://doi.org/10.1095/biolreprod.101.002402)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rawat D, Bains A, Chawla P, Kaushik R, Yadav R, Kumar A, Sridhar K & & Sharma M 2023 Hazardous impacts of glyphosate on human and environment health: occurrence and detection in food. Chemosphere 329 138676. (https://doi.org/10.1016/j.chemosphere.2023.138676)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ren X, Li R, Liu J, Huang K, Wu S, Li Y & & Li C 2018 Effects of glyphosate on the ovarian function of pregnant mice, the secretion of hormones and the sex ratio of their fetuses. Environmental Pollution 243 833–841. (https://doi.org/10.1016/j.envpol.2018.09.049)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rossi AS, Oliva ME, Ferreira MR, Chicco A & & Lombardo YB 2013 Dietary chia seed induced changes in hepatic transcription factors and their target lipogenic and oxidative enzyme activities in dyslipidaemic insulin-resistant rats. British Journal of Nutrition 109 1617–1627. (https://doi.org/10.1017/S0007114512003558)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Saadeldin IM, Hussein MA, Suleiman AH, Abohassan MG, Ahmed MM, Moustafa AA, Moumen AF & & Abdel-Aziz Swelum A 2018 Ameliorative effect of ginseng extract on phthalate and bisphenol A reprotoxicity during pregnancy in rats. Environmental Science and Pollution Research International 25 21205–21215. (https://doi.org/10.1007/s11356-018-2299-1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sanderson PA, Critchley HOD, Williams ARW, Arends MJ & & Saunders PTK 2016 New concepts for an old problem: the diagnosis of endometrial hyperplasia. Human Reproduction Update 23 232–254. (https://doi.org/10.1093/humupd/dmw042)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Séralini GE, Clair E, Mesnage R, Gress S, Defarge N, Malatesta M, Hennequin D & & de Vendômois JS 2014 Republished study: long-term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Environmental Sciences Europe 26 14. (https://doi.org/10.1186/s12302-014-0014-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Serra L, Estienne A, Vasseur C, Froment P & & Dupont J 2021 Review: mechanisms of glyphosate and glyphosate-based herbicides action in female and male fertility in humans and animal models. Cells 10 3079. (https://doi.org/10.3390/cells10113079)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shang CG, Liu ZH, Wang XH, Feng ZH & & Zhang Y 2017 Effect of high-fat diet-induced disorders on rat with endometrial hyperplasia and adiponectin system in circulation and uterus. Chinese Medical Journal 130 1831–1837. (https://doi.org/10.4103/0366-6999.211551)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Si CJ, Shu L, Zheng PF, Zhang XY, Yu XL, Gao W & & Zhang L 2017 Dietary patterns and endometrial cancer: a meta-analysis. European Journal of Cancer Prevention 26 336–345. (https://doi.org/10.1097/CEJ.0000000000000266)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Singh G & & Puckett Y 2022 Endometrial hyperplasia. In StatPearls. Treasure Island, FL, USA: StatPearls Publishing. (available at: https://www.ncbi.nlm.nih.gov/books/NBK560693/)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Soares D, Silva L, Duarte S, Pena A & & Pereira A 2021 Glyphosate use, toxicity and occurrence in food. Foods 10 2785. (https://doi.org/10.3390/foods10112785)

  • Sobczuk K & & Sobczuk A 2017 New classification system of endometrial hyperplasia WHO 2014 and its clinical implications. Menopausal Review 3 107–111. (https://doi.org/10.5114/pm.2017.70589)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sonavane M & & Gassman NR 2019 Bisphenol A co-exposure effects: a key factor in understanding BPA’s complex mechanism and health outcomes. Critical Reviews in Toxicology 49 371–386. (https://doi.org/10.1080/10408444.2019.1621263)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Stewart BW 2012 Priorities for cancer prevention: lifestyle choices versus unavoidable exposures. Lancet. Oncology 13 e126–e133. (https://doi.org/10.1016/S1470-2045(1170221-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Stoker C, Andreoli MF, Kass L, Bosquiazzo VL, Rossetti MF, Canesini G, Luque EH & & Ramos JG 2020 Perinatal exposure to bisphenol A (BPA) impairs neuroendocrine mechanisms regulating food intake and kisspetin system in adult male rats. Evidences of metabolic disruptor hypothesis. Molecular and Cellular Endocrinology 499 110614. (https://doi.org/10.1016/j.mce.2019.110614)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sun Q, Qi W, Xiao X, Yang SH, Kim D, Yoon KS, Clark JM & & Park Y 2017 Imidacloprid promotes high fat diet-induced adiposity in female C57BL/6J mice and enhances adipogenesis in 3T3-L1 adipocytes via the AMPKα-mediated pathway. Journal of Agricultural and Food Chemistry 65 6572–6581. (https://doi.org/10.1021/acs.jafc.7b02584)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Székács A & & Darvas B 2018 Re-registration challenges of glyphosate in the European Union. Frontiers in Environmental Science 6. (https://doi.org/10.3389/fenvs.2018.00078)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tarazona JV, Court-Marques D, Tiramani M, Reich H, Pfeil R, Istace F & & Crivellente F 2017 Response to the reply by C.J. Portier and P. Clausing, concerning our review “glyphosate toxicity and carcinogenicity: a review of the scientific basis of the European Union assessment and its differences with IARC.” Archives of Toxicology 91 3199–3203. (https://doi.org/10.1007/s00204-017-2032-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tracy AL, Wee CJM, Hazeltine GE & & Carter RA 2015 Characterization of attenuated food motivation in high-fat diet-induced obesity: critical roles for time on diet and reinforcer familiarity. Physiology and Behavior 141 69–77. (https://doi.org/10.1016/j.physbeh.2015.01.008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Travaglino A, Raffone A, Saccone G, Mascolo M, Guida M, Mollo A, Insabato L & & Zullo F 2020 Congruence between 1994 WHO classification of endometrial hyperplasia and endometrial intraepithelial neoplasia system. American Journal of Clinical Pathology 153 40–48. (https://doi.org/10.1093/ajcp/aqz132)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vigezzi L, Bosquiazzo VL, Kass L, Ramos JG, Muñoz-de-Toro M & & Luque EH 2015 Developmental exposure to bisphenol A alters the differentiation and functional response of the adult rat uterus to estrogen treatment. Reproductive Toxicology 52 83–92. (https://doi.org/10.1016/j.reprotox.2015.01.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Weibel ER 1969 Stereological principles for morphometry in electron microscopic cytology. International Review of Cytology 26 235–302. (https://doi.org/10.1016/s0074-7696(0861637-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yoshida M, Inoue K & & Takahashi M 2015 Predictive modes of action of pesticides in uterine adenocarcinoma development in rats. Journal of Toxicologic Pathology 28 207–216. (https://doi.org/10.1293/tox.2015-0026)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zanardi MV, Schimpf MG, Gastiazoro MP, Milesi MM, Muñoz-de-Toro M, Varayoud J & & Durando M 2020 Glyphosate-based herbicide induces hyperplastic ducts in the mammary gland of aging Wistar rats. Molecular and Cellular Endocrinology 501 110658. (https://doi.org/10.1016/j.mce.2019.110658)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhang X, Guo N, Jin H, Liu R, Zhang Z, Cheng C, Fan Z, Zhang G, Xiao M & Wu S et al.2022 Bisphenol A drives di(2-ethylhexyl) phthalate promoting thyroid tumorigenesis via regulating HDAC6/PTEN and c-MYC signaling. Journal of Hazardous Materials 425 127911. (https://doi.org/10.1016/j.jhazmat.2021.127911)

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  • Zheng XR, Pan X, Zhang J & & Cao X 2018 Hyperinsulinemia-induced PAX6 expression promotes endometrial epithelial cell proliferation via negatively modulating p27 signaling. Biomedicine and Pharmacotherapy 97 802–808. (https://doi.org/10.1016/j.biopha.2017.10.156)

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    • Search Google Scholar
    • Export Citation