{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T19:09:14Z","timestamp":1792782554097,"version":"4.5.0"},"reference-count":72,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T00:00:00Z","timestamp":1781654400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T00:00:00Z","timestamp":1781654400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Universidade Federal De Minas Gerais","id":[{"id":"https:\/\/ror.org\/0176yjw32","id-type":"ROR","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Arch Environ Contam Toxicol"],"published-print":{"date-parts":[[2026,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Estrone (E1) is one of the major natural estrogens influencing the reproductive system of vertebrates. However, it contaminates aquatic environments due to runoff from livestock waste and the discharge of domestic sewage. The aim of this study was to investigate the impact of exposure to environmentally relevant concentrations of E1 on oogenesis and spawning in zebrafish (\n                    <jats:italic>Danio rerio<\/jats:italic>\n                    ). Fish were exposed, in duplicate, to 20, 200, and 2000\u00a0ng\/L of E1 for 49\u00a0days for oogenesis analysis evaluating histology, sex steroids, morphometry, cell proliferation, apoptosis, immunohistochemistry for insulin-like growth factor (IGF) and inducible nitric oxide synthetase (iNOS). 17\u03b2-estradiol (E2) and 11-ketotestosterone (11-KT) were assessed by ELISA assay. Nitric oxide production was evaluated indirectly by quantifying nitrite. Results revealed that E1 exposure altered the proportions of ovarian follicles and somatic components, with significant increase of oogonia, follicular atresia and inflammatory infiltrate, and decrease of follicular cells. Levels of E2, and immunoreaction for IGF1 increased in E120 and 200\u00a0ng\/L groups, but 11-KT, IGF2 and IGF1R were not altered. Nitrite concentrations in ovaries were significantly elevated in E1 200 and 2000\u00a0ng\/L groups, but iNOS immunoreaction was not altered. These changes led to reduced egg production in all groups exposed to E1 and significatively decreased fertilization rates at 200 and 2000\u00a0ng\/L. Overall, the findings demonstrate that E1, even at concentrations commonly found in surface waters, has detrimental effects on ovarian development, gametogenesis and reproductive success in zebrafish. Monitoring environmental estrogens levels in aquatic environments is therefore essential for fish conservation.\n                  <\/jats:p>","DOI":"10.1007\/s00244-026-01202-8","type":"journal-article","created":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T13:17:13Z","timestamp":1781702233000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Exposure to Estrone Impairs Oogenesis and Spawning in Zebrafish (Danio rerio)"],"prefix":"10.1007","volume":"91","author":[{"given":"Yves Moreira","family":"Ribeiro","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Davidson Peruci","family":"Moreira","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alessandro Loureiro","family":"Paschoalini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nilo","family":"Bazzoli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8601-0856","authenticated-orcid":false,"given":"Elizete","family":"Rizzo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,6,17]]},"reference":[{"key":"1202_CR1","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/j.envint.2016.12.010","volume":"99","author":"M Adeel","year":"2017","unstructured":"Adeel M, Song X, Wang Y, Francis D, Yang Y (2017) Environmental impact of estrogens on human, animal and plant life: a critical review. Environ Int 99:107\u2013119. https:\/\/doi.org\/10.1016\/j.envint.2016.12.010","journal-title":"Environ Int"},{"key":"1202_CR2","doi-asserted-by":"publisher","first-page":"1197","DOI":"10.1007\/s10661-011-2032-8","volume":"184","author":"G Andaluri","year":"2012","unstructured":"Andaluri G, Suri RPS, Kumar K (2012) Occurrence of estrogen hormones in biosolids, animal manure and mushroom compost. Environ Monit Assess 184:1197\u20131205. https:\/\/doi.org\/10.1007\/s10661-011-2032-8","journal-title":"Environ Monit Assess"},{"key":"1202_CR3","doi-asserted-by":"publisher","first-page":"1748","DOI":"10.3390\/biomedicines13071748","volume":"13","author":"D Athanasiou","year":"2025","unstructured":"Athanasiou D, Voros C, Soyhan N, Panagou G, Sakellariou M, Mavrogianni D, Bikouvaraki ES, Daskalakis G, Pappa K (2025) The molecular landscape of nitric oxide in ovarian function and IVF success: bridging redox biology and reproductive outcomes. Biomedicines 13:1748. https:\/\/doi.org\/10.3390\/biomedicines13071748","journal-title":"Biomedicines"},{"key":"1202_CR4","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1016\/B978-0-12-815872-2.00014-2","volume-title":"Biology and physiology of freshwater neotropical fish","author":"MI Borella","year":"2020","unstructured":"Borella MI, Chehade C, Costa FG, Jesus LWO, Cassel M, Batlouni SR (2020) The brain-pituitary-gonad axis and the gametogenesis. In: Baldisserotto B, Urbinati EC, Cyrino JEP (eds) Biology and physiology of freshwater neotropical fish. Academic Press, London, pp 315\u2013341. https:\/\/doi.org\/10.1016\/B978-0-12-815872-2.00014-2"},{"key":"1202_CR5","doi-asserted-by":"publisher","unstructured":"Breves, JP, Duffy, TA, Einarsdottir, IE, Bj\u00f6rnsson, BT, McCormick, SD (2018) In vivo effects of 17\u03b1-ethinylestradiol, 17\u03b2-estradiol and 4-nonylphenol on insulin-like growth-factor binding proteins (igfbps) in Atlantic salmon. Aquatic Toxicol 203: 28\u201339 https:\/\/doi.org\/10.1016\/j.aquatox.2018.07.018","DOI":"10.1016\/j.aquatox.2018.07.018"},{"key":"1202_CR6","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0150469","volume":"11","author":"MG Choudhury","year":"2016","unstructured":"Choudhury MG, Saha N (2016) Induction of inducible nitric oxide synthase by lipopolysaccharide and the influences of cell volume changes, stress hormones and oxidative stress on nitric oxide efflux from the perfused liver of air-breathing catfish, Heteropneustes fossilis. PLoS ONE 11:e0150469. https:\/\/doi.org\/10.1371\/journal.pone.0150469","journal-title":"PLoS ONE"},{"key":"1202_CR7","doi-asserted-by":"publisher","first-page":"1743","DOI":"10.1210\/me.2015-1126","volume":"29","author":"L Chu","year":"2015","unstructured":"Chu L, Li J, Liu Y, Cheng CHK (2015) Gonadotropin signaling in zebrafish ovary and testis development: insights from gene knockout study. Mol Endocrinol 29:1743\u20131758. https:\/\/doi.org\/10.1210\/me.2015-1126","journal-title":"Mol Endocrinol"},{"key":"1202_CR8","unstructured":"CONAMA 357 (2005) Classification of water, fresh, brackish and saline in the National Territory. BRAZIL. https:\/\/www.siam.mg.gov.br\/sla\/download.pdf?idNorma=2747. Accessed 13 October 2025"},{"key":"1202_CR9","doi-asserted-by":"publisher","first-page":"1271","DOI":"10.1111\/jfd.13469","volume":"44","author":"A Corriero","year":"2021","unstructured":"Corriero A, Zupa R, Mylonas CC, Passantino L (2021) Atresia of ovarian follicles in fishes, and implications and uses in aquaculture and fisheries. J Fish Dis 44:1271\u20131291. https:\/\/doi.org\/10.1111\/jfd.13469","journal-title":"J Fish Dis"},{"key":"1202_CR10","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1016\/j.aquatox.2011.08.011","volume":"105","author":"AA Dammann","year":"2011","unstructured":"Dammann AA, Shappell NW, Bartell SE, Schoenfuss HL (2011) Comparing biological effects and potencies of estrone and 17\u03b2-estradiol in mature fathead minnows, Pimephales promelas. Aquat Toxicol 105:559\u2013568. https:\/\/doi.org\/10.1016\/j.aquatox.2011.08.011","journal-title":"Aquat Toxicol"},{"key":"1202_CR11","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1016\/j.ydbio.2017.06.029","volume":"430","author":"YM Elkouby","year":"2017","unstructured":"Elkouby YM, Mullins MC (2017) Coordination of cellular differentiation, polarity, mitosis and meiosis\u2014new findings from early vertebrate oogenesis. Dev Biol 430:275\u2013287. https:\/\/doi.org\/10.1016\/j.ydbio.2017.06.029","journal-title":"Dev Biol"},{"key":"1202_CR12","doi-asserted-by":"publisher","first-page":"829","DOI":"10.1093\/eurheartj\/ehr304","volume":"33","author":"U Forstermann","year":"2012","unstructured":"Forstermann U, Sessa WC (2012) Nitric oxide synthases: regulation and function. Eur Heart J 33:829\u2013837. https:\/\/doi.org\/10.1093\/eurheartj\/ehr304","journal-title":"Eur Heart J"},{"key":"1202_CR13","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1016\/j.yfrne.2014.05.002","volume":"35","author":"A Frank","year":"2014","unstructured":"Frank A, Brown LM, Clegg DJ (2014) The role of hypothalamic estrogen receptors in metabolic regulation. Front Neuroendocrinol 35:550\u2013557. https:\/\/doi.org\/10.1016\/j.yfrne.2014.05.002","journal-title":"Front Neuroendocrinol"},{"key":"1202_CR14","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1016\/j.aquatox.2015.08.011","volume":"167","author":"\u00c1 G\u00e1rriz","year":"2015","unstructured":"G\u00e1rriz \u00c1, Men\u00e9ndez-Helman RJ, Miranda LA (2015) Effects of estradiol and ethinylestradiol on sperm quality, fertilization, and embryo\u2013larval survival of pejerrey fish (Odontesthes bonariensis). Aquat Toxicol 167:191\u2013199. https:\/\/doi.org\/10.1016\/j.aquatox.2015.08.011","journal-title":"Aquat Toxicol"},{"key":"1202_CR15","doi-asserted-by":"publisher","first-page":"6857","DOI":"10.1007\/s11356-023-31698-9","volume":"31","author":"A Glineur","year":"2024","unstructured":"Glineur A, Nott K, Carbonnelle P et al (2024) Occurrence and environmental risk assessment of 4 estrogenic compounds in surface water in Belgium in the frame of the EU Watch List. Environ Sci Pollut Res 31:6857\u20136873. https:\/\/doi.org\/10.1007\/s11356-023-31698-9","journal-title":"Environ Sci Pollut Res"},{"key":"1202_CR16","doi-asserted-by":"publisher","unstructured":"Grzegorzek M, Wartalska K, Kowalik R. (2024) Occurrence and sources of hormones in water resources-environmental and health impact. Environ Sci Pollut Res Int. 26: 37907-37922 https:\/\/doi.org\/10.1007\/s11356-024-33713-z","DOI":"10.1007\/s11356-024-33713-z"},{"key":"1202_CR17","doi-asserted-by":"publisher","first-page":"1269","DOI":"10.2331\/fishsci.68.sup2_1269","volume":"68","author":"T Higashino","year":"2002","unstructured":"Higashino T, Miura T, Miura C, Yamauchi K (2002) Effects of 17 \u03b2-estradiol on oogonial proliferation in fish. Fish Sci 68:1269\u20131270. https:\/\/doi.org\/10.2331\/fishsci.68.sup2_1269","journal-title":"Fish Sci"},{"key":"1202_CR18","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1007\/s00244-019-00600-5","volume":"77","author":"LM Jackson","year":"2019","unstructured":"Jackson LM, Klerks PL (2019) Impact of long-term exposure to 17\u03b1-ethinylestradiol in the live-bearing fish Heterandria formosa. Arch Environ Contam Toxicol 77:51\u201361. https:\/\/doi.org\/10.1007\/s00244-019-00600-5","journal-title":"Arch Environ Contam Toxicol"},{"key":"1202_CR19","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/j.etap.2015.06.009","volume":"40","author":"ER Kabir","year":"2015","unstructured":"Kabir ER, Rahman MS, Rahman I (2015) A review on endocrine disruptors and their possible impacts on human health. Environ Toxicol Pharmacol 40:241\u2013258. https:\/\/doi.org\/10.1016\/j.etap.2015.06.009","journal-title":"Environ Toxicol Pharmacol"},{"key":"1202_CR20","doi-asserted-by":"publisher","first-page":"610","DOI":"10.1002\/tox.20585","volume":"26","author":"B Kaptaner","year":"2011","unstructured":"Kaptaner B, \u00dcnal G (2011) Effects of 17\u03b1-ethynylestradiol and nonylphenol on liver and gonadal apoptosis and histopathology in Chalcalburnus tarichi. Environ Toxicol 26:610\u2013622. https:\/\/doi.org\/10.1002\/tox.20585","journal-title":"Environ Toxicol"},{"key":"1202_CR21","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1002\/aja.1002030302","volume":"203","author":"CB Kimmel","year":"1995","unstructured":"Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253\u2013310. https:\/\/doi.org\/10.1002\/aja.1002030302","journal-title":"Dev Dyn"},{"key":"1202_CR22","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1038\/s41574-019-0273-8","volume":"16","author":"MA La Merrill","year":"2020","unstructured":"La Merrill MA, Vandenberg LN, Smith MT, Goodson W, Browne P, Patisaul HB, Guyton KZ, Kortenkamp A, Cogliano VJ, Woodruff TJ, Rieswijk L, Sone H, Korach KS, Gore AC, Zeise L, Zoeller RT (2020) Consensus on the key characteristics of endocrine-disrupting chemicals as a basis for hazard identification. Nat Rev Endocrinol 16:45\u201357. https:\/\/doi.org\/10.1038\/s41574-019-0273-8","journal-title":"Nat Rev Endocrinol"},{"key":"1202_CR23","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/1476-069X-14-13","volume":"14","author":"F Lagarde","year":"2015","unstructured":"Lagarde F, Beausoleil C, Belcher SM, Belzunces LP, Emond C, Guerbet M, Rousselle C (2015) Non-monotonic dose-response relationships and endocrine disruptors: a qualitative method of assessment. Environ Health 14:13. https:\/\/doi.org\/10.1186\/1476-069X-14-13","journal-title":"Environ Health"},{"key":"1202_CR24","doi-asserted-by":"publisher","DOI":"10.1016\/j.aquatox.2023.106457","volume":"257","author":"D-Q Lei","year":"2023","unstructured":"Lei D-Q, Guo-Yong HY, Qiu S-Q, Li X-P, Wang C-S, Fang G-Z, Xie L, Ying G-G (2023) Exposure to estrone disrupts the endocrine system of western mosquitofish (Gambusia affinis). Aquat Toxicol 257:106457. https:\/\/doi.org\/10.1016\/j.aquatox.2023.106457","journal-title":"Aquat Toxicol"},{"key":"1202_CR25","doi-asserted-by":"publisher","first-page":"1700031","DOI":"10.3389\/ftox.2025.1700031","volume":"7","author":"C Lima","year":"2026","unstructured":"Lima C, Gusso D, Disner GR, Pinto FJ, Falc\u00e3o MAP, Rosa JGS, Lopes-Ferreira RJGSA (2026) The zebrafish in toxicology: a bibliometric analysis reveals current trends and future avenues for predictive safety assessment. Front Toxicol 7:1700031. https:\/\/doi.org\/10.3389\/ftox.2025.1700031","journal-title":"Front Toxicol"},{"key":"1202_CR26","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/j.aquaculture.2016.10.029","volume":"472","author":"E Lubzens","year":"2017","unstructured":"Lubzens E, Bobe J, Young G, Sullivan CV (2017) Maternal investment in fish oocytes and eggs: The molecular cargo and its contributions to fertility and early development. Aquaculture 472:107\u2013143. https:\/\/doi.org\/10.1016\/j.aquaculture.2016.10.029","journal-title":"Aquaculture"},{"key":"1202_CR27","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1016\/j.ygcen.2009.05.022","volume":"165","author":"E Lubzens","year":"2010","unstructured":"Lubzens E, Young G, Bobe J, Cerd\u00e0 J (2010) Oogenesis in teleosts: How fish eggs are formed. Gen Com Endocrinol 165:367\u2013389. https:\/\/doi.org\/10.1016\/j.ygcen.2009.05.022","journal-title":"Gen Com Endocrinol"},{"key":"1202_CR28","doi-asserted-by":"publisher","unstructured":"Luo Y, Zhu Y, Basang W, Wang X, Li C, Zhou X. (2021) Roles of nitric oxide in the regulation of reproduction: a review. Front Endocrinol (Lausanne). 12: 752410 https:\/\/doi.org\/10.3389\/fendo.2021.752410","DOI":"10.3389\/fendo.2021.752410"},{"key":"1202_CR29","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1016\/j.aquatox.2011.06.017","volume":"105","author":"TV Madureira","year":"2011","unstructured":"Madureira TV, Rocha MJ, Cruzeiro C, Galante MH, Monteiro RAF, Rocha E (2011) The toxicity potential of pharmaceuticals found in the Douro River estuary (Portugal): assessing impacts on gonadal maturation with a histopathological and stereological study of zebrafish ovary and testis after sub-acute exposures. Aquat Toxicol 105:292\u2013299. https:\/\/doi.org\/10.1016\/j.aquatox.2011.06.017","journal-title":"Aquat Toxicol"},{"key":"1202_CR30","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.ygcen.2007.01.004","volume":"153","author":"A Mandich","year":"2007","unstructured":"Mandich A, Bottero S, Benfenati E, Cevasco A, Erratico C, Maggioni S, Massari A, Pedemonte F, Vigan\u00f2 L (2007) In vivo exposure of carp to graded concentrations of bisphenol A. Gen Comp Endocrinol 153:15\u201324. https:\/\/doi.org\/10.1016\/j.ygcen.2007.01.004","journal-title":"Gen Comp Endocrinol"},{"key":"1202_CR31","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1016\/j.tice.2015.10.002","volume":"47","author":"RMC Melo","year":"2015","unstructured":"Melo RMC, Martins YS, Luz RK, Rizzo E, Bazzoli N (2015) PCNA and apoptosis during post-spawning ovarian remodeling in the teleost Oreochromis niloticus. Tissue Cell 47:541\u2013549. https:\/\/doi.org\/10.1016\/j.tice.2015.10.002","journal-title":"Tissue Cell"},{"key":"1202_CR32","doi-asserted-by":"publisher","first-page":"5734","DOI":"10.1038\/sj.onc.1206663","volume":"22","author":"RB Mikkelsen","year":"2003","unstructured":"Mikkelsen RB, Wardman P (2003) Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 22:5734\u20135754. https:\/\/doi.org\/10.1038\/sj.onc.1206663","journal-title":"Oncogene"},{"key":"1202_CR33","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1093\/biolre\/iox124","volume":"97","author":"C Monson","year":"2017","unstructured":"Monson C, Forsgren K, Goetz G, Harding L, Swanson P, Young G (2017) A teleost androgen promotes development of primary ovarian follicles in coho salmon and rapidly alters the ovarian transcriptome. Biol Reprod 97:731\u2013745. https:\/\/doi.org\/10.1093\/biolre\/iox124","journal-title":"Biol Reprod"},{"issue":"10","key":"1202_CR34","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0311628","volume":"19","author":"C Monson","year":"2024","unstructured":"Monson C, Goetz G, Forsgren K, Swanson P, Young G (2024) In vivo treatment with a non-aromatizable androgen rapidly alters the ovarian transcriptome of previtellogenic secondary growth coho salmon (Oncorhynchus kisutch). PLoS ONE 19(10):e0311628. https:\/\/doi.org\/10.1371\/journal.pone.0311628","journal-title":"PLoS ONE"},{"key":"1202_CR35","doi-asserted-by":"publisher","first-page":"988","DOI":"10.1071\/RD20128","volume":"32","author":"DP Moreira","year":"2020","unstructured":"Moreira DP, Melo RMC, Weber AA, Rizzo E (2020) Insulin-like growth factors 1 and 2 are associated with testicular germ cell proliferation and apoptosis during fish reproduction. Reprod Fertil Dev 32:988\u2013998. https:\/\/doi.org\/10.1071\/RD20128","journal-title":"Reprod Fertil Dev"},{"issue":"1","key":"1202_CR36","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1007\/s00204-022-03390-3","volume":"97","author":"DP Moreira","year":"2023","unstructured":"Moreira DP, Ribeiro YM, Ferreira CS, dos Santos Nassif Lacerda SM, Rizzo E (2023) Exposure to acetaminophen impairs gametogenesis and fertility in zebrafish (Danio rerio). Arch Toxicol 97(1):263\u2013278. https:\/\/doi.org\/10.1007\/s00204-022-03390-3","journal-title":"Arch Toxicol"},{"key":"1202_CR37","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/j.jsbmb.2017.01.014","volume":"176","author":"A Nadal","year":"2018","unstructured":"Nadal A, Fuentes E, Ripoll C, Villar-Pazos S, Castellano-Mu\u00f1oz M, Soriano S, Martinez-Pinna J, Quesada I, Alonso-Magdalena P (2018) Extranuclear-initiated estrogenic actions of endocrine disrupting chemicals: Is there toxicology beyond paracelsus? J Steroid Biochem Mol Biol 176:16\u201322. https:\/\/doi.org\/10.1016\/j.jsbmb.2017.01.014","journal-title":"J Steroid Biochem Mol Biol"},{"key":"1202_CR38","doi-asserted-by":"publisher","first-page":"4440","DOI":"10.3390\/ijms20184440","volume":"20","author":"Y Neirijnck","year":"2019","unstructured":"Neirijnck Y, Papaioannou MD, Nef S (2019) The insulin\/IGF system in mammalian sexual development and reproduction. Int J Mol Sci 20:4440. https:\/\/doi.org\/10.3390\/ijms20184440","journal-title":"Int J Mol Sci"},{"key":"1202_CR39","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.ygcen.2013.03.032","volume":"192","author":"ER Nelson","year":"2023","unstructured":"Nelson ER, Habibi HR (2023) Estrogen receptor function and regulation in fish and other vertebrates. Gen Comp Endocrinol 192:15\u201324. https:\/\/doi.org\/10.1016\/j.ygcen.2013.03.032","journal-title":"Gen Comp Endocrinol"},{"key":"1202_CR40","doi-asserted-by":"publisher","unstructured":"Nevzati E, Shafighi M, Bakhtian KD, Treiber H, Fandino J, Fathi AR (2015) Estrogen induces nitric oxide production via nitric oxide synthase activation in endothelial cells. In: Fandino J, Marbacher S, Fathi A-R, Muroi C, Keller E (Eds.) Neurovascular events after subarachnoid hemorrhage. Acta Neurochirurgica Supplement, vol. 120. Springer International Publishing, Cham, pp 141\u2013145. https:\/\/doi.org\/10.1007\/978-3-319-04981-6_24","DOI":"10.1007\/978-3-319-04981-6_24"},{"key":"1202_CR41","doi-asserted-by":"publisher","first-page":"797","DOI":"10.1007\/s10695-021-00938-5","volume":"47","author":"AL Paschoalini","year":"2021","unstructured":"Paschoalini AL, Savassi LA, Weber AA, Moreira DP, Ribeiro YM, Rizzo E, Bazzoli N (2021) Evaluation of the oestrogenic potential of oestrone and bisphenol-A on the reproduction of Astyanax bimaculatus males after subacute exposure. Fish Physiol Biochem 47:797\u2013810. https:\/\/doi.org\/10.1007\/s10695-021-00938-5","journal-title":"Fish Physiol Biochem"},{"key":"1202_CR42","doi-asserted-by":"publisher","DOI":"10.1016\/j.yfrne.2021.100926","volume":"62","author":"M Pillerov\u00e1","year":"2021","unstructured":"Pillerov\u00e1 M, Borb\u00e9lyov\u00e1 V, Hodosy J, Riljak V, Rencz\u00e9s E, Frick KM, T\u00f3thov\u00e1 \u013d (2021) On the role of sex steroids in biological functions by classical and non-classical pathways. An Update Front Neuroendocrinol 62:100926. https:\/\/doi.org\/10.1016\/j.yfrne.2021.100926","journal-title":"An Update Front Neuroendocrinol"},{"key":"1202_CR43","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/j.envres.2014.03.002","volume":"131","author":"PS Prado","year":"2014","unstructured":"Prado PS, Pinheiro APB, Bazzoli N, Rizzo E (2014) Reproductive biomarkers responses induced by xenoestrogens in the characid fish Astyanax fasciatus inhabiting a South American reservoir: An integrated field and laboratory approach. Environ Res 131:165\u2013173. https:\/\/doi.org\/10.1016\/j.envres.2014.03.002","journal-title":"Environ Res"},{"key":"1202_CR44","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1007\/s10695-018-0550-9","volume":"45","author":"PS Prado","year":"2019","unstructured":"Prado PS, Pinheiro APB, Weber AA, Bazzoli N, Rizzo E (2019) Expression patterns and immunolocalisation of IGF-I and IGF-II in male and female gonads of the Neotropical characid fish Astyanax fasciatus. Fish Physiol Biochem 45:167\u2013176. https:\/\/doi.org\/10.1007\/s10695-018-0550-9","journal-title":"Fish Physiol Biochem"},{"key":"1202_CR45","doi-asserted-by":"publisher","first-page":"1290","DOI":"10.1002\/jmor.10981","volume":"272","author":"I Quagio-Grassiotto","year":"2011","unstructured":"Quagio-Grassiotto I, Grier H, Mazzoni TS, N\u00f3brega RH, Arruda Amorim JP (2011) Activity of the ovarian germinal epithelium in the freshwater catfish, Pimelodus maculatus (Teleostei: Ostariophysi: Siluriformes): Germline cysts, follicle formation and oocyte development. J Morphol 272:1290\u20131306. https:\/\/doi.org\/10.1002\/jmor.10981","journal-title":"J Morphol"},{"key":"1202_CR46","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1095\/biolreprod.109.080093","volume":"82","author":"M Reinecke","year":"2010","unstructured":"Reinecke M (2010) Insulin-like growth factors and fish reproduction. Biol Reprod 82:656\u2013661. https:\/\/doi.org\/10.1095\/biolreprod.109.080093","journal-title":"Biol Reprod"},{"key":"1202_CR47","doi-asserted-by":"publisher","first-page":"664","DOI":"10.1016\/j.tice.2017.09.003","volume":"49","author":"YM Ribeiro","year":"2017","unstructured":"Ribeiro YM, Matos AS, Domingos FFT, Santos HB, Vieira ABC, Bazzoli N, Rizzo E (2017) Germ cell proliferation and apoptosis during testicular regression in a seasonal breeding fish kept in captivity. Tissue Cell 49:664\u2013671. https:\/\/doi.org\/10.1016\/j.tice.2017.09.003","journal-title":"Tissue Cell"},{"key":"1202_CR48","doi-asserted-by":"publisher","DOI":"10.1016\/j.etap.2022.104058","volume":"98","author":"YM Ribeiro","year":"2023","unstructured":"Ribeiro YM, Moreira DP, Weber AA, Rodrigues Miranda TG, Bazzoli N, Rizzo E (2023) Chronic estrone exposure affects spermatogenesis and sperm quality in zebrafish (Danio rerio). Environ Toxicol Pharmacol 98:104058. https:\/\/doi.org\/10.1016\/j.etap.2022.104058","journal-title":"Environ Toxicol Pharmacol"},{"key":"1202_CR49","doi-asserted-by":"publisher","DOI":"10.1016\/j.ecoenv.2021.112670","volume":"224","author":"YM Ribeiro","year":"2021","unstructured":"Ribeiro YM, Weber AA, Paschoalini AL, Moreira DP, Sales CF, Almeida TVP, Neres MA, Bazzoli N, Rizzo E (2021) Biomarker responses induced by bisphenol A on spermatogenesis in a Neotropical teleost fish are temperature-dependent. Ecotoxicol Environ Saf 224:112670. https:\/\/doi.org\/10.1016\/j.ecoenv.2021.112670","journal-title":"Ecotoxicol Environ Saf"},{"key":"1202_CR50","first-page":"291","volume":"23","author":"AC Ruifrok","year":"2001","unstructured":"Ruifrok AC, Johnston DA (2001) Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 23:291\u2013299","journal-title":"Anal Quant Cytol Histol"},{"key":"1202_CR51","doi-asserted-by":"publisher","DOI":"10.1016\/j.ygcen.2019.113378","volume":"289","author":"R Rutherford","year":"2020","unstructured":"Rutherford R, Lister A, Bosker T, Blewett T, Gillio Meina E, Chehade I, Kanagasabesan T, MacLatchy D (2020) Mummichog (Fundulus heteroclitus) are less sensitive to 17\u03b1-ethinylestradiol (EE2) than other common model teleosts: a comparative review of reproductive effects. Gen Comp Endocrinol 289:113378. https:\/\/doi.org\/10.1016\/j.ygcen.2019.113378","journal-title":"Gen Comp Endocrinol"},{"key":"1202_CR52","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1007\/s00441-025-03982-2","volume":"401","author":"CF Sales","year":"2025","unstructured":"Sales CF, Ara\u00fajo BA, Souza SM, Rizzo E, Melo RMC (2025) Folliculogenesis and follicular growth in the endangered fish Brycon opalinus, with emphasis on ovarian matrix remodeling. Cell Tissue Res 401:167\u2013179. https:\/\/doi.org\/10.1007\/s00441-025-03982-2","journal-title":"Cell Tissue Res"},{"issue":"5","key":"1202_CR53","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1159\/000079100","volume":"79","author":"JE S\u00e1nchez-Criado","year":"2004","unstructured":"S\u00e1nchez-Criado JE, Mart\u00edn de las Mulas J, Bellido C, Tena-Sempere M, Aguilar R, Blanco A (2004) Biological role of pituitary estrogen receptors ER\u03b1 and ER\u03b2 on progesterone receptor expression and action and on gonadotropin and prolactin secretion in the rat. Neuroendocrinology 79(5):247\u2013258","journal-title":"Neuroendocrinology"},{"key":"1202_CR54","doi-asserted-by":"publisher","first-page":"768","DOI":"10.1080\/15287390701236470","volume":"70","author":"C Sch\u00e4fers","year":"2007","unstructured":"Sch\u00e4fers C, Teigeler M, Wenzel A, Maack G, Fenske M, Segner H (2007) Concentration- and time-dependent effects of the synthetic estrogen, 17\u03b1-ethinylestradiol, on reproductive capabilities of the zebrafish, Danio rerio. J Toxicol Environ Health, Part A 70:768\u2013779. https:\/\/doi.org\/10.1080\/15287390701236470","journal-title":"J Toxicol Environ Health, Part A"},{"key":"1202_CR55","doi-asserted-by":"publisher","first-page":"25727","DOI":"10.1074\/jbc.M112.349902","volume":"287","author":"M Shen","year":"2012","unstructured":"Shen M, Lin F, Zhang J, Tang Y, Chen WK, Liu H (2012) Involvement of the up-regulated FoxO1 expression in follicular granulosa cell apoptosis induced by oxidative stress. J Biol Chem 287:25727\u201325740. https:\/\/doi.org\/10.1074\/jbc.M112.349902","journal-title":"J Biol Chem"},{"key":"1202_CR56","doi-asserted-by":"publisher","unstructured":"Silva RL, Lima e Silva MA, Teixeira TP et al (2025) Systematic review of estrogens as emerging contaminants in water: a global overview study from the one health perspective. J Xenobiot 15:148. https:\/\/doi.org\/10.3390\/jox15050148","DOI":"10.3390\/jox15050148"},{"key":"1202_CR57","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.ygcen.2014.04.001","volume":"220","author":"VK Singh","year":"2015","unstructured":"Singh VK, Lal B (2015) Immunolocalization of nitric oxide synthase (NOS) isoforms in ovarian follicles of the catfish, Clarias batrachus and its relation with ovarian activity. Gen Comp Endocrinol 220:98\u2013102. https:\/\/doi.org\/10.1016\/j.ygcen.2014.04.001","journal-title":"Gen Comp Endocrinol"},{"issue":"2","key":"1202_CR58","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1530\/REP-16-0482","volume":"153","author":"VK Singh","year":"2017","unstructured":"Singh VK, Lal B (2017) Nitric oxide (NO) stimulates steroidogenesis and folliculogenesis in fish. Reproduction 153(2):133\u2013146. https:\/\/doi.org\/10.1530\/REP-16-0482","journal-title":"Reproduction"},{"key":"1202_CR59","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1016\/j.tice.2011.11.002","volume":"44","author":"RG Thom\u00e9","year":"2012","unstructured":"Thom\u00e9 RG, Domingos FFT, Santos HB, Martinelli PM, Sato Y, Rizzo E, Bazzoli N (2012) Apoptosis, cell proliferation and vitellogenesis during the folliculogenesis and follicular growth in teleost fish. Tissue Cell 44:54\u201362. https:\/\/doi.org\/10.1016\/j.tice.2011.11.002","journal-title":"Tissue Cell"},{"key":"1202_CR60","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.steroids.2015.06.011","volume":"103","author":"J Tokarz","year":"2015","unstructured":"Tokarz J, M\u00f6ller G, Hrab\u011b de Angelis M, Adamski J (2015) Steroids in teleost fishes: a functional point of view. Steroids 103:123\u2013144. https:\/\/doi.org\/10.1016\/j.steroids.2015.06.011","journal-title":"Steroids"},{"issue":"2","key":"1202_CR61","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1677\/joe-07-0509","volume":"199","author":"V Tripathi","year":"2008","unstructured":"Tripathi V, Krishna A (2008) Changes in nitric oxide (NO) synthase isoforms and NO in the ovary of Heteropneustes fossilis (Bloch.) during the reproductive cycle. J Endocrinol 199(2):307\u2013316. https:\/\/doi.org\/10.1677\/joe-07-0509","journal-title":"J Endocrinol"},{"key":"1202_CR62","unstructured":"USEPA (2002) National recommended water quality criteria: 2002. https:\/\/www.epa.gov\/sites\/default\/files\/2018-12\/documents\/national-recommended-hh-criteria-2002.pdf. Accessed 13 October 2025"},{"issue":"9","key":"1202_CR63","doi-asserted-by":"publisher","first-page":"503","DOI":"10.3390\/biom9090503","volume":"9","author":"D-KH Vo","year":"2019","unstructured":"Vo D-KH, Hartig R, Weinert S, Haybaeck J, Nass N (2019) G-protein-coupled estrogen receptor (GPER)-specific agonist G1 induces ER stress leading to cell death in MCF-7 cells. Biomolecules 9(9):503. https:\/\/doi.org\/10.3390\/biom9090503","journal-title":"Biomolecules"},{"key":"1202_CR64","doi-asserted-by":"publisher","first-page":"115","DOI":"10.3389\/fendo.2020.00115","volume":"11","author":"W Wang","year":"2020","unstructured":"Wang W, Zhu H, Tian Z, Sun A, Dong Y, Dong T, Hu H (2020) Effects of 11-ketotestosterone on development of the previtellogenic ovary in the sterlet. Acipenser Ruthenus Front Endocrinol 11:115. https:\/\/doi.org\/10.3389\/fendo.2020.00115","journal-title":"Acipenser Ruthenus Front Endocrinol"},{"issue":"1","key":"1202_CR65","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1007\/s10653-014-9637-0","volume":"37","author":"Y Wang","year":"2015","unstructured":"Wang Y, Wang Q, Hu L, Lu G, Li Y (2015) Occurrence of estrogens in water, sediment and biota and their ecological risk in Northern Taihu Lake in China. Environ Geochem Health 37(1):147\u2013156. https:\/\/doi.org\/10.1007\/s10653-014-9637-0","journal-title":"Environ Geochem Health"},{"key":"1202_CR66","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.ygcen.2018.12.016","volume":"279","author":"AA Weber","year":"2019","unstructured":"Weber AA, Moreira DP, Melo RMC, Ribeiro YM, Bazzoli N, Rizzo E (2019) Environmental exposure to oestrogenic endocrine disruptors mixtures reflecting on gonadal sex steroids and gametogenesis of the neotropical fish Astyanax rivularis. Gen Comp Endocrinol 279:99\u2013108","journal-title":"Gen Comp Endocrinol"},{"key":"1202_CR67","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1016\/j.scitotenv.2017.02.181","volume":"592","author":"AA Weber","year":"2017","unstructured":"Weber AA, Moreira DP, Melo RMC, Vieira ABC, Prado PS, Bazzoli N, Rizzo E (2017) Reproductive effects of oestrogenic endocrine disrupting chemicals in Astyanax rivularis inhabiting headwaters of the Velhas River, Brazil. Sci Total Environ 592:693\u2013703. https:\/\/doi.org\/10.1016\/j.scitotenv.2017.02.181","journal-title":"Sci Total Environ"},{"key":"1202_CR68","doi-asserted-by":"publisher","first-page":"367","DOI":"10.3390\/fishes8070367","volume":"8","author":"GM Weber","year":"2023","unstructured":"Weber GM (2023) Effects of IGF1 and IGF2 on in vitro ovarian follicle maturation in rainbow trout Oncorhynchus mykiss. Fishes 8:367. https:\/\/doi.org\/10.3390\/fishes8070367","journal-title":"Fishes"},{"key":"1202_CR69","doi-asserted-by":"publisher","first-page":"143736","DOI":"10.1016\/j.scitotenv.2020.143736","volume":"757","author":"C-C Wu","year":"2021","unstructured":"Wu C-C, Shields JN, Akemann C et al (2021) The phenotypic and transcriptomic effects of developmental exposure to nanomolar levels of estrone and bisphenol A in zebrafish. Sci Total Environ 757:143736. https:\/\/doi.org\/10.1016\/j.scitotenv.2020.143736","journal-title":"Sci Total Environ"},{"key":"1202_CR70","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/j.aquatox.2013.10.025","volume":"146","author":"T Ye","year":"2014","unstructured":"Ye T, Kang M, Huang Q, Fang C, Chen Y, Shen H, Dong S (2014) Exposure to DEHP and MEHP from hatching to adulthood causes reproductive dysfunction and endocrine disruption in marine medaka (Oryzias melastigma). Aquat Toxicol 146:115\u2013126. https:\/\/doi.org\/10.1016\/j.aquatox.2013.10.025","journal-title":"Aquat Toxicol"},{"key":"1202_CR71","doi-asserted-by":"publisher","first-page":"978","DOI":"10.3390\/antiox14080978","volume":"14","author":"T Zhao","year":"2025","unstructured":"Zhao T, Jia H, Zhao X, Gu X, Yong C, Wang S, Zhou J, Li L, Gan M, Niu L et al (2025) Oxidative stress triggers porcine ovarian granulosa cell apoptosis through MAPK signaling. Antioxidants 14:978. https:\/\/doi.org\/10.3390\/antiox14080978","journal-title":"Antioxidants"},{"key":"1202_CR72","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1210\/me.2012-1307","volume":"27","author":"P Zhou","year":"2013","unstructured":"Zhou P, Baumgarten SC, Wu Y, Bennett J, Winston N, Hirshfeld-Cytron J, Stocco C (2013) IGF-I signaling is essential for FSH stimulation of AKT and steroidogenic genes in granulosa cells. Mol Endocrinol 27:511\u2013523. https:\/\/doi.org\/10.1210\/me.2012-1307","journal-title":"Mol Endocrinol"}],"container-title":["Archives of Environmental Contamination and Toxicology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00244-026-01202-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00244-026-01202-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00244-026-01202-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T18:02:45Z","timestamp":1791482565000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00244-026-01202-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,17]]},"references-count":72,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2026,7]]}},"alternative-id":["1202"],"URL":"https:\/\/doi.org\/10.1007\/s00244-026-01202-8","relation":{},"ISSN":["0090-4341","1432-0703"],"issn-type":[{"value":"0090-4341","type":"print"},{"value":"1432-0703","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,17]]},"assertion":[{"value":"8 November 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 May 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 June 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no conflict of interest.","order":1,"name":"Ethics","label":"Conflict of interest","group":{"name":"EthicsHeading","label":"Declarations"}}],"article-number":"5"}}