{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T19:00:27Z","timestamp":1790362827435,"version":"4.1.0"},"reference-count":72,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,4,29]],"date-time":"2025-04-29T00:00:00Z","timestamp":1745884800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2025,4,29]],"date-time":"2025-04-29T00:00:00Z","timestamp":1745884800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"funder":[{"DOI":"10.13039\/100010661","name":"H2020","doi-asserted-by":"crossref","award":["862658"],"award-info":[{"award-number":["862658"]}],"id":[{"id":"10.13039\/100010661","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"DOI":"10.1038\/s41598-025-99372-3","type":"journal-article","created":{"date-parts":[[2025,4,29]],"date-time":"2025-04-29T16:13:17Z","timestamp":1745943197000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Spermatogenesis advancement in pre-pubertal meagre Argyrosomus regius treated with recombinant gonadotropins"],"prefix":"10.1038","volume":"15","author":[{"given":"Gianluca","family":"Ventriglia","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neil","family":"Duncan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ignacio","family":"Gim\u00e9nez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Constantinos C.","family":"Mylonas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chrysovalentinos","family":"Pousis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aldo","family":"Corriero","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rosa","family":"Zupa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,4,29]]},"reference":[{"key":"99372_CR1","unstructured":"Chao, L. N. & Trewavas, E. Sciaenidae in Check-list of the fishes the eastern tropical Atlantic (CLOFETA) Vol. 2 (eds. Quero, J. C., Hureau, J. C., Karrer, C., Post, A. & Saldanha, L.) 813\u2013826 (JNICT, Lisbon; SEI, Paris; and UNESCO, Paris, 1990)."},{"key":"99372_CR2","unstructured":"EUMOFA, European Market Observatory for Fisheries and Aquaculture Products-Meagre in the EU. ISBN 978-92-76-47640-5 (2022). https:\/\/www.eumofa.eu Accessed 12 June 2023."},{"key":"99372_CR3","unstructured":"FAO, Global aquaculture production Quantity. License: CC BY-NC-SA 3.0 IGO. Extracted from (1950\u20132020). https:\/\/www.fao.org\/fishery\/statistics-query\/en\/aquaculture\/aquaculture_quantity (2022). (Accessed 12 June 2023)"},{"key":"99372_CR4","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1016\/S0044-8486(03)00120-0","volume":"221","author":"CC Mylonas","year":"2003","unstructured":"Mylonas, C. C. et al. Multiple spawning and egg quality of individual European sea bass (Dicentrarchus labrax) females after repeated injections of GnRHa. Aquaculture 221, 605\u2013620. https:\/\/doi.org\/10.1016\/S0044-8486(03)00120-0 (2003).","journal-title":"Aquaculture"},{"key":"99372_CR5","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/j.aquaculture.2004.04.015","volume":"237","author":"CC Mylonas","year":"2004","unstructured":"Mylonas, C. C. et al. Induction of spawning of cultured greater Amberjack (Seriola dumerili) using GnRHa implants. Aquaculture 237, 141\u2013154. https:\/\/doi.org\/10.1016\/j.aquaculture.2004.04.015 (2004).","journal-title":"Aquaculture"},{"key":"99372_CR6","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1111\/j.1439-0426.2012.02045.x","volume":"29","author":"R Zupa","year":"2013","unstructured":"Zupa, R. et al. Comparative analysis of male germ cell proliferation and apoptosis in wild and captive Atlantic Bluefin tuna (Thunnus Thynnus L). J. Appl. Ichthyol. 29, 71\u201381. https:\/\/doi.org\/10.1111\/j.1439-0426.2012.02045.x (2013).","journal-title":"J. Appl. Ichthyol."},{"key":"99372_CR7","doi-asserted-by":"publisher","first-page":"1733","DOI":"10.1111\/are.12110","volume":"45","author":"R Zupa","year":"2014","unstructured":"Zupa, R. et al. Male germ cell proliferation and apoptosis during the reproductive cycle of captive-reared Atlantic Bluefin tuna Thunnus thynnus (Linnaeus). Aquac Res. 45, 1733\u20131736. https:\/\/doi.org\/10.1111\/are.12110 (2014).","journal-title":"Aquac Res."},{"issue":"1","key":"99372_CR8","doi-asserted-by":"publisher","first-page":"e0169645","DOI":"10.1371\/journal.pone.0169645","volume":"12","author":"R Zupa","year":"2017","unstructured":"Zupa, R. et al. Comparative study of reproductive development in wild and captive-reared greater Amberjack Seriola dumerili (Risso, 1810). PLoS ONE. 12 (1), e0169645. https:\/\/doi.org\/10.1371\/journal.pone.0169645 (2017).","journal-title":"PLoS ONE"},{"key":"99372_CR9","doi-asserted-by":"publisher","first-page":"4085","DOI":"10.2527\/jas.2017.1708","volume":"95","author":"R Zupa","year":"2017","unstructured":"Zupa, R. et al. Rearing in captivity affects spermatogenesis and sperm quality in greater Amberjack Seriola dumerili (Risso, 1810). J. Anim. Sci. 95, 4085\u20134100. https:\/\/doi.org\/10.2527\/jas.2017.1708 (2017).","journal-title":"J. Anim. Sci."},{"key":"99372_CR10","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1111\/are.13453","volume":"49","author":"C Pousis","year":"2018","unstructured":"Pousis, C. et al. The observed oogenesis impairment in greater Amberjack Seriola dumerili (Risso, 1810) reared in captivity is not related to an insufficient liver transcription or oocyte uptake of vitellogenin. Aquac Res. 49, 243\u2013252. https:\/\/doi.org\/10.1111\/are.13453 (2018).","journal-title":"Aquac Res."},{"key":"99372_CR11","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.theriogenology.2019.08.014","volume":"140","author":"C Pousis","year":"2019","unstructured":"Pousis, C. et al. Vitellogenin receptor and fatty acid profiles of individual lipid classes of oocytes from wild and captive-reared greater Amberjack (Seriola dumerili) during the reproductive cycle. Theriogenology 140, 73\u201383. https:\/\/doi.org\/10.1016\/j.theriogenology.2019.08.014 (2019).","journal-title":"Theriogenology"},{"key":"99372_CR12","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1007\/s10695-020-00910-9","volume":"47","author":"I Fakriadis","year":"2021","unstructured":"Fakriadis, I. & Mylonas, C. C. Sperm quality of greater Amberjack Seriola dumerili throughout the reproductive season and in response to GnRHa treatment with controlled release implants. Fish. Physiol. Biochem. 47, 281\u2013292. https:\/\/doi.org\/10.1007\/s10695-020-00910-9 (2021).","journal-title":"Fish. Physiol. Biochem."},{"key":"99372_CR13","doi-asserted-by":"publisher","first-page":"13662","DOI":"10.1038\/s41598-023-40597-5","volume":"13","author":"A Lavecchia","year":"2023","unstructured":"Lavecchia, A. et al. Dysregulation of testis mRNA expression levels in hatchery-produced vs wild greater Amberjack Seriola dumerili. Sci. Rep. 13, 13662. https:\/\/doi.org\/10.1038\/s41598-023-40597-5 (2023).","journal-title":"Sci. Rep."},{"key":"99372_CR14","doi-asserted-by":"publisher","first-page":"18034","DOI":"10.1038\/s41598-024-69091-2","volume":"14","author":"A Lavecchia","year":"2024","unstructured":"Lavecchia, A. et al. Comparison of ovarian mRNA expression levels in wild and hatchery\u2013produced greater Amberjack Seriola dumerili. Sci. Rep. 14, 18034. https:\/\/doi.org\/10.1038\/s41598-024-69091-2 (2024).","journal-title":"Sci. Rep."},{"key":"99372_CR15","doi-asserted-by":"publisher","first-page":"1273","DOI":"10.1007\/s10695-012-9615-3","volume":"38","author":"N Duncan","year":"2012","unstructured":"Duncan, N. et al. Reproductive development, GnRHa-induced spawning and egg quality of wild meagre (Argyrosomus regius) acclimatised to captivity. Fish. Physiol. Biochem. 38, 1273\u20131286. https:\/\/doi.org\/10.1007\/s10695-012-9615-3 (2012).","journal-title":"Fish. Physiol. Biochem."},{"key":"99372_CR16","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1533\/9780857097460.3.519","volume-title":"Advances in Aquaculture Hatchery Technology","author":"NJ Duncan","year":"2013","unstructured":"Duncan, N. J. et al. Aquaculture, production of meagre (Argyrosomus regius), hatchery techniques, ongrowing and market. in Advances in Aquaculture Hatchery Technology (eds Allan, G. & Burnell, G.) 519\u2013541 (Woodhead Publishing Limited, Cambridge, UK, 2013)."},{"key":"99372_CR17","doi-asserted-by":"publisher","first-page":"506","DOI":"10.1016\/j.aquaculture.2018.06.017","volume":"495","author":"NJ Duncan","year":"2018","unstructured":"Duncan, N. J. et al. Paired spawning with male rotation of meagre Argyrosomus regius using GnRHa injections, as a method for producing multiple families for breeding selection programs. Aquaculture 495, 506\u2013512. https:\/\/doi.org\/10.1016\/j.aquaculture.2018.06.017 (2018).","journal-title":"Aquaculture"},{"key":"99372_CR18","doi-asserted-by":"publisher","first-page":"1038","DOI":"10.5424\/sjar\/2014124-6276","volume":"12","author":"H Fernandez-Palacios","year":"2014","unstructured":"Fernandez-Palacios, H. et al. Dose-dependent effect of a single GnRHa injection on the spawning of meagre (Argyrosomus regius) broodstock reared in captivity. Span. J. Agri Res. 12, 1038\u20131048. https:\/\/doi.org\/10.5424\/sjar\/2014124-6276 (2014).","journal-title":"Span. J. Agri Res."},{"key":"99372_CR19","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1016\/j.aquaculture.2013.09.008","volume":"414\u2013415","author":"CC Mylonas","year":"2013","unstructured":"Mylonas, C. C. et al. Reproduction of hatchery-produced meagre Argyrosomus regius in captivity II. Hormonal induction of spawning and monitoring of spawning kinetics, egg production and egg quality. Aquaculture 414\u2013415, 318\u2013327. https:\/\/doi.org\/10.1016\/j.aquaculture.2013.09.008 (2013).","journal-title":"Aquaculture"},{"key":"99372_CR20","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/j.aquaculture.2013.09.009","volume":"414\u2013415","author":"CC Mylonas","year":"2013","unstructured":"Mylonas, C. C., Mitrizakis, N., Papadaki, M. & Sigelaki, I. Reproduction of hatchery-produced meagre Argyrosomus regius in captivity I. Description of the annual reproductive cycle. Aquaculture 414\u2013415, 309\u2013317. https:\/\/doi.org\/10.1016\/j.aquaculture.2013.09.009 (2013).","journal-title":"Aquaculture"},{"key":"99372_CR21","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.aquaculture.2015.05.036","volume":"448","author":"CC Mylonas","year":"2015","unstructured":"Mylonas, C. C. et al. Reproduction of hatchery-produced meagre Argyrosomus regius in captivity III. Comparison between GnRHa implants and injections on spawning kinetics and egg\/larval performance parameters. Aquaculture 448, 44\u201353. https:\/\/doi.org\/10.1016\/j.aquaculture.2015.05.036 (2015).","journal-title":"Aquaculture"},{"key":"99372_CR22","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1016\/j.aquaculture.2016.07.006","volume":"464","author":"CC Mylonas","year":"2016","unstructured":"Mylonas, C. C. et al. Enhancement of oogenesis\/spermatogenesis in meagre Argyrosomus regius using a combination of temperature control and GnRHa treatments. Aquaculture 464, 323\u2013330. https:\/\/doi.org\/10.1016\/j.aquaculture.2016.07.006 (2016).","journal-title":"Aquaculture"},{"key":"99372_CR23","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/j.aquaculture.2019.05.033","volume":"509","author":"S Ramos-J\u00fadez","year":"2019","unstructured":"Ramos-J\u00fadez, S. et al. Gamete quality and management for in vitro fertilisation in meagre (Argyrosomus regius). Aquaculture 509, 227\u2013235. https:\/\/doi.org\/10.1016\/j.aquaculture.2019.05.033 (2019).","journal-title":"Aquaculture"},{"key":"99372_CR24","doi-asserted-by":"publisher","first-page":"223","DOI":"10.3390\/ani13020223","volume":"13","author":"R Zupa","year":"2023","unstructured":"Zupa, R. et al. Reproductive maturation of meagre Argyrosomus regius (Asso, 1801) reared in floating cages. Animals 13, 223. https:\/\/doi.org\/10.3390\/ani13020223 (2023).","journal-title":"Animals"},{"key":"99372_CR25","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1111\/j.1749-6632.2008.03645.x","volume":"1163","author":"M Carrillo","year":"2009","unstructured":"Carrillo, M. et al. Hormonal and environmental control of puberty in perciform fish: The case of sea bass. Ann. N Y Acad. Sci. 1163, 49\u201359. https:\/\/doi.org\/10.1111\/j.1749-6632.2008.03645.x (2009).","journal-title":"Ann. N Y Acad. Sci."},{"key":"99372_CR26","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1016\/j.ygcen.2009.05.004","volume":"165","author":"GL Taranger","year":"2010","unstructured":"Taranger, G. L. et al. Control of puberty in farmed fish. Gen. Comp. Endocrinol. 165, 483\u2013515. https:\/\/doi.org\/10.1016\/j.ygcen.2009.05.004 (2010).","journal-title":"Gen. Comp. Endocrinol."},{"key":"99372_CR27","doi-asserted-by":"publisher","first-page":"390","DOI":"10.1016\/j.ygcen.2009.02.013","volume":"165","author":"RW Schulz","year":"2010","unstructured":"Schulz, R. W. et al. Spermatogenesis in fish. Gen. Comp. Endocrinol. 165, 390\u2013411. https:\/\/doi.org\/10.1016\/j.ygcen.2009.02.013 (2010).","journal-title":"Gen. Comp. Endocrinol."},{"key":"99372_CR28","doi-asserted-by":"publisher","first-page":"1153","DOI":"10.1095\/biolreprod59.5.1153","volume":"59","author":"MCH Holland","year":"1998","unstructured":"Holland, M. C. H., Hassin, S. & Zohar, Y. Effects of long-term testosterone, gonadotropin-releasing hormone agonist, and Pimozide treatments on gonadotropin II levels and ovarian development in juvenile female striped bass (Morone saxatilis). Biol. Reprod. 59, 1153\u20131162. https:\/\/doi.org\/10.1095\/biolreprod59.5.1153 (1998).","journal-title":"Biol. Reprod."},{"key":"99372_CR29","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1023\/B:FISH.0000030465.56876.97","volume":"28","author":"U Klenke","year":"2004","unstructured":"Klenke, U. & Zohar, Y. Gonadal regulation of gonadotropin subunit expression and pituitary LH protein content in female hybrid striped bass. Fish. Physiol. Biochem. 28, 25\u201327. https:\/\/doi.org\/10.1023\/B:FISH.0000030465.56876.97 (2004).","journal-title":"Fish. Physiol. Biochem."},{"key":"99372_CR30","unstructured":"Klenke, U. & Zohar, Y. Direct pituitary regulation of brain and pituitary reproductive hormone expression by estrogen: An in vitro study. 5th Intl. Symp. Fish Endocrinol. Sept. 5\u20139, (2004)."},{"key":"99372_CR31","unstructured":"Klenke, U. & Zohar, Y. Seasonal hormonal regulation of the reproductive brain: An in vitro brain-slice study. 15th Intl. Congr. Comp. Endocrinol. May 22\u201327, (2005)."},{"key":"99372_CR32","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, C. H. Gonadotropin signaling in zebrafish ovary and testis development: Insights from gene knockout study. Mol. Endocrinol. 29, 1743. https:\/\/doi.org\/10.1210\/ME.2015-1126 (2015).","journal-title":"Mol. Endocrinol."},{"key":"99372_CR33","doi-asserted-by":"publisher","first-page":"3017","DOI":"10.1210\/en.2015-1157","volume":"156","author":"R Nobrega","year":"2015","unstructured":"Nobrega, R. et al. (ed, H.) Fsh stimulates spermatogonial proliferation and differentiation in zebrafish via Igf3. Endocrinology 156 3017\u20133084 https:\/\/doi.org\/10.1210\/en.2015-1157 (2015).","journal-title":"Endocrinology"},{"key":"99372_CR34","doi-asserted-by":"publisher","first-page":"114576","DOI":"10.1016\/j.ygcen.2024.114576","volume":"356","author":"\u00c1 Gonz\u00e1lez-Cid","year":"2024","unstructured":"Gonz\u00e1lez-Cid, \u00c1., Gim\u00e9nez, I. & Duncan, N. In vivo effect of Recombinant Fsh and Lh administered to meagre (Argyrosomus regius) at the initial stages of sex differentiation. Gen. Comp. Endocrinol. 356, 114576. https:\/\/doi.org\/10.1016\/j.ygcen.2024.114576 (2024).","journal-title":"Gen. Comp. Endocrinol."},{"key":"99372_CR35","doi-asserted-by":"publisher","first-page":"741401","DOI":"10.1016\/j.aquaculture.2024.741401","volume":"594","author":"S Lancerotto","year":"2024","unstructured":"Lancerotto, S. et al. Overcoming dysfunctional gametogenesis in hatchery-produced greater Amberjack, Seriola dumerili using recombinant gonadotropins, and spawning induction using gonadotropin releasing hormone agonist-loaded implants. Aquaculture 594, 741401. https:\/\/doi.org\/10.1016\/j.aquaculture.2024.741401 (2024).","journal-title":"Aquaculture"},{"key":"99372_CR36","doi-asserted-by":"publisher","first-page":"e0174387","DOI":"10.1371\/journal.pone.0174387","volume":"12","author":"F Chauvign\u00e9","year":"2017","unstructured":"Chauvign\u00e9, F. et al. Toward developing Recombinant gonadotropin-based hormone therapies for increasing fertility in the flatfish Senegalese sole. PLoS ONE  12, e0174387. https:\/\/doi.org\/10.1371\/journal.pone.0174387 (2017).","journal-title":"PLoS ONE"},{"key":"99372_CR37","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.cbpa.2018.06.022","volume":"225","author":"F Chauvign\u00e9","year":"2018","unstructured":"Chauvign\u00e9, F. et al. Seasonal-and dose-dependent effects of recombinant gonadotropins on sperm production and quality in the flatfish Solea senegalensis. Comp. Biochem. Physiol. Mol. Integr. Physiol. 225, 59\u201364. https:\/\/doi.org\/10.1016\/j.cbpa.2018.06.022 (2018).","journal-title":"Comp. Biochem. Physiol. Mol. Integr. Physiol."},{"key":"99372_CR38","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1016\/j.theriogenology.2017.11.002","volume":"107","author":"D Pe\u00f1aranda","year":"2018","unstructured":"Pe\u00f1aranda, D. et al. Using specific recombinant gonadotropins to induce spermatogenesis and spermiation in the European eel (Anguilla anguilla). Theriogenology 107, 6\u201320. https:\/\/doi.org\/10.1016\/j.theriogenology.2017.11.002 (2018).","journal-title":"Theriogenology"},{"key":"99372_CR39","doi-asserted-by":"publisher","first-page":"123","DOI":"10.3390\/fishes8030123","volume":"8","author":"P J\u00e9hannet","year":"2023","unstructured":"J\u00e9hannet, P. et al. Recombinant gonadotropins to induce oocyte development in vitro and in vivo in the European eel Anguilla anguilla. Fishes 8, 123. https:\/\/doi.org\/10.3390\/fishes8030123 (2023).","journal-title":"Fishes"},{"key":"99372_CR40","doi-asserted-by":"publisher","unstructured":"Ramos-J\u00fadez, S. et al. Providing recombinant gonadotropin-based therapies that induce oogenesis from previtellogenic oocytes to produce viable larvae in a teleost, the flathead grey mullet (Mugil cephalus). Aquaculture 536, 736418.  https:\/\/doi.org\/10.1016\/j.aquaculture.2021.736418 (2021).","DOI":"10.1016\/j.aquaculture.2021.736418"},{"key":"99372_CR41","doi-asserted-by":"publisher","first-page":"6563","DOI":"10.1038\/s41598-022-10371-0","volume":"12","author":"S Ramos\u2013J\u00fadez","year":"2022","unstructured":"Ramos\u2013J\u00fadez, S. et al. Recombinant Fsh and Lh therapy for spawning induction of previtellogenic and early spermatogenic arrested teleost, the Flathead grey mullet (Mugil cephalus). Sci. Rep. 12, 6563. https:\/\/doi.org\/10.1038\/s41598-022-10371-0 (2022).","journal-title":"Sci. Rep."},{"key":"99372_CR42","doi-asserted-by":"publisher","first-page":"7013","DOI":"10.1038\/s41598-023-34102-1","volume":"13","author":"R Zupa","year":"2023","unstructured":"Zupa, R. et al. Male germ cell proliferation and apoptosis in sexually immature meagre Argyrosomus regius (Asso, 1801) treated with Recombinant follicle stimulating hormone. Sci. Rep. 13, 7013. https:\/\/doi.org\/10.1038\/s41598-023-34102-1 (2023).","journal-title":"Sci. Rep."},{"key":"99372_CR43","doi-asserted-by":"publisher","first-page":"851","DOI":"10.3390\/ani10050851","volume":"10","author":"R Zupa","year":"2020","unstructured":"Zupa, R., Martino, N. A., Marzano, G., Dell\u2019Aquila, M. E. & Corriero, A. Meagre Argyrosomus regius (Asso, 1801) stem spermatogonia: histological characterization, immunostaining, in vitro proliferation, and cryopreservation. Animals 10, 851. https:\/\/doi.org\/10.3390\/ani10050851 (2020).","journal-title":"Animals"},{"key":"99372_CR44","doi-asserted-by":"publisher","first-page":"677","DOI":"10.1530\/rep.0.1220677","volume":"122","author":"KA Young","year":"2001","unstructured":"Young, K. A. & Nelson, R. J. Mediation of seasonal testicular regression by apoptosis. Reproduction 122, 677\u2013685. https:\/\/doi.org\/10.1530\/rep.0.1220677 (2001).","journal-title":"Reproduction"},{"key":"99372_CR45","unstructured":"Sokal, R. R. & Rohlf, F. J. Biometry The Principles and Practice of Statistics in Biological Research (Freeman WH and Company, 1981)."},{"key":"99372_CR46","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1023\/A:1012279814708","volume":"10","author":"CC Mylonas","year":"2001","unstructured":"Mylonas, C. C. & Zohar, Y. Use of GnRHa-delivery systems for the control of reproduction in fish. Rev. Fish. Biol. Fisher. 10, 463\u2013491. https:\/\/doi.org\/10.1023\/A:1012279814708 (2001).","journal-title":"Rev. Fish. Biol. Fisher"},{"key":"99372_CR47","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1016\/j.ygcen.2009.03.007","volume":"165","author":"CC Mylonas","year":"2010","unstructured":"Mylonas, C. C., Fostier, A. & Zanuy, S. Broodstock management and hormonal manipulations of fish reproduction. Gen. Comp. Endocrinol. 165, 516\u2013534. https:\/\/doi.org\/10.1016\/j.ygcen.2009.03.007 (2010).","journal-title":"Gen. Comp. Endocrinol."},{"key":"99372_CR48","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1016\/S0016-6480(03)00012-1","volume":"131","author":"N Kumakura","year":"2003","unstructured":"Kumakura, N., Okuzawa, K., Gen, K. & Kagawa, H. Effects of gonadotropin-releasing hormone agonist and dopamine antagonist on hypothalamus-pituitary-gonadal axis of pre-pubertal female red seabream (Pagrus major). Gen. Comp. Endocrinol. 131, 264\u2013273. https:\/\/doi.org\/10.1016\/S0016-6480(03)00012-1 (2003).","journal-title":"Gen. Comp. Endocrinol."},{"key":"99372_CR49","doi-asserted-by":"publisher","first-page":"1587","DOI":"10.1210\/en.2003-1164","volume":"145","author":"CM Allan","year":"2004","unstructured":"Allan, C. M. et al. Complete Sertoli cell proliferation induced by follicle stimulating hormone (FSH) independently of luteinizing hormone activity: Evidence from genetic models of isolated FSH action. Endocrinology 145, 1587\u20131593. https:\/\/doi.org\/10.1210\/en.2003-1164 (2004).","journal-title":"Endocrinology"},{"key":"99372_CR50","doi-asserted-by":"publisher","first-page":"771e5","DOI":"10.1016\/j.aquaculture.2006.08.039","volume":"261","author":"H Kamei","year":"2006","unstructured":"Kamei, H., Kaneko, T. & Aida, K. Vivo gonadotropic effects of recombinant Japanese eel follicle-stimulating hormone. Aquaculture 261, 771e5. https:\/\/doi.org\/10.1016\/j.aquaculture.2006.08.039 (2006).","journal-title":"Aquaculture"},{"key":"99372_CR51","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1095\/biolreprod.113.110569","volume":"90","author":"MJ Maz\u00f3n","year":"2014","unstructured":"Maz\u00f3n, M. J., G\u00f3mez, A., Yilmaz, O., Carrillo, M. & Zanuy, S. Administration of follicle-stimulating hormone in vivo triggers testicular recrudescence of juvenile European sea bass (Dicentrarchus labrax). Biol. Reprod. 90, 6. https:\/\/doi.org\/10.1095\/biolreprod.113.110569 (2014).","journal-title":"Biol. Reprod."},{"key":"99372_CR52","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/j.ygcen.2016.03.001","volume":"241","author":"PJ Sanch\u00eds-Benlloch","year":"2017","unstructured":"Sanch\u00eds-Benlloch, P. J. et al. In-vitro and in-vivo biological activity of Recombinant Yellowtail kingfish (Seriola lalandi) follicle stimulating hormone. Gen. Comp. Endocrinol. 241, 41\u201349. https:\/\/doi.org\/10.1016\/j.ygcen.2016.03.001 (2017).","journal-title":"Gen. Comp. Endocrinol."},{"key":"99372_CR53","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1002\/mrd.10267","volume":"64","author":"M Prisco","year":"2003","unstructured":"Prisco, M. et al. Apoptosis during spermatogenesis in the spotted ray Torpedo marmorata. Mol. Reprod. Dev. 64, 341\u2013348. https:\/\/doi.org\/10.1002\/mrd.10267 (2003).","journal-title":"Mol. Reprod. Dev."},{"key":"99372_CR54","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1111\/j.1095-8649.2006.01257.x","volume":"70","author":"A Corriero","year":"2007","unstructured":"Corriero, A. et al. Germ cell proliferation and apoptosis during different phases of swordfish (Xiphias gladius L.) spermatogenetic cycle. J. Fish. Biol. 70, 83\u201399. https:\/\/doi.org\/10.1111\/j.1095-8649.2006.01257.x (2007).","journal-title":"J. Fish. Biol."},{"key":"99372_CR55","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1016\/j.anireprosci.2009.02.013","volume":"116","author":"A Corriero","year":"2009","unstructured":"Corriero, A. et al. Proliferation and apoptosis of male germ cells in captive Atlantic Bluefin tuna (Thunnus Thynnus L.) treated with gonadotropin-releasing hormone agonist (GnRHa). Anim. Reprod. Sci. 116, 346\u2013357. https:\/\/doi.org\/10.1016\/j.anireprosci.2009.02.013 (2009).","journal-title":"Anim. Reprod. Sci."},{"key":"99372_CR56","doi-asserted-by":"publisher","first-page":"114447","DOI":"10.1016\/j.ygcen.2024.114447","volume":"348","author":"G Ventriglia","year":"2024","unstructured":"Ventriglia, G. et al. Effects of different hormonal treatments on spermatogenesis advancement in hatchery-produced greater Amberjack Seriola dumerili (Risso 1810). Gen. Comp. Endocrinol. 348, 114447. https:\/\/doi.org\/10.1016\/j.ygcen.2024.114447 (2024).","journal-title":"Gen. Comp. Endocrinol."},{"key":"99372_CR57","doi-asserted-by":"publisher","first-page":"461","DOI":"10.1071\/rd06079","volume":"19","author":"LK Jenkins","year":"2007","unstructured":"Jenkins, L. K., Ross, W. L. & Young, K. A. Increases in apoptosis and declines in Bcl-XL protein characterise testicular regression in American crows (Corvus brachyrhynchos). Reprod. Fertil. Dev. 19, 461\u2013469. https:\/\/doi.org\/10.1071\/rd06079 (2007).","journal-title":"Reprod. Fertil. Dev."},{"key":"99372_CR58","doi-asserted-by":"publisher","first-page":"e39920","DOI":"10.1371\/journal.pone.00399207","volume":"7","author":"DH Wang","year":"2012","unstructured":"Wang, D. H. et al. The apoptotic function analysis of p53, Apaf1, Caspase3 and Caspase7 during the spermatogenesis of the Chinese fire-bellied Newt Cynops orientalis. PLoS ONE. 7, e39920. https:\/\/doi.org\/10.1371\/journal.pone.00399207 (2012).","journal-title":"PLoS ONE"},{"key":"99372_CR59","doi-asserted-by":"publisher","first-page":"412","DOI":"10.1002\/jmor.20507","volume":"277","author":"MF Scaia","year":"2016","unstructured":"Scaia, M. F., Czuchlej, S. C., Cervino, N. & Ceballos, N. R. Apoptosis, proliferation and presence of estradiol receptors in the testes and bidder\u2019s organ of the Toad Rhinella arenarum (Amphibia, Anura). J. Morphol. 277, 412\u2013423. https:\/\/doi.org\/10.1002\/jmor.20507 (2016).","journal-title":"J. Morphol."},{"key":"99372_CR60","doi-asserted-by":"publisher","first-page":"188","DOI":"10.3389\/fphys.2017.00188","volume":"8","author":"T Liu","year":"2017","unstructured":"Liu, T. et al. Molecular and cellular mechanisms of apoptosis during dissociated spermatogenesis. Front. Physiol. 8, 188. https:\/\/doi.org\/10.3389\/fphys.2017.00188 (2017).","journal-title":"Front. Physiol."},{"key":"99372_CR61","doi-asserted-by":"publisher","first-page":"106307","DOI":"10.1016\/j.anireprosci.2020.106307","volume":"214","author":"H Chen","year":"2020","unstructured":"Chen, H. et al. Characteristics of seasonal spermatogenesis in the soft-shelled turtle. Anim. Reprod. Sci. 214, 106307. https:\/\/doi.org\/10.1016\/j.anireprosci.2020.106307 (2020).","journal-title":"Anim. Reprod. Sci."},{"key":"99372_CR62","doi-asserted-by":"publisher","first-page":"447","DOI":"10.3390\/vetsci9080447","volume":"9","author":"L Valentini","year":"2022","unstructured":"Valentini, L., Zupa, R., Pousis, C., Cuko, R. & Corriero, A. Proliferation and apoptosis of cat (Felis Catus) male germ cells during breeding and non-breeding seasons. Vet. Sci. 9, 447. https:\/\/doi.org\/10.3390\/vetsci9080447 (2022).","journal-title":"Vet. Sci."},{"key":"99372_CR63","doi-asserted-by":"publisher","first-page":"320","DOI":"10.1016\/0093-691X(95)00187-D","volume":"44","author":"S Blottner","year":"1995","unstructured":"Blottner, S., Hingst, O. & Meyer, H. H. D. Inverse relationship between testicular proliferation and apoptosis in mammalian seasonal breeders. Theriogenology 44, 320\u2013328. https:\/\/doi.org\/10.1016\/0093-691X(95)00187-D (1995).","journal-title":"Theriogenology"},{"key":"99372_CR64","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1095\/biolreprod61.1.70","volume":"61","author":"S Nandi","year":"1999","unstructured":"Nandi, S., Banerjee, P. P. & Zirkin, B. R. Germ cell apoptosis in the testes of Sprague Dawley rats following testosterone withdrawal by ethane 1,2-dimethanesulfonate administration: Relationship to fas? Biol. Reprod. 61, 70\u201375. https:\/\/doi.org\/10.1095\/biolreprod61.1.70 (1999).","journal-title":"Biol. Reprod."},{"key":"99372_CR65","doi-asserted-by":"publisher","first-page":"461","DOI":"10.1095\/biolreprod60.2.461","volume":"60","author":"I Woolveridge","year":"1999","unstructured":"Woolveridge, I. et al. Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: Changes in apoptosis-related genes. Biol. Reprod. 60, 461\u2013470. https:\/\/doi.org\/10.1095\/biolreprod60.2.461 (1999).","journal-title":"Biol. Reprod."},{"key":"99372_CR66","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1046\/j.1439-0264.2003.00437.x","volume":"32","author":"M \u0160trbenc","year":"2003","unstructured":"\u0160trbenc, M., Fazarinc, G., Bavdek, V. & Poga\u010dnik, A. Apoptosis and proliferation during seasonal testis regression in the brown hare (Lupus Europaeus L). Anat. Histol. Embryol. 32, 48\u201353. https:\/\/doi.org\/10.1046\/j.1439-0264.2003.00437.x (2003).","journal-title":"Anat. Histol. Embryol."},{"key":"99372_CR67","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1095\/biolreprod.109.076299","volume":"81","author":"MC Leal","year":"2009","unstructured":"Leal, M. C. et al. Histological and Stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol. Reprod. 81, 177\u2013187. https:\/\/doi.org\/10.1095\/biolreprod.109.076299 (2009).","journal-title":"Biol. Reprod."},{"key":"99372_CR68","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1051\/rnd:19690208","volume":"9","author":"R Billard","year":"1969","unstructured":"Billard, R. La spermatogen\u00e8se de Poecilia reticulata. I\u2013estimation du Nombre de g\u00e9n\u00e9rations goniales et rendement de La spermatogen\u00e8se. Ann. Biol. Anim. Biochim. Biophys. 9, 251\u2013271. https:\/\/doi.org\/10.1051\/rnd:19690208 (1969).","journal-title":"Ann. Biol. Anim. Biochim. Biophys."},{"key":"99372_CR69","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1095\/biolreprod.107.063669","volume":"78","author":"FFL Almeida","year":"2008","unstructured":"Almeida, F. F. L., Kristoffersen, C., Taranger, G. L. & Schulz, R. W. Spermatogenesis in Atlantic Cod (Gadus morhua): A novel model of cystic germ cell development. Biol. Reprod. 78, 27\u201334. https:\/\/doi.org\/10.1095\/biolreprod.107.063669 (2008).","journal-title":"Biol. Reprod."},{"key":"99372_CR70","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1023\/B:FISH.0000030523.16010.62","volume":"28","author":"DAR Vilela","year":"2003","unstructured":"Vilela, D. A. R., Silva, S. G. B., Peixoto, M. T. D., Godinho, H. P. & Fran\u00e7a, L. R. Spermatogenesis in teleost: Insights from the nile tilapia (Oreochromis niloticus) model. Fish. Physiol. Biochem. 28, 187\u2013190. https:\/\/doi.org\/10.1023\/B:FISH.0000030523.16010.62 (2003).","journal-title":"Fish. Physiol. Biochem."},{"key":"99372_CR71","doi-asserted-by":"publisher","first-page":"657192","DOI":"10.3389\/fcell.2021.657192","volume":"9","author":"KO Skaftnesmo","year":"2021","unstructured":"Skaftnesmo, K. O. et al. Loss of stra8 increases germ cell apoptosis but is still compatible with sperm production in Atlantic salmon (Salmo salar). Front. Cell. Dev. Biol. 9, 657192. https:\/\/doi.org\/10.3389\/fcell.2021.657192 (2021).","journal-title":"Front. Cell. Dev. Biol."},{"key":"99372_CR72","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1038\/s42003-021-01708-y","volume":"4","author":"D Crespo","year":"2021","unstructured":"Crespo, D. et al. Insulin-like 3 affects zebrafish spermatogenic cells directly and via sertoli cells. Commun. Biol. 4, 204. https:\/\/doi.org\/10.1038\/s42003-021-01708-y (2021).","journal-title":"Commun. Biol."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-99372-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-99372-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-99372-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,4,29]],"date-time":"2025-04-29T16:13:24Z","timestamp":1745943204000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-99372-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,4,29]]},"references-count":72,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["99372"],"URL":"https:\/\/doi.org\/10.1038\/s41598-025-99372-3","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,4,29]]},"assertion":[{"value":"25 July 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 April 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 April 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Gianluca Ventriglia, Neil Duncan, Constantinos C. Mylonas, Chrysovalentinos Pousis, Aldo Corriero and Rosa Zupa declare no competing interest. Ignacio Gimen\u00e9z is associated with the biotech company Rara Avis Biotech, S. L., which produced the recombinant gonadotropin employed in this study.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"15113"}}