{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,6]],"date-time":"2026-06-06T13:56:17Z","timestamp":1780754177801,"version":"3.54.1"},"reference-count":71,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2025,9,11]],"date-time":"2025-09-11T00:00:00Z","timestamp":1757548800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"project NewTechAqua","award":["GA 862658"],"award-info":[{"award-number":["GA 862658"]}]},{"name":"POR PUGLIA FESR-FSE 2014\/2020\u2014Asse X-Azione 10.4\u2014Research for Innovation\u2014REFIN","award":["GA 862658"],"award-info":[{"award-number":["GA 862658"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>To overcome reproductive dysfunctions, recombinant gonadotropin hormones have been synthesised in different fish species. We were interested in gaining further insight into the effects of recombinant follicle-stimulating hormone (rFsh) in meagre Argyrosomus regius spermatogenesis and in improving the existing knowledge on the role of testicular apoptosis. Germ cell composition and testicular apoptosis were compared in pre-pubertal fish treated with rFsh (PreP-Fsh) and controls (PreP-C), and adult meagre with testes in the proliferative (Adult-Pro) and meiotic (Adult-Meio) spermatogenesis phases. A lower density of committed spermatogonia was observed in PreP-Fsh compared with PreP-C and in Adult-Meio compared with Adult-Pro. In pre-pubertal fish and in Adult-Pro, apoptosis affected mainly individual germ cells and Sertoli cells. In Adult-Meio, a high number of cysts containing apoptotic germ cells was observed, and apoptosis often involved entire clones of germ cells. rFsh reduced testicular apoptosis in pre-pubertal fish, whereas the advancement of spermatogenesis in adults was associated with an increased density of apoptotic cells. The present study corroborated previous observations on the effects of rFsh on spermatogenesis in pre-pubertal meagre and provided further insights on the changing role of apoptosis in the pre-pubertal phase versus different phases of spermatogenesis.<\/jats:p>","DOI":"10.3390\/ani15182668","type":"journal-article","created":{"date-parts":[[2025,9,12]],"date-time":"2025-09-12T07:52:28Z","timestamp":1757663548000},"page":"2668","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Histological Insights into Testicular Apoptosis Associated with Spermatogenesis in Pre-Pubertal and Adult Meagre (Argyrosomus regius)"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6267-7592","authenticated-orcid":false,"given":"Gianluca","family":"Ventriglia","sequence":"first","affiliation":[{"name":"Department of Veterinary Medicine, University of Bari Aldo Moro, 70010 Valenzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neil","family":"Duncan","sequence":"additional","affiliation":[{"name":"Institute of Agrifood Research and Technology, 43540 La R\u00e0pita, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ignacio","family":"Gim\u00e9nez","sequence":"additional","affiliation":[{"name":"Rara Avis Biotec, S. L., 46002 Valencia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1805-4392","authenticated-orcid":false,"given":"Constantinos C.","family":"Mylonas","sequence":"additional","affiliation":[{"name":"Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Center for Marine Research, 71003 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chrysovalentinos","family":"Pousis","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, University of Bari Aldo Moro, 70010 Valenzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caterina","family":"Varvara","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, University of Bari Aldo Moro, 70010 Valenzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luisa","family":"Valentini","sequence":"additional","affiliation":[{"name":"DiMePRe-J, University of Bari Aldo Moro, 70010 Valenzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Letizia","family":"Passantino","sequence":"additional","affiliation":[{"name":"DiMePRe-J, University of Bari Aldo Moro, 70010 Valenzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7068-9438","authenticated-orcid":false,"given":"Aldo","family":"Corriero","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, University of Bari Aldo Moro, 70010 Valenzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5516-1299","authenticated-orcid":false,"given":"Rosa","family":"Zupa","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, University of Bari Aldo Moro, 70010 Valenzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,9,11]]},"reference":[{"key":"ref_1","first-page":"813","article-title":"Sciaenidae","volume":"Volume 2","author":"Quero","year":"1990","journal-title":"Check-List of the Fishes of the Eastern Tropical Atlantic (CLOFETA)"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Allan, G., and Burnell, G. (2013). Aquaculture production of meagre (Argyrosomus regius): Hatchery Techniques, Ongrowing and Market. Advances in Aquaculture Hatchery Technology, Woodhead Publishing Limited.","DOI":"10.1533\/9780857097460"},{"key":"ref_3","unstructured":"(2025, January 20). Global Aquaculture Production Quantity (1950\u20132020). Available online: https:\/\/www.fao.org\/fishery\/statistics-query\/en\/aquaculture\/aquaculture_quantity."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.aquaculture.2013.09.009","article-title":"Reproduction of hatchery-produced meagre Argyrosomus regius in captivity I. Description of the annual reproductive cycle","volume":"414\u2013415","author":"Mylonas","year":"2013","journal-title":"Aquaculture"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1038","DOI":"10.5424\/sjar\/2014124-6276","article-title":"Dose-dependent effect of a single GnRHa injection on the spawning of meagre (Argyrosomus regius) broodstock reared in captivity","volume":"12","author":"Schuchardt","year":"2014","journal-title":"Span. J. Agri. Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1273","DOI":"10.1007\/s10695-012-9615-3","article-title":"Reproductive development, GnRHa-induced spawning and egg quality of wild meagre (Argyrosomus regius) acclimatised to captivity","volume":"38","author":"Duncan","year":"2012","journal-title":"Fish Physiol. Biochem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.aquaculture.2016.07.006","article-title":"Enhancement of oogenesis\/spermatogenesis in meagre Argyrosomus regius using a combination of temperature control and GnRHa treatments","volume":"464","author":"Mylonas","year":"2016","journal-title":"Aquaculture"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.fishres.2011.01.031","article-title":"Life-history of the meagre Argyrosomus regius in the Gulf of Cadiz (SW Iberian Peninsula)","volume":"109","author":"Naranjo","year":"2011","journal-title":"Fish. Res."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Zupa, R., Duncan, N., Gim\u00e9nez, I., Mylonas, C.C., Pousis, C., Passantino, L., Cuko, R., and Corriero, A. (2023). Male germ cell proliferation and apoptosis in sexually immature meagre Argyrosomus regius (Asso, 1801) treated with recombinant follicle stimulating hormone. Sci. Rep., 13.","DOI":"10.1038\/s41598-023-34102-1"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Ventriglia, G., Duncan, N., Gim\u00e9nez, I., Mylonas, C.C., Pousis, C., Corriero, A., and Zupa, R. (2025). Spermatogenesis advancement in pre-pubertal meagre Argyrosomus regius treated with recombinant gonadotropins. Sci. Rep., 15.","DOI":"10.1038\/s41598-025-99372-3"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Xie, X., N\u00f3brega, R., and P\u0161eni\u010dka, M. (2020). Spermatogonial Stem Cells in Fish: Characterization, Isolation, Enrichment, and Recent Advances of In Vitro Culture Systems. Biomolecules, 10.","DOI":"10.3390\/biom10040644"},{"key":"ref_12","first-page":"13","article-title":"Spontaneous germ cell death in the testis of the adult rat takes the form of apoptosis: Re-evaluation of cell types that exhibit the ability to die during spermatogenesis","volume":"29","year":"1996","journal-title":"Cell Proliferat."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1530\/rep.0.1220677","article-title":"Mediation of seasonal testicular regression by apoptosis","volume":"122","author":"Young","year":"2001","journal-title":"Reproduction"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/S1096-7192(02)00142-7","article-title":"Transgenic mouse models and germ cell transplantation: Two excellent tools for the analysis of genes regulating male fertility","volume":"77","author":"Wistuba","year":"2002","journal-title":"Mol. Genet. Metab."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.ygcen.2009.02.013","article-title":"Spermatogenesis in fish","volume":"165","author":"Schulz","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1111\/j.1439-0426.2012.02045.x","article-title":"Comparative analysis of male germ cell proliferation in wild and captive Atlantic bluefin tuna Thunnus thynnus","volume":"29","author":"Zupa","year":"2013","journal-title":"J. Appl. Ichthyol."},{"key":"ref_17","first-page":"4085","article-title":"Rearing in captivity affects spermatogenesis and sperm quality in greater amberjack Seriola dumerili (Risso, 1810)","volume":"95","author":"Zupa","year":"2017","journal-title":"J. Anim. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"114447","DOI":"10.1016\/j.ygcen.2024.114447","article-title":"Effects of different hormonal treatments on spermatogenesis advancement in hatchery-produced greater amberjack Seriola dumerili (Risso 1810)","volume":"348","author":"Ventriglia","year":"2024","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/S0044-8486(01)00584-1","article-title":"Endocrine manipulations of spawning in cultured fish: From hormones to genes","volume":"197","author":"Zohar","year":"2001","journal-title":"Aquaculture"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1095\/biolreprod.108.071340","article-title":"Photoperiod-Modulated Testis Maturation in Atlantic Cod (Gadus morhua, L.)","volume":"80","author":"Almeida","year":"2009","journal-title":"Biol. Reprod."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Zupa, R., Hala, E., Ventriglia, G., Pousis, C., Passantino, L., Quaranta, A., Corriero, A., and De Virgilio, C. (2023). Reproductive maturation of meagre Argyrosomus regius (Asso, 1801) reared in floating cages. Animals, 13.","DOI":"10.1038\/s41598-023-34102-1"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.ejar.2012.12.002","article-title":"Reproductive biology of Argyrosomus regius (Asso, 1801) inhabiting the south eastern Mediterranean Sea, Egypt","volume":"38","author":"Assem","year":"2012","journal-title":"Egypt. J. Aquat. Res."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Zupa, R., Martino, N.A., Marzano, G., Dell\u2019Aquila, M.E., and Corriero, A. (2020). Meagre Argyrosomus regius (Asso, 1801) stem spermatogonia: Histological characterization, immunostaining, in vitro proliferation, and cryopreservation. Animals, 10.","DOI":"10.3390\/ani10050851"},{"key":"ref_24","unstructured":"Sokal, R.R., and Rohlf, F.J. (1981). Biometry: The Principles and Practice of Statistics in Biological Research, Freeman WH and Company. [3rd ed.]."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1023\/A:1023303427191","article-title":"Spermatogenesis and its endocrine regulation","volume":"26","author":"Schulz","year":"2002","journal-title":"Fish Physiol. Biochem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1051\/rnd:19690208","article-title":"La spermatogen\u00e8se de Poecilia reticulata I. Estimation du nombre de generations goniales et rendement de la spermatog\u00e8nese","volume":"9","author":"Billard","year":"1969","journal-title":"Ann. Biol. Biochem. Biophys."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1002\/mrd.10267","article-title":"Apoptosis during spermatogenesis in the spotted ray Torpedo marmorata","volume":"64","author":"Prisco","year":"2003","journal-title":"Mol. Reprod. Dev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1095\/biolreprod.104.036103","article-title":"An overview of cell renewal in the testis throughout the reproductive cycle of a seasonal breeding teleost, the gilthead seabream (Sparus aurata L.)","volume":"72","author":"Mulero","year":"2005","journal-title":"Biol. Reprod."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1095\/biolreprod.105.039891","article-title":"Sertoli cell proliferation in the adult testis-evidence from two fish species belonging to different orders","volume":"73","author":"Schulz","year":"2005","journal-title":"Biol. Reprod."},{"key":"ref_30","unstructured":"N\u00f3brega, R.H. (2006). Altera\u00e7\u00f5es do Epit\u00e9lio Germinativo Masculino, C\u00e9lulas End\u00f3crinas Testiculares e C\u00e9lulas Gonadotr\u00f3picas Durante o Ciclo Reprodutivo de Serrasalmus spilopleura (Kner, 1859) e Pimelodus maculatus (Lac\u00e9p\u00e8de, 1803). [Master\u2019s Thesis, Universidade Estadual de Campinas]."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1007\/s10695-008-9252-z","article-title":"An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish","volume":"35","author":"Batlouni","year":"2009","journal-title":"Fish Physiol. Biochem."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1095\/biolreprod.107.063669","article-title":"Spermatogenesis in Atlantic cod (Gadus morhua): A novel model of cystic germ cell development","volume":"78","author":"Almeida","year":"2008","journal-title":"Biol. Reprod."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"101450","DOI":"10.1016\/j.tice.2020.101450","article-title":"Apoptosis of germ cells in the normal testis of the Japanese quail (Coturnix coturnix japonica)","volume":"67","author":"Zakariah","year":"2020","journal-title":"Tissue Cell"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1046\/j.1365-2605.1998.00133.x","article-title":"A matter of death and life: The significance of germ cell death during spermatogenesis","volume":"21","year":"1998","journal-title":"Int. J. Androl."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1530\/rep.0.1210347","article-title":"Proliferation and differentiation of spermatogonial stem cells","volume":"121","year":"2001","journal-title":"Reproduction"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/j.theriogenology.2003.10.022","article-title":"Germ cell apoptosis in the testes of normal stallions","volume":"62","author":"Heninger","year":"2004","journal-title":"Theriogenology"},{"key":"ref_37","first-page":"643","article-title":"Hormonal control of apoptotic cell death in the testis: Gonadotropins and androgens as testicular cell survival factors","volume":"7","author":"Tapanainen","year":"1993","journal-title":"Mol. Endocrinol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.1095\/biolreprod55.6.1368","article-title":"In situ demonstration of germinal cell apoptosis during diethylstilbestrol-induced testis regression in adult male Syrian hamsters","volume":"55","author":"Nonclercq","year":"1996","journal-title":"Biol. Reprod."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1095\/biolreprod60.2.461","article-title":"Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: Changes in apoptosis-related genes","volume":"60","author":"Woolveridge","year":"1999","journal-title":"Biol. Reprod."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1177\/074873001129002079","article-title":"Photo-periodic control of seasonality in birds","volume":"16","author":"Dawson","year":"2001","journal-title":"J. Biol. Rhythms."},{"key":"ref_41","first-page":"355","article-title":"Photoperiodic control of the annual cycle in birds and comparison with mammals","volume":"90","author":"Dawson","year":"2002","journal-title":"Ardea"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1095\/biolreprod.107.062299","article-title":"Follicle stimulating hormone induces spermatogenesis mediated by androgen production in Japanese eel, Anguilla japonica","volume":"77","author":"Ohta","year":"2007","journal-title":"Biol. Reprod."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1677\/JOE-07-0171","article-title":"Production of recombinant channel catfish (Ictalurus punctatus) FSH and LH in S2 Drosophila cell line and an indication of their different actions","volume":"194","author":"Zmora","year":"2007","journal-title":"J. Endocrinol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1095\/biolreprod.107.065912","article-title":"Follicle-stimulating hormone affects spermatogonial survival by regulating the intrinsic apoptotic pathway in adult rats","volume":"78","author":"Ruwanpura","year":"2008","journal-title":"Biol. Reprod."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1016\/j.anireprosci.2009.02.013","article-title":"Proliferation and apoptosis of male germ cells in captive Atlantic bluefin tuna (Thunnus thynnus L.) treated with gonadotropin-releasing hormone agonist (GnRHa)","volume":"116","author":"Corriero","year":"2009","journal-title":"Anim. Reprod. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1016\/0093-691X(95)00187-D","article-title":"Inverse relationship between testicular proliferation and apoptosis in mammalian seasonal breeders","volume":"44","author":"Blottner","year":"1995","journal-title":"Theriogenology"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1046\/j.1439-0264.2003.00437.x","article-title":"Apoptosis and proliferation during seasonal testis regression in the brown hare (Lupus europaeus L.)","volume":"32","author":"Fazarinc","year":"2003","journal-title":"Anat. Histol Embryol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Valentini, L., Zupa, R., Pousis, C., Cuko, R., and Corriero, A. (2022). Proliferation and apoptosis of cat (Felis catus) male germ cells during breeding and non-breeding seasons. Vet. Sci., 9.","DOI":"10.3390\/vetsci9080447"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1071\/RD06079","article-title":"Increases in apoptosis and declines in Bcl-XL protein characterise testicular regression in American crows (Corvus brachyrhynchos)","volume":"19","author":"Jenkin","year":"2007","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1854","DOI":"10.1016\/j.theriogenology.2012.01.002","article-title":"Apoptosis-mediated seasonal testicular regression in the Japanese Jungle crow (Corvus macrorhynchos)","volume":"77","author":"Tsukahara","year":"2012","journal-title":"Theriogenology"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"106307","DOI":"10.1016\/j.anireprosci.2020.106307","article-title":"Characteristics of seasonal spermatogenesis in the soft-shelled Turtle","volume":"214","author":"Chen","year":"2020","journal-title":"Anim. Reprod. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1111\/j.1469-7580.2006.00582.x","article-title":"Apoptosis during the seasonal spermatogenic cycle of Rana catesbeiana","volume":"209","author":"Cerri","year":"2006","journal-title":"J. Anat."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1002\/jmor.20507","article-title":"Apoptosis, Proliferation and Presence of Estradiol Receptors in the Testes and Bidder\u2019s Organ of the Toad Rhinella Arenarum (Amphibia, Anura)","volume":"277","author":"Scaia","year":"2016","journal-title":"J. Morphol."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Zirkin, B.R. (1998). Hormonal Regulation of Germ Cell Apoptosis. Germ Cell Development, Division, Disruption and Death, Springer.","DOI":"10.1007\/978-1-4612-2206-4"},{"key":"ref_55","unstructured":"Norris, D.O., and Lopez, K.H. (2011). Avian Testicular Structure, Function, and Regulation. Hormones and Reproduction of Vertebrates, Academic Press."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"250","DOI":"10.4161\/spmg.1.3.18092","article-title":"Reptilian spermatogenesis: A histological and ultrastructural perspective","volume":"1","author":"Gribbins","year":"2011","journal-title":"Spermatogenesis"},{"key":"ref_57","first-page":"114e122","article-title":"Developmental changes in the histological structure of the testes, and testosterone profiles in male guinea fowls (Numida meleagris)","volume":"101","author":"Obese","year":"2017","journal-title":"Theriogenology"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Beltr\u00e1n-Frutos, E., Seco-Rovira, V., Mart\u00ednez-Hern\u00e1ndez, J., Ferrer, C., Serrano-S\u00e1nchez, M.I., and Pastor, L.M. (2022). Cellular Modifications in Spermatogenesis during Seasonal Testicular Regression: An Update Review in Mammals. Animals, 12.","DOI":"10.3390\/ani12131605"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1023\/B:FISH.0000030523.16010.62","article-title":"Spermatogenesis in teleost: Insights from the Nile tilapia (Oreochromis niloticus) model","volume":"28","author":"Vilela","year":"2003","journal-title":"Fish Physiol. Biochem."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1007\/s00435-017-0362-y","article-title":"The structure of spermatogenic cysts and number of Sertoli cells in the testes of Bombina bombina and Bombina variegata (Bombinatoridae, Anura, Amphibia)","volume":"136","author":"Piprek","year":"2017","journal-title":"Zoomorphology"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Roco, \u00c1.S., Ruiz-Garc\u00eda, A., and Bullejos, M. (2021). Testis Development and Differentiation in Amphibians. Genes, 12.","DOI":"10.3390\/genes12040578"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1111\/j.1095-8649.2006.01257.x","article-title":"Germ cell proliferation and apoptosis during different phases of swordfish (Xiphias gladius L.) spermatogenetic cycle","volume":"70","author":"Corriero","year":"2007","journal-title":"J. Fish Biol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1002\/jemt.22173","article-title":"Role of HSP70 in the regulation of the testicular apoptosis in a seasonal breeding teleost Prochilodus argenteus from the S\u00e3o Francisco River, Brazil","volume":"76","author":"Domingos","year":"2013","journal-title":"Microsc. Res. Tech."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1016\/j.tice.2017.09.003","article-title":"Germ cell proliferation and apoptosis during testicular regression in a seasonal breeding fish kept in captivity","volume":"49","author":"Ribeiro","year":"2017","journal-title":"Tissue Cell"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1665","DOI":"10.1007\/s10695-013-9818-2","article-title":"Analysis of germ cell proliferation, apoptosis, and androgenesis in the Lake Van fish (Chalcalburnus tarichi) during testicular development","volume":"39","author":"Kaptaner","year":"2013","journal-title":"Fish Physiol. Biochem."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1071\/RD20128","article-title":"Insulin-like growth factors 1 and 2 are associated with testicular germ cell proliferation and apoptosis during fish reproduction","volume":"32","author":"Moreira","year":"2020","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Crespo, D., Assis, L.H.C., Zhang, Y.T., Safian, D., Furmanek, T., Skaftnesmo, K.O., Norberg, B., Ge, W., Choi, Y.-C., and den Broeder, M.J. (2021). Insulin-like 3 affects zebrafish spermatogenic cells directly and via Sertoli cells. Commun. Biol., 4.","DOI":"10.1038\/s42003-021-01708-y"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"dev178665","DOI":"10.1242\/dev.178665","article-title":"Endocrine and local signaling interact to regulate spermatogenesis in zebrafish: Follicle-stimulating hormone, retinoic acid and androgens","volume":"146","author":"Crespo","year":"2019","journal-title":"Development"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1007\/BF00354791","article-title":"Resorption of unemitted gametes in Lithognathus mormyrus (Sparidae, Teleostei): A possible synergic action of somatic and immune cells","volume":"276","author":"Besseau","year":"1994","journal-title":"Cell. Tissue Res."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1095\/biolreprod.106.056036","article-title":"17Beta-Estradiol Triggers Postspawning in Spermatogenically Active Gilthead Seabream (Sparus aurata L.) Males","volume":"76","author":"Liarte","year":"2007","journal-title":"Biol. Reprod."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1038\/sj.cdd.4400634","article-title":"Changes in intercellular junctions during apoptosis precede nuclear condensation or phosphatidylserine exposure on the cell surface","volume":"7","author":"Corfe","year":"2000","journal-title":"Cell Death Differ."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/15\/18\/2668\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:44:15Z","timestamp":1760035455000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/15\/18\/2668"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,9,11]]},"references-count":71,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2025,9]]}},"alternative-id":["ani15182668"],"URL":"https:\/\/doi.org\/10.3390\/ani15182668","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,9,11]]}}}