{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:38:50Z","timestamp":1760150330890,"version":"build-2065373602"},"reference-count":44,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2023,11,16]],"date-time":"2023-11-16T00:00:00Z","timestamp":1700092800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Shandong Province Agricultural Major Application Technology Innovation Project","award":["SD2019YY003","AB22013011","26660173"],"award-info":[{"award-number":["SD2019YY003","AB22013011","26660173"]}]},{"name":"Guangxi Fangchenggang Key Research and Development Plan","award":["SD2019YY003","AB22013011","26660173"],"award-info":[{"award-number":["SD2019YY003","AB22013011","26660173"]}]},{"name":"Ministry of Education, Science, Sports and Culture Grant-in-Aid for Scientific Research","award":["SD2019YY003","AB22013011","26660173"],"award-info":[{"award-number":["SD2019YY003","AB22013011","26660173"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>(1) Fsh\u03b2 and Lh\u03b2 showed stronger signals and higher transcript levels from 590 to 1050 dph than at earlier stages, implying their active involvement during primary oocyte development. (2) Fsh\u03b2 and Lh\u03b2 at lower levels were detected during the phases of ovarian differentiation and oogonial proliferation. (3) E2 concentrations increased significantly at 174, 333, and 1435 dph, while T concentrations exhibited significant increases at 174 and 333 dph. These findings suggest potential correlations between serum E2 concentrations and the phases of oogonial proliferation and pre-vitellogenesis.<\/jats:p>","DOI":"10.3390\/cells12222634","type":"journal-article","created":{"date-parts":[[2023,11,16]],"date-time":"2023-11-16T01:56:29Z","timestamp":1700099789000},"page":"2634","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Chronological Changes in Gonadotropin-Releasing Hormone 1, Gonadotropins, and Sex Steroid Hormones along the Brain\u2013Pituitary\u2013Gonadal Axis during Gonadal Sex Differentiation and Development in the Longtooth Grouper, Epinephelus bruneus"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4820-9108","authenticated-orcid":false,"given":"Wengang","family":"Xu","sequence":"first","affiliation":[{"name":"School of Ocean, Yantai University, Yantai 264005, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hisashi","family":"Chuda","sequence":"additional","affiliation":[{"name":"Aquaculture Research Institute, Kindai University, Wakayama 649-2211, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kiyoshi","family":"Soyano","sequence":"additional","affiliation":[{"name":"Institute for East China Sea Research, Organization for Marine Science and Technology, Nagasaki University, Nagasaki 851-2213, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jun","family":"Zeng","sequence":"additional","affiliation":[{"name":"Guangxi Academy of Sciences, Nanning 530007, China"},{"name":"Institute of Beibu Gulf Marine Industry, Fangchenggang 538000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Weiping","family":"Mei","sequence":"additional","affiliation":[{"name":"Guangxi Academy of Sciences, Nanning 530007, China"},{"name":"Institute of Beibu Gulf Marine Industry, Fangchenggang 538000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6994-9586","authenticated-orcid":false,"given":"Huafeng","family":"Zou","sequence":"additional","affiliation":[{"name":"Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai 201306, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,11,16]]},"reference":[{"key":"ref_1","unstructured":"Lovatelli, A., and Holthus, P.F. (2008). Capture-Based Aquaculture: Global Overview, Food and Agriculture Organization of the United Nations. Available online: https:\/\/hdl.handle.net\/20.500.12348\/1540."},{"key":"ref_2","unstructured":"Soyano, K., Teruya, K., and Chuda, H. (2015). Frontiers of Fisheries Science in Groupers, Kouseisha. (In Japanese)."},{"key":"ref_3","unstructured":"Soyano, K., Teruya, K., and Chuda, H. (2015). Frontiers of Fisheries Science in Groupers, Kouseisha. (In Japanese)."},{"key":"ref_4","unstructured":"Baldisserotto, B., Urbinati, E.C., and Cyrino, J.E.P. (2020). Biology and Physiology of Freshwater Neotropical Fish, Academic Press."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Wang, H.P., Piferrer, F., Chen, S.L., and Shen, Z.G. (2018). Sex Control in Aquaculture, John Wiley & Sons.","DOI":"10.1002\/9781119127291"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1697","DOI":"10.1007\/s10695-019-00656-z","article-title":"Molecular cloning, characterization, and mRNA expression of gonadotropins during larval development in turbot (Scophthalmus maximus)","volume":"45","author":"Gao","year":"2019","journal-title":"Fish Physiol. Biochem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1016\/j.ygcen.2009.04.017","article-title":"Neuroendocrinology of reproduction in teleost fish","volume":"165","author":"Zohar","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1006\/gcen.2001.7687","article-title":"Immunocytochemical identification of GtH1 and GtH2 cells during the temperature-sensitive period for sex differentiation in pejerrey, Odontesthes bonariensis","volume":"124","author":"Miranda","year":"2001","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"367","DOI":"10.12717\/DR.2016.20.4.367","article-title":"Gene expression of aromatases, steroid receptor, GnRH and GTHs in the brain during the formation of ovarian cavity in red spotted grouper, Epinephelus akaara","volume":"20","author":"Kim","year":"2016","journal-title":"Dev. Reprod."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"5210","DOI":"10.1210\/en.2004-0558","article-title":"Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata)","volume":"145","author":"Wong","year":"2004","journal-title":"Endocrinology"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Wu, Y., He, Z., Zhang, L., Jiang, H., and Zhang, W. (2012). Ontogeny of immunoreactive Lh and Fsh cells in relation to early ovarian differentiation and development in protogynous hermaphroditic ricefield eel Monopterus albus. Biol. Reprod., 86.","DOI":"10.1095\/biolreprod.111.095646"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1375","DOI":"10.1095\/biolreprod54.6.1375","article-title":"Validation of radioimmunoassays for two salmon gonadotropins (GTH I and GTH II) and their plasma concentrations throughout the reproductive cycle in male and female rainbow trout (Oncorhynchus mykiss)","volume":"54","author":"Prat","year":"1996","journal-title":"Biol. Reprod."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1095\/biolreprod57.5.1238","article-title":"Salmonid follicle-stimulating hormone (GtH I) mediates vitellogenic development of oocytes in the rainbow trout, Oncorhynchus mykiss","volume":"57","author":"Tyler","year":"1997","journal-title":"Biol. Reprod."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.1095\/biolreprod62.5.1262","article-title":"Regulation of ovarian steroidogenesis in vitro by follicle-stimulating hormone and luteinizing hormone during sexual maturation in salmonid fish","volume":"62","author":"Planas","year":"2000","journal-title":"Biol. Reprod."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1046\/j.1444-2906.2001.00361.x","article-title":"Changes in the levels of mRNA coding for gonadotropin I\u03b2 and II\u03b2 subunits during vitellogenesis in the common Japanese conger Conger myriaster","volume":"67","author":"Kajimura","year":"2001","journal-title":"Fish. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1046\/j.1444-2906.2002.00424.x","article-title":"Differential expression of two gonadotropin (GTH) \u03b2 subunit genes during ovarian maturation induced by repeated injection of salmon GTH in the Japanese eel Anguilla japonica","volume":"68","author":"Suetake","year":"2002","journal-title":"Fish. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1095\/biolreprod.111.091868","article-title":"Determination of Fsh quantity and bioactivity during sex differentiation and oogenesis in European sea bass","volume":"85","author":"Carrillo","year":"2011","journal-title":"Biol. Reprod."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.aquaculture.2008.11.024","article-title":"The efficacy of 2-phenoxyethanol, metomidate, clove oil and MS-222 as anaesthetic agents in the Senegalese sole (Solea senegalensis Kaup 1858)","volume":"288","author":"Weber","year":"2009","journal-title":"Aquaculture"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"734497","DOI":"10.1016\/j.aquaculture.2019.734497","article-title":"Changes in expression of reproduction-related hormones in the brain and pituitary during early ovarian differentiation and development in the red spotted grouper Epinephelus akaara, with emphasis on FSH\u03b2 and LH\u03b2","volume":"514","author":"Xu","year":"2020","journal-title":"Aquaculture"},{"key":"ref_20","first-page":"101360","article-title":"Kisspeptins, gonadotropins, and their receptors in the brain-pituitary-gonadal axis of Epinephelus akaara: Their relationship with oogonial proliferation and primary oocyte development","volume":"27","author":"Xu","year":"2022","journal-title":"Aquacult. Rep."},{"key":"ref_21","first-page":"185","article-title":"Gonadal sex differentiation of hatchery reared longtooth grouper (Epinephelus bruneus)","volume":"16","author":"Sao","year":"2012","journal-title":"Dev. Reprod."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1006\/gcen.2001.7741","article-title":"Purification of mummichog (Fundulus heteroclitus) gonadotropins and their subunits, using an immunochemical assay with antisera raised against synthetic peptides","volume":"125","author":"Shimizu","year":"2002","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"55","DOI":"10.12717\/DR.2013.17.1.055","article-title":"Characterization of pubertal development phases in female Longtooth grouper, Epinephelus bruneus via classification of bodyweight","volume":"17","author":"Ryu","year":"2013","journal-title":"Dev. Reprod."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1007\/s10641-018-0722-6","article-title":"Understanding the role of climatic and environmental variables in gonadal maturation and spawning periodicity of spotted snakehead, Channa punctata (Bloch, 1793) in a tropical floodplain wetland, India","volume":"101","author":"Karnatak","year":"2018","journal-title":"Environ. Biol. Fish."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1623","DOI":"10.1111\/are.14509","article-title":"Influence of photoperiod and temperature manipulation on gonadal development and spawning in Caspian roach (Rutilus rutilus caspicus): Implications for artificial propagation","volume":"51","author":"Akhoundian","year":"2020","journal-title":"Aquac. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/S0044-8486(02)00057-1","article-title":"Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences","volume":"208","author":"Devlin","year":"2002","journal-title":"Aquaculture"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.aquaculture.2009.04.031","article-title":"Gonadal sex differentiation in the Malabar grouper, Epinephelus malabaricus","volume":"293","author":"Murata","year":"2009","journal-title":"Aquaculture"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1387\/ijdb.103181rm","article-title":"Differentiation of steroid-producing cells during ovarian differentiation in the protogynous Malabar grouper, Epinephelus malabaricus","volume":"55","author":"Murata","year":"2011","journal-title":"Int. J. Dev. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1786","DOI":"10.1210\/en.2007-1015","article-title":"Cyp11b1 is induced in the murine gonad by luteinizing hormone\/human chorionic gonadotropin and involved in the production of 11-ketotestosterone, a major fish androgen: Conservation and evolution of the androgen metabolic pathway","volume":"149","author":"Yazawa","year":"2008","journal-title":"Endocrinology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/0016-6480(81)90318-X","article-title":"Estrogen synthesis in vitro and in vivo in the brain of a marine teleost (Myoxocephalus)","volume":"43","author":"Callard","year":"1981","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1093\/icb\/18.3.511","article-title":"Conversion of androgen to estrogen and other steroids in the vertebrate brain","volume":"18","author":"Callard","year":"1978","journal-title":"Am. Zool."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/0016-6480(82)90151-4","article-title":"Role of testosterone, estradiol-17\u03b2, and cortisol during vitellogenin synthesis in the catfish, Heteropneustes fossilis (Bloch)","volume":"48","author":"Sundararaj","year":"1982","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0016-6480(77)90184-8","article-title":"Seasonal changes in plasma cortisol, testosterone and oestradiol-17\u03b2 in the plaice, Pleuronectes platessa L","volume":"31","author":"Wingfield","year":"1977","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_34","first-page":"1500","article-title":"Endocrine regulation of fish reproduction","volume":"Volume 2","author":"Farrell","year":"2011","journal-title":"Encyclopedia of Fish Physiology: From Genome to Environment"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1095\/biolreprod.107.061408","article-title":"A progestin and an estrogen regulate early stages of oogenesis in fish","volume":"77","author":"Miura","year":"2007","journal-title":"Biol. Reprod."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1111\/j.1095-8649.1997.tb01992.x","article-title":"Gonadal development and sex steroids in a female Arctic charr broodstock","volume":"51","author":"Frantzen","year":"1997","journal-title":"J. Fish Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1330","DOI":"10.1111\/j.0022-1112.2004.00395.x","article-title":"Serum levels of testosterone, 11-ketotestosterone and oestradiol-17\u03b2 in three species of sturgeon during gonadal development and final maturation induced by hormonal treatment","volume":"64","author":"Barannikova","year":"2004","journal-title":"J. Fish Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"739150","DOI":"10.1016\/j.aquaculture.2022.739150","article-title":"Hormonal profile during the reproductive cycle and induced breeding of the dusky grouper Epinephelus marginatus (Teleostei: Serranidae) in captivity","volume":"566","author":"Mello","year":"2023","journal-title":"Aquaculture"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1111\/are.15660","article-title":"Seasonal changes of plasma sex steroids in captive longtooth grouper Epinephelus bruneus (Bloch) in subtropical regions","volume":"53","author":"Masuma","year":"2022","journal-title":"Aquac. Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1095\/biolreprod.105.041830","article-title":"Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout","volume":"73","author":"Baron","year":"2005","journal-title":"Biol. Reprod."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/j.ygcen.2008.01.022","article-title":"Appearances and chronological changes of mummichog Fundulus heteroclitus FSH cells and LH cells during ontogeny, sexual differentiation, and gonadal development","volume":"156","author":"Shimizu","year":"2008","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1002\/jez.1879","article-title":"Relationships between gonadal and gonadotrophic differentiation during early gonadal sex differentiation in several strains from the southern population of japanese medaka (Oryzias latipes)","volume":"321","author":"Horie","year":"2014","journal-title":"J. Exp. Zool."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1016\/j.ygcen.2012.07.012","article-title":"The role of pituitary gonadotropins in gonadal sex differentiation in the protogynous Malabar grouper, Epinephelus malabaricus","volume":"178","author":"Murata","year":"2012","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1007\/s12562-011-0380-5","article-title":"Immunoreactive changes in pituitary FSH and LH cells during seasonal reproductive and spawning cycles of female chub mackerel Scomber japonicus","volume":"77","author":"Nyuji","year":"2011","journal-title":"Fish. Sci."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/22\/2634\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:23:46Z","timestamp":1760131426000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/22\/2634"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,11,16]]},"references-count":44,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2023,11]]}},"alternative-id":["cells12222634"],"URL":"https:\/\/doi.org\/10.3390\/cells12222634","relation":{},"ISSN":["2073-4409"],"issn-type":[{"type":"electronic","value":"2073-4409"}],"subject":[],"published":{"date-parts":[[2023,11,16]]}}}