{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T01:17:04Z","timestamp":1760059024861,"version":"build-2065373602"},"reference-count":41,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T00:00:00Z","timestamp":1747353600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"the National Key R&amp;D Program of China","doi-asserted-by":"publisher","award":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"],"award-info":[{"award-number":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"name":"the Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS","award":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"],"award-info":[{"award-number":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"]}]},{"name":"the Taishan Scholars Program","award":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"],"award-info":[{"award-number":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"]}]},{"name":"the Shandong Key Research and Development Program for Academician team","award":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"],"award-info":[{"award-number":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"]}]},{"name":"the Central Public interest Scientific Institute Basal Research Fund, CAFS","award":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"],"award-info":[{"award-number":["2022YFD2400405","20603022024006","tsqn202408298","2023ZLYS02","2023TD20"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Chinese tongue sole (Cynoglossus semilaevis) is an important marine fish in China. It has sexual dimorphism. The weight and growth rate of female fish are much greater than those of male fish. However, high temperatures can induce sex reversal in genetic female fish (ZW) to phenotypic male fish; thus, identifying the genetic elements involved in temperature perception will provide the molecular basis for sex control. The heat shock transcription factor (hsf) is known as an important component of temperature sensing and mediates the heat shock response in fish such as Danio rerio; however, its function in C. semilaevis is unclear. In this study, five hsf genes (hsf1, hsf2, hsf4, hsf5a, and hsf5b) were identified in tongue sole and found to be expressed in the gonads at different developmental stages, peaking from 7M to 1Y. Gonadal in situ hybridization revealed that hsf gene signals were mainly localized in germ cells, e.g., sperm in the testis and all-stage oocytes in the ovary. Upon high-temperature stimulation, the expression of the hsf gene in the gonads increased gradually with increasing stimulation time, but different hsf genes presented different response patterns. After the RNA interference of hsf in the testis and ovarian cell lines, a series of sex-related genes, such as foxl2 and dmrt1, significantly changed. In vivo RNA interference had an effect on the female gonads and mainly affected neurl3 expression. On the basis of these data, we speculate that hsf responds to temperature stimulation and plays an important role in sex differentiation. This study helps elucidate the relationship between temperature sensing and sex differentiation in C. semilaevis.<\/jats:p>","DOI":"10.3390\/ani15101443","type":"journal-article","created":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T09:30:38Z","timestamp":1747387838000},"page":"1443","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["The Function of Heat Shock Transcription Factors in Sex Differentiation in Cynoglossus semilaevis"],"prefix":"10.3390","volume":"15","author":[{"given":"Zhijie","family":"Li","sequence":"first","affiliation":[{"name":"School of Marine Science and Fisheries, Jiangsu Ocean University, Lianyungang 222005, China"},{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xuexue","family":"Sun","sequence":"additional","affiliation":[{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Haipeng","family":"Yan","sequence":"additional","affiliation":[{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lijun","family":"Wang","sequence":"additional","affiliation":[{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2772-0908","authenticated-orcid":false,"given":"Xihong","family":"Li","sequence":"additional","affiliation":[{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2135-090X","authenticated-orcid":false,"given":"Na","family":"Wang","sequence":"additional","affiliation":[{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Min","family":"Wei","sequence":"additional","affiliation":[{"name":"School of Marine Science and Fisheries, Jiangsu Ocean University, Lianyungang 222005, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3887-9973","authenticated-orcid":false,"given":"Wenteng","family":"Xu","sequence":"additional","affiliation":[{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,16]]},"reference":[{"key":"ref_1","first-page":"45","article-title":"Histological study on the digestive gland of Cynoglossus semilaevis","volume":"15","author":"Lingkun","year":"2015","journal-title":"Friends Farmers Get. Rich."},{"key":"ref_2","first-page":"63","article-title":"Biological characteristics of Cynoglossus semilaevis and its development prospect of aquaculture","volume":"3","author":"Liu","year":"2005","journal-title":"Chin. Aquat. Prod."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Wang, P., Zheng, M., Liu, J., Liu, Y., Lu, J., and Sun, X. (2016). Sexually Dimorphic Gene Expression Associated with Growth and Reproduction of Tongue Sole (Cynoglossus semilaevis) Revealed by Brain Transcriptome Analysis. Int. J. Mol. Sci., 17.","DOI":"10.3390\/ijms17091402"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1111\/j.1365-2761.2010.01183.x","article-title":"Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: A review","volume":"33","author":"Roberts","year":"2010","journal-title":"J. Fish Dis."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Wang, Q., Liu, K., Feng, B., Zhang, Z., Wang, R., Tang, L., Li, W., Li, Q., Piferrer, F., and Shao, C. (2019). Transcriptome of gonads from high temperature induced sex reversal during sex determination and differentiation in chinese tongue sole, Cynoglossus semilaevis. Front. Genet., 10.","DOI":"10.3389\/fgene.2019.01128"},{"key":"ref_6","first-page":"1118","article-title":"Regulation of the heat shock response by the heat shock transcription factors","volume":"15","author":"Hietakangas","year":"2005","journal-title":"Chaperons Top. Curr. Genet."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1016\/0092-8674(82)90249-5","article-title":"A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene","volume":"30","author":"Pelham","year":"1982","journal-title":"Cell"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"102951","DOI":"10.1016\/j.isci.2021.102951","article-title":"Structures of heat shock factor trimers bound to DNA","volume":"24","author":"Feng","year":"2021","journal-title":"iScience"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Telonis-Scott, M., Ali, Z., Hangartner, S., and Sgr\u00f2, C.M. (2021). Temporal specific coevolution of Hsp70 and co-chaperone stv expression in Drosophila melanogaster under selection for heat tolerance. J. Therm. Biol., 102.","DOI":"10.1016\/j.jtherbio.2021.103110"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1118","DOI":"10.1096\/fj00-0294rev","article-title":"Roles of the heat shock transcription factors in regulation of the heat shock response and beyond","volume":"15","author":"Pirkkala","year":"2001","journal-title":"FASEB J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"E5669","DOI":"10.1073\/pnas.1516219112","article-title":"Direct link between metabolic regulation and the heat-shock response through the transcriptional regulator PGC-1\u03b1","volume":"112","author":"Minsky","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"21987","DOI":"10.1016\/S0021-9258(18)41621-3","article-title":"Transcriptional regulation of heat shock genes. A paradigm for inducible genomic responses","volume":"267","author":"Morimoto","year":"1992","journal-title":"J. Biol. Chem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"7163","DOI":"10.1128\/MCB.21.21.7163-7171.2001","article-title":"Stress-specific activation and repression of heat shock factors 1 and 2","volume":"21","author":"Mathew","year":"2001","journal-title":"Mol. Cell Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1962","DOI":"10.1111\/j.1742-4658.2009.06923.x","article-title":"Differential recognition of heat shock elements by members of the heat shock transcription factor family","volume":"276","author":"Yamamoto","year":"2009","journal-title":"FEBS J."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/S0378-1119(98)00208-X","article-title":"Novel testis-specific protein that interacts with heat shock factor 2","volume":"214","author":"Yoshima","year":"1998","journal-title":"Gene"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1007\/s12038-007-0058-4","article-title":"Heat shock transcription factors regulate heat induced cell death in a rat histiocytoma","volume":"32","author":"Prasad","year":"2007","journal-title":"J. Biosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1046\/j.1432-1327.1998.2550356.x","article-title":"Proteasome inhibition leads to the activation of all members of the heat-shock-factor family","volume":"255","author":"Kawazoe","year":"1998","journal-title":"Eur. J. Biochem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"5091","DOI":"10.1128\/MCB.18.9.5091","article-title":"Heat Shock Response and protein degradation: Regulation of HSF2 by the ubiquitin-proteasome pathway","volume":"18","author":"Mathew","year":"1998","journal-title":"Mol. Cell Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1750","DOI":"10.1093\/emboj\/17.6.1750","article-title":"Disruption of the HSF3 gene results in the severe reduction of heat shock gene expression and loss of thermotolerance","volume":"17","author":"Tanabe","year":"1998","journal-title":"EMBO J."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1083\/jcb.201402002","article-title":"Expression of HSF2 decreases in mitosis to enable stress-inducible transcription and cell survival","volume":"206","author":"Elsing","year":"2014","journal-title":"J. Cell Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"44497","DOI":"10.1074\/jbc.M405813200","article-title":"Developmentally dictated expression of heat shock factors: Exclusive expression of HSF4 in the postnatal lens and its specific interaction with alphaB-crystallin heat shock promoter","volume":"279","author":"Somasundaram","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1128\/MCB.17.1.469","article-title":"HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator","volume":"17","author":"Nakai","year":"1997","journal-title":"Mol. Cell Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1007\/978-3-319-51409-3_3","article-title":"The Role of Heat Shock Factors in Mammalian Spermatogenesis","volume":"Volume 222","author":"Wieslawa","year":"2017","journal-title":"Advances in Anatomy, Embryology and Cell Biology"},{"key":"ref_24","first-page":"787","article-title":"SCAR transformation of sex-specific microsatellite markers in Cynoglossus semilaevis and its application","volume":"22","author":"Liu","year":"2014","journal-title":"J. Agric. Biotechnol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_26","first-page":"1558","article-title":"Diversity of Plant Heat Shock Factors: Regulation, Interactions and Functions","volume":"72","author":"Szabados","year":"2020","journal-title":"J. Exp. Bot."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Liu, B.B., Hu, J.J., and Zhang, J. (2019). Evolutionary Divergence of Duplicated Hsf Genes in Populus. Cells, 8.","DOI":"10.3390\/cells8050438"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Yang, Z., Wang, Y., Gao, Y., Zhou, Y., Zhang, E., Hu, Y., Yuan, Y., Liang, G., and Xu, C. (2014). Adaptive evolution and divergent expression of heat stress transcription factors in grasses. BMC Evol. Biol., 14.","DOI":"10.1186\/1471-2148-14-147"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1007\/s42977-022-00138-z","article-title":"Functional diversification of heat shock factors","volume":"73","author":"Ahmed","year":"2022","journal-title":"Biol. Futur."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1038\/nrm2938","article-title":"Heat shock factors: Integrators of cell stress, development and lifespan","volume":"11","author":"Akerfelt","year":"2010","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Takii, R., Fujimoto, M., Pandey, A., Jaiswal, K., Shearwin-Whyatt, L., Grutzner, F., and Nakai, A. (2024). HSF1 is required for cellular adaptation to daily temperature fluctuations. Sci. Rep., 14.","DOI":"10.1038\/s41598-024-72415-x"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Dutta, N., Garcia, G., and Higuchi, S.R. (2022). Hijacking Cellular Stress Responses to Promote Lifespan. Front. Aging, 24.","DOI":"10.3389\/fragi.2022.860404"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.dci.2018.06.013","article-title":"Heat shock factor 1 regulates heat shock proteins and immune-related genes in Penaeus monodon under thermal stress","volume":"88","author":"Phornphan","year":"2018","journal-title":"Dev. Comp. Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1817","DOI":"10.1242\/jeb.203.12.1817","article-title":"Tissue-specific expression of zebrafish (Danio rerio) heat shock factor 1 mRNAs in response to heat stress","volume":"203","author":"Airaksinen","year":"2000","journal-title":"J. Exp. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Liu, Q., Wang, Y., Tan, L.L., Ma, W., Zhao, X.N., Shao, C.W., and Wang, Q. (2023). The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (Cynoglossus semilaevis). Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24043761"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1038\/nrm.2017.73","article-title":"Regulation of heat shock transcription factors and their roles in physiology and disease","volume":"19","author":"Rocio","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3252","DOI":"10.1016\/j.celrep.2018.11.090","article-title":"Heat Shock Factor 5 Is Essential for Spermatogenesis in Zebrafish","volume":"25","author":"Saju","year":"2018","journal-title":"Cell Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1002\/gene.20005","article-title":"Essential requirement for both hsf1 and hsf2 transcriptional activity in spermatogenesis and male fertility","volume":"38","author":"Wang","year":"2004","journal-title":"Genesis"},{"key":"ref_39","first-page":"293","article-title":"Heat shock factor 5 is essential for spermatogenesis in mice: Detected by a new monoclonal antibody","volume":"23","author":"Hemati","year":"2020","journal-title":"Iran. J. Basic Med. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1006\/dbio.2002.0780","article-title":"Forkhead transcription factors: Key players in development and metabolism","volume":"250","author":"Carlsson","year":"2002","journal-title":"Dev. Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.gene.2016.07.062","article-title":"Ubiquitin ligase gene neurl3 plays a role in spermatogenesis of half-smooth tongue sole (Cynoglossus semilaevis) by regulating testis protein ubiquitination","volume":"592","author":"Xu","year":"2016","journal-title":"Gene"}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/15\/10\/1443\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:34:00Z","timestamp":1760031240000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/15\/10\/1443"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,16]]},"references-count":41,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["ani15101443"],"URL":"https:\/\/doi.org\/10.3390\/ani15101443","relation":{},"ISSN":["2076-2615"],"issn-type":[{"type":"electronic","value":"2076-2615"}],"subject":[],"published":{"date-parts":[[2025,5,16]]}}}