Reproductive hormones affect follicular cells and ooplasm of Stage I and II oocytes in zebrafish
Maria Lígia Sousa A B , Ana Silva B , Fernanda Malhão A B , Maria João Rocha A B C , Eduardo Rocha A B and Ralph Urbatzka A D
+ Author Affiliations
- Author Affiliations
A CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, CIMAR Associated Laboratory, UPorto – University of Porto, Laboratory of Cellular, Molecular and Analytical Studies, Rua dos Bragas 289, 4050-123 Porto, Portugal.
B ICBAS – Institute of Biomedical Sciences Abel Salazar, UPorto – University of Porto, Laboratory of Histology and Embryology, R. Jorge Viterbo Ferreira 228, 4050-313 Porto, Portugal.
C ISCS-N – Superior Institute of Health Sciences-North, CESPU, Cooperative Higher Education, Polytechnic and University, Rua Central de Gandra 1317, 4585-116 Gandra, Paredes, Portugal.
D Corresponding author. Email: rurbatzka@ciimar.up.pt
Reproduction, Fertility and Development 28(12) 1945-1952 https://doi.org/10.1071/RD15100
Submitted: 11 March 2015 Accepted: 26 May 2015 Published: 25 June 2015
Abstract
The basic pathway of oocyte development and its regulation is evolutionarily conserved among vertebrates; however, little is known about the role of hormones at the first stages (Stages I and II) of follicle development in fish. In the present study, zebrafish follicles at Stages I and II were exposed in vitro to the reproductive hormones 17β-oestradiol (E2), 11-ketotestosterone (11KT), 17,20β-dihydroxy-4-pregnen-3-one (DHP) and to the secondary messenger dibutyryl cyclic adenosine monophosphate (db-cAMP) at a concentration of 1 µM for a 48-h period. Morphological alterations of the ooplasm were assessed by transmission electron microscopy and of the granulosa cell layer by quantitative stereology. Expression of mRNA was analysed for cell-cycle genes (cyclin B and E) and resident proteins of the endoplasmic reticulum (calnexin and 78-kDa glucose-regulated protein (grp78/bip)). E2 and db-cAMP stimulated the presence of endoplasmic reticulum in the ooplasm and calnexin mRNA increased in the db-cAMP treatment, but also in response to 11KT and DHP. 11KT, DHP and db-cAMP inhibited the progression of the cell cycle in the granulosa–theca cell layer, indicated by a reduction of the nucleus volume-weighted size of granulosa cells and of increased cyclin E mRNA expression. Reproductive hormones had different effects on the ooplasm and the granulosa–theca cell layer of zebrafish follicles, predominantly at Stage II.
Additional keywords: cell cycle, endoplasmic reticulum, follicles, oocyte development.
References
Balakier, H., Dziak, E., Sojecki, A., Librach, C., Michalak, M., and Opas, M. (2002). Calcium-binding proteins and calcium-release channels in human maturing oocytes, pronuclear zygotes and early preimplantation embryos. Hum. Reprod. 17, 2938–2947.| Calcium-binding proteins and calcium-release channels in human maturing oocytes, pronuclear zygotes and early preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptFOrurc%3D&md5=40043ba69a539f8c0a70aec868310a05CAS | 12407053PubMed |
Barrett, C. B., and Powers, R. D. (1993). Progestins inhibit murine oocyte meiotic maturation in vitro. J. Exp. Zool. 265, 231–239.
| Progestins inhibit murine oocyte meiotic maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitVGns74%3D&md5=3fec987ab0ec9cca164725a5e93c4819CAS | 8436917PubMed |
Campbell, B., Dickey, J., Beckman, B., Young, G., Pierce, A., Fukada, H., and Swanson, P. (2006). Previtellogenic oocyte growth in salmon: relationships among body growth, plasma insulin-like growth factor-1, oestradiol-17beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic acute regulatory protein and receptors for gonadotrophins, growth hormone and somatolactin. Biol. Reprod. 75, 34–44.
| Previtellogenic oocyte growth in salmon: relationships among body growth, plasma insulin-like growth factor-1, oestradiol-17beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic acute regulatory protein and receptors for gonadotrophins, growth hormone and somatolactin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlyisLs%3D&md5=e27e4f60f73b08cd85b2fed9bb0ef134CAS | 16554413PubMed |
Cavalier-Smith, T. (1978). Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate and the solution of the DNA C-value paradox. J. Cell Sci. 34, 247–278.
| 1:CAS:528:DyaE1MXot1GrtA%3D%3D&md5=d94eadbc4a3761b41e442247179410e7CAS | 372199PubMed |
Clelland, E. S., and Kelly, S. P. (2010). Tight-junction proteins in zebrafish ovarian follicles: stage-specific mRNA abundance and response to 17β-oestradiol, human chorionic gonadotrophin and maturation-inducing hormone. Gen. Comp. Endocrinol. 168, 388–400.
| Tight-junction proteins in zebrafish ovarian follicles: stage-specific mRNA abundance and response to 17β-oestradiol, human chorionic gonadotrophin and maturation-inducing hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVertrvO&md5=6953293810726fa3ace1c4e13e7d3b2eCAS | 20553723PubMed |
Clelland, E., and Peng, C. (2009). Endocrine–paracrine control of zebrafish ovarian development. Mol. Cell. Endocrinol. 312, 42–52.
| Endocrine–paracrine control of zebrafish ovarian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFKnsL3F&md5=9e1186b3f1443692c2546ea49c28c17bCAS | 19406202PubMed |
Coudreuse, D., and Nurse, P. (2010). Driving the cell cycle with a minimal CDK control network. Nature 468, 1074–1079.
| Driving the cell cycle with a minimal CDK control network.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVSlsw%3D%3D&md5=80c82db0a427a74b96c920bd17d3d2f0CAS | 21179163PubMed |
Delpino, A., and Castelli, M. (2002). The 78-kDa glucose-regulated protein (GRP78/BIP) is expressed on the cell membrane, is released into cell culture medium and is also present in human peripheral circulation. Biosci. Rep. 22, 407–420.
| The 78-kDa glucose-regulated protein (GRP78/BIP) is expressed on the cell membrane, is released into cell culture medium and is also present in human peripheral circulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosVertb0%3D&md5=aaf6507896a138be55309db51c5f7468CAS | 12516782PubMed |
Devlin, R. H., and Nagahama, Y. (2002). Sex determination and sex differentiation in fish: an overview of genetic, physiological and environmental influences. Aquaculture 208, 191–364.
| Sex determination and sex differentiation in fish: an overview of genetic, physiological and environmental influences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFKjsbY%3D&md5=a7316650015a659de55e39ac676e834bCAS |
Fidorra, J., Mielke, T., Booz, J., and Feinendegen, L. E. (1981). Cellular and nuclear volume of human cells during the cell cycle. Radiat. Environ. Biophys. 19, 205–214.
| Cellular and nuclear volume of human cells during the cell cycle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3ntl2itA%3D%3D&md5=ab916a967bff5c75000f39abfcba9461CAS | 7267987PubMed |
García-López, A., Sánchez-Amaya, M. I., and Prat, F. (2011). Targeted gene expression profiling in European sea bass (Dicentrarchus labrax, L.) follicles from primary growth to late vitellogenesis. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 160, 374–380.
| Targeted gene expression profiling in European sea bass (Dicentrarchus labrax, L.) follicles from primary growth to late vitellogenesis.Crossref | GoogleScholarGoogle Scholar | 21782032PubMed |
Ge, W. (2005). Intrafollicular paracrine communication in the zebrafish ovary: the state of the art of an emerging model for the study of vertebrate folliculogenesis. Mol. Cell. Endocrinol. 237, 1–10.
| Intrafollicular paracrine communication in the zebrafish ovary: the state of the art of an emerging model for the study of vertebrate folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVentbY%3D&md5=f20c1e5866f86ed812f514b1d4018effCAS | 15921848PubMed |
Gioacchini, G., Giorgini, E., Merrifield, D. L., Hardiman, G., Borini, A., Vaccari, L., and Carnevali, O. (2012). Probiotics can induce follicle maturational competence: the Danio rerio case. Biol. Reprod. 86, 65.
| Probiotics can induce follicle maturational competence: the Danio rerio case.Crossref | GoogleScholarGoogle Scholar | 22088919PubMed |
Gundersen, H. J., and Jensen, E. B. (1985). Stereological estimation of the volume-weighted mean volume of arbitrary particles observed on random sections. J. Microsc. 138, 127–142.
| Stereological estimation of the volume-weighted mean volume of arbitrary particles observed on random sections.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M3msVOrsg%3D%3D&md5=60d674bbe6e27e873b14e99760f1092cCAS | 4020857PubMed |
Haas, I. G. (1994). BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia 50, 1012–1020.
| BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXivFegtb0%3D&md5=06e0df53615d0e4057467f440deed343CAS | 7988659PubMed |
Han, J., Wang, Q., Wang, X., Li, Y., Wen, S., Liu, S., Ying, G., Guo, Y., and Zhou, B. (2014). The synthetic progestin megestrol acetate adversely affects zebrafish reproduction. Aquat. Toxicol. 150, 66–72.
| The synthetic progestin megestrol acetate adversely affects zebrafish reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVCgu7c%3D&md5=b9acce38910549674bca68004d1f574aCAS | 24647012PubMed |
Hanna, R. N., and Zhu, J. (2009). Expression of membrane progestin receptors in zebrafish (Danio rerio) oocytes, testis and pituitary. Gen. Comp. Endocrinol. 161, 153–157.
| Expression of membrane progestin receptors in zebrafish (Danio rerio) oocytes, testis and pituitary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXis1Citr0%3D&md5=38349afda9b0835929af37a8b01a544cCAS | 18957293PubMed |
Hebert, D. N., Foellmer, B., and Helenius, A. (1995). Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 81, 425–433.
| Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsFSrsLk%3D&md5=053b36e8f3c16194b28c3d771d978749CAS | 7736594PubMed |
Ings, J. S., and Van der Kraak, G. J. (2006). Characterisation of the mRNA expression of StAR and steroidogenic enzymes in zebrafish ovarian follicles. Mol. Reprod. Dev. 73, 943–954.
| Characterisation of the mRNA expression of StAR and steroidogenic enzymes in zebrafish ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1Cktr0%3D&md5=4af808e9a0dd8ab404816f05e3be5e6dCAS | 16700073PubMed |
Kah, O., and Dufour, S. (2011). Conserved and divergent features of reproductive neuroendocrinology in teleost fishes. In ‘Hormones and Reproduction of Vertebrates’. (Ed(s) D. O. Norris, K. H. Lopez.) pp. 15–42. (Academic Press: London.)
Khoo, K. H. (1979). The histochemistry and endocrine control of vitellogenesis in goldfish ovaries. Can. J. Zool. 57, 617–626.
| The histochemistry and endocrine control of vitellogenesis in goldfish ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktVart70%3D&md5=ebc2d67323e514d25b706027a50a33b1CAS |
Kortner, T. M., Rocha, E., Silva, P., Castro, L. F. C., and Arukwe, A. (2008). Genomic approach in evaluating the role of androgens on the growth of Atlantic cod (Gadus morhua) previtellogenic oocytes. Comp. Biochem. Physiol. Part D Genomics Proteomics 3, 205–218.
| 20483219PubMed |
Lee, A. S. (2005). The ER chaperone and signalling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35, 373–381.
| The ER chaperone and signalling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVSntLg%3D&md5=d77a5d738912a004849205ad808a1ca1CAS | 15804610PubMed |
Lokman, P. M., George, K. A. N., Divers, S. L., Algie, M., and Young, G. (2007). 11-Ketotestosterone and IGF-I increase the size of previtellogenic oocytes from short-finned eel, Anguilla australis, in vitro. Reproduction 133, 955–967.
| 11-Ketotestosterone and IGF-I increase the size of previtellogenic oocytes from short-finned eel, Anguilla australis, in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlGnu7k%3D&md5=a82e9dfcf7f253e4ac4a6174b23a0e8dCAS | 17616725PubMed |
Lubzens, E., Young, G., Bobe, J., and Cerdà, J. (2010). Oogenesis in teleosts: how fish eggs are formed. Gen. Comp. Endocrinol. 165, 367–389.
| Oogenesis in teleosts: how fish eggs are formed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktVegug%3D%3D&md5=73417344a8dcebb0b2f6128761be656aCAS | 19505465PubMed |
Meijide, F. J., Nostro, F. L. L., and Guerrero, G. A. (2005). Gonadal development and sex differentiation in the cichlid fish Cichlasoma dimerus (Teleostei, perciformes): a light- and electron-microscopic study. J. Morphol. 264, 191–210.
| Gonadal development and sex differentiation in the cichlid fish Cichlasoma dimerus (Teleostei, perciformes): a light- and electron-microscopic study.Crossref | GoogleScholarGoogle Scholar | 15789420PubMed |
Menuet, A., Pellegrini, E., Anglade, I., Blaise, O., Laudet, V., Kah, O., and Pakdel, F. (2002). Molecular characterisation of three oestrogen receptor forms in zebrafish: binding characteristics, transactivation properties and tissue distributions. Biol. Reprod. 66, 1881–1892.
| Molecular characterisation of three oestrogen receptor forms in zebrafish: binding characteristics, transactivation properties and tissue distributions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFensrc%3D&md5=3254f98d18a4f40ccab08f80aefa4fecCAS | 12021076PubMed |
Menuet, A., Pellegrini, E., Brion, F., Gueguen, M. M., Anglade, I., Pakdel, F., and Kah, O. (2005). Expression and oestrogen-dependent regulation of the zebrafish brain aromatase gene. J. Comp. Neurol. 485, 304–320.
| Expression and oestrogen-dependent regulation of the zebrafish brain aromatase gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFyqtLc%3D&md5=291785b4e5e64ee76cd9bdf140ec8299CAS | 15803511PubMed |
Miura, C., Higashino, T., and Miura, T. (2007). A progestin and an oestrogen regulate early stages of oogenesis in fish. Biol. Reprod. 77, 822–828.
| A progestin and an oestrogen regulate early stages of oogenesis in fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1CnurfE&md5=475157326c13c8331f2093ec04240ebbCAS | 17687117PubMed |
Polanowska, J., Fabbrizio, E., Le Cam, L., Trouche, D., Emiliani, S., Herrera, R., and Sardet, C. (2001). The periodic down regulation of cyclin E gene expression from exit of mitosis to end of G(1) is controlled by a deacetylase- and E2F-associated bipartite repressor element. Oncogene 20, 4115–4127.
| The periodic down regulation of cyclin E gene expression from exit of mitosis to end of G(1) is controlled by a deacetylase- and E2F-associated bipartite repressor element.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXls1Wltb8%3D&md5=40528d9c8fb46db2f0f28f4dbc52d68eCAS | 11464278PubMed |
Prat, F., Sumpter, J. P., and Tyler, C. R. (1996). Validation of radioimmunoassays for two salmon gonadotrophins (GTH I and GTH II) and their plasma concentrations throughout the reproductive cycle in male and female rainbow trout (Oncorhynchus mykiss). Biol. Reprod. 54, 1375–1382.
| Validation of radioimmunoassays for two salmon gonadotrophins (GTH I and GTH II) and their plasma concentrations throughout the reproductive cycle in male and female rainbow trout (Oncorhynchus mykiss).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtVyntrc%3D&md5=9f104362aed1b48cedcc80100943bf8fCAS | 8724367PubMed |
Richards, J. S. (2001). New signalling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol. Endocrinol. 15, 209–218.
| 1:CAS:528:DC%2BD3MXpsFOltQ%3D%3D&md5=775d1f9b616ec434fbfacc657e117bc3CAS | 11158328PubMed |
Robker, R. L., and Richards, J. S. (1998). Hormonal control of the cell cycle in ovarian cells: proliferation versus differentiation. Biol. Reprod. 59, 476–482.
| Hormonal control of the cell cycle in ovarian cells: proliferation versus differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvVSls7c%3D&md5=05aa4205c1a84a3eec6adecb84585788CAS | 9716543PubMed |
Romanel, A., Jensen, L. J., Cardelli, L., and Csikász-Nagy, A. (2012). Transcriptional regulation is a major controller of cell-cycle transition dynamics. PLoS One 7, e29716.
| Transcriptional regulation is a major controller of cell-cycle transition dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFOqu7k%3D&md5=1c57f11ea24041fa1761a2d5e95b9e4eCAS | 22238641PubMed |
Schrag, J. D., Bergeron, J. J. M., Li, Y., Borisova, S., Hahn, M., Thomas, D. Y., and Cygler, M. (2001). The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell 8, 633–644.
| The structure of calnexin, an ER chaperone involved in quality control of protein folding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslGmtrc%3D&md5=a7ae5243782bcb09e9dd68c786788506CAS | 11583625PubMed |
Selman, K., Wallace, R. A., Sarka, A., and Qi, X. (1993). Stages of oocyte development in the zebrafish, Brachydanio rerio. J. Morphol. 218, 203–224.
| Stages of oocyte development in the zebrafish, Brachydanio rerio.Crossref | GoogleScholarGoogle Scholar |
Sousa, M. L., Silva, A., Malhão, F., Rocha, M. J., Rocha, E., and Urbatzka, R. (2014). Viability analysis of oocyte–follicle complexes and gonadal fragments of zebrafish as baseline for toxicity testing. Toxicol. Mech. Methods 24, 42–49.
| Viability analysis of oocyte–follicle complexes and gonadal fragments of zebrafish as baseline for toxicity testing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFSlur%2FK&md5=b118e4ba6434232acb8f09283cd362b1CAS | 24053232PubMed |
Steen, H. B., and Lindmo, T. (1978). Cellular and nuclear volume during the cell cycle of NHIK 3025 cells. Cell Tissue Kinet. 11, 69–81.
| Cellular and nuclear volume during the cell cycle of NHIK 3025 cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c7gsFeitw%3D%3D&md5=fb581fa5e494ae5d2f2708c29481fd5eCAS | 564239PubMed |
Tan, Q., Zagrodny, A., Bernaudo, S., and Peng, C. (2009). Regulation of membrane progestin receptors in the zebrafish ovary by gonadotrophin, activin, TGF-β and BMP-15. Mol. Cell. Endocrinol. 312, 72–79.
| Regulation of membrane progestin receptors in the zebrafish ovary by gonadotrophin, activin, TGF-β and BMP-15.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFKnsLrO&md5=d41addfabf16f4cf916f7f6dfaea43fdCAS | 19773085PubMed |
Urbatzka, R., Rocha, M. J., and Rocha, E. (2011). Regulation of ovarian development and function in teleosts. In ‘Hormones and Reproduction of Vertebrates’. (Eds D. O. Norris, K. H. Lopez.) pp. 65–82. (Academic Press: London.)
Urbatzka, R., Galante-Oliveira, S., Rocha, E., Castro, L. F. C., and Cunha, I. (2013). Normalisation strategies for gene expression studies by real-time PCR in a marine fish species, Scophthalmus maximus. Mar. Genomics 10, 17–25.
| Normalisation strategies for gene expression studies by real-time PCR in a marine fish species, Scophthalmus maximus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3svosVyqug%3D%3D&md5=2362d2dd43bc07307b1eb24fde4a7717CAS | 23517768PubMed |
Van’t Hof, J., and Sparrow, A. H. (1963). A relationship between DNA content, nuclear volume and minimum mitotic cycle time. Proc. Natl. Acad. Sci. USA 49, 897–902.
| A relationship between DNA content, nuclear volume and minimum mitotic cycle time.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF387ovVSiug%3D%3D&md5=a5158c33569e33774dd29823527d35d4CAS | 13996145PubMed |
Wallace, R. A., and Selman, K. (1990). Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J. Electron Microsc. Tech. 16, 175–201.
| Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M%2Fls1eksw%3D%3D&md5=58ae0576a4d48c8ca6d839ddafdbbee3CAS | 2243277PubMed |
Williams, D. B. (2006). Beyond lectins: the calnexin–calreticulin chaperone system of the endoplasmic reticulum. J. Cell Sci. 119, 615–623.
| Beyond lectins: the calnexin–calreticulin chaperone system of the endoplasmic reticulum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislSrtrc%3D&md5=3df098f8fd0c6eaac2febe00c5cf3d8dCAS | 16467570PubMed |
Zucchi, S., Castiglioni, S., and Fent, K. (2013). Progesterone alters global transcription profiles at environmental concentrations in brain and ovary of female zebrafish (Danio rerio). Environ. Sci. Technol. 47, 12 548–12 556.
| Progesterone alters global transcription profiles at environmental concentrations in brain and ovary of female zebrafish (Danio rerio).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFCjt7jP&md5=89cfdcf833ececc32f2a5d74bd4d0522CAS |
