Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T11:49:38.623Z Has data issue: false hasContentIssue false
  • English
  • Français

Puberty visualized: sexual maturation in the transparent Casper zebrafish

Published online by Cambridge University Press:  28 April 2020

Charles A. Lessman Open the ORCID record for Charles A. Lessman [Opens in a new window]  and
Nikki A. Brantley
Charles A. Lessman*
Affiliation:
Department of Biological Sciences, University of Memphis, Memphis, TN38152, USA
Nikki A. Brantley
Affiliation:
Department of Biological Sciences, University of Memphis, Memphis, TN38152, USA
*
Author for correspondence: Charles Lessman. University of Memphis, Life Sciences Building, 3774 Walker Avenue, Memphis, TN38152, USA. Tel: +1 901 678 2963. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Transparent Casper zebrafish allow studies of vertebrate sexual maturation and gonad development in vivo. Casper gonad dynamics can be observed longitudinally over time and non-invasively. Gonad maturation and reproduction are complex processes subject to disruption by endocrine-disrupting chemicals (EDCs), such as diethylstilbestrol (DES). DES was used as a ‘proof of principle’ to ascertain the usefulness of the Casper model to determine EDC effects on gonad maturation. Puberty onset in control juvenile Casper zebrafish (N = 43) averaged 13.2 weeks post fertilization (WPF) for females and included increased vent size, while in males puberty occurred at 11.7 WPF along with maintenance of small vents. DES treatment for 6 days in early juveniles (N = 20) induced an average delay in puberty of 5 weeks in females and 10 weeks in males. DES induced loss of breeding tubercles and vent enlargement in post-pubescent males. Puberty in control fish was correlated with an average body length of 1.7 cm for males and 1.8 cm for females. Increased testes opacity, small vent and breeding tubercles denoted male puberty. Puberty in females was defined as ovarian follicle diameters reaching 400 µm with increasingly opaque follicles and by an increased vent size. These results are like those for wild-type zebrafish and indicate that the Casper model is a useful system for studying gonad dynamics in vivo. Future use of transgenic reporter lines in Casper will allow new avenues of investigation into the reproductive biology of this vertebrate model.

Keywords

DiethylstilbestrolGonadLongitudinal in vivo imagingPubertySecondary sex characteristics
Type
Research Article
Information
Zygote , Volume 28 , Issue 4 , August 2020 , pp. 322 - 332
Copyright
© Cambridge University Press 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asahina, K, Hanyu, I, Aida, K, Nishina, H and Kobayashi, M (1985). Effects of hypophyseal, placental and steroid hormones on ovipositor elongation and ovulation in the rose bitterling, Rhodeus ocellatus ocellatus. In Current Trends in Comparative Endocrinology (eds Loft, B and Holmes, WN), pp. 235–6. Hong Kong: Hong Kong University Press.Google Scholar
Brion, F, Tyler, CR, Palazzi, X, Laillet, B, Porcher, JM, Garric, J and Flammarion, P (2004). Impacts of 17beta-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult-life stages in zebrafish (Danio rerio). Aquat Toxicol 68, 193–217.CrossRefGoogle Scholar
Campinho, M and Power, D (2013). Waterborne exposure of zebrafish embryos to micromole concentrations of ioxynil and diethylstilbestrol disrupts thymocyte development. Aquat Toxicol 140, 279–87.CrossRefGoogle Scholar
Chen, W and Ge, W (2013). Gonad differentiation and puberty onset in the zebrafish: evidence for the dependence of puberty onset on body growth but not age in females. Mol Reprod Dev 80, 384–92.CrossRefGoogle Scholar
D’Agati, G, Beltre, R, Sessa, A, Burger, A, Zhou, Y, Mosimann, C and White, RM (2017). A defect in the mitochondrial protein Mpv17 underlies the transparent Casper zebrafish. Dev Biol 430, 11–7.CrossRefGoogle ScholarPubMed
Dobrydneva, Y, Williams, RL, Katzenellenbogen, JA, Ratz, PH and Blackmore, PF (2003). Diethylstilbestrol and tetrahydrochrysenes are calcium channel blockers in human platelets: relationship to the stilbene pharmacophore. Thromb Res 110, 23–31.CrossRefGoogle ScholarPubMed
Dobrydneva, Y, Williams, RL and Blackmore, PF (2010). Diethylstilbestrol and other nonsteroidal estrogens: novel class of store-operated calcium channel modulators. J Cardiovasc Pharmacol 55, 522–30.Google ScholarPubMed
Duan, Z, Zhu, L, Zhu, L, Kun, Y and Zhu, X (2008). Individual and joint toxic effects of pentachlorophenol and bisphenol A on the development of zebrafish (Danio rerio) embryo. Ecotoxicol Environ Saf 71, 774–80.CrossRefGoogle ScholarPubMed
Hill, AJ, Teraoka, H, Heideman, W and Peterson, RE (2005). Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86, 6–19.CrossRefGoogle ScholarPubMed
Hill, RL Jr and Janz, DM (2003). Developmental estrogenic exposure in zebrafish (Danio rerio): I. Effects on sex ratio and breeding success. Aquat Toxicol 63, 417–29.CrossRefGoogle ScholarPubMed
Iguchi, T, Watanabe, H and Katsu, Y (2001). Developmental effects of estrogenic agents on mice, fish, and frogs: A mini-review. Horm Behav 40, 248–51.CrossRefGoogle ScholarPubMed
Jones, KD and Lessman, CA (2014). Age determination of gonad maturation and puberty onset in the transparent Casper zebrafish juvenile. In Zebrafish: Topics in Reproduction, Toxicology and Development (eds Lessman, CA and Carver, EA), pp. 3–13. New York: Nova Science Publishers Inc.Google Scholar
Kim, SD, Cho, J, Kim, IS, Vanderford, BJ and Snyder, SA (2007). Occurrence and removal of pharmaceuticals and endocrine disruptors in south Korean surface, drinking, and waste waters. Water Res 41, 1013–21.CrossRefGoogle ScholarPubMed
Lawson, ND and Weinstein, BM (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248, 307–18.CrossRefGoogle ScholarPubMed
Lessman, CA and Carver, EA (2014). Zebrafish: Topics in Reproduction, Toxicology and Development, 302 pp. New York: Nova Science Publishers Inc.Google Scholar
Lister, JA, Robertson, CP, Lepage, T, Johnson, SL and Raible, DW (1999). Nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126, 3757–67.Google ScholarPubMed
Maack, G and Segner, H (2003). Morphological development of the gonads in zebrafish. J Fish Biol 62, 895–906.CrossRefGoogle Scholar
McMillan, SC, Xu, ZT, Zhang, J, Teh, C, Korzh, V, Trudeau, VL and Akimenko, M (2013). Regeneration of breeding tubercles on zebrafish pectoral fins requires androgens and two waves of revascularization. Development 140, 4323–34.CrossRefGoogle ScholarPubMed
McMillan, SC, Geraudie, J and Akimenko, M (2015). Pectoral fin breeding tubercle clusters: a method to determine zebrafish sex. Zebrafish 12, 121–3.CrossRefGoogle ScholarPubMed
Reed, CE and Fenton, SE (2013). Exposure to diethylstilbestrol during sensitive life stages: a legacy of heritable health effects. Birth Defects Res C: Embryo Today: Reviews 99, 134–46.CrossRefGoogle ScholarPubMed
Segner, H (2009). Zebrafish (Danio rerio) as a model organism for investigating endocrine disruption. Comp Biochem Physiol C: Toxicol Pharm 149, 187–95.Google ScholarPubMed
Selman, K, Wallace, RA, Sarka, A and Qi, X (1993). Stages of oocyte development in the zebrafish Brachydanio rerio. J Morphol 218, 203–24.CrossRefGoogle ScholarPubMed
Shirai, K (1962). Correlation between the growth of the ovipositor and ovarian conditions in the bitterling Rhodeus ocellatus. Bull Fac Fish Hokkaido Univ 13, 137–51.Google Scholar
Sumpter, JP, and Jobling, S (1995). Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ Health Perspect 103, Suppl 7, 173–8.Google ScholarPubMed
Takatsu, K, Miyaoku, K, Roy, SR, Murono, Y, Sago, T, Itagaki, H, Nakamura, M and Tokumoto, T (2013). Induction of female-to-male sex change in adult zebrafish by aromatase inhibitor treatment. Sci Rep 3, 3400, 1–7.CrossRefGoogle ScholarPubMed
Taranger, GL, Carrillo, M, Schulz, RW, Fontaine, P, Zanuy, S, Felip, A, Weltzien, F, Dufour, S, Karlsen, Ø and Norberg, B (2010). Control of puberty in farmed fish. Gen Comp Endocrinol 165, 483–515.CrossRefGoogle ScholarPubMed
Tokumoto, T, Tokumoto, M, Horiguchi, R, Ishikawa, K and Nagahama, Y (2004). Diethylstilbestrol induces fish oocyte maturation. Proc Natl Acad Sci USA 101, 3686–90.CrossRefGoogle ScholarPubMed
Tokumoto, T, Tokumoto, M and Nagahama, Y (2005). Induction and inhibition of oocyte maturation by EDCs in zebrafish. Reprod Biol Endocrinol. 3, 69.CrossRefGoogle ScholarPubMed
Tokumoto, T, Tokumoto, M and Thomas, P (2007). Interactions of diethylstilbestrol (DES) and DES analogs with membrane progestin receptor-α and the correlation with their nongenomic progestin activities. Endocrinology 148, 3459–67.CrossRefGoogle ScholarPubMed
Tokumoto, T, Yamaguchi, T, Ii, S and Tokumoto, M (2011). In vivo induction of oocyte maturation and ovulation in zebrafish. PLoS One 6, e25206.CrossRefGoogle ScholarPubMed
Tyler, C, Van der Eerden, B, Jobling, S, Panter, G and Sumpter, J (1996). Measurement of vitellogenin a biomarker for exposure to oestrogenic chemicals in a wide variety of cyprinid fish. J Comp Physiol B: Biochem Syst Environ Physiol 166, 418–26.CrossRefGoogle Scholar
Umans, RA, Henson, HE, Mu, F, Parupalli, C, Ju, B, Peters, JL, Lanham, KA, Plavicki, JS and Taylor, MR (2017). CNS angiogenesis and barriergenesis occur simultaneously. Dev Biol 425, 101–8.CrossRefGoogle ScholarPubMed
van der Ven, L, van den Brandhof, EJ, Vos, JH and Wester, PW (2007). Effects of the estrogen agonist 17-estradiol and antagonist tamoxifen in a partial life-cycle assay with zebrafish (Danio rerio). Environ Toxicol Chem 26, 92–9.CrossRefGoogle Scholar
vom Saal, FS, Timms, BG, Montano, MM, Palanza, P, Thayer, KA, Nagel, SC, Dhar, MD, Ganjam, VK, Parmigiani, S and Welshons, WV (1997). Prostate enlargement in mice due to fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses. Proc Natl Acad Sci USA 94, 2056–61.CrossRefGoogle ScholarPubMed
Wakamatsu, Y, Pristyazhnyuk, S, Kinoshita, M, Tanaka, M and Ozato, K (2001). The see-through medaka: a fish model that is transparent throughout life. Proc Natl Acad Sci USA 98, 10046–50.CrossRefGoogle ScholarPubMed
Wang, X, Bartfai, R, Sleptsova-Freidrich, I and Orban, L (2007). The timing and extent of ‘juvenile ovary’ phase are highly variable during zebrafish testis differentiation. J Fish Biol 70, 33–44.CrossRefGoogle Scholar
Weber, LP, Hill, RL Jr and Janz, DM (2003). Developmental estrogenic exposure in zebrafish (Danio rerio). II. Histological evaluation of gametogenesis and organ toxicity. Aquat Toxicol 63, 431–46.CrossRefGoogle ScholarPubMed
White, RM, Sessa, A, Burke, C, Bowman, T, LeBlanc, J, Ceol, C, Bourque, C, Dovey, M, Goessling, W and Burns, CE (2008). Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2, 183–9.CrossRefGoogle ScholarPubMed
Yang, L, Lin, L, Weng, S, Feng, Z and Luan, T (2008). Sexually disrupting effects of nonylphenol and diethylstilbestrol on male silver carp (Carassius auratus) in aquatic microcosms. Ecotoxicol Environ Saf 71, 400–11.CrossRefGoogle Scholar
Yossa, R, Sarker, PK, Proulx, E, Saxena, V, Ekker, M and Vandenberg, GW (2013). A practical approach for sexing zebrafish Danio rerio. J Appl Aquacult 25, 148–53.CrossRefGoogle Scholar