Skip to main content
Log in

Transient effects of methyltestosterone injection on different reproductive parameters of the hermaphrodite fish Kryptolebias marmoratus

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

To elucidate the action mechanism of environmental androgenic chemicals on fish reproductive activity by transient stimulation in heavily polluted areas, individuals of the hermaphrodite fish Kryptolebias marmoratus were injected once with six concentrations of methyltestosterone (MT) (0.1, 1, 5, 10, 50, and 100 μg/g BW) intraperitoneally. The fish were sampled at intervals of 7, 15, and 30 days after a single injection. At 7 days after injection, mature oocytes were not observed in the MT-exposed groups except for the group exposed to 0.1 μg MT, while testicular development was not remarkably different between any of the groups. Also, at 7 days after injection, hepatic estrogen receptor α (ERα) and vitellogenin (VTG) mRNA abundance decreased significantly in the MT-exposed groups despite no significant difference in plasma 17β-estradiol (E2) levels between any of the groups. This significant difference in VTG mRNA between the control and the MT-exposed groups persisted until 30 days after injection, although ERα mRNA abundance was not statistically different between any groups at 30 days after injection. Our results clearly show that a single injection of MT inhibits ovarian development rather than testicular development in the hermaphroditic gonad of K. marmoratus. Furthermore, our results demonstrate that a single injection of MT interfered with hepatic VTG mRNA synthesis mediated by the suppression of hepatic ERα mRNA transcription.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andersen L, Goto-Kazeto R, Trant JM, Nash JP, Korsgaard B, Bjerregaard P (2006) Short-term exposure to low concentrations of the synthetic androgen methyltestosterone affects vitellogenin and steroid levels in adult male zebrafish (Danio rerio). Aquat Toxicol 76:343–352

    Article  CAS  Google Scholar 

  • Arslan T, Phelps RP (2004) Production of monosex male black crappie, Pomoxis nigromaculatus, populations by multiple androgen immersion. Aquaculture 234:561–573

    Article  Google Scholar 

  • Babin PJ, Carnevali O, Lubzens E, Schneider WJ (2007) Molecular aspects of oocyte vitellogenesis in fish. In: Babin PJ, Cerdà J, Lubzens E (eds) The fish oocyte: from basic studies to biotechnological applications. Springer, Netherlands, pp 39–76

    Google Scholar 

  • Baron D, Fostier A, Breton B, Guiguen Y (2005) Androgen and estrogen treatments alter steady state messengers RNA (mRNA) levels of testicular steroidogenic enzymes in the rainbow trout, Oncorhynchus mykiss. Mol Reprod Develop 71:471–479

    Article  CAS  Google Scholar 

  • Belfroid AC, Van der Horst A, Vethaak AD, Schäfer AJ, Rijs GBJ, Wegener J, Cofino WP (1999) Analysis and occurrence of estrogenic hormones and their glucuronides in surface water and waste water in the Netherlands. Sci Total Environ 225:101–108

    Article  CAS  Google Scholar 

  • Bhasin S, Bagatell CJ, Bremner WJ, Plymate SR, Tenover JL, Korenman SG, Nielschlag E (1998) Issues in testosterone replacement in old man. J Clin Endocrinol Metab 83:3435–3448

    Article  CAS  Google Scholar 

  • Blankvoort BMG, Rodenburg RJT, Murk AJ, Koeman JH, Schilt R, Aarts JMMJG (2005) Androgenic activity in surface water samples detected using the AR-LUX assay: indication for mixture effect. Environ Toxicol Pharmacol 19:263–272

    Article  CAS  Google Scholar 

  • Blázquez M, Piferrer F, Zanuy S, Carrillo M, Donaldson EM (1995) Development of sex control techniques for European sea bass (Dicentrarchus labrax L.) aquaculture: effects of dietary 17α-methyltestosterone prior to sex differentiation. Aquaculture 135:329–342

    Article  Google Scholar 

  • Boudreau M, Courtenay SC, MacLatchy DL, Bérubé CH, Hewitt LM, Van Der Kraak GJ (2005) Morphological abnormalities during early-life development of the estuarine mummichog, Fundulus heteroclitus, as an indicator of androgenic and anti-androgenic endocrine disruption. Aquat Toxicol 71:357–369

    Article  CAS  Google Scholar 

  • Cole KS, Noakes DLG (1997) Gonadal development and sexual allocation in mangrove killifish, Rivulus marmoratus (Pisces: atherionmorpha). Copeia 3:596–600

    Article  Google Scholar 

  • Denslow N, Sepúlveda M (2007) Ecotoxicological effects of endocrine disrupting compounds on fish reproduction. In: Babin PJ, Cerdà J, Lubzens E (eds) The fish oocyte: from basic studies to biotechnological applications. Springer, Netherlands, pp 255–322

    Google Scholar 

  • Desbrow C, Routledge EJ, Brighty GC, Sumpter JP, Waldock M (1998) Identification of estrogenic chemicals in STW effluent: 1. Chemical fraction and in vitro biological screening. Environ Sci Technol 32:1549–1558

    Article  CAS  Google Scholar 

  • Ding JL (2005) Vitellogenesis and vitellogenin uptake into oocyte. In: Melamed P, Sherwood N (eds) Hormones and their receptors in fish reproduction. World Scientific Publishing Co. Pte. Ltd., Singapore, pp 254–276

    Chapter  Google Scholar 

  • Durhan EJ, Lambright C, Wilson V, Butterworth BC, Kuehl DW, Orando EF, Guillette LJ Jr, Gray LE, Ankley GT (2002) Evaluation of androstenedione as an androgenic component of river water downstream of a paper mill effluent. Environ Toxicol Chem 21:1973–1976

    Article  CAS  Google Scholar 

  • Flouriot G, Pakdel F, Valotaire Y (1996) Transcriptional and post-transcriptional regulation of rainbow trout estrogen receptor and vitellogenin gene expression. Mol Cell Endocrinol 124:173–183

    Article  CAS  Google Scholar 

  • Harrington RW Jr (1961) Oviparous hermaphroditic fish with internal self-fertilization. Science 134:1749–1750

    Article  Google Scholar 

  • Hiramatsu N, Cheek AO, Sullivan CV, Matsubara T, Hara A (2005) Vitellogenesis and endocrine disruption. In: Mommsen TP, Moon TW (eds) Biochemistry and molecular biology of fishes, vol 6. Elsevier, Amsterdam, p 562

    Google Scholar 

  • Hiramatsu N, Matsubara T, Fujita T, Sullivan CV, Hara A (2006) Multiple piscine vitellogenins: biomarkers of fish exposure to estrogenic endocrine disruptors in aquatic environments. Mar Biol 149:35–47

    Article  CAS  Google Scholar 

  • Jenkins R, Angus RA, McNatt H, Howell WM, Kemppainen JA, Kirk M, Wilson EM (2001) Identification of androstenedion in a river containing pulp and paper mill effluent. Environ Toxicol Chem 20:1325–1331

    Article  CAS  Google Scholar 

  • Johnstone R, Macintosh DJ, Wright RS (1983) Elimination of orally administered 17α Methyltestosterone by Oreochromis mossambicus (tilapia) and Salmo gairadneri (rainbow trout) juveniles. Aquaculture 35:249–257

    Article  CAS  Google Scholar 

  • Kanamori A, Yamamura A, Koshiba S, Lee JS, Orlando EF, Hori H (2006) Methyltestosterone efficiently induces male development in the self-fertilizing hermaphrodite fish, Kryptolebias marmoratus. Genesis 44:495–503

    Article  CAS  Google Scholar 

  • Kang IJ, Yokota H, Oshima Y, Tsuruda Y, Shimasaki Y, Honjo T (2008) The effects of methyltestosterone on the sexual development and reproduction of adult medaka (Oryzias latipes). Aquat Toxicol 87:37–46

    Article  CAS  Google Scholar 

  • Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance. Environ Sci Technol 36:1202–1211

    Article  CAS  Google Scholar 

  • Layton AC, Gregory BW, Seward JR, Schultz TW, Sayler GS (2000) Mineralization of steroidal hormones by biosolids in wastewater treatment systems in Tennessee USA. Environ Sci Technol 34:3925–3931

    Article  CAS  Google Scholar 

  • Lazier CB, Langley S, Ramsey NB, Wright JM (1996) Androgen inhibition of vitellogenin gene expression in tilapia (Oreochromis niloticus). Gen Comp Endocrinol 104:321–329

    Article  CAS  Google Scholar 

  • Lee Y-M, Seo JS, Kim I-C, Yoon Y-D, Lee J-S (2006) Endocrine disrupting chemicals (bisphenol A, 4-nonylphenol, 4-tert-octylphenol) modulate expression of two distinct cytochrome P450 armatase genes differently in gender types of the hermaphrodite fish Rivulus marmoratus. Biochem Biophys Res Commun 345:894–903

    Article  CAS  Google Scholar 

  • Macintosh DJ (2008) Risks associated with using methyl testosterone in tilapia farming. Desde http://media.sustainablefish.org/MT_WP.pdf. Accessed 10 March 2013

  • Menuet A, Adrio F, Pakdel F (2005) Regulation and function of estrogen receptors: Comparative aspects. In: Melamed P, Sherwood N (eds) Hormones and their receptors in fish reproduction. World Scientific Publishing Co. Pte. Ltd., Singapore, pp 224–253

    Chapter  Google Scholar 

  • Mommsen TP, Walsh PJ (1988) Vitellogenesis and oocyte assembly. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol XI., aAcademic Press, New York, pp 347–406

    Google Scholar 

  • Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229

    CAS  Google Scholar 

  • Pawlowski S, Sauer A, Shears JA, Tyler CR, Braunbeck T (2004) Androgenic and estrogenic effects of the synthetic androgen 17α-methyltestosterone on sexual development and reproductive performance in the fathead minnow (Pimephales promelas) determined using the gonadal recrudescence assay. Aquat Toxicol 68:277–291

    Article  CAS  Google Scholar 

  • Phumyu N, Boonanuntanasarn S, Jangprai A, Yoshizaki G (2012) Pubertal effects of 17α-methyltestosterone on GH-IGH-related genes of the hypothalamic-pituitary-liver-gonadal axis and other biological parameters in male, female and sex-reversed Nile tilapia. Gen Comp Endocrinol 177:278–292

    Article  CAS  Google Scholar 

  • Sakakura Y, Noakes DLG (2000) Age, growth, and sexual development in the self-fertilizing hermaphroditic fish Rivulus marmoratus. Environ Biol Fishes 59:309–317

    Article  Google Scholar 

  • Seo JS, Lee Y-M, Jung SO, Kim I-C, Yoon Y-D, Lee J-S (2006) Nonylphenol modulates expression of androgen receptor and estrogen receptor genes differently in gender types of the hermaphroditic fish Rivulus marmoratus. Biochem Biophys Res Commun 346:213–223

    Article  CAS  Google Scholar 

  • Sharpe RL, MacLatchy DL, Courtenay SC, Van Der Kraak GJ (2004) Effects of a model androgen (methyl testosterone) and a model anti-androgen (cyproterone acetate) on reproductive endocrine endpoints in a short-term adult mummichog (Fundulus heteroclitus) bioassay. Aquat Toxicol 67:203–215

    Article  CAS  Google Scholar 

  • Soto CG, Leatherland JF, Noakes DLG (1992) Gonadal histology in the self-fertilization hermaphroditic fish Rivulus marmoratus (Pisces, Cyprinodontidae). Can J Zool 70:2338–2347

    Article  Google Scholar 

  • Sumpter JP (2005) Endocrine disrupters in the aquatic environment: an overview. Acta Hydrochim Hydrobiol 33:9–16

    Article  CAS  Google Scholar 

  • USEPA (U.S. Environmental Protection Agency), 2002. Draft detailed review paper on a fish two-generation toxicity test. EPA/68/W-01/023, U.S. Environmental Protection Agency, Washington

  • West G (1990) Methods of assessing ovarian development in fishes: a review. Aust J Mar Fresh Res 41:199–222

    Article  Google Scholar 

Download references

Acknowledgments

Part of this work was supported by Core Research for Evolutional Science and Technology (CREST), “Innovative Technology and Systems for Sustainable Water Use Research Area” of the Japan Science and Technology Agency.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chang-Beom Park.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, CB., Soyano, K., Kiros, S. et al. Transient effects of methyltestosterone injection on different reproductive parameters of the hermaphrodite fish Kryptolebias marmoratus . Ecotoxicology 22, 1145–1154 (2013). https://doi.org/10.1007/s10646-013-1101-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-013-1101-x

Keywords

Navigation