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Effects of gonadotropins, 11-ketotestosterone, and insulin-like growth factor-1 on target gene expression and growth of previtellogenic oocytes from shortfinned eels, Anguilla australis, in vitro

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Abstract

Pituitary gonadotropins, metabolic hormones, and sex steroids are known factors affecting the advanced stages of ovarian development in teleost fish. However, the effects of these hormones and of the interactions between them on the growth of previtellogenic ovarian follicles are not known. In order to address this void in understanding, previtellogenic ovarian fragments from eel, Anguilla australis, were incubated in vitro with recombinant Japanese eel follicle-stimulating hormone (rec-Fsh), human chorionic gonadotropin (hCG), or 11-ketotestosterone (11-KT) in the presence or absence of recombinant human insulin-like growth factor-1 (IGF1). The results of long-term in vitro culture (21 days) demonstrated that rec-Fsh and 11-KT, rather than hCG, caused significant increases in the diameter of previtellogenic oocytes. Meanwhile, only 11-KT induced a significant increase in lipid accumulation. Moreover, a greater effect on oocyte growth was observed when IGF1 supplementation was combined with 11-KT rather than with rec-Fsh or hCG. For short-term culture (24 h), treatment with 11-KT in the presence or absence of IGF1 had no significant effects on mRNA levels of target genes (lhr, cyp19, cyp11b, lpl, and ldr) except for upregulation of fshr. There were no significant effects of rec-Fsh on expression of any target gene, whereas hCG downregulated the expression of these genes. There was no evidence for any interaction between the gonadotropins and IGF1 that resulted in growth of previtellogenic oocytes. Taken together, these results suggest that hormones from both the reproductive and the metabolic axes regulate the growth of previtellogenic oocytes in Anguilla australis.

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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We acknowledge the help from Ken Miller with preparation of the illustrations and we are grateful to Professor Sally McCormick (Department of Biochemistry, University of Otago) for the use of the ultracentrifuge.

Funding

The leading author of this study was supported by a New Zealand ASEAN scholarship. Contributions to research expenses were made by a Research Enhancement Grant (2016 PBRF support to PML).

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Authors and Affiliations

  1. University of Agriculture and Forestry, Hue University, 6 Le Loi Street, Hue, Vietnam

    Anh Tuan Nguyen

  2. Department of Zoology, University of Otago, 340 Great King Street, PO Box 56, Dunedin, 9054, New Zealand

    Anh Tuan Nguyen, Erin L. Damsteegt, Jolyn H. Z. Chia & P. Mark Lokman

  3. Fisheries Technology Institute, Japan Fisheries Research and Education Agency, 183-2 Minamiizu, Kamo, Shizuoka, 415-0156, Japan

    Yukinori Kazeto

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  1. Anh Tuan Nguyen
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  5. P. Mark Lokman
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Contributions

These experiments were conceptualized and designed by PML, ATN, and ELD and conducted by ATN and JHZC; ATN and PML analyzed the data; YK provided rec-Fsh; the manuscript was drafted by ATN and edited and proof-read by ELD, JHZC, YK, and PML. All authors read and approved the final manuscript.

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Correspondence to Anh Tuan Nguyen.

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Animal handling and manipulations were approved and conducted in accordance with the guidelines of the University of Otago Animal Ethics Committee.

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Nguyen, A.T., Damsteegt, E.L., Chia, J.H.Z. et al. Effects of gonadotropins, 11-ketotestosterone, and insulin-like growth factor-1 on target gene expression and growth of previtellogenic oocytes from shortfinned eels, Anguilla australis, in vitro. Fish Physiol Biochem 48, 853–867 (2022). https://doi.org/10.1007/s10695-022-01090-4

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