Initiation of sex change and gonadal gene expression in black sea bass (Centropristis striata) exposed to exemestane, an aromatase inhibitor

Many teleost fishes exhibit sequential hermaphroditism, where male or female gonads develop first and later undergo sex change. Model sex change species are characterized by social hierarchies and coloration changes, which enable experimental manipulations to better understand these processes. Howev...

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Bibliographic Details
Published in:Comparative biochemistry and physiology. Part A, Molecular & integrative physiology Molecular & integrative physiology, 2019-02, Vol.228, p.51-61
Main Authors: Breton, Timothy S., Kenter, Linas W., Greenlaw, Katherine, Montgomery, Jacob, Goetz, Giles W., Berlinsky, David L., Luckenbach, J. Adam
Format: Article
Language:English
Subjects:
Androstadienes - pharmacology
Animals
Apoptosis - genetics
Aromatase
Aromatase Inhibitors - pharmacology
Atresia
Bass - growth & development
Black Sea bass
Estrogen
Exemestane
Female
Gene Expression - drug effects
Hermaphroditism
Male
Ovary - drug effects
Ovary - metabolism
Protogynous
RNA, Messenger - metabolism
Sex change
Sex Differentiation - drug effects
Testis - drug effects
Testis - metabolism
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Summary:Many teleost fishes exhibit sequential hermaphroditism, where male or female gonads develop first and later undergo sex change. Model sex change species are characterized by social hierarchies and coloration changes, which enable experimental manipulations to better understand these processes. However, other species such as the protogynous black sea bass (Centropristis striata) do not exhibit these characteristics and instead receive research attention due to their importance in fisheries or aquaculture. Black sea bass social structure is unknown, which makes sex change sampling difficult, and few molecular resources are available. The purpose of the present study was to induce sex change using exemestane, an aromatase inhibitor, and assess gonadal gene expression using sex markers (amh, zpc2) and genes involved in steroidogenesis (cyp19a1a, cyp11b), estrogen signaling (esr1, esr2b), and apoptosis or atresia (aen, casp9, fabp11, parg, pdcd4, rif1). Overall, dietary exemestane treatment was effective, and most exposed females exhibited early histological signs of sex change and significantly higher rates of ovarian atresia relative to control females. Genes associated with atresia did not reflect this, however, as expression patterns in sex changing gonads were overall similar to those of ovaries, likely due to a whole ovary dilution effect of the RNA. Still, small but insignificant expression decreases during early sex change were detected for ovary-related genes (aen, casp9, fabp11, zpc2) and anti-apoptotic factors (parg, rif1). Exemestane treatment did not impact spermatogenesis or testicular gene expression, but testes were generally characterized by elevated steroidogenic enzyme and estrogen receptor mRNAs. Further research will be needed to understand these processes in black sea bass, using isolated ovarian follicles and multiple stages of sex change. •Exemestane induced the initiation of female-to-male sex change in black sea bass.•Exemestane-exposed females exhibited significantly greater ovarian atresia than control fish.•Males did not exhibit gonadal effects from exemestane treatment.•All testes exhibited elevated steroidogenic enzyme and estrogen receptor mRNAs.•Small decreases in apoptosis-related mRNAs were evident in sex changing gonads.
ISSN:1095-6433
1531-4332
DOI:10.1016/j.cbpa.2018.10.024