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Two Foxo1 homologues in the orange-spotted grouper Epinephelus coioides: sequences, expression, and possible involvement in the activation of cyp19a1a expression in the ovary

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Abstract

Foxo1, a member of Foxo transcription factor family, is involved in a number of physiological processes including metabolism, cell cycle progression, aging, and apoptosis. In the ovarian granulosa cell of mouse, Foxo1 is implicated to inhibit the expression of Cyp19a1, a gene encoding the aromatase that converts androgens into estrogens. Currently, the information about the expression and physiological relevance of Foxo1 homologues in the ovary of teleosts is scarce. In the present study, cDNAs encoding two forms of Foxo1, Foxo1a and Foxo1b, were isolated from the orange-spotted grouper. Phylogenetic analysis indicated that the orange-spotted groupers Foxo1a and Foxo1b were closely related to the counterparts of the ricefield eel. RT-PCR analysis showed that the orange-spotted groupers foxo1a and foxo1b were expressed in a wide range of tissues, with high levels detected in the brain regions, liver, and intestine. Quantitative real-time PCR analysis showed similar expression profiles for cyp19a1a, foxo1a, and foxo1b in the ovary during development from the primary growth to mature stages, with peak values detected at the vitellogenic stage. In situ hybridization detected mRNA of foxo1a, foxo1b, and cyp19a1a in granulosa cells surrounding vitellogenic oocytes. In vitro transfection showed that both Foxo1a and Foxo1b upregulated the orange-spotted grouper cyp19a1a promoter activities, possibly through the conserved Foxo binding site. Collectively, these results suggest that both Foxo1a and Foxo1b may be involved in the regulation of the ovarian functions in the orange-spotted grouper and the physiological roles of Foxo1 homologues in the ovary may be diversified in vertebrates.

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Acknowledgements

We thank Guangdong Daya Bay Fishery Development Center (Huizhou City 516081, Guangdong, People’s Republic of China) for providing experimental fish.

Funding

This work was supported by Guangzhou Municipal Science and Technology Project (201804020013) and the National Natural Science Foundation of China (32072956, 31672638).

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All authors meet the authorship requirements. YN, LZ, and WZ conceived and designed the study. YN, MF, QL, HL, SQ, XC, FM, XL, XX, SS, and YZ carried out experiments and analyzed data. YN, LZ, and WZ drafted the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Lihong Zhang or Weimin Zhang.

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All experimental procedures and investigations were reviewed and approved by the Animal Research and Ethics Committees of Sun Yat-Sen University and were performed in accordance with the guidelines of the committee.

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All authors have read and approved the manuscript for submission to Fish Physiology and Biochemistry.

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The authors declare no competing interests.

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Ning, Y., Fan, M., Liu, Q. et al. Two Foxo1 homologues in the orange-spotted grouper Epinephelus coioides: sequences, expression, and possible involvement in the activation of cyp19a1a expression in the ovary. Fish Physiol Biochem 47, 1597–1610 (2021). https://doi.org/10.1007/s10695-021-01002-y

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  • DOI: https://doi.org/10.1007/s10695-021-01002-y

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