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Identification, functional characterization, and estrogen regulation on gonadotropin-releasing hormone in the spotted scat, Scatophagus argus

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Abstract

Gonadotropin-releasing hormone (GnRH) is a key neuropeptide of the reproductive system. However, little is known about the role of GnRH in the spotted scat (Scatophagus argus). Here, three GnRH subtypes (cGnRH-II, sGnRH, and sbGnRH) were identified in the spotted scat. cGnRH-II and sGnRH were only expressed in the brains and gonads of both male and female fish, exhibiting a tissue-specific expression pattern, while sbGnRH was expressed at different transcription levels in all examined tissues. During ovarian maturation, hypothalamus-associated sbGnRH was upregulated, while the expression of sGnRH was variable and cGnRH-II first increased and then decreased. In vivo experiments showed that sbGnRH significantly promoted the expression of fsh and lh genes in a dose-dependent manner and exhibited a desensitization effect on lh expression at high concentrations. For sGnRH and cGnRH-II, only high concentrations could induce fsh and lh expression. Furthermore, treatment with highly concentrated sbGnRH peptide also induced fsh and lh expression, whereas the sGnRH and cGnRH-II peptides only induced fsh expression in vitro. 17β-Estradiol (E2) significantly inhibited the expression of sbGnRH mRNA in a dose-dependent manner and did not impact sGnRH and cGnRH-II mRNA levels in vivo or in vitro. The inhibitory effect of E2 on sbGnRH expression was attenuated by the estrogen receptor (ER) broad-spectrum antagonist (fulvestrant) and the ERα-specific antagonist (methyl-piperidinopyrazole), respectively, implying that the feedback regulation on sbGnRH is mediated via ERα. This study provides a theoretical basis for the reproductive endocrinology of the spotted scat by studying GnRH.

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Abbreviations

ER:

Estrogen receptors

E2 :

17β-Estradiol

GnRH:

Gonadotropin-releasing hormone

GtH:

Gonadotropin

LH:

Luteinizing hormone

FSH:

Follicle-stimulating hormone

sGnRH:

Salmon GnRH

cGnRH-II:

Chicken GnRH-II

sbGnRH:

Seabream GnRH

ERα:

Estrogen receptor alpha

gbw:

Gram body weight

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Funding

This study was supported by grants from Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang) (ZJW-2019-06), National Key R&D Program of China (2018YFD0901203), Special key projects of Guangdong science and Technology Department’s science and technology innovation strategy (2018B030311050), National Natural Science Foundation of China (Nos. 41706174 and 31702326) and Guangdong South China Sea Key Laboratory of Aquaculture for Aquatic Economic Animals, Guangdong Ocean University (No. KFKT2019ZD07).

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Contributions

Experiments were designed by HC, SL, and GL; HC and XC performed the experiments; HC, YW, and YZ analyzed the data; CT, DJ, and ZL contributed to reagent preparation; HC and XC prepared the original manuscript draft; CZ, YZ, and GL reviewed and edited the manuscript; HC and GL conducted project administration.

Corresponding authors

Correspondence to Shui-sheng Li or Guang-li Li.

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Animal ethics

All animal experiments throughout the study were conducted in accordance with the Regulations for the Administration of Affairs Concerning Experimental Animals for the Science and Technology Bureau of China.

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The authors declare that they have no conflict of interest.

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Chen, Hp., Cui, Xf., Wang, Yr. et al. Identification, functional characterization, and estrogen regulation on gonadotropin-releasing hormone in the spotted scat, Scatophagus argus. Fish Physiol Biochem 46, 1743–1757 (2020). https://doi.org/10.1007/s10695-020-00825-5

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  • DOI: https://doi.org/10.1007/s10695-020-00825-5

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