MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckii

Abstract Background Sex differentiation can be viewed as a controlled regulatory balance between sex differentiation-related mRNAs and post-transcriptional mechanisms mediated by non-coding RNAs. In mammals, increasing evidence has been reported regarding the importance of gonad-specific microRNAs (...

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Main Authors: Xiujuan Zhang, Wenhua Wu, Jiabin Zhou, Linmiao Li, Haiying Jiang, Jinping Chen
Format: Article
Language:English
Published: BMC 2022-09-01
Series:Frontiers in Zoology
Subjects:
Online Access:https://doi.org/10.1186/s12983-022-00469-6
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author Xiujuan Zhang
Wenhua Wu
Jiabin Zhou
Linmiao Li
Haiying Jiang
Jinping Chen
author_facet Xiujuan Zhang
Wenhua Wu
Jiabin Zhou
Linmiao Li
Haiying Jiang
Jinping Chen
author_sort Xiujuan Zhang
collection DOAJ
description Abstract Background Sex differentiation can be viewed as a controlled regulatory balance between sex differentiation-related mRNAs and post-transcriptional mechanisms mediated by non-coding RNAs. In mammals, increasing evidence has been reported regarding the importance of gonad-specific microRNAs (miRNAs) in sex differentiation. Although many fishes express a large number of gonadal miRNAs, the effects of these sex-biased miRNAs on sex differentiation in teleost fish remain unknown. Previous studies have shown the exclusive and sexually dimorphic expression of miR-34b/c in the gonads of the Amur sturgeon (Acipenser schrenckii), suggesting its potential role in the sex differentiation process. Results Using quantitative real-time PCR (qPCR), we observed that miR-34b/c showed consistent spatiotemporal expression patterns; the expression levels significantly increased during early sex differentiation. Using in situ hybridization, miR-34c was found to be located in the germ cells. In primary germ cells in vitro, the group subjected to overexpression and inhibition of miR-34c showed significantly higher proliferation ability and lower apoptosis, respectively, compared to the corresponding control group. Luciferase reporter assays using the ar-3′UTR-psiCHECK-2 luciferase vector suggested a targeted regulatory interaction between miR-34b/c and the 3′UTR of the androgen receptor (ar) mRNA. Furthermore, miR-34b/c and ar showed negative expression patterns during early sex differentiation. Additionally, a negative feedback regulation pattern was observed between foxl2 expression in the ovaries and amh and sox9 expression in the testes during early sex differentiation. Conclusions This study sheds new light on the roles of miR-34b/c in gonad development of Amur sturgeon, and provides the first comprehensive evidence that the gonad-predominant microRNAs may have a major role in sex differentiation in teleost fish.
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spelling doaj.art-e74d0790b4fa4bfe90f2d8b106c031cf2022-12-22T04:28:55ZengBMCFrontiers in Zoology1742-99942022-09-0119111710.1186/s12983-022-00469-6MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckiiXiujuan Zhang0Wenhua Wu1Jiabin Zhou2Linmiao Li3Haiying Jiang4Jinping Chen5Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of SciencesHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery SciencesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of SciencesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of SciencesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of SciencesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of SciencesAbstract Background Sex differentiation can be viewed as a controlled regulatory balance between sex differentiation-related mRNAs and post-transcriptional mechanisms mediated by non-coding RNAs. In mammals, increasing evidence has been reported regarding the importance of gonad-specific microRNAs (miRNAs) in sex differentiation. Although many fishes express a large number of gonadal miRNAs, the effects of these sex-biased miRNAs on sex differentiation in teleost fish remain unknown. Previous studies have shown the exclusive and sexually dimorphic expression of miR-34b/c in the gonads of the Amur sturgeon (Acipenser schrenckii), suggesting its potential role in the sex differentiation process. Results Using quantitative real-time PCR (qPCR), we observed that miR-34b/c showed consistent spatiotemporal expression patterns; the expression levels significantly increased during early sex differentiation. Using in situ hybridization, miR-34c was found to be located in the germ cells. In primary germ cells in vitro, the group subjected to overexpression and inhibition of miR-34c showed significantly higher proliferation ability and lower apoptosis, respectively, compared to the corresponding control group. Luciferase reporter assays using the ar-3′UTR-psiCHECK-2 luciferase vector suggested a targeted regulatory interaction between miR-34b/c and the 3′UTR of the androgen receptor (ar) mRNA. Furthermore, miR-34b/c and ar showed negative expression patterns during early sex differentiation. Additionally, a negative feedback regulation pattern was observed between foxl2 expression in the ovaries and amh and sox9 expression in the testes during early sex differentiation. Conclusions This study sheds new light on the roles of miR-34b/c in gonad development of Amur sturgeon, and provides the first comprehensive evidence that the gonad-predominant microRNAs may have a major role in sex differentiation in teleost fish.https://doi.org/10.1186/s12983-022-00469-6Amur sturgeon (Acipenser schrenckii)miR-34bmiR-34cSex differentiationGerm cell culture
spellingShingle Xiujuan Zhang
Wenhua Wu
Jiabin Zhou
Linmiao Li
Haiying Jiang
Jinping Chen
MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckii
Frontiers in Zoology
Amur sturgeon (Acipenser schrenckii)
miR-34b
miR-34c
Sex differentiation
Germ cell culture
title MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckii
title_full MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckii
title_fullStr MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckii
title_full_unstemmed MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckii
title_short MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckii
title_sort mir 34b c play a role in early sex differentiation of amur sturgeon acipenser schrenckii
topic Amur sturgeon (Acipenser schrenckii)
miR-34b
miR-34c
Sex differentiation
Germ cell culture
url https://doi.org/10.1186/s12983-022-00469-6
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