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10.3390/genes14040946
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Article

Intrafollicular Retinoic Acid Signaling Is Important for Luteinizing Hormone-Induced Oocyte Meiotic Resumption

by
Fupeng Wang
†,
Yawen Tang
†,
Yijie Cai
,
Ran Yang
,
Zongyu Wang
,
Xiaodong Wang
,
Qianying Yang
,
Wenjing Wang
,
Jianhui Tian
and
Lei An
*
State Key Laboratory of Animal Biotech Breeding, National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, China Agricultural University, No. 2 Yuanmingyuan West Road, Beijing 100193, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to the work.
Genes 2023, 14(4), 946; https://doi.org/10.3390/genes14040946
Submission received: 28 February 2023 / Revised: 15 April 2023 / Accepted: 16 April 2023 / Published: 20 April 2023
(This article belongs to the Special Issue Genetic Regulation of Animal Reproduction)
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Abstract

It has been clear that retinoic acid (RA), the most active vitamin A (VA) derivative, plays a central role in governing oocyte meiosis initiation. However, it has not been functionally determined if RA participates in luteinizing hormone (LH)-induced resumption from long-lasting oocyte meiotic arrest, which is essential for haploid oocyte formation. In the present study, using well-established in vivo and in vitro models, we identified that intrafollicular RA signaling is important for normal oocyte meiotic resumption. A mechanistic study indicated that mural granulosa cells (MGCs) are the indispensable follicular compartment for RA-prompted meiotic resumption. Moreover, retinoic acid receptor (RAR) is essential for mediating RA signaling to regulate meiotic resumption. Furthermore, we found zinc finger protein 36 (ZFP36) is the transcriptional target of RAR. Both RA signaling and epidermal growth factor (EGF) signaling were activated in MGCs in response to LH surge, and two intrafollicular signalings cooperate to induce rapid Zfp36 upregulation and Nppc mRNA decrease, which is critical to LH-induced meiotic resumption. These findings extend our understanding of the role of RA in oocyte meiosis: RA not only governs meiotic initiation but also regulates LH-induced meiotic resumption. We also emphasize the importance of LH-induced metabolic changes in MGCs in this process.
Keywords: LH; Retinoic acid; EGF; oocyte meiotic resumption; C-natriuretic peptide; zinc finger protein 36 LH; Retinoic acid; EGF; oocyte meiotic resumption; C-natriuretic peptide; zinc finger protein 36

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MDPI and ACS Style

Wang, F.; Tang, Y.; Cai, Y.; Yang, R.; Wang, Z.; Wang, X.; Yang, Q.; Wang, W.; Tian, J.; An, L. Intrafollicular Retinoic Acid Signaling Is Important for Luteinizing Hormone-Induced Oocyte Meiotic Resumption. Genes 2023, 14, 946. https://doi.org/10.3390/genes14040946

AMA Style

Wang F, Tang Y, Cai Y, Yang R, Wang Z, Wang X, Yang Q, Wang W, Tian J, An L. Intrafollicular Retinoic Acid Signaling Is Important for Luteinizing Hormone-Induced Oocyte Meiotic Resumption. Genes. 2023; 14(4):946. https://doi.org/10.3390/genes14040946

Chicago/Turabian Style

Wang, Fupeng, Yawen Tang, Yijie Cai, Ran Yang, Zongyu Wang, Xiaodong Wang, Qianying Yang, Wenjing Wang, Jianhui Tian, and Lei An. 2023. "Intrafollicular Retinoic Acid Signaling Is Important for Luteinizing Hormone-Induced Oocyte Meiotic Resumption" Genes 14, no. 4: 946. https://doi.org/10.3390/genes14040946

APA Style

Wang, F., Tang, Y., Cai, Y., Yang, R., Wang, Z., Wang, X., Yang, Q., Wang, W., Tian, J., & An, L. (2023). Intrafollicular Retinoic Acid Signaling Is Important for Luteinizing Hormone-Induced Oocyte Meiotic Resumption. Genes, 14(4), 946. https://doi.org/10.3390/genes14040946

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