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Regulation of Miwi-mediated mRNA stabilization by Ck137956/Tssa is essential for male fertility

BACKGROUND: Sperm is formed through spermiogenesis, a highly complex process involving chromatin condensation that results in cessation of transcription. mRNAs required for spermiogenesis are transcribed at earlier stages and translated in a delayed fashion during spermatid formation. However, it re...

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Autores principales: Chen, Yu, Zhang, Xiangzheng, Jiang, Jiayin, Luo, Mengjiao, Tu, Haixia, Xu, Chen, Tan, Huanhuan, Zhou, Xin, Chen, Hong, Han, Xudong, Yue, Qiuling, Guo, Yueshuai, Zheng, Ke, Qi, Yaling, Situ, Chenghao, Cui, Yiqiang, Guo, Xuejiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10111675/
https://www.ncbi.nlm.nih.gov/pubmed/37069605
http://dx.doi.org/10.1186/s12915-023-01589-z
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author Chen, Yu
Zhang, Xiangzheng
Jiang, Jiayin
Luo, Mengjiao
Tu, Haixia
Xu, Chen
Tan, Huanhuan
Zhou, Xin
Chen, Hong
Han, Xudong
Yue, Qiuling
Guo, Yueshuai
Zheng, Ke
Qi, Yaling
Situ, Chenghao
Cui, Yiqiang
Guo, Xuejiang
author_facet Chen, Yu
Zhang, Xiangzheng
Jiang, Jiayin
Luo, Mengjiao
Tu, Haixia
Xu, Chen
Tan, Huanhuan
Zhou, Xin
Chen, Hong
Han, Xudong
Yue, Qiuling
Guo, Yueshuai
Zheng, Ke
Qi, Yaling
Situ, Chenghao
Cui, Yiqiang
Guo, Xuejiang
author_sort Chen, Yu
collection PubMed
description BACKGROUND: Sperm is formed through spermiogenesis, a highly complex process involving chromatin condensation that results in cessation of transcription. mRNAs required for spermiogenesis are transcribed at earlier stages and translated in a delayed fashion during spermatid formation. However, it remains unknown that how these repressed mRNAs are stabilized. RESULTS: Here we report a Miwi-interacting testis-specific and spermiogenic arrest protein, Ck137956, which we rename Tssa. Deletion of Tssa led to male sterility and absence of sperm formation. The spermiogenesis arrested at the round spermatid stage and numerous spermiogenic mRNAs were down-regulated in Tssa(−/−) mice. Deletion of Tssa disrupted the localization of Miwi to chromatoid body, a specialized assembly of cytoplasmic messenger ribonucleoproteins (mRNPs) foci present in germ cells. We found that Tssa interacted with Miwi in repressed mRNPs and stabilized Miwi-interacting spermiogenesis-essential mRNAs. CONCLUSIONS: Our findings indicate that Tssa is indispensable in male fertility and has critical roles in post-transcriptional regulations by interacting with Miwi during spermiogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01589-z.
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spelling pubmed-101116752023-04-19 Regulation of Miwi-mediated mRNA stabilization by Ck137956/Tssa is essential for male fertility Chen, Yu Zhang, Xiangzheng Jiang, Jiayin Luo, Mengjiao Tu, Haixia Xu, Chen Tan, Huanhuan Zhou, Xin Chen, Hong Han, Xudong Yue, Qiuling Guo, Yueshuai Zheng, Ke Qi, Yaling Situ, Chenghao Cui, Yiqiang Guo, Xuejiang BMC Biol Research Article BACKGROUND: Sperm is formed through spermiogenesis, a highly complex process involving chromatin condensation that results in cessation of transcription. mRNAs required for spermiogenesis are transcribed at earlier stages and translated in a delayed fashion during spermatid formation. However, it remains unknown that how these repressed mRNAs are stabilized. RESULTS: Here we report a Miwi-interacting testis-specific and spermiogenic arrest protein, Ck137956, which we rename Tssa. Deletion of Tssa led to male sterility and absence of sperm formation. The spermiogenesis arrested at the round spermatid stage and numerous spermiogenic mRNAs were down-regulated in Tssa(−/−) mice. Deletion of Tssa disrupted the localization of Miwi to chromatoid body, a specialized assembly of cytoplasmic messenger ribonucleoproteins (mRNPs) foci present in germ cells. We found that Tssa interacted with Miwi in repressed mRNPs and stabilized Miwi-interacting spermiogenesis-essential mRNAs. CONCLUSIONS: Our findings indicate that Tssa is indispensable in male fertility and has critical roles in post-transcriptional regulations by interacting with Miwi during spermiogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01589-z. BioMed Central 2023-04-17 /pmc/articles/PMC10111675/ /pubmed/37069605 http://dx.doi.org/10.1186/s12915-023-01589-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Chen, Yu
Zhang, Xiangzheng
Jiang, Jiayin
Luo, Mengjiao
Tu, Haixia
Xu, Chen
Tan, Huanhuan
Zhou, Xin
Chen, Hong
Han, Xudong
Yue, Qiuling
Guo, Yueshuai
Zheng, Ke
Qi, Yaling
Situ, Chenghao
Cui, Yiqiang
Guo, Xuejiang
Regulation of Miwi-mediated mRNA stabilization by Ck137956/Tssa is essential for male fertility
title Regulation of Miwi-mediated mRNA stabilization by Ck137956/Tssa is essential for male fertility
title_full Regulation of Miwi-mediated mRNA stabilization by Ck137956/Tssa is essential for male fertility
title_fullStr Regulation of Miwi-mediated mRNA stabilization by Ck137956/Tssa is essential for male fertility
title_full_unstemmed Regulation of Miwi-mediated mRNA stabilization by Ck137956/Tssa is essential for male fertility
title_short Regulation of Miwi-mediated mRNA stabilization by Ck137956/Tssa is essential for male fertility
title_sort regulation of miwi-mediated mrna stabilization by ck137956/tssa is essential for male fertility
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10111675/
https://www.ncbi.nlm.nih.gov/pubmed/37069605
http://dx.doi.org/10.1186/s12915-023-01589-z
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