RNA binding protein HuR regulated by OIP5-AS1 may be involved in maternal transcript degradation during the human maternal-to-zygotic transition

Abstract Background The maternal-to-zygotic transition (MZT) is a critical process in early human development, involving the degradation of maternal gene transcripts and activation of zygotic genes. Any disruption in the degradation of maternal transcripts may be associated with some reproductive di...

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Main Authors: Yan-na Liu, Ke-Yi Li, Hao Wei, Wen-xiu Li, Yue-hua Zhang, Jia-jun Qiu, Fanyi Zeng, Jing-bin Yan
Format: Article
Language:English
Published: BMC 2025-07-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-025-11807-3
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author Yan-na Liu
Ke-Yi Li
Hao Wei
Wen-xiu Li
Yue-hua Zhang
Jia-jun Qiu
Fanyi Zeng
Jing-bin Yan
author_facet Yan-na Liu
Ke-Yi Li
Hao Wei
Wen-xiu Li
Yue-hua Zhang
Jia-jun Qiu
Fanyi Zeng
Jing-bin Yan
author_sort Yan-na Liu
collection DOAJ
description Abstract Background The maternal-to-zygotic transition (MZT) is a critical process in early human development, involving the degradation of maternal gene transcripts and activation of zygotic genes. Any disruption in the degradation of maternal transcripts may be associated with some reproductive disorders. However, the precise mechanism by which maternal gene transcripts are degraded during this transition remains unclear. Results Through an analysis of weighted gene co-expression networks, an oocyte-specific module was identified, showing high consistency with the expression pattern of maternal transcripts degraded at the 8-cell stage, which is associated with the cell cycle and transcription factor binding. Within this module, a maternal long non-coding RNA known as OIP5 antisense RNA 1 (OIP5-AS1) was identified. It was observed that OIP5-AS1 can bind to the RNA binding protein human antigen R (HuR), potentially limiting its availability for other mRNAs and contributing to the degradation of maternal transcripts during MZT. Moreover, RNA immunoprecipitation sequencing in human induced pluripotent stem cells (iPSCs) revealed HuR and OIP5-AS1 are likely to tightly bind together and involved in functions related to the cell cycle and transcriptional regulation. Upon knocking down OIP5-AS1 and the ELAVL1 gene, which encodes the HuR protein in human iPSCs, a significant reduction in the expression levels of maternal transcripts was observed, suggesting an essential role of these factors in regulating maternal transcript stability during early development. Conclusions The HuR protein plays a critical role in influencing the degradation of maternal transcripts during the MZT in early human embryonic development. Understanding the role of OIP5-AS1 in regulating HuR protein could provide valuable insights into developmental biology and potentially lead to new therapeutic strategies for developmental disorders.
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spelling doaj-art-95c1ac1687ba4f11872c6f4e27a600d72025-08-20T04:01:24ZengBMCBMC Genomics1471-21642025-07-0126111410.1186/s12864-025-11807-3RNA binding protein HuR regulated by OIP5-AS1 may be involved in maternal transcript degradation during the human maternal-to-zygotic transitionYan-na Liu0Ke-Yi Li1Hao Wei2Wen-xiu Li3Yue-hua Zhang4Jia-jun Qiu5Fanyi Zeng6Jing-bin Yan7Shanghai Children’s Hospital, Shanghai Institute of Medical Genetics, Shanghai Jiao Tong University School of MedicineBio-X Institutes, Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Shanghai Jiao Tong UniversityShanghai Children’s Hospital, Shanghai Institute of Medical Genetics, Shanghai Jiao Tong University School of MedicineShanghai Children’s Hospital, Shanghai Institute of Medical Genetics, Shanghai Jiao Tong University School of MedicineShanghai Children’s Hospital, Shanghai Institute of Medical Genetics, Shanghai Jiao Tong University School of MedicineShanghai Children’s Hospital, Shanghai Institute of Medical Genetics, Shanghai Jiao Tong University School of MedicineShanghai Children’s Hospital, Shanghai Institute of Medical Genetics, Shanghai Jiao Tong University School of MedicineShanghai Children’s Hospital, Shanghai Institute of Medical Genetics, Shanghai Jiao Tong University School of MedicineAbstract Background The maternal-to-zygotic transition (MZT) is a critical process in early human development, involving the degradation of maternal gene transcripts and activation of zygotic genes. Any disruption in the degradation of maternal transcripts may be associated with some reproductive disorders. However, the precise mechanism by which maternal gene transcripts are degraded during this transition remains unclear. Results Through an analysis of weighted gene co-expression networks, an oocyte-specific module was identified, showing high consistency with the expression pattern of maternal transcripts degraded at the 8-cell stage, which is associated with the cell cycle and transcription factor binding. Within this module, a maternal long non-coding RNA known as OIP5 antisense RNA 1 (OIP5-AS1) was identified. It was observed that OIP5-AS1 can bind to the RNA binding protein human antigen R (HuR), potentially limiting its availability for other mRNAs and contributing to the degradation of maternal transcripts during MZT. Moreover, RNA immunoprecipitation sequencing in human induced pluripotent stem cells (iPSCs) revealed HuR and OIP5-AS1 are likely to tightly bind together and involved in functions related to the cell cycle and transcriptional regulation. Upon knocking down OIP5-AS1 and the ELAVL1 gene, which encodes the HuR protein in human iPSCs, a significant reduction in the expression levels of maternal transcripts was observed, suggesting an essential role of these factors in regulating maternal transcript stability during early development. Conclusions The HuR protein plays a critical role in influencing the degradation of maternal transcripts during the MZT in early human embryonic development. Understanding the role of OIP5-AS1 in regulating HuR protein could provide valuable insights into developmental biology and potentially lead to new therapeutic strategies for developmental disorders.https://doi.org/10.1186/s12864-025-11807-3Early embryonic developmentLong non-coding RNAsMaternal transcript degradationRNA binding proteinMaternal-to-zygotic transition
spellingShingle Yan-na Liu
Ke-Yi Li
Hao Wei
Wen-xiu Li
Yue-hua Zhang
Jia-jun Qiu
Fanyi Zeng
Jing-bin Yan
RNA binding protein HuR regulated by OIP5-AS1 may be involved in maternal transcript degradation during the human maternal-to-zygotic transition
BMC Genomics
Early embryonic development
Long non-coding RNAs
Maternal transcript degradation
RNA binding protein
Maternal-to-zygotic transition
title RNA binding protein HuR regulated by OIP5-AS1 may be involved in maternal transcript degradation during the human maternal-to-zygotic transition
title_full RNA binding protein HuR regulated by OIP5-AS1 may be involved in maternal transcript degradation during the human maternal-to-zygotic transition
title_fullStr RNA binding protein HuR regulated by OIP5-AS1 may be involved in maternal transcript degradation during the human maternal-to-zygotic transition
title_full_unstemmed RNA binding protein HuR regulated by OIP5-AS1 may be involved in maternal transcript degradation during the human maternal-to-zygotic transition
title_short RNA binding protein HuR regulated by OIP5-AS1 may be involved in maternal transcript degradation during the human maternal-to-zygotic transition
title_sort rna binding protein hur regulated by oip5 as1 may be involved in maternal transcript degradation during the human maternal to zygotic transition
topic Early embryonic development
Long non-coding RNAs
Maternal transcript degradation
RNA binding protein
Maternal-to-zygotic transition
url https://doi.org/10.1186/s12864-025-11807-3
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