CircMYH9/miR-133a-3p/CXCR4 axis: a novel regulatory network in sperm fertilization and embryo development

Abstract This study aimed to investigate the influence of sperm miRNAs on fertilization rates (FR) in in vitro fertilization (IVF) and to explore potential regulatory mechanisms in sperm-mediated fertilization and embryo development. Through high-throughput sequencing, we identified differentially e...

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Main Authors: Qian Sun, Yanyu Li, Wen Yang, Wen Feng, Jiayun Zhou, Yijuan Cao, Bei Zhang, Zuobin Zhu, Conghui Han
Format: Article
Language:English
Published: Springer 2024-12-01
Series:Molecular Biomedicine
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Online Access:https://doi.org/10.1186/s43556-024-00236-5
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author Qian Sun
Yanyu Li
Wen Yang
Wen Feng
Jiayun Zhou
Yijuan Cao
Bei Zhang
Zuobin Zhu
Conghui Han
author_facet Qian Sun
Yanyu Li
Wen Yang
Wen Feng
Jiayun Zhou
Yijuan Cao
Bei Zhang
Zuobin Zhu
Conghui Han
author_sort Qian Sun
collection DOAJ
description Abstract This study aimed to investigate the influence of sperm miRNAs on fertilization rates (FR) in in vitro fertilization (IVF) and to explore potential regulatory mechanisms in sperm-mediated fertilization and embryo development. Through high-throughput sequencing, we identified differentially expressed miRNAs in sperm, with miR-133a-3p significantly upregulated in samples associated with low FR and available embryo rate (AER). Key regulatory circRNAs and mRNAs were further identified via the Starbase database, intersected with differentially expressed RNA, and analyzed through GO, KEGG, and PPI analyses. The circMYH9/miR-133a-3p/CXCR4 axis emerged as a critical regulatory network. In vitro assays using the GC-2 spd mouse spermatogenic cell line revealed that miR-133a-3p inhibited cell growth and proliferation while promoting apoptosis. circMYH9, acting as a competing endogenous RNA (ceRNA) for miR-133a-3p, modulated CXCR4 expression, enhancing GC-2 spd cell growth and inhibiting apoptosis through the miR-133a-3p/CXCR4 axis. In vivo experiments using a mouse model confirmed that circMYH9 overexpression increased IVF success rates and promoted embryo development via this axis. Mechanistically, miR-133a-3p suppresses sperm fertilization and embryo development by targeting the circMYH9/miR-133a-3p/CXCR4 axis. These findings suggest that this regulatory network could serve as a novel biomarker for assessing fertilization potential and embryo quality in clinical settings and as a potential therapeutic target to improve IVF outcomes and address infertility. This study provides valuable insights into the molecular mechanisms governing sperm function and early embryonic development.
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spelling doaj-art-ff8f196b90fd4e9088b4475a07b5d44e2024-12-15T12:05:14ZengSpringerMolecular Biomedicine2662-86512024-12-015111610.1186/s43556-024-00236-5CircMYH9/miR-133a-3p/CXCR4 axis: a novel regulatory network in sperm fertilization and embryo developmentQian Sun0Yanyu Li1Wen Yang2Wen Feng3Jiayun Zhou4Yijuan Cao5Bei Zhang6Zuobin Zhu7Conghui Han8Suzhou Medical College, Soochow UniversitySuzhou Medical College, Soochow UniversityDepartment of Gynecology, The First Affiliated Hospital of Kangda College of Nanjing Medical UniversityDepartment of Gynecology, The First Affiliated Hospital of Kangda College of Nanjing Medical UniversityDepartment of Gynecology, Xuzhou Central HospitalDepartment of Reproductive Medicine, Xuzhou Central HospitalSuzhou Medical College, Soochow UniversityXuzhou Engineering Research Center of Medical Genetics and Transformation, Key Laboratory of Genetic Foundation and Clinical Application, Department of Genetics, Xuzhou Medical UniversityClinical Medicine Postgraduate Workstation, Soochow UniversityAbstract This study aimed to investigate the influence of sperm miRNAs on fertilization rates (FR) in in vitro fertilization (IVF) and to explore potential regulatory mechanisms in sperm-mediated fertilization and embryo development. Through high-throughput sequencing, we identified differentially expressed miRNAs in sperm, with miR-133a-3p significantly upregulated in samples associated with low FR and available embryo rate (AER). Key regulatory circRNAs and mRNAs were further identified via the Starbase database, intersected with differentially expressed RNA, and analyzed through GO, KEGG, and PPI analyses. The circMYH9/miR-133a-3p/CXCR4 axis emerged as a critical regulatory network. In vitro assays using the GC-2 spd mouse spermatogenic cell line revealed that miR-133a-3p inhibited cell growth and proliferation while promoting apoptosis. circMYH9, acting as a competing endogenous RNA (ceRNA) for miR-133a-3p, modulated CXCR4 expression, enhancing GC-2 spd cell growth and inhibiting apoptosis through the miR-133a-3p/CXCR4 axis. In vivo experiments using a mouse model confirmed that circMYH9 overexpression increased IVF success rates and promoted embryo development via this axis. Mechanistically, miR-133a-3p suppresses sperm fertilization and embryo development by targeting the circMYH9/miR-133a-3p/CXCR4 axis. These findings suggest that this regulatory network could serve as a novel biomarker for assessing fertilization potential and embryo quality in clinical settings and as a potential therapeutic target to improve IVF outcomes and address infertility. This study provides valuable insights into the molecular mechanisms governing sperm function and early embryonic development.https://doi.org/10.1186/s43556-024-00236-5SpermCircMYH9miR-133a-3pCXCR4In vitro fertilization rateEmbryo development
spellingShingle Qian Sun
Yanyu Li
Wen Yang
Wen Feng
Jiayun Zhou
Yijuan Cao
Bei Zhang
Zuobin Zhu
Conghui Han
CircMYH9/miR-133a-3p/CXCR4 axis: a novel regulatory network in sperm fertilization and embryo development
Molecular Biomedicine
Sperm
CircMYH9
miR-133a-3p
CXCR4
In vitro fertilization rate
Embryo development
title CircMYH9/miR-133a-3p/CXCR4 axis: a novel regulatory network in sperm fertilization and embryo development
title_full CircMYH9/miR-133a-3p/CXCR4 axis: a novel regulatory network in sperm fertilization and embryo development
title_fullStr CircMYH9/miR-133a-3p/CXCR4 axis: a novel regulatory network in sperm fertilization and embryo development
title_full_unstemmed CircMYH9/miR-133a-3p/CXCR4 axis: a novel regulatory network in sperm fertilization and embryo development
title_short CircMYH9/miR-133a-3p/CXCR4 axis: a novel regulatory network in sperm fertilization and embryo development
title_sort circmyh9 mir 133a 3p cxcr4 axis a novel regulatory network in sperm fertilization and embryo development
topic Sperm
CircMYH9
miR-133a-3p
CXCR4
In vitro fertilization rate
Embryo development
url https://doi.org/10.1186/s43556-024-00236-5
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