NUSAP1 regulates mouse oocyte meiotic maturation

Author:

Yu Lina12,Kong Na13,Lin Yuling2,Qiu Panpan3,Xu Qian4,Zhang Yang3,Zhen Xin3,Yan Guijun3,Sun Haixiang2,Mei Jie13,Cao Guangyi135ORCID

Affiliation:

1. Center for Reproductive Medicine and Obstetrics and Gynecology Nanjing Drum Tower Hospital Clinical College of Nanjing Medical University Nanjing China

2. State Key Laboratory of Reproductive Medicine and Offspring Health Nanjing Medical University Nanjing China

3. Center for Molecular Reproductive Medicine Nanjing University Nanjing China

4. Center for Reproductive Medicine and Obstetrics and Gynecology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School Nanjing University Nanjing China

5. Guangdong Provincial Key Laboratory of Reproductive Medicine Guangzhou China

Abstract

AbstractThe correct assembly of the spindle apparatus directly regulates the precise separation of chromosomes in mouse oocytes, which is crucial for obtaining high‐quality oocytes capable of successful fertilization. The localization, assembly, migration, and disassembly of the spindle are regulated by a series of spindle‐associated proteins, which exhibit unique expression level variations and specific localization in oocytes. Proteomic analysis revealed that among many representative spindle‐associated proteins, the expression level of nucleolar and spindle‐associated protein 1 (NUSAP1) significantly increased after meiotic resumption, with a magnitude of change higher than that of other proteins. However, the role of NUSAP1 during oocyte meiosis maturation has not been reported. Here, we report that NUSAP1 is distributed within the cell nucleus during the germinal vesicle (GV) oocytes with non‐surrounded nucleolus stage and is not enriched in the nucleus during the GV‐surrounded nucleolus stage. Interestingly, NUSAP1 forms distinct granular aggregates near the spindle poles during the prophase of the first meiotic division (Pro‐MI), metaphase I, and anaphase I/telophase I stages. Nusap1 depletion leads to chromosome misalignment, increased aneuploidy, and abnormal spindle assembly, particularly a decrease in spindle pole width. Correspondingly, RNA‐seq analysis revealed significant suppression of the “establishment of spindle orientation” signaling pathway. Additionally, the attenuation of F‐actin in NUSAP1‐deficient oocytes may affect the asymmetric division process. Gene ontology analysis of NUSAP1 interactomes, identified through mass spectrometry here, revealed significant enrichment for RNA binding. As an RNA‐binding protein, NUSAP1 is likely involved in the regulation of messenger RNA homeostasis by influencing the dynamics of processing (P)‐body components. Overall, our results demonstrate the critical importance of precise regulation of NUSAP1 expression levels and protein localization for maintaining mouse oocyte meiosis.

Funder

National Natural Science Foundation of China

Publisher

Wiley

Subject

Cell Biology,Molecular Biology,Biochemistry

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