Oocyte meiosis-coupled poly(A) polymerase α phosphorylation and activation trigger maternal mRNA translation in mice

Jiang, Jun‐Chao; Zhang, Hua; Cao, Lan-Rui; Dai, Xing‐Xing; Zhao, Long‐Wen; Liu, Hongbin; Fan, Heng‐Yu

doi:10.1093/nar/gkab431

Cited by 22 publications

(10 citation statements)

References 51 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…HPG signals were detected using a Click-iT®HPG Alexa Fluor®Protein Synthesis Assay Kit (Life Technologies). Mean intensity of the HPG signal was measured across the middle of each oocyte and quantified using ImageJ software 53 .…”

Section: Methodsmentioning

confidence: 99%

Dynamic mRNA degradome analyses indicate a role of histone H3K4 trimethylation in association with meiosis-coupled mRNA decay in oocyte aging

Zheng

et al. 2022

Nat Commun

Self Cite

View full text Add to dashboard Cite

A decrease in oocyte developmental potential is a major obstacle for successful pregnancy in women of advanced age. However, the age-related epigenetic modifications associated with dynamic transcriptome changes, particularly meiotic maturation-coupled mRNA clearance, have not been adequately characterized in human oocytes. This study demonstrates a decreased storage of transcripts encoding key factors regulating the maternal mRNA degradome in fully grown oocytes of women of advanced age. A similar defect in meiotic maturation-triggered mRNA clearance is also detected in aged mouse oocytes. Mechanistically, the epigenetic and cytoplasmic aspects of oocyte maturation are synchronized in both the normal development and aging processes. The level of histone H3K4 trimethylation (H3K4me3) is high in fully grown mouse and human oocytes derived from young females but decreased during aging due to the decreased expression of epigenetic factors responsible for H3K4me3 accumulation. Oocyte-specific knockout of the gene encoding CxxC-finger protein 1 (CXXC1), a DNA-binding subunit of SETD1 methyltransferase, causes ooplasm changes associated with accelerated aging and impaired maternal mRNA translation and degradation. These results suggest that a network of CXXC1-maintained H3K4me3, in association with mRNA decay competence, sets a timer for oocyte deterioration and plays a role in oocyte aging in both mouse and human oocytes.

show abstract

Section: Methodsmentioning

confidence: 99%

Dynamic mRNA degradome analyses indicate a role of histone H3K4 trimethylation in association with meiosis-coupled mRNA decay in oocyte aging

Zheng

et al. 2022

Nat Commun

Self Cite

View full text Add to dashboard Cite

show abstract

“…Our previous studies demonstrated that ERK1/2 regulates the maternal mRNA translation and decay in mouse oocytes from the GV to MII stage (Sha et al , 2017 ; Jiang et al , 2021 ), and defects in maternal mRNA degradation is associate with early embryonic arrest (Sha et al , 2020a , 2020b ). However, whether MOS is required for maternal mRNA decay in human oocytes is unclear.…”

Section: Resultsmentioning

confidence: 99%

Biallelic mutations in MOS cause female infertility characterized by human early embryonic arrest and fragmentation

et al. 2021

Self Cite

View full text Add to dashboard Cite

Early embryonic arrest and fragmentation (EEAF) is a common phenomenon leading to female infertility, but the genetic determinants remain largely unknown. The Moloney sarcoma oncogene (MOS) encodes a serine/threonine kinase that activates the ERK signaling cascade during oocyte maturation in vertebrates. Here, we identified four rare variants of MOS in three infertile female individuals with EEAF that followed a recessive inheritance pattern. These MOS variants encoded proteins that resulted in decreased phosphorylated ERK1/2 level in cells and oocytes, and displayed attenuated rescuing effects on cortical F‐actin assembly. Using oocyte‐specific Erk1/2 knockout mice, we verified that MOS‐ERK signal pathway inactivation in oocytes caused EEAF as human. The RNA sequencing data revealed that maternal mRNA clearance was disrupted in human mature oocytes either with MOS homozygous variant or with U0126 treatment, especially genes relative to mitochondrial function. Mitochondrial dysfunction was observed in oocytes with ERK1/2 deficiency or inactivation. In conclusion, this study not only uncovers biallelic MOS variants causes EEAF but also demonstrates that MOS‐ERK signaling pathway drives human oocyte cytoplasmic maturation to prevent EEAF.

show abstract

“…PAPγ exhibits monoadenylation activity toward small RNAs and is active during tumorigenesis (Topalian et al, 2001). Very recently, Jiang et al (2021) identified PAPα as the elusive enzyme that catalyses cytoplasmic polyadenylation of maternal mRNAs in mouse oocytes (Table 2). Inhibition of PAPα activity through overexpression of a PAPα mutant impaired cytoplasmic polyadenylation and translation of maternal mRNAs, thus preventing meiotic progression.…”

Section: Translational Regulation Of Maternal Mrnasmentioning

confidence: 99%

Spatiotemporal regulation of maternalmRNAsduring vertebrate oocyte meiotic maturation

Jiang

Adhikari

et al. 2023

Biological Reviews

View full text Add to dashboard Cite

Vertebrate oocytes face a particular challenge concerning the regulation of gene expression during meiotic maturation. Global transcription becomes quiescent in fully grown oocytes, remains halted throughout maturation and fertilization, and only resumes upon embryonic genome activation. Hence, the oocyte meiotic maturation process is largely regulated by protein synthesis from pre‐existing maternal messenger RNAs (mRNAs) that are transcribed and stored during oocyte growth. Rapidly developing genome‐wide techniques have greatly expanded our insights into the global translation changes and possible regulatory mechanisms during oocyte maturation. The storage, translation, and processing of maternal mRNAs are thought to be regulated by factors interacting with elements in the mRNA molecules. Additionally, posttranscriptional modifications of mRNAs, such as methylation and uridylation, have recently been demonstrated to play crucial roles in maternal mRNA destabilization. However, a comprehensive understanding of the machineries that regulate maternal mRNA fate during oocyte maturation is still lacking. In particular, how the transcripts of important cell cycle components are stabilized, recruited at the appropriate time for translation, and eliminated to modulate oocyte meiotic progression remains unclear. A better understanding of these mechanisms will provide invaluable insights for the preconditions of developmental competence acquisition, with important implications for the treatment of infertility. This review discusses how the storage, localization, translation, and processing of oocyte mRNAs are regulated, and how these contribute to oocyte maturation progression.

show abstract

Oocyte meiosis-coupled poly(A) polymerase α phosphorylation and activation trigger maternal mRNA translation in mice

Cited by 22 publications

References 51 publications

Dynamic mRNA degradome analyses indicate a role of histone H3K4 trimethylation in association with meiosis-coupled mRNA decay in oocyte aging

Dynamic mRNA degradome analyses indicate a role of histone H3K4 trimethylation in association with meiosis-coupled mRNA decay in oocyte aging

Biallelic mutations in MOS cause female infertility characterized by human early embryonic arrest and fragmentation

Spatiotemporal regulation of maternalmRNAsduring vertebrate oocyte meiotic maturation

Contact Info

Product

Resources

About