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Transcriptional Regulation of Late Oogenesis and Early Embryogenesis

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Biology".

Deadline for manuscript submissions: 15 May 2024 | Viewed by 15615

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Dr. Dmitry S. Bogolyubov

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Laboratory of Cell Morphology, Institute of Cytology of the Russian Academy of Sciences, 4 Tikhoretsky Ave., 194064 St. Petersburg, Russia
Interests: gametogenesis; oocyte nucleus; nuclear compartmentalization; heterochromatin; karyosphere; Cajal body; nuclear speckles; membraneless organelles; molecular morphology; electron microscopy

Special Issue Information

Dear Colleagues,

Oocytes and early embryos are unique cells that give rise to new life. It is not surprising that the formation of the female germ cell and cleavage of the zygote are extremely dynamic and finely regulated processes regardless of species-specific strategies of female gametogenesis and embryonic development. The most important aspect of the development of a new organism is drastic alterations of the transcriptional activity occurring in late oogenesis and early embryogenesis. Transcriptional silencing of the oocyte nucleus (germinal vesicle, GV), which often occurs before the resumption of meiosis, seems to be essential for the transition from the end of oogenesis to fertilization and further embryonic development. On the contrary, the cleavage period is characterized by a gradual reactivation of transcriptional activity, the so-called zygotic genome activation accompanied by a complexly coordinated and finely balanced replacement of the regulatory molecules accumulated during oogenesis by the expression products of the embryonic genome. The regulation of transcriptional activity in late oogenesis and early embryogenesis involves DNA methylation, post-translational histone modifications, and ATP-dependent chromatin remodeling involving specific chromatin-associated non-histone proteins. Besides, alternative histone variants can replace canonical histones, thereby switching the state of chromatin. Dysregulation of all these and many other nuclear processes virtually related to transcription can lead to the disruption of normal development.

Led by Dr. Dmitry S. Bogolyubov and assisted by our Topical Advisory Panel Member Dr. Irina Bogolyubova (Institute of Cytology of the Russian Academy of Sciences), this Special Issue “Transcriptional Regulation of Late Oogenesis and Early Embryogenesis”, will cover any aspects of the regulatory mechanisms of both mRNA and rRNA synthesis, involved in development of female germ cells and their derivatives, zygotes and early embryos. Studies in animals outside mammals, both vertebrates and invertebrates, are encouraged. Papers dedicated to current views on the transcriptional activity of lampbrush chromosomes and the importance of non-coding DNA transcription in oogenesis and embryogenesis are also appreciated. Experimental and bioinformatics papers, up-to-date review articles, and commentaries are welcome.

Dr. Dmitry S. Bogolyubov
Guest Editor

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Keywords

transcription activity of oocytes, zygotes and early embryos
transcriptomes of oocytes and early embryos
chromatin remodeling
histone and non-histone proteins
coding and non-coding RNAs
DNA methylation

Published Papers (10 papers)

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Research

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15 pages, 4163 KiB

Open AccessArticle

3-Methyl-4-nitrophenol Exposure Deteriorates Oocyte Maturation by Inducing Spindle Instability and Mitochondrial Dysfunction

by Fan Chen, An-Feng Luo, Ming-Guo Li, Li-Xiang Zheng, Hao Gu, Chang-Fan Zhou, Wei Zeng, Adrian Molenaar, Hong-Yan Ren and Yan-Zhen Bi

Int. J. Mol. Sci. 2024, 25(7), 3572; https://doi.org/10.3390/ijms25073572 - 22 Mar 2024

Viewed by 590

Abstract

3-methyl-4-nitrophenol (PNMC), a well-known constituent of diesel exhaust particles and degradation products of insecticide fenitrothion, is a widely distributed environmental contaminant. PNMC is toxic to the female reproductive system; however, how it affects meiosis progression in oocytes is unknown. In this study, in vitro maturation of mouse oocytes was applied to investigate the deleterious effects of PNMC. We found that exposure to PNMC significantly compromised oocyte maturation. PNMC disturbed the spindle stability; specifically, it decreased the spindle density and increased the spindle length. The weakened spindle pole location of microtubule-severing enzyme Fignl1 may result in a defective spindle apparatus in PNMC-exposed oocytes. PNMC exposure induced significant mitochondrial dysfunction, including mitochondria distribution, ATP production, mitochondrial membrane potential, and ROS accumulation. The mRNA levels of the mitochondria-related genes were also significantly impaired. Finally, the above-mentioned alterations triggered early apoptosis in the oocytes. In conclusion, PNMC exposure affected oocyte maturation and quality through the regulation of spindle stability and mitochondrial function. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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17 pages, 3385 KiB

Open AccessArticle

PDGFRβ Activation Induced the Bovine Embryonic Genome Activation via Enhanced NFYA Nuclear Localization

by Chalani Dilshani Perera, Muhammad Idrees, Abdul Majid Khan, Zaheer Haider, Safeer Ullah, Ji-Su Kang, Seo-Hyun Lee, Seon-Min Kang and Il-Keun Kong

Int. J. Mol. Sci. 2023, 24(23), 17047; https://doi.org/10.3390/ijms242317047 - 01 Dec 2023

Viewed by 841

Abstract

Embryonic genome activation (EGA) is a critical step during embryonic development. Several transcription factors have been identified that play major roles in initiating EGA; however, this gradual and complex mechanism still needs to be explored. In this study, we investigated the role of nuclear transcription factor Y subunit A (NFYA) in bovine EGA and bovine embryonic development and its relationship with the platelet-derived growth factor receptor-β (PDGFRβ) by using a potent selective activator (PDGF-BB) and inhibitor (CP-673451) of PDGF receptors. Activation and inhibition of PDGFRβ using PDGF-BB and CP-673451 revealed that NFYA expression is significantly (p < 0.05) affected by the PDGFRβ. In addition, PDGFRβ mRNA expression was significantly increased (p < 0.05) in the activator group and significantly decreased (p < 0.05) in the inhibitor group when compared with PDGFRα. Downregulation of NFYA following PDGFRβ inhibition was associated with the expression of critical EGA-related genes, bovine embryo development rate, and implantation potential. Moreover, ROS and mitochondrial apoptosis levels and expression of pluripotency-related markers necessary for inner cell mass development were also significantly (p < 0.05) affected by the downregulation of NFYA while interrupting trophoblast cell (CDX2) differentiation. In conclusion, the PDGFRβ-NFYA axis is critical for bovine embryonic genome activation and embryonic development. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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17 pages, 5263 KiB

Open AccessArticle

Combined Exogenous Activation of Bovine Oocytes: Effects on Maturation-Promoting Factor, Mitogen-Activated Protein Kinases, and Embryonic Competence

by Cecilia Valencia, Felipe Pérez-García, Luis Aguila, Ricardo Felmer and María Elena Arias

Int. J. Mol. Sci. 2023, 24(21), 15794; https://doi.org/10.3390/ijms242115794 - 31 Oct 2023

Viewed by 895

Abstract

Oocyte activation via dual inhibition of protein synthesis and phosphorylation has improved in vitro embryo production in different mammalian species. In this study, we evaluated the effects of the combination of cycloheximide (CHX), dimethyl amino purine (DMAP), and anisomycin (ANY) on the activation of bovine oocytes, particularly on dynamics of MPF and MAPKs, embryonic developmental potential, and quality. The results showed that the cleavage and blastocyst rates, as well as levels of CCNB1, CDK1, p-CDK1^Thr161, and p-CDK1^Thr14-Tyr15, were similar among groups; ANY and ANY + CHX reduced the expression of ERK1/2 compared to DMAP-combinations (p < 0.05), whereas ANY + DMAP, CHX + DMAP, and ANY + CHX + DMAP reduced p-ERK1/2 compared to ANY and ANY + CHX treatments (p < 0.05). The quality of blastocysts in terms of cell counts, their allocation, and the numbers of TUNEL-positive cells did not differ among groups. However, transcript levels of POU5F1 were higher in embryos derived from ANY + CHX + DMAP treatment compared to other groups, while expression levels of CDX2 did not show differences. In addition, the BCL2A1/BAX ratio of the ANY + CHX + DMAP treatment was significantly low compared to the ANY treatment (p < 0.05) and did not differ significantly from the other treatments. In conclusion, oocyte activation by dual inhibition of protein synthesis and phosphorylation induces MPF inactivation without degradation of CCNB1, while MAPK inactivation occurs differentially between these inhibitors. Thus, although the combined use of these inhibitors does not affect early developmental competence in vitro, it positively impacts the expression of transcripts associated with embryonic quality. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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15 pages, 2127 KiB

Open AccessArticle

The Novel Role of Zfp296 in Mammalian Embryonic Genome Activation as an H3K9me3 Modulator

by Lu Gao, Zihan Zhang, Xiaoman Zheng, Fan Wang, Yi Deng, Qian Zhang, Guoyan Wang, Yong Zhang and Xu Liu

Int. J. Mol. Sci. 2023, 24(14), 11377; https://doi.org/10.3390/ijms241411377 - 12 Jul 2023

Viewed by 1481

Abstract

The changes in epigenetic modifications during early embryonic development significantly impact mammalian embryonic genome activation (EGA) and are species-conserved to some degree. Here, we reanalyzed the published RNA-Seq of human, mouse, and goat early embryos and found that Zfp296 (zinc finger protein 296) expression was higher at the EGA stage than at the oocyte stage in all three species (adjusted p-value < 0.05 |log2(foldchange)| ≥ 1). Subsequently, we found that Zfp296 was conserved across human, mouse, goat, sheep, pig, and bovine embryos. In addition, we identified that ZFP296 interacts with the epigenetic regulators KDM5B, SMARCA4, DNMT1, DNMT3B, HP1β, and UHRF1. The Cys₂-His₂(C2H2) zinc finger domain TYPE2 TYPE3 domains of ZFP296 co-regulated the modification level of the trimethylation of lysine 9 on the histone H3 protein subunit (H3K9me3). According to ChIP-seq analysis, ZFP296 was also enriched in Trim28, Suv39h1, Setdb1, Kdm4a, and Ehmt2 in the mESC genome. Then, knockdown of the expression of Zfp296 at the late zygote of the mouse led to the early developmental arrest of the mouse embryos and failure resulting from a decrease in H3K9me3. Together, our results reveal that Zfp296 is an H3K9me3 modulator which is essential to the embryonic genome activation of mouse embryos. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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16 pages, 4561 KiB

Open AccessArticle

A Subpathway and Target Gene Cluster-Based Approach Uncovers lncRNAs Associated with Human Primordial Follicle Activation

by Li Zhang, Jiyuan Zou, Zhihao Wang and Lin Li

Int. J. Mol. Sci. 2023, 24(13), 10525; https://doi.org/10.3390/ijms241310525 - 23 Jun 2023

Viewed by 978

Abstract

Long non-coding RNAs (lncRNAs) are emerging as a critical regulator in controlling the expression level of genes involved in cell differentiation and development. Primordial follicle activation (PFA) is the first step for follicle maturation, and excessive PFA results in premature ovarian insufficiency (POI). However, the correlation between lncRNA and cell differentiation was largely unknown, especially during PFA. In this study, we observed the expression level of lncRNA was more specific than protein-coding genes in both follicles and granulosa cells, suggesting lncRNA might play a crucial role in follicle development. Hence, a systematical framework was needed to infer the functions of lncRNAs during PFA. Additionally, an increasing number of studies indicate that the subpathway is more precise in reflecting biological processes than the entire pathway. Given the complex expression patterns of lncRNA target genes, target genes were further clustered based on their expression similarity and classification performance to reveal the activated/inhibited gene modules, which intuitively illustrated the diversity of lncRNA regulation. Moreover, the knockdown of SBF2-AS1 in the A549 cell line and ZFAS1 in the SK-Hep1 cell line further validated the function of SBF2-AS1 in regulating the Hippo signaling subpathway and ZFAS1 in the cell cycle subpathway. Overall, our findings demonstrated the importance of subpathway analysis in uncovering the functions of lncRNAs during PFA, and paved new avenues for future lncRNA-associated research. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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10 pages, 2569 KiB

Open AccessArticle

Single Copies of the 5S rRNA Inserted into 45S rDNA Intergenic Spacers in the Genomes of Nototheniidae (Perciformes, Actinopterygii)

by Alexander Dyomin, Svetlana Galkina, Arina Ilina and Elena Gaginskaya

Int. J. Mol. Sci. 2023, 24(8), 7376; https://doi.org/10.3390/ijms24087376 - 17 Apr 2023

Cited by 1 | Viewed by 1023

Abstract

In the vast majority of Animalia genomes, the 5S rRNA gene repeats are located on chromosomes outside of the 45S rDNA arrays of the nucleolar organiser (NOR). We analysed the genomic databases available and found that a 5S rDNA sequence is inserted into the intergenic spacer (IGS) between the 45S rDNA repeats in ten species of the family Nototheniidae (Perciformes, Actinopterigii). We call this sequence the NOR-5S rRNA gene. Along with Testudines and Crocodilia, this is the second case of a close association between four rRNA genes within one repetitive unit in deuterostomes. In both cases, NOR-5S is oriented opposite the 45S rDNA. None of the three nucleotide substitutions compared to the canonical 5S rRNA gene influenced the 5S rRNA secondary structure. In transcriptomes of the Patagonian toothfish, we only found NOR-5S rRNA reads in ovaries and early embryos, but not in testis or somatic tissues of adults. Thus, we consider the NOR-5S gene to be a maternal-type 5S rRNA template. The colocalization of the 5S and 45S ribosomal genes appears to be essential for the equimolar production of all four rRNAs in the species that show rDNA amplification during oogenesis. Most likely, the integration of 5S and NOR rRNA genes occurred prior to Nototheniidae lineage diversification. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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Review

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24 pages, 1230 KiB

Open AccessReview

The Dynamics of Histone Modifications during Mammalian Zygotic Genome Activation

by Francisco Sotomayor-Lugo, Nataly Iglesias-Barrameda, Yandy Marx Castillo-Aleman, Imilla Casado-Hernandez, Carlos Agustin Villegas-Valverde, Antonio Alfonso Bencomo-Hernandez, Yendry Ventura-Carmenate and Rene Antonio Rivero-Jimenez

Int. J. Mol. Sci. 2024, 25(3), 1459; https://doi.org/10.3390/ijms25031459 - 25 Jan 2024

Viewed by 1531

Abstract

Mammalian fertilization initiates the reprogramming of oocytes and sperm, forming a totipotent zygote. During this intricate process, the zygotic genome undergoes a maternal-to-zygotic transition (MZT) and subsequent zygotic genome activation (ZGA), marking the initiation of transcriptional control and gene expression post-fertilization. Histone modifications are pivotal in shaping cellular identity and gene expression in many mammals. Recent advances in chromatin analysis have enabled detailed explorations of histone modifications during ZGA. This review delves into conserved and unique regulatory strategies, providing essential insights into the dynamic changes in histone modifications and their variants during ZGA in mammals. The objective is to explore recent advancements in leading mechanisms related to histone modifications governing this embryonic development phase in depth. These considerations will be useful for informing future therapeutic approaches that target epigenetic regulation in diverse biological contexts. It will also contribute to the extensive areas of evolutionary and developmental biology and possibly lay the foundation for future research and discussion on this seminal topic. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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13 pages, 785 KiB

Open AccessReview

Comparative Analysis of Bivalve and Sea Urchin Genetics and Development: Investigating the Dichotomy in Bilateria

by Anatoliy Drozdov, Egor Lebedev and Leonid Adonin

Int. J. Mol. Sci. 2023, 24(24), 17163; https://doi.org/10.3390/ijms242417163 - 05 Dec 2023

Viewed by 924

Abstract

This comprehensive review presents a comparative analysis of early embryogenesis in Protostomia and Deuterostomia, the first of which exhibit a mosaic pattern of development, where cells are fated deterministically, while Deuterostomia display a regulatory pattern of development, where the fate of cells is indeterminate. Despite these fundamental differences, there are common transcriptional mechanisms that underline their evolutionary linkages, particularly in the field of functional genomics. By elucidating both conserved and unique regulatory strategies, this review provides essential insights into the comparative embryology and developmental dynamics of these groups. The objective of this review is to clarify the shared and distinctive characteristics of transcriptional regulatory mechanisms. This will contribute to the extensive areas of functional genomics, evolutionary biology and developmental biology, and possibly lay the foundation for future research and discussion on this seminal topic. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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13 pages, 2218 KiB

Open AccessReview

Chromatin Configuration in Diplotene Mouse and Human Oocytes during the Period of Transcriptional Activity Extinction

by Irina Bogolyubova, Daniil Salimov and Dmitry Bogolyubov

Int. J. Mol. Sci. 2023, 24(14), 11517; https://doi.org/10.3390/ijms241411517 - 15 Jul 2023

Cited by 1 | Viewed by 1073

Abstract

In the oocyte nucleus, called the germinal vesicle (GV) at the prolonged diplotene stage of the meiotic prophase, chromatin undergoes a global rearrangement, which is often accompanied by the cessation of its transcriptional activity. In many mammals, including mice and humans, chromatin condenses around a special nuclear organelle called the atypical nucleolus or formerly nucleolus-like body. Chromatin configuration is an important indicator of the quality of GV oocytes and largely predicts their ability to resume meiosis and successful embryonic development. In mice, GV oocytes are traditionally divided into the NSN (non-surrounded nucleolus) and SN (surrounded nucleolus) based on the specific chromatin configuration. The NSN–SN transition is a key event in mouse oogenesis and the main prerequisite for the normal development of the embryo. As for humans, there is no single nomenclature for the chromatin configuration at the GV stage. This often leads to discrepancies and misunderstandings, the overcoming of which should expand the scope of the application of mouse oocytes as a model for developing new methods for assessing and improving the quality of human oocytes. As a first approximation and with a certain proviso, the mouse NSN/SN classification can be used for the primary characterization of human GV oocytes. The task of this review is to analyze and discuss the existing classifications of chromatin configuration in mouse and human GV oocytes with an emphasis on transcriptional activity extinction at the end of oocyte growth. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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14 pages, 1755 KiB

Open AccessReview

Oogenesis in Women: From Molecular Regulatory Pathways and Maternal Age to Stem Cells

by Kornelia Krajnik, Klaudia Mietkiewska, Agnieszka Skowronska, Pawel Kordowitzki and Mariusz T. Skowronski

Int. J. Mol. Sci. 2023, 24(7), 6837; https://doi.org/10.3390/ijms24076837 - 06 Apr 2023

Cited by 3 | Viewed by 5166

Abstract

It is a well-known fact that the reproductive organs in women, especially oocytes, are exposed to numerous regulatory pathways and environmental stimuli. The maternal age is one cornerstone that influences the process of oocyte fertilization. More precisely, the longer a given oocyte is in the waiting-line to be ovulated from menarche to menopause, the longer the duration from oogenesis to fertilization, and therefore, the lower the chances of success to form a viable embryo. The age of menarche in girls ranges from 10 to 16 years, and the age of menopause in women ranges from approximately 45 to 55 years. Researchers are paying attention to the regulatory pathways that are impacting the oocyte at the very beginning during oogenesis in fetal life to discover genes and proteins that could be crucial for the oocyte’s lifespan. Due to the general trend in industrialized countries in the last three decades, women are giving birth to their first child in their thirties. Therefore, maternal age has become an important factor impacting oocytes developmental competence, since the higher a woman’s age, the higher the chances of miscarriage due to several causes, such as aneuploidy. Meiotic failures during oogenesis, such as, for instance, chromosome segregation failures or chromosomal non-disjunction, are influencing the latter-mentioned aging-related phenomenon too. These errors early in life of women can lead to sub- or infertility. It cannot be neglected that oogenesis is a precisely orchestrated process, during which the oogonia and primary oocytes are formed, and RNA synthesis takes place. These RNAs are crucial for oocyte growth and maturation. In this review, we intend to describe the relevance of regulatory pathways during the oogenesis in women. Furthermore, we focus on molecular pathways of oocyte developmental competence with regard to maternal effects during embryogenesis. On the background of transcriptional mechanisms that enable the transition from a silenced oocyte to a transcriptionally active embryo, we will briefly discuss the potential of induced pluripotent stem cells. Full article

(This article belongs to the Special Issue Transcriptional Regulation of Late Oogenesis and Early Embryogenesis)

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