Studies on Developmental Genetic Programs of Animal Early Embryogenesis

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Animal Genetics and Genomics".

Deadline for manuscript submissions: closed (15 November 2023) | Viewed by 14423

Special Issue Editor


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Guest Editor
1. Laboratory Animal Center, Xi’an Jiaotong University, Xi’an, China
2. Translational Medicine Institute, Institute of Cardiovascular Science, Xi’an Jiaotong University, Xi’an, China
Interests: animal model; embryogenesis; transgenic; genetics; lipid metabolism
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Special Issue Information

Dear Colleagues,

The fertilization of oocyte and sperm, to produce a new organism, is the culmination of numerous intricately regulated cellular processes. After fertilization, gametes develop from a highly differentiated state to a pluripotent state, and then undergo early embryogenesis, which is considered to be one of the most crucial phases of the entire lifespan. During this process, paternal and maternal chromatin structures and genomes undergo dramatic changes, with the latter experiencing genome-wide epigenetic modifications or reprogramming. The transcriptome, proteome, and metabolome of the early embryo also exhibit significant transformations, all of which could regulate the events of embryonic development and even the entire lifespan or offspring.

Until now, several important theories and mechanisms concerning the regulation of animal early embryogenesis have been elucidated, triggering the emergence of important technologies such as assisted reproduction, animal breeding, the creation of gene-editing animals, and so on. However, the early embryonic development process is complex, and its mechanisms are not fully understood.

This Special Issue will focus on valuable findings associated with the genetic programs of animal early embryogenesis, exploiting a new understanding for animal embryos.

Prof. Dr. Enqi Liu
Guest Editor

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Keywords

  • animal
  • embryogenesis
  • fertilization
  • zygotic genome activation
  • reprogramming
  • chromatin structure
  • epigenetics

Published Papers (7 papers)

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Research

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11 pages, 1852 KiB  
Article
Transcriptomic Profiling at the Maternal-to-Zygotic Transition in Leech, Helobdella austinensis
by Samuel Hsaio, Naim Saglam, David Morrow and Daniel H. Shain
Genes 2024, 15(3), 283; https://doi.org/10.3390/genes15030283 - 24 Feb 2024
Viewed by 860
Abstract
The glossiphoniid leech, Helobdella austinensis, is an experimentally tractable member of the superphylum, Lophotrochozoa. Its large embryonic cells, stereotyped asymmetric cell divisions and ex vivo development capabilities makes it a favorable model for studying the molecular and cellular events of a representative [...] Read more.
The glossiphoniid leech, Helobdella austinensis, is an experimentally tractable member of the superphylum, Lophotrochozoa. Its large embryonic cells, stereotyped asymmetric cell divisions and ex vivo development capabilities makes it a favorable model for studying the molecular and cellular events of a representative spiralian. In this study, we focused on a narrow developmental time window of ~6–8 h, comprising stages just prior to and immediately following zygote deposition. Employing RNA-Seq methodology, we identified differentially expressed transcripts at this fundamental ontogenic boundary, known as the maternal-to-zygotic transition (MZT). Gene expression changes were characterized by the massive degradation of maternal RNAs (~45%) coupled with the rapid transcription of ~5000 zygotic genes (~20% of the genome) in the first mitotic cell cycle. The latter transcripts encoded a mixture of cell maintenance and regulatory proteins that predictably influence downstream developmental events. Full article
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13 pages, 2973 KiB  
Article
Effect of Dietetic Obesity on Testicular Transcriptome in Cynomolgus Monkeys
by Yanru Zhang, Jia Qi, Juan Zhao, Miaojing Li, Yulin Zhang, Huizhong Hu, Liangliang Wei, Kai Zhou, Hongyu Qin, Pengxiang Qu, Wenbin Cao and Enqi Liu
Genes 2023, 14(3), 557; https://doi.org/10.3390/genes14030557 - 23 Feb 2023
Cited by 2 | Viewed by 1913
Abstract
Obesity is a metabolic disorder resulting from behavioral, environmental and heritable causes, and can have a negative impact on male reproduction. There have been few experiments in mice, rats, and rabbits on the effects of obesity on reproduction, which has inhibited the development [...] Read more.
Obesity is a metabolic disorder resulting from behavioral, environmental and heritable causes, and can have a negative impact on male reproduction. There have been few experiments in mice, rats, and rabbits on the effects of obesity on reproduction, which has inhibited the development of better treatments for male subfertility caused by obesity. Nonhuman primates are most similar to human beings in anatomy, physiology, metabolism, and biochemistry and are appropriate subjects for obesity studies. In this investigation, we conducted a transcriptome analysis of the testes of cynomolgus monkeys on high-fat, high-fructose, and cholesterol-rich diets to determine the effect of obesity on gene expression in testes. The results showed that the testes of obese monkeys had abnormal morphology, and their testes transcriptome was significantly different from that of non-obese animals. We identified 507 differentially abundant genes (adjusted p value < 0.01, log2 [FC] > 2) including 163 up-regulated and 344 down-regulated genes. Among the differentially abundant genes were ten regulatory genes, including IRF1, IRF6, HERC5, HERC6, IFIH1, IFIT2, IFIT5, IFI35, RSAD2, and UBQLNL. Gene ontology (GO) and KEGG pathway analysis was conducted, and we found that processes and pathways associated with the blood testes barrier (BTB), immunity, inflammation, and DNA methylation in gametes were preferentially enriched. We also found abnormal expression of genes related to infertility (TDRD5, CLCN2, MORC1, RFX8, SOHLH1, IL2RB, MCIDAS, ZPBP, NFIA, PTPN11, TSC22D3, MAPK6, PLCB1, DCUN1D1, LPIN1, and GATM) and down-regulation of testosterone in monkeys with dietetic obesity. This work not only provides an important reference for research and treatment on male infertility caused by obesity, but also valuable insights into the effects of diet on gene expression in testes. Full article
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15 pages, 6634 KiB  
Article
Transcriptome Analysis Provides Insights into Copulation, Fertilization, and Gestation in Sebastes schlegelii
by Xueying Wang, Ning Zhao, Tao Wang, Shuran Du, Qinghua Liu and Jun Li
Genes 2022, 13(10), 1812; https://doi.org/10.3390/genes13101812 - 07 Oct 2022
Cited by 2 | Viewed by 1432
Abstract
Among the viviparous marine teleosts of China, the black rockfish (Sebastes schlegelii Hilgendorf) is one of the most economically important. In addition to copulation and internal fertilization, it features lengthy sperm storage in the female ovary as well as a high rate [...] Read more.
Among the viviparous marine teleosts of China, the black rockfish (Sebastes schlegelii Hilgendorf) is one of the most economically important. In addition to copulation and internal fertilization, it features lengthy sperm storage in the female ovary as well as a high rate of abortion. A network of gene regulation is necessary for these processes. To elucidate the mechanisms of copulation, fertilization, and gestation, it is essential to determine the genetic basis of viviparous teleost oogenesis and embryogenesis. In this study, we analyzed the transcriptome of the ovary during different developmental phases to investigate the dynamic changes that occur. We constructed 24 ovary transcriptomes. In order to investigate the regulation of embryogenesis, differentially expressed genes (DEGs) with specific expression patterns were subjected to gene ontology annotation, pathway analyses, and weighted gene co-expression network analysis (WGCNA). The up-regulated genes were significantly enriched in focal adhesion, regulation of the actin cytoskeleton, Wnt, and ECM-receptor interaction signaling pathways. As a result of our study, we provide omics evidence for copulation, fertilization, and gestation in viviparous marine teleosts. Decoding the S. schlegelii gene regulation network, as well as providing new insights into embryogenesis, is highly valuable to researchers in the marine teleost reproduction sciences. Full article
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24 pages, 8318 KiB  
Article
Single Cell Sequencing Reveals Mechanisms of Persistent Truncus Arteriosus Formation after PDGFRα and PDGFRβ Double Knockout in Cardiac Neural Crest Cells
by Tianyun Chen, Shen Song, Haobin Jiang, Hong Lian and Shengshou Hu
Genes 2022, 13(10), 1708; https://doi.org/10.3390/genes13101708 - 23 Sep 2022
Cited by 1 | Viewed by 2036
Abstract
Persistent truncus arteriosus (PTA) is an uncommon and complex congenital cardiac malformation accounting for about 1.2% of all congenital heart diseases (CHDs), which is caused by a deficiency in the embryonic heart outflow tract’s (OFT) septation and remodeling. PDGFRα and PDGFRβ double knockout [...] Read more.
Persistent truncus arteriosus (PTA) is an uncommon and complex congenital cardiac malformation accounting for about 1.2% of all congenital heart diseases (CHDs), which is caused by a deficiency in the embryonic heart outflow tract’s (OFT) septation and remodeling. PDGFRα and PDGFRβ double knockout (DKO) in cardiac neural crest cells (CNCCs) has been reported to cause PTA, but the underlying mechanisms remain unclear. Here, we constructed a PTA mouse model with PDGFRα and PDGFRβ double knockout in Pax3+ CNCCs and described the condensation failure into OFT septum of CNCC-derived cells due to disturbance of cell polarity in the DKO group. In addition, we further explored the mechanism with single-cell RNA sequencing. We found that two main cell differentiation trajectories into vascular smooth muscle cells (VSMCs) from cardiomyocytes (CMs) and mesenchymal cells (MSs), respectively, were interrupted in the DKO group. The process of CM differentiation into VSMC stagnated in a transitional CM I-like state, which contributed to the failure of OFT remodeling and muscular septum formation. On the other hand, a Penk+ transitional MS II cluster closely related to cell condensation into the OFT septum disappeared, which led to the OFT’s septation absence directly. In conclusion, the disturbance of CNCC-derived cells caused by PDGFRα and PDGFRβ knockout can lead to the OFT septation disorder and the occurrence of PTA. Full article
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14 pages, 2565 KiB  
Article
RNA-Seq Reveals the Underlying Molecular Mechanism of First Cleavage Time Affecting Porcine Embryo Development
by Xinhui Song, Tiantian Li, Xin Xiong, Huiquan Shan, Tong Feng, Kuiqing Cui, Deshun Shi, Qingyou Liu and Zhipeng Li
Genes 2022, 13(7), 1251; https://doi.org/10.3390/genes13071251 - 15 Jul 2022
Cited by 3 | Viewed by 1940
Abstract
The selection and evaluation of high-quality embryos are the key factors affecting in vitro embryo development and pregnancy outcome. The timing of first embryonic cleavage has been considered a positive indicator of the in vitro developmental potential of embryos, while the underlying molecular [...] Read more.
The selection and evaluation of high-quality embryos are the key factors affecting in vitro embryo development and pregnancy outcome. The timing of first embryonic cleavage has been considered a positive indicator of the in vitro developmental potential of embryos, while the underlying molecular mechanism is still not fully understood. In this study, the embryos generated by parthenogenetic activation (PA) or in vitro fertilization (IVF) were monitored and recorded every 2 h and divided into two groups (early cleavage or late cleavage) based on the cleavage rate and blastocyst formation data. RNA sequencing was used to analyze the gene expression pattern of the embryos. We identified 667 and 71 different expression genes (DEGs) in early cleavage and late cleavage porcine PA and IVF embryos, respectively. Further Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses showed that the DEGs are mainly enriched in pathways concerning the proteasome, DNA repair, cell cycle arrest, autophagy, and apoptosis, suggesting that severe endoplasmic reticulum stress (ERS) and DNA damage may be the key factors that led to the low development potential of late cleavage embryos. This study provides a theoretical basis for the following application and offers important information about the understanding of the timely manner of porcine embryo development. Full article
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14 pages, 4854 KiB  
Article
Tubulin TUBB4B Is Involved in Spermatogonia Proliferation and Cell Cycle Processes
by Meiying Feng, Kai Wang, Shuying Fu, Hengxi Wei, Xiaokun Mu, Li Li and Shouquan Zhang
Genes 2022, 13(6), 1082; https://doi.org/10.3390/genes13061082 - 17 Jun 2022
Cited by 4 | Viewed by 2236
Abstract
Tubb4b (tubulin β-4b chain) is essential for cell growth and development as a microtubule network protein. Previous studies have shown that TUBB4B affects mouse pronucleus migration, but the gene function has yet to be elucidated. To study TUBB4B-related functions in mouse reproductive development, [...] Read more.
Tubb4b (tubulin β-4b chain) is essential for cell growth and development as a microtubule network protein. Previous studies have shown that TUBB4B affects mouse pronucleus migration, but the gene function has yet to be elucidated. To study TUBB4B-related functions in mouse reproductive development, we designed a single sgRNA in chromosome 2 and generated a knockout spermatogonia cell line of the β-tubulin isoform Tubb4b by the CRISPR/Cas9 system. Tubb4b-KO spermatogonia recognized abnormal lysosomal membranes and cell morphology defects. Compared to control mouse spermatogonia, the proliferation rate was significantly slower and cycling stagnated in the G1/0 population. Although spermatogonia lacking TUBB4B have abnormal divisions, they are not lethal. We detected the mRNA levels of the cell-regulating cyclins CyclinsD1, CyclinsE, Cdk2, Cdk4, P21, Skp2 and the cell growth factors C/EBP α, C/EBP β, and G-CSF in the spermatogonia of Tubb4b-KO and found that the expressions of CyclinsD1, Skp2 and cell growth factors were significantly reduced. Further analysis revealed that 675 genes were expressed differently after Tubb4b deletion and were enriched in negative regulation of cell population proliferation (GO:0008285), negative regulation of cell cycle G2/M phase transition (GO:1902750), and positive regulation of cell death (GO: 0010942). We also found that there is a common gene Cdkn1a (P21) in these three GO pathways related to cell proliferation and cell cycle, and both quantitative analysis and transcriptome sequencing results showed that the expression of this gene was up-regulated in Tubb4b knockout cells. This implies that Tubb4b may be involved in the division of spermatogonia with multiple cell cycle regulatory proteins. Overall, these data indicate that Tubb4b has a specific role in regulating spermatogonia proliferation and cell cycle. Full article
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Review

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17 pages, 1505 KiB  
Review
Ferroptosis: A Novel Type of Cell Death in Male Reproduction
by Yanjing Su, Zelan Liu, Keyu Xie, Yingxin Ren, Chunyun Li and Wei Chen
Genes 2023, 14(1), 43; https://doi.org/10.3390/genes14010043 - 23 Dec 2022
Cited by 8 | Viewed by 2916
Abstract
Ferroptosis, an iron-dependent type of regulated cell death, is triggered by the accumulation of lethal lipid peroxides. Due to its potential in exploring disease progression and highly targeted therapies, it is still a widely discussed topic nowadays. In recent studies, it was found [...] Read more.
Ferroptosis, an iron-dependent type of regulated cell death, is triggered by the accumulation of lethal lipid peroxides. Due to its potential in exploring disease progression and highly targeted therapies, it is still a widely discussed topic nowadays. In recent studies, it was found that ferroptosis was induced when testicular tissue was exposed to some high-risk factors, such as cadmium (Cd), busulfan, and smoking accompanied by a variety of reproductive damage characteristics, including changes in the specific morphology and ferroptosis-related features. In this literature-based review, we summarize the related mechanisms of ferroptosis and elaborate upon its relationship network in the male reproductive system in terms of three significant events: the abnormal iron metabolism, dysregulation of the Cyst(e)ine/GSH/GPX4 axis, and lipid peroxidation. It is meaningful to deeply explore the relationship between ferroptosis and the male reproductive system, which may provide suggestions regarding pristine therapeutic targets and novel drugs. Full article
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