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EMBO Reports Jan 2024Maternal mRNAs are essential for protein synthesis during oogenesis and early embryogenesis. To adapt translation to specific needs during development, maternal mRNAs...
Maternal mRNAs are essential for protein synthesis during oogenesis and early embryogenesis. To adapt translation to specific needs during development, maternal mRNAs are translationally repressed by shortening the polyA tails. While mRNA deadenylation is associated with decapping and degradation in somatic cells, maternal mRNAs with short polyA tails are stable. Here we report that the germline-specific eIF4E paralog, eIF4E1b, is essential for zebrafish oogenesis. eIF4E1b localizes to P-bodies in zebrafish embryos and binds to mRNAs with reported short or no polyA tails, including histone mRNAs. Loss of eIF4E1b results in reduced histone mRNA levels in early gonads, consistent with a role in mRNA storage. Using mouse and human eIF4E1Bs (in vitro) and zebrafish eIF4E1b (in vivo), we show that unlike canonical eIF4Es, eIF4E1b does not interact with eIF4G to initiate translation. Instead, eIF4E1b interacts with the translational repressor eIF4ENIF1, which is required for eIF4E1b localization to P-bodies. Our study is consistent with an important role of eIF4E1b in regulating mRNA dormancy and provides new insights into fundamental post-transcriptional regulatory principles governing early vertebrate development.
Topics: Animals; Humans; Mice; RNA, Messenger, Stored; Zebrafish; Histones; Eukaryotic Initiation Factor-4E; RNA, Messenger; Protein Biosynthesis
PubMed: 38177902
DOI: 10.1038/s44319-023-00006-4 -
Cell Reports Jan 2024Environmental factors influence an organism's reproductive ability by regulating germline development and physiology. While the reproductive adaptations in response to...
Environmental factors influence an organism's reproductive ability by regulating germline development and physiology. While the reproductive adaptations in response to extrinsic stress cues offer fitness and survival advantages to individuals, the mechanistic understanding of these modifications remains unclear. Here, we find that parasitoid wasps' stress signaling regulates Drosophila melanogaster oogenesis. We show that fruit flies dwelling in the wasp-infested area elevate their fecundity, and the observed reproductive response is specific to Pachycrepoideus sp., a pupal parasitoid wasp. Pachycrepoideus-specific olfactory and visual cues recruit the signaling pathways that promote germline stem cell proliferation and accelerate follicle development, increasing egg production in Drosophila females. Downregulation of signaling engaged in oocyte development by shifting flies to a non-wasp-infested environment increases apoptosis of the developing follicles. Thus, this study establishes host germline responsiveness to parasitoid-specific signals and supports a predator strategy to increase hosts for infection.
Topics: Humans; Animals; Female; Drosophila; Drosophila melanogaster; Parasites; Cues; Wasps; Cell Proliferation; Germ Cells; Host-Parasite Interactions
PubMed: 38175752
DOI: 10.1016/j.celrep.2023.113657 -
Scientific Reports Jan 2024Oocyte maturation is a key process during which the female germ cell undergoes resumption of meiosis and completes its preparation for embryonic development including...
Oocyte maturation is a key process during which the female germ cell undergoes resumption of meiosis and completes its preparation for embryonic development including cytoplasmic and epigenetic maturation. The cumulus cells directly surrounding the oocyte are involved in this process by transferring essential metabolites, such as pyruvate, to the oocyte. This process is controlled by cyclic adenosine monophosphate (cAMP)-dependent mechanisms recruited downstream of follicle-stimulating hormone (FSH) signaling in cumulus cells. As mitochondria have a critical but poorly understood contribution to this process, we defined the effects of FSH and high cAMP concentrations on mitochondrial dynamics and function in porcine cumulus cells. During in vitro maturation (IVM) of cumulus-oocyte complexes (COCs), we observed an FSH-dependent mitochondrial elongation shortly after stimulation that led to mitochondrial fragmentation 24 h later. Importantly, mitochondrial elongation was accompanied by decreased mitochondrial activity and a switch to glycolysis. During a pre-IVM culture step increasing intracellular cAMP, mitochondrial fragmentation was prevented. Altogether, the results demonstrate that FSH triggers rapid changes in mitochondrial structure and function in COCs involving cAMP.
Topics: Pregnancy; Swine; Female; Animals; Follicle Stimulating Hormone; Cumulus Cells; Oocytes; Oogenesis; Follicle Stimulating Hormone, Human; Mitochondria; Meiosis
PubMed: 38172520
DOI: 10.1038/s41598-023-50586-3 -
Genome Research Feb 2024Chromatin organization in the germline is tightly regulated and critical for germ cell differentiation. Although certain germline epigenetic regulatory mechanisms have...
Chromatin organization in the germline is tightly regulated and critical for germ cell differentiation. Although certain germline epigenetic regulatory mechanisms have been identified, how they influence chromatin structure and ultimately gene expression remains unclear, in part because most genomic studies have focused on data collected from intact worms comprising both somatic and germline tissues. We therefore analyzed histone modification and chromatin accessibility data from isolated germ nuclei representing undifferentiated proliferating and meiosis I populations to define chromatin states. We correlated these states with overall transcript abundance, spatiotemporal expression patterns, and the function of small RNA pathways. Because the essential role of the germline is to transmit genetic information and establish gene expression in the early embryo, we compared epigenetic and transcriptomic profiles from undifferentiated germ cells to those of embryos to define the epigenetic changes during this developmental transition. The active histone modification H3K4me3 shows particularly dynamic remodeling as germ cells differentiate into oocytes, which suggests a mechanism for establishing early transcription of essential genes during zygotic genome activation. This analysis highlights the dynamism of the chromatin landscape across developmental transitions and provides a resource for future investigation into epigenetic regulatory mechanisms in germ cells.
Topics: Animals; Chromatin; Caenorhabditis elegans; Oogenesis; Germ Cells; Gene Expression Regulation, Developmental; Histones
PubMed: 38164610
DOI: 10.1101/gr.278247.123 -
Reproductive Sciences (Thousand Oaks,... May 2024This paper will review a remarkable new approach to in vitro maturation "IVM" of oocytes from ovarian tissue, based on our results with in vitro oogenesis from somatic... (Review)
Review
This paper will review a remarkable new approach to in vitro maturation "IVM" of oocytes from ovarian tissue, based on our results with in vitro oogenesis from somatic cells. As an aside benefit we also have derived a better understanding of ovarian longevity from ovary transplant. We have found that primordial follicle recruitment is triggered by tissue pressure gradients. Increased pressure holds the follicle in meiotic arrest and prevents recruitment. Therefore recruitment occurs first in the least dense inner tissue of the cortico-medullary junction. Many oocytes can be obtained from human ovarian tissue and mature to metaphase 2 in vitro with no need for ovarian stimulation. Ovarian stimulation may only be necessary for removing the oocyte from the ovary, but this can also be accomplished by simple dissection at the time of ovary tissue cryopreservation. By using surgical dissection of the removed ovary, rather than a needle stick, we can obtain many oocytes from very small follicles not visible with ultrasound. A clearer understanding of ovarian function has come from in vitro oogenesis experiments, and that explains why IVM has now become so simple and robust. Tissue pressure (and just a few "core genes" in the mouse) direct primordial follicle recruitment and development to mature oocyte, and therefore also control ovarian longevity. There are three distinct phases to oocyte development both in vitro and in vivo: in vitro differentiation "IVD" which is not gonadotropin sensitive (the longest phase), in vitro gonadotropin sensitivity "IVG" which is the phase of gonadotropin stimulation to prepare for meiotic competence, and IVM to metaphase II. On any given day 35% of GVs in ovarian tissue have already undergone "IVD" and "IVG" in vivo, and therefore are ready for IVM.
Topics: Female; Animals; Oogenesis; Humans; Ovary; In Vitro Oocyte Maturation Techniques; Oocytes; Ovarian Follicle; Mice
PubMed: 38160209
DOI: 10.1007/s43032-023-01427-1 -
The octopamine receptor OAα1 influences oogenesis and reproductive performance in Rhodnius prolixus.PloS One 2023The control of reproductive processes in Rhodnius prolixus involves a variety of neuroactive chemicals. Among these, several studies have suggested that the biogenic...
The control of reproductive processes in Rhodnius prolixus involves a variety of neuroactive chemicals. Among these, several studies have suggested that the biogenic amine octopamine (OA), might play an active role in these processes. Here, we investigate the molecular profile of the R. prolixus α adrenergic-like OA receptor 1 (RpOAα1-R) and its role in egg production. Comparative molecular analyses confirm that the RpOAα1-R gene codes for a true OAα1 receptor. The RpOAα1-R transcript is highly expressed in tissues associated with egg production, and after a blood meal, which is the stimulus for full egg production in R. prolixus, the RpOAα1-R transcript is upregulated in the ovaries and spermatheca. After RNAi-mediated RpOAα1-R knockdown, an ovarian phenotype characterized by slow egg development is observed. Furthermore, an altered egg phenotype has been characterized with eggs that are deformed. Interestingly, there is no evidence of disruption in vitellogenin (Vg) synthesis by the fat body or uptake by the oocytes. On the other hand, RpOAα1-R downregulation is correlated with defective choriogenesis in the eggs. These results provide critical information concerning the role of OAα1-R in oogenesis in R. prolixus.
Topics: Animals; Rhodnius; Oogenesis; Oocytes; Reproduction
PubMed: 38157386
DOI: 10.1371/journal.pone.0296463 -
International Journal of Molecular... Dec 2023The red imported fire ant ( Buren) is a social pest species with a robust reproductive ability that causes extensive damage. Identification of the genes involved in...
The red imported fire ant ( Buren) is a social pest species with a robust reproductive ability that causes extensive damage. Identification of the genes involved in queen fertility is critical in order to better understand the reproductive biology and screening for the potential molecular targets in . Here, we used the mRNA deep sequencing (RNA-seq) approach to identify differentially expressed genes (DEGs) in the transcriptomes of three reproductive caste types of , including queen (QA) and winged female (FA) and male (MA) ants. The genes that were specific to and highly expressed in the queens were then screened, and the and genes were chosen as targets to explore their functions in oogenesis and fertility. A minimum of 6.08 giga bases (Gb) of clean reads was obtained from all samples, with a mapping rate > 89.78%. There were 7524, 7133, and 977 DEGs identified in the MA vs. QA, MA vs. FA, and FA vs. QA comparisons, respectively. qRT-PCR was used to validate 10 randomly selected DEGs, including () and (), and their expression patterns were mostly consistent with the RNA-seq data. The Vgs included conserved domains and motifs that are commonly found in most insect Vgs. and were highly expressed in queens and winged females and were most highly expressed in the thorax, followed by the fat body, head, and epidermis. Evaluation based on a loss-of-function-based knockdown analysis showed that the downregulation of either or both of these genes resulted in smaller ovaries, less oogenesis, and less egg production. The results of transcriptional sequencing provide a foundation for clarifying the regulators of queen fertility in . The functions of and as regulators of oogenesis highlight their importance in queen fecundity and their potential as targets of reproductive disruption in control.
Topics: Animals; Female; Male; Vitellogenins; Fire Ants; Reproduction; Fertility; Ants
PubMed: 38138959
DOI: 10.3390/ijms242417130 -
Communications Biology Dec 2023Reproduction is highly dependent on environmental and physiological factors including nutrition, mating stimuli and microbes. Among these factors, microbes facilitate...
Reproduction is highly dependent on environmental and physiological factors including nutrition, mating stimuli and microbes. Among these factors, microbes facilitate vital functions for host animals such as nutritional intake, metabolic regulation, and enhancing fertility under poor nutrition conditions. However, detailed molecular mechanisms by which microbes control germline maturation, leading to reproduction, remain largely unknown. In this study, we show that environmental microbes exert a beneficial effect on Drosophila oogenesis by promoting germline stem cell (GSC) proliferation and subsequent egg maturation via acceleration of ovarian cell division and suppression of apoptosis. Moreover, insulin-related signaling is not required; rather, the ecdysone pathway is necessary for microbe-induced increase of GSCs and promotion of egg maturation, while juvenile hormone contributes only to increasing GSC numbers, suggesting that hormonal pathways are activated at different stages of oogenesis. Our findings reveal that environmental microbes can enhance host reproductivity by modulating host hormone release and promoting oogenesis.
Topics: Animals; Female; Drosophila; Oogenesis; Ovary; Stem Cells; Germ Cells
PubMed: 38123715
DOI: 10.1038/s42003-023-05660-x -
ELife Dec 2023Changes in the intracellular concentration of free calcium (Ca) underpin egg activation and initiation of development in animals and plants. In mammals, the Ca release...
Changes in the intracellular concentration of free calcium (Ca) underpin egg activation and initiation of development in animals and plants. In mammals, the Ca release is periodical, known as Ca oscillations, and mediated by the type 1 inositol 1,4,5-trisphosphate receptor (IPR1). Another divalent cation, zinc (Zn), increases exponentially during oocyte maturation and is vital for meiotic transitions, arrests, and polyspermy prevention. It is unknown if these pivotal cations interplay during fertilization. Here, using mouse eggs, we showed that basal concentrations of labile Zn are indispensable for sperm-initiated Ca oscillations because Zn-deficient conditions induced by cell-permeable chelators abrogated Ca responses evoked by fertilization and other physiological and pharmacological agonists. We also found that chemically or genetically generated eggs with lower levels of labile Zn displayed reduced IPR1 sensitivity and diminished ER Ca leak despite the stable content of the stores and IPR1 mass. Resupplying Zn restarted Ca oscillations, but excessive Zn prevented and terminated them, hindering IPR1 responsiveness. The findings suggest that a window of Zn concentrations is required for Ca responses and IPR1 function in eggs, ensuring optimal response to fertilization and egg activation.
Topics: Male; Animals; Mice; Oocytes; Semen; Oogenesis; Fertilization; Spermatozoa; Calcium; Calcium Signaling; Mammals
PubMed: 38099643
DOI: 10.7554/eLife.88082 -
Ecotoxicology and Environmental Safety Jan 2024Flame retardants (FRs) have raised public concerns because of their environmental persistence and negative impacts on human health. Recent evidence has revealed that...
Flame retardants (FRs) have raised public concerns because of their environmental persistence and negative impacts on human health. Recent evidence has revealed that many FRs exhibit reproductive toxicities and transgenerational impacts, whereas the toxic effects of FRs on germ cells remain barely explored. Here we investigated the multigenerational effects of three flame retardants (TBBPA, TCEP and TCPP) on germ cell development in Caenorhabditis elegans, and examined the germ cell mutagenicity of these FRs by using whole genome sequencing. Parental exposure to three FRs markedly increased germ cell apoptosis, and impeded oogenesis in F1-F6 offspring. In addition, the double-increased mutation frequencies observed in progeny genomes uncover the mutagenic actions of FRs on germ cells. Analysis of mutation spectra revealed that these FRs predominantly induced point mutations at A:T base pairs, whereas both small and large indels were almost unaffected. These results revealed the long-term effects of FRs on development and genomic stability of germ cells, which may pose risks to environmental organisms and human reproductive health. Taken together, our findings suggest that germ cell mutagenicity should be carefully examined for the environmental risk assessment of FRs and other emerging pollutants.
Topics: Animals; Humans; Flame Retardants; Caenorhabditis elegans; Mutagens; Environmental Pollutants; Risk Assessment; Halogenated Diphenyl Ethers
PubMed: 38091675
DOI: 10.1016/j.ecoenv.2023.115815