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Frontiers in Cell and Developmental... 2024The establishment of the embryonic dorsoventral axis in occurs when the radial symmetry around the egg's animal-vegetal axis is broken to give rise to the typical...
The establishment of the embryonic dorsoventral axis in occurs when the radial symmetry around the egg's animal-vegetal axis is broken to give rise to the typical symmetry of Bilaterians. We have previously shown that the Notch1 protein is ventrally enriched during early embryogenesis in and zebrafish and exerts ventralizing activity through β-Catenin destabilization and the positive regulation of ventral center genes in . These findings led us to further investigate when these asymmetries arise. In this work, we show that the asymmetrical distribution of Notch1 protein and mRNA precedes cortical rotation and even fertilization in Moreover, we found that in unfertilized eggs transcripts encoded by the ventralizing gene are also asymmetrically distributed in the animal hemisphere and transcripts accumulate consistently on the same side of the eccentric maturation point. Strikingly, a Notch1 asymmetry orthogonal to the animal-vegetal axis appears during oogenesis. Thus, we show for the first time a maternal bias in the distribution of molecules that are later involved in ventral patterning during embryonic axialization, strongly supporting the hypothesis of a dorsoventral prepattern or intrinsic bilaterality of eggs before fertilization.
PubMed: 38572484
DOI: 10.3389/fcell.2024.1365705 -
PLoS Biology Mar 2024The rising interest and success in deploying inherited microorganisms and cytoplasmic incompatibility (CI) for vector control strategies necessitate an explanation of...
The rising interest and success in deploying inherited microorganisms and cytoplasmic incompatibility (CI) for vector control strategies necessitate an explanation of the CI mechanism. Wolbachia-induced CI manifests in the form of embryonic lethality when sperm from Wolbachia-bearing testes fertilize eggs from uninfected females. Embryos from infected females however survive to sustain the maternally inherited symbiont. Previously in Drosophila melanogaster flies, we demonstrated that CI modifies chromatin integrity in developing sperm to bestow the embryonic lethality. Here, we validate these findings using wMel-transinfected Aedes aegypti mosquitoes released to control vector-borne diseases. Once again, the prophage WO CI proteins, CifA and CifB, target male gametic nuclei to modify chromatin integrity via an aberrant histone-to-protamine transition. Cifs are not detected in the embryo, and thus elicit CI via the nucleoprotein modifications established pre-fertilization. The rescue protein CifA in oogenesis localizes to stem cell, nurse cell, and oocyte nuclei, as well as embryonic DNA during embryogenesis. Discovery of the nuclear targeting Cifs and altered histone-to-protamine transition in both Aedes aegypti mosquitoes and D. melanogaster flies affirm the Host Modification Model of CI is conserved across these host species. The study also newly uncovers the cell biology of Cif proteins in the ovaries, CifA localization in the embryos, and an impaired histone-to-protamine transition during spermiogenesis of any mosquito species. Overall, these sperm modification findings may enable future optimization of CI efficacy in vectors or pests that are refractory to Wolbachia transinfections.
Topics: Animals; Female; Male; Aedes; Drosophila melanogaster; Wolbachia; Histones; Arboviruses; Mosquito Vectors; Semen; Drosophila; Chromatin; Protamines
PubMed: 38547237
DOI: 10.1371/journal.pbio.3002573 -
Biochemical Society Transactions Apr 2024A large number of mRNAs of maternal origin are produced during oogenesis and deposited in the oocyte. Since transcription stops at the onset of meiosis during oogenesis... (Review)
Review
A large number of mRNAs of maternal origin are produced during oogenesis and deposited in the oocyte. Since transcription stops at the onset of meiosis during oogenesis and does not resume until later in embryogenesis, maternal mRNAs are the only templates for protein synthesis during this period. To ensure that a protein is made in the right place at the right time, the translation of maternal mRNAs must be activated at a specific stage of development. Here we summarize our current understanding of the sophisticated mechanisms that contribute to the temporal repression of maternal mRNAs, termed maternal mRNA dormancy. We discuss mechanisms at the level of the RNA itself, such as the regulation of polyadenine tail length and RNA modifications, as well as at the level of RNA-binding proteins, which often block the assembly of translation initiation complexes at the 5' end of an mRNA or recruit mRNAs to specific subcellular compartments. We also review microRNAs and other mechanisms that contribute to repressing translation, such as ribosome dormancy. Importantly, the mechanisms responsible for mRNA dormancy during the oocyte-to-embryo transition are also relevant to cellular quiescence in other biological contexts.
Topics: Animals; Humans; Oocytes; Oogenesis; RNA, Messenger; MicroRNAs; RNA, Messenger, Stored; RNA-Binding Proteins; Protein Biosynthesis; Gene Expression Regulation, Developmental; Female; Embryonic Development
PubMed: 38477334
DOI: 10.1042/BST20231122 -
International Journal of Molecular... Feb 2024CTP synthase (CTPS) catalyzes the final step of de novo synthesis of CTP. CTPS was first discovered to form filamentous structures termed cytoophidia in ovarian cells....
CTP synthase (CTPS) catalyzes the final step of de novo synthesis of CTP. CTPS was first discovered to form filamentous structures termed cytoophidia in ovarian cells. Subsequent studies have shown that cytoophidia are widely present in cells of three life domains. In the ovary model, our previous studies mainly focused on the early and middle stages, with less involvement in the later stages. In this work, we focus on the later stages of female germline cells in . We use live-cell imaging to capture the continuous dynamics of cytoophidia in Stages 10-12. We notice the heterogeneity of cytoophidia in the two types of germline cells (nurse cells and oocytes), manifested in significant differences in morphology, distribution, and dynamics. Surprisingly, we also find that neighboring nurse cells in the same egg chamber exhibit multiple dynamic patterns of cytoophidia over time. Although the described dynamics may be influenced by the in vitro incubation conditions, our observation provides an initial understanding of the dynamics of cytoophidia during late-stage oogenesis.
Topics: Animals; Female; Drosophila; Carbon-Nitrogen Ligases; Oogenesis; Cytoskeleton; Oocytes
PubMed: 38473824
DOI: 10.3390/ijms25052575 -
Cellular and Molecular Life Sciences :... Mar 2024Reproduction, a fundamental feature of all known life, closely correlates with energy homeostasis. The control of synthesizing and mobilizing lipids are dynamic and...
Reproduction, a fundamental feature of all known life, closely correlates with energy homeostasis. The control of synthesizing and mobilizing lipids are dynamic and well-organized processes to distribute lipid resources across tissues or generations. However, how lipid homeostasis is precisely coordinated during insect reproductive development is poorly understood. Here we describe the relations between energy metabolism and reproduction in the silkworm, Bombyx mori, a lepidopteran model insect, by using CRISPR/Cas9-mediated mutation analysis and comprehensively functional investigation on two major lipid lipases of Brummer (BmBmm) and hormone-sensitive lipase (BmHsl), and the sterol regulatory element binding protein (BmSrebp). BmBmm is a crucial regulator of lipolysis to maintain female fecundity by regulating the triglyceride (TG) storage among the midgut, the fat body, and the ovary. Lipidomics analysis reveals that defective lipolysis of females influences the composition of TG and other membrane lipids in the BmBmm mutant embryos. In contrast, BmHsl mediates embryonic development by controlling sterol metabolism rather than TG metabolism. Transcriptome analysis unveils that BmBmm deficiency significantly improves the expression of lipid synthesis-related genes including BmSrebp in the fat body. Subsequently, we identify BmSrebp as a key regulator of lipid accumulation in oocytes, which promotes oogenesis and cooperates with BmBmm to support the metabolic requirements of oocyte production. In summary, lipid homeostasis plays a vital role in supporting female reproductive success in silkworms.
Topics: Animals; Female; Bombyx; Oogenesis; Ovary; Embryonic Development; Lipids; Insect Proteins
PubMed: 38472536
DOI: 10.1007/s00018-024-05173-8 -
Development (Cambridge, England) Mar 2024Gametogenesis is the process through which germ cells differentiate into sexually dimorphic gametes, eggs and sperm. In the teleost fish medaka (Oryzias latipes), a germ...
Gametogenesis is the process through which germ cells differentiate into sexually dimorphic gametes, eggs and sperm. In the teleost fish medaka (Oryzias latipes), a germ cell-intrinsic sex determinant, foxl3, triggers germline feminization by activating two genetic pathways that regulate folliculogenesis and meiosis. Here, we identified a pathway involving a dome-shaped microtubule structure that may be the basis of oocyte polarity. This structure was first established in primordial germ cells in both sexes, but was maintained only during oogenesis and was destabilized in differentiating spermatogonia under the influence of Sertoli cells expressing dmrt1. Although foxl3 was dispensable for this pathway, dazl was involved in the persistence of the microtubule dome at the time of gonocyte development. In addition, disruption of the microtubule dome caused dispersal of bucky ball RNA, suggesting the structure may be prerequisite for the Balbiani body. Collectively, the present findings provide mechanistic insight into the establishment of sex-specific polarity through the formation of a microtubule structure in germ cells, as well as clarifying the genetic pathways implementing oocyte-specific characteristics.
Topics: Animals; Female; Male; Oryzias; Semen; Germ Cells; Gametogenesis; Oogenesis
PubMed: 38471539
DOI: 10.1242/dev.201840 -
Integrative Organismal Biology (Oxford,... 2024For many fishes, reproductive function is thermally constrained such that exposure to temperatures above some upper threshold has detrimental effects on gametic...
For many fishes, reproductive function is thermally constrained such that exposure to temperatures above some upper threshold has detrimental effects on gametic development and maturation, spawning frequency, and mating behavior. Such impairment of reproductive performance at elevated temperatures involves changes to hypothalamic-pituitary-gonadal (HPG) axis signaling and diminished gonadal steroidogenesis. However, how HPG pathways respond to consistently high versus temporally elevated temperatures is not clear. Here, sexually mature Amargosa River Pupfish () were maintained under thermal regimes of either stable ∼25°C (low temperature), diurnal cycling temperatures between ∼27 and 35°C (fluctuating temperature), or stable ∼35°C (high temperature) conditions for 50 days to examine effects of these conditions on HPG endocrine signaling components in the pituitary gland and gonad, ovarian and testicular gametogenesis status, and liver gene expression relating to oogenesis. Female pupfish maintained under stable high and fluctuating temperature treatments showed reduced gonadosomatic index values as well as a lower proportion of oocytes in the lipid droplet and vitellogenic stages. Females in both fluctuating and stable 35°C conditions exhibited reduced ovarian mRNAs for steroid acute regulatory protein (), cholesterol side chain-cleavage enzyme, P450scc (), and 3β-hydroxysteroid dehydrogenase (), while ovarian transcripts encoding 11β-hydroxysteroid dehydrogenase () and sex hormone-binding globulin () were elevated in females at constant 35°C only. Ovarian aromatase () mRNA levels were unaffected, but circulating 17β-estradiol (E) was lower in females at 35°C compared to the fluctuating temperature condition. In the liver, mRNA levels for choriogenins and vitellogenin were downregulated in both the fluctuating and 35°C conditions, while hepatic estrogen receptor 2a () and mRNAs were elevated in 35°C females. Taken together, these results demonstrate the potential for elevated temperatures to impair ovarian steroidogenesis and reduce egg envelope and vitellogenin protein production in female pupfish, while also shedding light on how thermal regimes that only intermittently reach the upper thermal range for reproduction have differential impacts on reproductive endocrine pathways than constantly warm conditions.
PubMed: 38464886
DOI: 10.1093/iob/obae003 -
Cell Reports Mar 2024Reproduction is an energy-intensive process requiring systemic coordination. However, the inter-organ signaling mechanisms that relay nutrient status to modulate...
Reproduction is an energy-intensive process requiring systemic coordination. However, the inter-organ signaling mechanisms that relay nutrient status to modulate reproductive output are poorly understood. Here, we use Drosophila melanogaster as a model to establish the integrated stress response (ISR) transcription factor, Atf4, as a fat tissue metabolic sensor that instructs oogenesis. We demonstrate that Atf4 regulates lipase activity to mediate yolk lipoprotein synthesis in the fat body. Depletion of Atf4 in the fat body also blunts oogenesis recovery after amino acid deprivation and re-feeding, suggestive of a nutrient-sensing role for Atf4. We also discovered that Atf4 promotes secretion of a fat-body-derived neuropeptide, CNMamide, which modulates neural circuits that promote egg-laying behavior (ovulation). Thus, we posit that ISR signaling in fat tissue acts as a "metabolic sensor" that instructs female reproduction-directly by impacting yolk lipoprotein production and follicle maturation and systemically by regulating ovulation.
Topics: Animals; Female; Drosophila melanogaster; Oogenesis; Ovulation; Oocytes; Lipoproteins
PubMed: 38457339
DOI: 10.1016/j.celrep.2024.113863 -
Journal of Chemical Ecology Apr 2024Many plant species, particularly legumes, protect themselves with saponins. Previously, a correlation was observed between levels of oleanolic acid-derived saponins,...
Many plant species, particularly legumes, protect themselves with saponins. Previously, a correlation was observed between levels of oleanolic acid-derived saponins, such as hederagenin-derived compounds, in the legume Medicago truncatula and caterpillar deterrence. Using concentrations that reflect the foliar levels of hederagenin-type saponins, the sapogenin hederagenin was not toxic to 4th instar caterpillars of the cabbage looper Trichoplusia ni nor did it act as a feeding deterrent. Female caterpillars consumed more diet than males, presumably to obtain the additional nutrients required for oogenesis, and are, thus, exposed to higher hederagenin levels. When fed the hederagenin diet, male caterpillars expressed genes encoding trypsin-like proteins (LOC113500509, LOC113501951, LOC113501953, LOC113501966, LOC113501965, LOC113499659, LOC113501950, LOC113501948, LOC113501957, LOC113501962, LOC113497819, LOC113501946, LOC113503910) as well as stress-responsive (LOC113503484, LOC113505107) proteins and cytochrome P 6B2-like (LOC113493761) at higher levels than females. In comparison, female caterpillars expressed higher levels of cytochrome P 6B7-like (LOC113492289). Bioinformatic tools predict that cytochrome Ps could catalyze the oxygenation of hederagenin which would increase the hydrophilicity of the compound. Expression of a Major Facilitator Subfamily (MFS) transporter (LOC113492899) showed a hederagenin dose-dependent increase in gene expression suggesting that this transporter may be involved in sapogenin efflux. These sex-related differences in feeding and detoxification should be taken into consideration in insecticide evaluations to minimize pesticide resistance.
Topics: Animals; Female; Male; Saponins; Oleanolic Acid; Moths; Transcriptome; Larva; Sex Characteristics
PubMed: 38443712
DOI: 10.1007/s10886-024-01482-1 -
ISME Communications Jan 2024Insects typically acquire their beneficial microbes early in development. Endosymbionts housed intracellularly are commonly integrated during oogenesis or embryogenesis,...
Insects typically acquire their beneficial microbes early in development. Endosymbionts housed intracellularly are commonly integrated during oogenesis or embryogenesis, whereas extracellular microbes are only known to be acquired after hatching by immature instars such as larvae or nymphs. Here, however, we report on an extracellular symbiont that colonizes its host during embryo development. Tortoise beetles (: ) host their digestive bacterial symbiont extracellularly within foregut symbiotic organs and in ovary-associated glands to ensure its vertical transmission. We outline the initial stages of symbiont colonization and observe that although the foregut symbiotic organs develop 3 days prior to larval emergence, they remain empty until the final 24 h of embryo development. Infection by occurs during that timeframe and prior to hatching. By experimentally manipulating symbiont availability to embryos in the egg, we describe a 12-h developmental window governing colonization by . Symbiotic organs form normally in aposymbiotic larvae, demonstrating that these -bearing structures develop autonomously. In adults, the foregut symbiotic organs are already colonized following metamorphosis and host a stable population to facilitate folivory. The ovary-associated glands, however, initially lack . Symbiont abundance subsequently increases within these transmission organs, thereby ensuring sufficient titers at the onset of oviposition ~29 days following metamorphosis. Collectively, our findings reveal that colonization precedes larval emergence, where its proliferation is eventually decoupled in adult beetles to match the nutritional and reproductive requirements of its host.
PubMed: 38439943
DOI: 10.1093/ismeco/ycae005