Biochemical research on oogenesis. RNA accumulation during oogenesis of the dogfish Scyliorhinus caniculus.
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Animals↗
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Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology.
In mutagenesis screens for recessive female sterile mutations on the second chromosome of Drosophila melanogaster 528 lines were isolated which allow the homozygous females to survive but cause sterility. In 62 of these lines early stages of oogenesis are affected, and these females usually do not lay any eggs. In 333 lines oogenesis proceeds apparently normally to stage 8 of oogenesis, but morphological defects become often apparent during later stages of oogenesis, and are visible in the defective eggs produced by these females whereas 133 lay eggs that appear morphologically normal, but do not support normal embryonic development. Of the lines 341 have been genetically characterized and define a total of 140 loci on the second chromosome. Not all the loci are specific for oogenesis. From the numbers obtained we estimate that the second chromosome of Drosophila contains about 13 loci that are relatively specific for early oogenesis, 70 loci that are specifically required in mid to late oogenesis, and around 30 maternal-effect lethals.
Animals↗
Origin and spatial distribution of maternal messenger RNA during oogenesis of an insect, Oncopeltus fasciatus.
In order to investigate the origin and spatial distribution of maternal mRNA during oogenesis, in situ hybridization with [3H]-poly(U) was utilized for the detection of poly(A)-containing RNA [poly(A)+RNA] in histological sections of Oncopeltus fasciatus ovaries. In the germarium poly(A)+RNA was found to accumulate in the trophocyte cytoplasm concomitant with the maturation of these cells. Poly(A)+RNA was also detected in the trophic cores and nutritive tubes suggesting that these channels participate in the transport of trophocyte-derived mRNA to the oocytes. Although large amounts of poly(A)+RNA were also detected in the cytoplasm of the follicle cells, particularly during late vitellogenesis when pseudopod-like processes projected into the ooplasm, no evidence was obtained for the transport of poly(A)+RNA from these processes to the oocytes. The content of poly(A)+RNA in the oocyte cytoplasm continually increased during oogenesis. In stage 2--4 oocytes poly(A)+RNA accumulation occurred in the apparent absence of transcriptional activity in the germinal vesicle nuclei suggesting that most maternal mRNA molecules synthesized during early oogenesis are of trophocyte origin. Poly(A)+RNA also continued to accumulate after chorion formation, when the nutritive tubes are longer active in RNA transport. This implies that other sources of maternal mRNA may exist during late oogenesis. The distribution of poly(A)+RNA molecules in the oocyte cytoplasm appeared to be uniform throughout oogenesis with one exception. During late vitellogenesis poly(A)+RNA activity was significantly enhanced in the anterior and posterior periplasmic cytoplasms relative to the lateral periplasm and the endoplasm. After chorion formation these variations disappeared. The results suggest that maternal mRNA molecules arise from at least 2 sources during oogenesis. During late vitellogenesis these molecules appear to be subject to differential localization in the polar perimeters of the oocyte cytoplasm.
Animals↗
The effects of orchidectomy and gonadotropins on steroidogenesis and oogenesis in Bidder's organs of the toad Bufo woodhousii.
In the family Bufonidae, male toads possess rudimentary ovaries, called Bidder's organs, which are attached to the testes. The mechanisms involved in the inhibition of oogenesis in these structures were investigated in male Bufo woodhousii. Orchidectomized and sham-operated animals were injected with gonadotropins (pregnant mare serum gonadotropin [PMSG] + human chorionic gonadotropin [hCG]) for 26 days and the effects of these hormones on oogenesis and steroidogenic activity (3 beta-hydroxysteroid dehydrogenase [3 beta-HSD] and 17 beta-HSD) in the Bidder's organ were quantified. Bilateral orchidectomy alone resulted in the growth of bidderian oocytes and a shift towards later stages of oogenesis. Gonadotropins enhanced this effect and stimulated the proliferation of new germ cells. In the presence of testes, however, bidderian oogenesis remained inhibited despite high levels of circulating gonadotropins. In both ooplasm and follicular layers of the bidderian oocytes of all toads, 3 beta-HSD and 17 beta-HSD activities were detected by histochemistry. Follicular enzymatic activity increased in orchidectomized toads treated with PMSG + hCG but decreased in sham-operated toads treated with gonadotropins. Testis weights, rudimentary oviduct weights, and plasma steroid levels increased in intact toads injected with hCG + PMSG. Gonadotropins had no effect on plasma steroid levels in orchidectomized toads, however. These results suggest that the testes play a major role in the inhibition of oogenesis in Bidder's organs of B. woodhousii and are a major source of androgens. High circulating levels of gonadotropins do not overcome the inhibitory effects of the testes.
Analysis of Variance↗
Polymorphism and reproductive mode in the rotifer, Asplanchna sieboldi: relationship between meiotic oogenesis and shape of body-wall outgrowths.
Sexuality and polymorphism are closely coupled in the rotifer Asplanchna sieboldi. In a graded response to dietary tocopherol, embryos develop body-wall outgrowths of various sizes and shapes. Also in a graded response to this compound, some of the affected females produce eggs undergoing meiotic instead of mitotic oogenesis. The haploid eggs of such mictic females develop parthenogenetically into males instead of females. The incidence of mictic females among animals with different shapes was studied among cohorts from mothers subjected to different inducing conditions. The hypothesis that external tocopherol concentrations absolutely fix the probability of meiotic oogenesis was rejected. The other extreme hypothesis, that the probability of meiotic oogenesis is fixed by morphotype, was rejected for animals at the low end of the morphotypic scale but accepted for the more strongly-affected individuals. The probability of meiotic oogenesis is thus constant for the higher morphotypes. The ascertainment of morphotype frequencies in natural or laboratory populations may suffice for estimating the incidence of sexual forms; furthermore studies of factors affecting the body-wall-outgrowth response may also bear directly upon regulation of sexual reproduction in this species.
Animals↗
Regulation of the Xenopus laevis transcription factor IIIA gene during oogenesis and early embryogenesis: negative elements repress the O-TFIIIA promoter in embryonic cells.
Expression of the Xenopus laevis transcription factor IIIA (TFIIIA) gene is developmentally regulated. In this study we have used defined nucleotide mutations to map cis-elements involved in transcriptional regulation of the promoter for oocyte-TFIIIA (O-TFIIIA) in stage II-IV oocytes, stage VI oocytes, and tail bud embryos. During oogenesis O-TFIIIA mRNA levels decline 5- to 10-fold, and during early embryogenesis O-TFIIIA mRNA levels decline approximately 10(6)-fold per cell. In stage II-IV oocytes we find evidence for at least three distinct positive-acting cis-elements that contribute to the efficient expression of O-TFIIIA. These elements are located between -1800 to -425, -280 to -235, and -235 to -220. The most distal cis-element(s) appears to be developmentally regulated during oogenesis, since deletion of nucleotide sequences from -1800 to -425 does not reduce O-TFIIIA expression in stage VI oocytes. However, the two cis-elements located between -280 to -235 and -235 to -220 are required for the efficient expression of O-TFIIIA in stage VI oocytes. In tail bud embryos we find evidence for several developmentally regulated positive and negative cis-elements involved in O-TFIIIA expression. The positive-acting cis-elements are located between -159 to -110 and -110 to -58. The negative-acting cis-elements are found at positions -425 to -350 and -200 to -159. In addition to the developmentally regulated elements controlling O-TFIIIA gene expression in tail bud embryos, the positive-acting cis-elements active during oogenesis (located between -280 to -235 and -235 to -220) are also active during early embryogenesis. Thus, transcription from the O-TFIIIA promoter appears to be regulated by a combination of constitutive positive factors and developmentally regulated positive and negative factors during oogenesis and early embryogenesis.
Animals↗
Gene expression during oogenesis in mice.
A mouse egg is the end-product of oogenesis--a process initiated during fetal development and completed months later at the time of sperm-egg fusion. Oogenesis includes many important events. Among these are formation of female germ cells, initiation and completion of meiosis, and establishment of a maternal store of materials to support fertilization and preimplantation development. The latter takes place largely during germ cell growth in sexually mature females and involves extensive gene expression. Ribonucleic acid and protein accumulate to unusually high levels during this relatively short phase of oogenesis. Recent studies have demonstrated that establishment of a maternal store of materials in the growing mouse egg is both transcriptionally and translationally regulated. Specific examples of both types of regulation are presented here in the context of gene expression during oogenesis in mice.
Animals↗
Mitochondrial development during Drosophila oogenesis: distribution, density and in situ RNA hybridizations.
The changes in distribution and density of mitochondria and the level of mitochondrial RNA during Drosophila oogenesis were studied simultaneously in the 3 cell types ie follicle cells, nurse cells and oocyte, making up the egg chamber. Up to stage 6, mitochondrial density (mitochondrial and cellular areas ratio) was elevated and increased similarly in both follicle and nurse cells. Thereafter the mitochondrial density of follicle cells continued to increase and that of the nurse cells declined markedly while the nurse cell mitochondria assembled in dense groups and decreased in size. This can be related to a transfer of nurse cell cytoplasm, including mitochondria, to the oocyte. In the oocyte from stage 4 to stage 7 we observed a significant decrease of the mitochondrial density due to the absence of mitochondrial biogenesis. Then the cytoplasm transfer caused mitochondrial density to increase up to the level found in the nurse cells at the end of oogenesis. The mature oocyte contains enough mitochondria to supply 15,000 somatic cells. Our results strongly suggest that the variations in size, distribution and density of mitochondria relate to the particular energetic requirements of the different cell types during the first half of oogenesis. Later they relate to the developmental requirements of the nurse cells and the oocyte, in particular the storage of mitochondria in the oocyte. The level of mitochondrial RNA was studied through in situ hybridization. Throughout oogenesis the follicle and nurse cell RNA evolved similarly. Up to stage 9, there was no change in RNA densities in these cells, suggesting a correlation with the cell volume and/or the nuclear DNA content. Thereafter the cellular RNA concentration declined rapidly. In the oocyte the RNA concentration evolved differently especially from stage 10 to the end, the RNA density being stabilized. This can be related to the injection of nurse cell mitochondria, followed by their assignment to reserve status. Our results suggest that the mt RNA density is under extramitochondrial control mechanisms.
Animals↗
RNA Pol I activity is required for meiotic chromatin organization and the H3K4me3 gradient essential for oogenesis, independent of ribosome synthesis.
Oogenesis requires extensive and dynamic chromatin remodeling that primes gene promoters for later transcriptional activation during embryonic development. Here, we uncover a pivotal, non-canonical role for RNA Polymerase I (Pol I) in driving these chromatin state transitions during Caenorhabditis elegans oogenesis. Using the auxin-inducible degron system to selectively deplete either Pol I catalytic subunits or ribosome assembly factors, we disentangle the consequences of impaired nucleolar integrity from reductions in ribosome biogenesis. Strikingly, although disrupting ribosome assembly caused minimal effects on oocyte production, loss of Pol I activity led to widespread changes in chromatin accessibility, a dampening of the distal-proximal H3K4me3 gradient required for oogenesis, reduced synapsis, and elevated ATM/ATR phosphorylation, resulting in fewer but significantly larger oocytes. Despite their promoters becoming more accessible, oogenesis genes did not show large changes in steady-state mRNA, consistent with transcriptional repression prior to fertilization. Instead, Pol I depletion prematurely remodeled oogenic chromatin, through a misdirection of H3K4me3 deposition towards promoters normally primed for zygotic genome activation. These findings reveal an epigenetic gating function for nucleolar integrity in oocyte maturation: Pol I preserves three-dimensional chromatin organization and maintains proper spatiotemporal regulation of histone modifications, independent of ribosome production. Given the evolutionary conservation of nucleolar dynamics and histone modifications during gametogenesis, our work suggests that nucleolar stress, whether from environmental factors, aging, or genetic disorders, could broadly compromise fertility by disrupting oogenic chromatin priming.
Journal Article↗
Oogenesis and germinal bed morphology of the brown anole (A. sagrei).
BACKGROUND: The brown anole is a model species of the genus Anolis, a squamate (encompassing lizards and snakes) group widely studied in evolutionary, behavioral, and developmental biology. Full genome annotation, the establishment of gene editing techniques, and comprehensive description of reproductive tract morphology and embryogenesis in this species, has laid the foundation for functional studies. However, analysis of brown anole oogenesis is still required and vital to optimize genome modification, mutant line establishment, and analyses of the evolution of reproductive developmental mechanisms. RESULTS: Here, we characterize ovary morphology and gametogenesis in the female brown anole, A. sagrei using brightfield imaging, microCT, histology staining, electron microscopy, and confocal imaging. We define 10 stages of oocyte maturation which commences inside the oogonial nest within the germinal bed and concludes with the mature follicle ready to ovulate based on follicle size, yolk-acquisition, and follicular, cellular, and basement membrane architecture. CONCLUSIONS: We describe the complete oogenesis of the brown anole in 10 stages and report that oogenesis is highly conserved within iguanids, a suborder of lizards. With our staging framework, we lay the foundation for functional studies of oogenesis and optimized gene-editing.
Journal Article↗
Quantitative determination of amplified rDNA and its distribution during oogenesis in Xenopus laevis.
The number of extra-chromosomal nucleoli and their rDNA content were determined during oogenesis in Xenopus laevis. The highly variable number of nucleoli (500 to 2,500) in oocytes of the same stage and from the same female or of different stages or from different females is not a measure of the extent of amplification. In all oocytes examined, a inversely proportional relation was found between the number of nucleoli in an oocyte and their mean rDNA content. These results indicate that there is no variation of the rDNA content of oocytes during oogenesis nor between oocytes of different females. The varying nucleolar numbers found in oocytes result thus from fusion and fission of pre-existing nucleoli. The determination of the rDNA content, in absolute units (35 pg), after amplification which occurs at the beginning of oogenesis, makes it possible to calculate the rDNA content of one nucleolus. This ranged from 0.7.10(-2) pg to 15.10(-2) pg, corresponding to about 500--11,000 cistrons of rDNA. No distinct size classes between these two extremes were observed.
Animals↗
RNA-protein interactions of stored 5S RNA with TFIIIA and ribosomal protein L5 during Xenopus oogenesis.
We studied the pathway of 5S RNA during oogenesis in Xenopus laevis from its storage in the cytoplasm to accumulation in the nucleus, the sequence requirements for the 5S RNA to follow that pathway, and the 5S RNA-protein interactions that occur during the mobilization of stored 5S RNA for assembly into ribosomes. In situ hybridization to sections of oocytes indicates that 5S RNA first becomes associated with the amplified nucleoli during vitellogenesis when the nucleoli are activity synthesizing ribosomal RNA and assembling ribosomes. When labeled 5S RNA is microinjected into the cytoplasm of stage V oocytes, it migrates into the nucleus, whether microinjected naked or complexed with the protein TFIIIA as a 7S RNP storage particle. During vitellogenesis, a nonribosome bound pool of 5S RNA complexed with ribosomal protein L5 (5S RNPs) is formed, which is present throughout the remainder of oogenesis. Immunoprecipitation assays on homogenates of microinjected oocytes showed that labeled 5S RNA can become complexed either with L5 or with TFIIIA. Nucleotides 11 through 108 of the 5S RNA molecule provide the necessary sequence and conformational information required for the formation of immunologically detectable complexes with TFIIIA or L5 and for nuclear accumulation. Furthermore, labeled 5S RNA from microinjected 7S RNPs can subsequently become associated with L5. Such labeled 5S RNA is found in both 5S RNPs and 7S RNPs in the cytoplasm, but only in 5S RNPs in the nucleus of microinjected oocytes. These data suggest that during oogenesis a major pathway for incorporation of 5S RNA into nascent ribosomes involves the migration of 5S RNA from the nucleus to the cytoplasm for storage in an RNP complex with TFIIIA, exchange of that protein association for binding with ribosomal protein L5, and a return to the nucleus for incorporation into ribosomes as they are being assembled in the amplified nucleoli.
Animals↗
Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila.
Oogenesis in Drosophila involves specification of both germ cells and the surrounding somatic follicle cells, as well as the determination of oocyte polarity. We found that two neurogenic genes, Notch and Delta, are required in oogenesis. These genes encode membrane proteins with epidermal growth factor repeats and are essential in the decision of an embryonic ectodermal cell to take on the fate of neuroblast or epidermoblast. In oogenesis, mutation in either gene leads to an excess of posterior follicle cells, a cell fate change reminiscent of the hyperplasia of neuroblasts seen in neurogenic mutant embryos. Furthermore, the Notch mutation in somatic cells causes mislocalization of bicoid in the oocyte. These results suggest that the neurogenic genes Notch and Delta are involved in both follicle cell development and the establishment of anterior-posterior polarity in the oocyte.
Animals↗
Trade-off between antibacterial immune defense and oogenesis progression in female Drosophila melanogaster.
Trade-offs between reproduction and immunity are common in animals, potentially due to preferential allocation of limiting resources. In Drosophila melanogaster, mating stimulates egg production but also triggers a rapid and persistent decrease in female immune defense. Proteins essential for both processes are produced in fat body tissue, which may result in competition for cellular resources that could drive a functional trade-off between reproduction and immune defense. We predicted that arrest of oogenesis prior to egg provisioning would alleviate postmating immune suppression because cellular stress would be relieved, but that postmating immune suppression would be observed in genotypes that fully provision eggs even if fertility is compromised. In the present study, we test these predictions by evaluating postmating immune competence in mated D. melanogaster mutants that arrest oogenesis either prior to, or subsequent to, vitellogenesis. Consistent with our prediction, we find that mated female immune defense is maintained when egg development is arrested prior to vitellogenesis. We find that progression through the vitellogenic stages of oogenesis results in postmating immune suppression, except in the case of a mutant with an egg-retention phenotype, where we infer that the failure to lay eggs results in feedback that inhibits subsequent egg development. We additionally show that elimination of yolk protein synthesis in the fat body and follicle cells of the ovary partially restores female immune capacity. Nevertheless, females that lack yolk protein genes still experience partially reduced immune capacity after mating, suggesting that other reproductive demands also suppress immune defense.
Animals↗
tudor, a posterior-group gene of Drosophila melanogaster, encodes a novel protein and an mRNA localized during mid-oogenesis.
The tudor (tud) locus of Drosophila melanogaster is required during oogenesis for the formation of primordial germ cells and for normal abdominal segmentation. The tud locus was cloned, and its product was identified by Northern analysis of wild-type and tud mutant RNAs. The locus encodes a single mRNA of approximately 8.0 kb that is expressed throughout the life cycle, beginning in the early stages of germ-line development in the female. During oogenesis, tud mRNA appears to be present in the oocyte precursor within the germarial cysts, and in stages 1-3 it accumulates within the developing oocyte. The transcript is localized to the posterior half of the oocyte during oogenetic stages 4-7 but is not detectable within the ooplasm by egg deposition and throughout early embryogenesis. The tud protein has a predicted molecular mass of 285,000 daltons and has no distinctive sequence similarity to known proteins or protein structural motifs. Taken together, these results indicate that the tud product is a novel protein required during oogenesis for establishment of a functional center of morphogenetic activity in the posterior tip of the Drosophila embryo.
Amino Acid Sequence↗
The involvement of the Notch locus in Drosophila oogenesis.
The Notch gene in Drosophila encodes a transmembrane protein with homology to EGF that, in a variety of tissues, appears to mediate cell interactions necessary for cell fate choices. Here we demonstrate that oogenesis and spermatogenesis depend on Notch. We examine the phenotypes of the temperature-sensitive Notch allele, Nts1, and, using a monoclonal antibody, determine the cellular and subcellular distribution of Notch protein during oogenesis. We show that Nts1 is associated with a missense mutation in the extracellular, EGF homologous region of Notch and that at non-permissive temperatures oogenesis is blocked and the subcellular distribution of the protein is altered. In wild-type ovaries, Notch protein is found on the apical surface of somatically derived follicle cells, while in the germline-derived cells the protein is not polarized. These findings are discussed in view of the hypothesis that Notch acts as a multifunctional receptor to mediate developmentally important cell interactions.
Animals↗
[Karyosphere in oogenesis].
The purpose of this review is to draw attention to the peculiar phenomenon during gametogenesis: the formation of the karyosphere. This phenomenon is characterized by concentration of all chromosomes in the limited area of the nucleus and may be considered as alternative of the genome in the state of lumpbrush chromosomes. The formation of the karyosphere is a widely spread phenomenon during oogenesis of different animal classes. The karyosphere can be developed during different stages of oogenesis in different organisms; but as a rule the chromosomes of diploten stage of meiosis take part in its formation. As to functional identity of the karyosphere in different species, special investigations are to be done, but contemporary knowledge of the karyosphere formation reveals some common feature:1) in the karyosphere the chromosomes are in a relatively spiral state as demonstrated by the positive Feulgen reaction; 2) there is a low level of RNA synthesis or the absence of it in the karyosphere; 3) during the karyosphere formation the nucleus is enriched by the acid proteins and a lot of protein granules and structures appearing in a close contact with the karysphere. The more typical examples of the karyosphere formation can be observed in the insect oocytes belonging to the nutrimentary type of oogenesis. In the oocytes of some animals the peculiar protein substances are formed around the chromosome knot and appear as a fibrillar zone. Such karyosphere appears to be a kind of capsule inside the nucleus. The capsules are developed as a result of complex interaction between the main nuclear structures; chromosomes, nucleoli, and nuclear membrane as it is manifested by the analysis of some recent ultrastructural date obtained in some insect and amphibian oocytes. The function of the karyosphere capsule and the role of the nuclear structure (sinaptonemal complex, extrachromosomal DNA, and nuclear membrane) in formation of the capsule, are discussed as well as the ultrastructural and cytochemical similarity between the karyosphere capsule of oocytes and nuclear bodies of somatic cells.
Amphibians↗
Broad-complex function during oogenesis in Drosophila melanogaster.
The Broad-Complex (BR-C) appears to encode factors that mediate ecdysone effects during the larva-adult transition. The main goal of this study was to gain insight into what roles the BR-C might play during oogenesis. The main findings are as follows. First, as determined by heteroallele studies and clonal analysis, de12 is a somatic line mutation that appears to fall into the broad domain of the BR-C. Second, the de12 mutation is associated with the insertion of the gypsy transposon at position 169.5 (Chao and Guild, Embo J, 1986, 5:143-150) in the BR-C domain. In its new context this gypsy element exhibits ovarian-specific activation. Both this gypsy activation and the de12 phenotype are partially suppressible by su(f) and su(Hw). Third, we have identified a set of transcripts that cross-hybridize with BR-C sequence spanning the gypsy insertion site (166-179). There are significant differences in these cross-hybridizing species, both in size and relative abundance, between de12 and its parent strain. Finally we have determined that in de12 there is a premature arrest of chorion gene amplification in the late stages of oogenesis.
Animals↗