RNA Synthesis and Storage During Insect Oogenesis

Berry, Spencer J.

doi:10.1007/978-1-4615-6814-8_8

Cited by 6 publications

(4 citation statements)

References 70 publications

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“…Our findings demonstrated that during mid-previtellogenesis, dark follicle cells add RNA to the oocyte cytoplasm; thus, cortical vesicles containing RNA appear in the oocyte cortex. This transfer is similar to that observed in insects and other invertebrates, where nurse cells support oocyte development by supplying nutrients, RNAs, proteins and organelles (Bonhag, 1958;King & Devine, 1958;Berry, 1985;Robinson et al, 1994;Nezis et al, 2003). The same process was observed in lizards between the pyriform cells and the oocyte (Andreuccetti, 1992).…”

Section: Discussionsupporting

confidence: 80%

Ultrastructural changes in the follicular epithelium ofCeratophrys cranwelliprevitellogenic oocytes

Villecco

Mónaco

Sánchez

2007

Zygote

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In this work we carried out ultrastructural, autoradiographic and biochemical analyses of the follicular epithelium during C. cranwelli previtellogenesis. This study revealed that the follicular epithelium in early previtellogenesis is constituted of a single layer of squamous homogeneous cells. During mid-previtellogenesis two types of cells develop: dark cells and clear cells. The follicular dark cells are actively involved in the synthesis of RNA, which is transferred to the oocyte through the interface. In late previtellogenesis the dark cells show apoptotic characteristics such as chromatin condensation, DNA fragmentation and cytoplasm shrinkage. This process forms apoptotic bodies that seem to be engulfed by the oocyte. Our results show evidence that, during mid- and late C. cranwelli previtellogenesis, the follicular epithelium undergoes remodelling processes interacting with the oocyte.

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Section: Discussionsupporting

confidence: 80%

Ultrastructural changes in the follicular epithelium ofCeratophrys cranwelliprevitellogenic oocytes

Villecco

Mónaco

Sánchez

2007

Zygote

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“…However, this theory was contradicted by miR-309 depletion, which caused a decrease in many crucial enzymes involved, such as Acyl-CoA dehydrogenases (ACADs, AAEL014452) and Stearoyl-CoA desaturase (SCD, AAEL007213) (41), likely resulting in fewer UFAs in mature oocytes and insufficient energy for embryogenesis. In addition, mature eggs contained large amounts of RNAs in the form of ribosomes, transfer RNA, and maternal mRNA to support programmed protein synthesis during early embryogenesis due to the absence of zygotic transcription (42). Purine metabolism is the one basic de novo synthesis pathway of purine nucleotides, starting from 5-phosphoribosyl-1-pyrophosphate, and finally purine nucleoside triphosphates such as ATP and GTP are produced after a series of steps, providing the basic blocks for RNA synthesis (43).…”

Section: Discussionmentioning

confidence: 99%

microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti

Zhang

Zhao

Roy

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

103

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Obligatory blood-triggered reproductive strategy is an evolutionary adaptation of mosquitoes for rapid egg development. It contributes to the vectorial capacity of these insects. Therefore, understanding the molecular mechanisms underlying reproductive processes is of particular importance. Here, we report that microRNA-309 (miR-309) plays a critical role in mosquito reproduction. A spatiotemporal expression profile of miR-309 displayed its blood feeding-dependent onset and ovary-specific manifestation in female Aedes aegypti mosquitoes. Antagomir silencing of miR-309 impaired ovarian development and resulted in nonsynchronized follicle growth. Furthermore, the genetic disruption of miR-309 by CRISPR/Cas9 system led to the developmental failure of primary follicle formation. Examination of genomic responses to miR-309 depletion revealed that several pathways associated with ovarian development are down-regulated. Comparative analysis of genes obtained from the high-throughput RNA sequencing of ovarian tissue from the miR-309 antagomirsilenced mosquitoes with those from the in silico computation target prediction identified that the gene-encoding SIX homeobox 4 protein (SIX4) is a putative target of miR-309. Reporter assay and RNA immunoprecipitation confirmed that SIX4 is a direct target of miR-309. RNA interference of SIX4 was able to rescue phenotypic manifestations caused by miR-309 depletion. Thus, miR-309 plays a critical role in mosquito reproduction by targeting SIX4 in the ovary and serves as a regulatory switch permitting a stage-specific degradation of the ovarian SIX4 mRNA. In turn, this microRNA (miRNA)-targeted degradation is required for appropriate initiation of a blood feeding-triggered phase of ovarian development, highlighting involvement of this miRNA in mosquito reproduction.Homeobox protein gene | microRNA | CRISPR/Cas9 | ovary | fast evolution T ransmission of mosquito-borne diseases brings enormous human suffering, with more than 1 million deaths worldwide annually. The yellow fever mosquito Aedes aegypti has reemerged as one of the most dangerous vectors of human diseases, transmitting Dengue fever, Yellow fever, Chikungunya, and Zika virus (1-4). Because of the lack of effective vaccines and increasing drug resistance in pathogens, biological control is considered one of the most promising strategies for preventing disease transmission. In particular, female hematophagous mosquitoes rely on acquisition of blood to initiate a series of physiological events promoting egg development (5, 6). Therefore, understanding the molecular mechanisms underlying ovarian activation is of great significance for the development of effective approaches to control mosquito-borne diseases (7,8).MicroRNAs (miRNAs) are small noncoding RNAs that regulate gene expression at the posttranscriptional level through translational repression or mRNA decay (9). Hence, miRNAs play significant roles in governing multiple functions in animals and plants via integrating sophisticated miRNA-mRNA regulatory networks (10, 11...

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“…We have analysed the distribution of poly(A) + RNA and some molecular compounds linked to mRNA export in transcriptionally active and inert nuclei of insect oocytes. Inactivation of the oocyte genome seems to be a rule for organisms with ‘nutrimental’ oogenesis when growing oocytes are accompanied by polyploid and highly active nurse cells that provide an oocyte with RNA (Berry, 1985). Correspondingly, oocyte chromosomes of such animals condense to form a karyosphere at a defined stage of oocyte growth (Gruzova and Parfenov, 1993; Bogolyubov and Parfenov, 2008).…”

Section: Discussionmentioning

confidence: 99%

Interchromatin granule clusters of the scorpionfly oocytes contain poly(A)⁺ RNA, heterogeneous ribonucleoproteins A/B and mRNA export factor NXF1

Batalova

Bogolyubov

Parfenov

2010

Cell Biology International

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IGCs (interchromatin granule clusters), or nuclear speckles, are one of the most universal subnuclear organelles of eukaryotic cells. We have used insect oocytes to study the possible association of poly(A)+ RNA and some factors involved in mRNA export with IGCs. Oogenesis of the mecopteran, Panorpa communis, used as a model object, is characterized by a strict cessation of oocyte genome transcription activity towards the end of oocyte growth. Our previous studies on P. communis oocyte nuclei have shown that oocyte IGC counterparts in this species are very unusual, both in morphology and molecular composition, compared with the typical IGCs of mammalian somatic cells traditionally used as a model system. We have now used microinjections of 2'-O-Me(U)₂₂ probes conjugated with the fluorochrome TAMRA to localize poly(A)+ RNA in IGCs. RNA export proteins were also detected by immunofluorescent/confocal and immunogold labelling electron microscopy. We found that poly(A)+ RNA, hnRNPs A/B and NXF1 mRNA export factors are located in IGCs regardless of the transcriptional status of the nucleus. Our data support the idea of IGCs as universal and conserved nuclear domains that serve not only as splicing factor reservoirs, but also take part in mRNA retention and export.

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RNA Synthesis and Storage During Insect Oogenesis

Cited by 6 publications

References 70 publications

Ultrastructural changes in the follicular epithelium ofCeratophrys cranwelliprevitellogenic oocytes

Ultrastructural changes in the follicular epithelium ofCeratophrys cranwelliprevitellogenic oocytes

microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti

Interchromatin granule clusters of the scorpionfly oocytes contain poly(A)⁺ RNA, heterogeneous ribonucleoproteins A/B and mRNA export factor NXF1

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RNA Synthesis and Storage During Insect Oogenesis

Cited by 6 publications

References 70 publications

Ultrastructural changes in the follicular epithelium ofCeratophrys cranwelliprevitellogenic oocytes

Ultrastructural changes in the follicular epithelium ofCeratophrys cranwelliprevitellogenic oocytes

microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti

Interchromatin granule clusters of the scorpionfly oocytes contain poly(A)+ RNA, heterogeneous ribonucleoproteins A/B and mRNA export factor NXF1

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Interchromatin granule clusters of the scorpionfly oocytes contain poly(A)⁺ RNA, heterogeneous ribonucleoproteins A/B and mRNA export factor NXF1