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Developmental regulation of oocyte lipid intake through 'patent' follicular epithelium in Drosophila melanogaster.

ABSTRACT: Epithelia form protective permeability barriers that selectively allow the exchange of material while maintaining tissue integrity under extreme mechanical, chemical, and bacterial loads. Here, we report in the Drosophila follicular epithelium a developmentally regulated and evolutionarily conserved process "patency", wherein a breach is created in the epithelium at tricellular contacts during mid-vitellogenesis. In Drosophila, patency exhibits a strict temporal range potentially delimited by the transcription factor Tramtrack69 and a spatial pattern influenced by the dorsal-anterior signals of the follicular epithelium. Crucial for growth and lipid uptake by the oocyte, patency is also exploited by endosymbionts such as Spiroplasma pulsonii. Our findings reveal an evolutionarily conserved and developmentally regulated non-typical epithelial function in a classic model system.

SUBMITTER: Row S

PROVIDER: S-EPMC8005764 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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Developmental regulation of oocyte lipid intake through 'patent' follicular epithelium in Drosophila melanogaster.

Row Sarayu S Huang Yi-Chun YC Deng Wu-Min WM

iScience 20210306 4

Epithelia form protective permeability barriers that selectively allow the exchange of material while maintaining tissue integrity under extreme mechanical, chemical, and bacterial loads. Here, we report in the Drosophila follicular epithelium a developmentally regulated and evolutionarily conserved process "patency", wherein a breach is created in the epithelium at tricellular contacts during mid-vitellogenesis. In Drosophila, patency exhibits a strict temporal range potentially d ...[more]

PMID: 33817579

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Project description:BackgroundFerlins are membrane proteins with multiple C2 domains and proposed functions in Ca2+ mediated membrane-membrane interactions in animals. Caenorhabditis elegans has two ferlin genes, one of which is required for sperm function. Mammals have several ferlin genes and mutations in the human dysferlin (DYSF) and otoferlin (OTOF) genes result in muscular dystrophy and hearing loss, respectively. Drosophila melanogaster has a single ferlin gene called misfire (mfr). A previous study showed that a mfr mutation caused male sterility because of defects in fertilization. Here we analyze the expression and structure of the mfr gene and the consequences of multiple mutations to better understand the developmental function of ferlins.ResultsWe show that mfr is expressed in the testis and ovaries of adult flies, has tissue-specific promoters, and expresses alternatively spliced transcripts that are predicted to encode distinct protein isoforms. Studies of 11 male sterile mutations indicate that a predicted Mfr testis isoform with five C2 domains and a transmembrane (TM) domain is required for sperm plasma membrane breakdown (PMBD) and completion of sperm activation during fertilization. We demonstrate that Mfr is not required for localization of Sneaky, another membrane protein necessary for PMBD. The mfr mutations vary in their effects in females, with a subset disrupting egg patterning and causing a maternal effect delay in early embryonic development. Locations of these mutations indicate that a short Mfr protein isoform carries out ferlin activities during oogenesis.ConclusionThe mfr gene exhibits complex transcriptional and post-transcriptional regulation and functions in three developmental processes: sperm activation, egg patterning, and early embryogenesis. These functions are in part due to the production of protein isoforms that vary in the number of C2 domains. These findings help establish D. melanogaster as model system for understanding ferlin function and dysfunction in animals, including humans.

Project description:The piRNA pathway is studied in great detail in Drosophila female germline. In this study we show that unlike the female germline where all Piwi proteins are expressed throughout oogenesis, Ago3 - a Piwi family protein shows a spatial expression male germline. To understand dynamics of piRNA pathway during spermatogonia and primary spermatocyte stages of male germline development, we used arrest mutants. The bag of marbles (bam) and benign gonial cell neoplasm (bgcn) mutants have only early mitotic dividing germline cells in the testes due to failure to progress to primary spermatocyte stage, the cannonball (can) and spermatocyte arrest (sa) mutant germline cells cannot progress beyond primary spermatocyte stage. To investigate the dynamics of the piRNA pathway during spermatogenesis in spermatogonia and primary spermatocyte stages, we used testicular tissues from these stage-specific arrested mutants. While we used entire bam and bgcn mutant testes for spermatogonia purification, we while we manually removed the apical regions of can and sa mutant testes to exclude mitotically dividing undifferentiated germline cells for primary spermatocytes purification. Our results show that piRNAs mapping to transposons are more abundant in spermatogonia, whereas those mapping to Suppressor of Stellate [Su(Ste)] and AT-chX are mostly expressed in primary spermatocytes. Furthermore we observed that transposon-mapping piRNAs with ping-pong signature are more abundant in spermatogonia albeit still detectable in primary spermatocytes where Ago3 is not expressed. These results suggest that robust piRNA production via ping-pong cycle takes place in spermatogonia, and to a lesser extent in primary spermatocytes even in the absence of Ago3. Consistently, piRNAs from ago3 mutant testes also exhibit the ping-pong signature, confirming that a non-canonical ping-pong cycle is acting during spermatogenesis. Our study provides a developmental dimension to the piRNA pathway and uncovers a new mechanism used in the male germline to silence transposons.

Dataset Information

Developmental regulation of oocyte lipid intake through 'patent' follicular epithelium in Drosophila melanogaster.

Publications

Developmental regulation of oocyte lipid intake through 'patent' follicular epithelium in <i>Drosophila melanogaster</i>.

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