Drosophila sperm development is characterized by extensive post-transcriptional regulation whereby thousands of transcripts are preserved for translation during later stages. A key step in translation initiation is the binding of eukaryotic initiation factor 4E (eIF4E) to the 5’ mRNA cap. In addition to canonical eIF4E-1, Drosophila has multiple eIF4E paralogs, including four (eIF4E-3, -4, -5, and -7) that are highly expressed in the testis. Among these, only eIF4E-3 has been characterized genetically. Here, using CRISPR/Cas9 mutagenesis, we determined that eIF4E-5 is essential for male fertility. eIF4E-5 protein localizes to the distal ends of elongated spermatid cysts, and eIF4E-5 mutants exhibit defects during post-meiotic stages, including a mild defect in spermatid cyst polarization. eIF4E-5 mutants also have a fully penetrant defect in individualization, resulting in failure to produce mature sperm. Indeed, our data indicate that eIF4E-5 regulates non-apoptotic caspase activity during individualization by promoting local accumulation of the E3 ubiquitin ligase inhibitor Soti. Our results further extend the diversity of non-canonical eIF4Es that carry out distinct spatiotemporal roles during spermatogenesis.
Eukaryotic translation initiation factor eIF4E-5 is required for spermiogenesis in Drosophila melanogaster
Present address: Clarivate Analytics, 150 King St. W, Toronto, Ontario, M5H 1J9, Canada
Present address: Faculty of Medicine, University of Toronto, 1 King's College Circle, Toronto, Ontario, M5S 1A8, Canada
Present address: Internal Medicine, Montreal General Hospital, 1650 Cedar Ave., Montreal, QC, H3G 1A4
- Award Group:
- Funder(s): Natural Sciences and Engineering Research Council of Canada
- Award Id(s): RGPIN-2016-06775
- Funder(s):
- Award Group:
- Funder(s): Canadian Institutes of Health Research
- Award Id(s): IOP-107945
- Funder(s):
- Award Group:
- Funder(s): Consejo Nacional de Ciencia y Tecnologia
- Award Id(s): 749487
- Funder(s):
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- Accepted Manuscript 25 January 2023
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Lisa Shao, Jaclyn M. Fingerhut, Brook L. Falk, Hong Han, Giovanna Maldonado, Yuemeng Qiao, Vincent Lee, Elizabeth Hall, Liang Chen, Gordon Polevoy, Greco Hernández, Paul Lasko, Julie A. Brill; Eukaryotic translation initiation factor eIF4E-5 is required for spermiogenesis in Drosophila melanogaster. Development 2023; dev.200477. doi: https://doi.org/10.1242/dev.200477
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