Regulation of protamine incorporation and nuclear reorganization during Drosophila spermatogenesis

NIH RePORTER · NIH · F30 · $51,752 · view on reporter.nih.gov ↗

Abstract

ABSTRACT In many species, sperm maturation requires a process of nuclear compaction, which occurs via dramatic chromatin reorganization from histone to protamine-based architecture. Nuclear compaction is essential for sperm fertility, functioning to enhance hydrodynamics and genomic integrity. While several genes have been identified to be involved in this process, it is unknown how these genes are regulated. Here, we have utilized the Drosophila testis model system to identify Modulo, the Drosophila homolog of Nucleolin, as a key player in sperm nuclear reorganization. In somatic cells, modulo has been shown to be involved in chromatin remodeling, cell proliferation, and morphogenesis. Viable modulo mutant allele that specifically influences testis-specific isoform has been known to be sterile, but the reason underlying this sterility remained unknown. We find that modulo mutants display nuclear compaction defects during late spermatogenesis alongside decreased protamine protein incorporation. Importantly, modulo’s unique phenotype cannot be explained simply by lack of protamine incorporation: compound mutant that lacks protamines Prot A/B and Mst77F causes only mild nuclear deformation rather than complete nuclear decompaction as observed in modulo mutant. Indeed, in addition to decreased incorporation of main protamines in mutant, we have detected increased expression of Mst77Y, a lesser-studied protamine gene with numerous duplications on the Y-chromosome. Thus, we hypothesize that modulo mediates sperm nuclei compaction by coordinating expression of multiple genes that are specifically involved in nuclear compaction during spermiogenesis. To test this hypothesis, we will conclusively establish the cytological defects of modulo mutant by inducing expression of mst77Y in wild-type nuclei and assessing protamine protein expression in whole testis vs. in spermatid nuclei. Additionally, we will investigate transcription and/or splicing as modulo’s mechanism for regulating its target genes. Previous literature has identified modulo to interact with testis-specific transcription factors while protein sequence analysis and gene ontology have predicted modulo as being involved in splicing. Therefore, we further hypothesize that modulo regulates its target genes at the RNA level either by functioning during transcription or splicing. If our hypothesis is true, it would result in the identification of a previously uncharacterized regulatory network governing nuclear reorganization in late stage spermatogenesis and have implications for male infertility.

Key facts

NIH application ID
10462097
Project number
1F30HD105324-01A1
Recipient
UNIVERSITY OF MICHIGAN AT ANN ARBOR
Principal Investigator
Jun Il Park
Activity code
F30
Funding institute
NIH
Fiscal year
2022
Award amount
$51,752
Award type
1
Project period
2022-05-01 → 2023-10-31