Summary auto-generated
This study investigated the ultrastructural expression of the Drosophila endogenous retrovirus gypsy in ovaries of flies carrying the permissive flamenco (flam1) allele. Researchers used electron microscopy, in situ hybridization, and immunological methods to examine ovaries from 2-4 day-old flies. They found non-enveloped, intracytoplasmic virus-like particles (VLPs) measuring 40-45 nm accumulating in the apical regions of follicle cells (somatic cells surrounding the egg) in flam1 flies, but not in flam+ control flies. These A-type particles contained gypsy RNA and clustered near membrane regions where gypsy envelope proteins were localized. Smaller numbers of similar particles were observed in oocytes (egg precursor cells). The particles were consistently absent in flam+ females, despite similar gypsy provirus copy numbers. The authors propose that gypsy derepression and virion production occur in somatic follicle cells rather than in the germline itself, and that germ-line infection by particles from follicle cells may be necessary for new gypsy insertions to occur in offspring. This represents the first ultrastructural evidence of retrovirus particle production in invertebrates.
Key findings
- Non-enveloped gypsy virus-like particles (40-45 nm diameter) accumulate specifically in apical regions of flam1 follicle cells, while absent in restrictive flam+ controls
- Approximately 10% of the particles hybridize with gypsy RNA probe, indicating they contain viral genetic material
- Gypsy envelope proteins localize to membranes adjacent to VLP accumulation sites, suggesting targeted assembly near specific membrane domains
- Particles are rare or absent in the germline proper (oocytes and nurse cells) despite being abundant in surrounding somatic follicle cells
- No enveloped virions were detected in extracellular spaces, despite abundant intracellular particle production
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Abstract
The endogenous retrovirus gypsy is controlled by the Drosophila gene flamenco (flam). New insertions of gypsy occur in any individual Drosophila if its mother is homozygous for the flam1 permissive allele and contains functional gypsy proviruses. The ovaries of flam1 females also contain high amounts of gypsy RNAs. Unexpectedly however, gypsy derepression does not occur in the flam1 female germ-line proper but in the somatic follicular epithelium of the ovary. Since extracts from these females are able to efficiently infect the germ-line of a strain devoid of active gypsy proviruses, we assume that a similar kind of germ-line infection, which would occur inside the flam1 females themselves, could be required for gypsy insertions to occur in their progeny. This hypothesis was confirmed by electron microscopy observations showing that non-enveloped intracytoplasmic particles containing gypsy RNAs accumulate in the apical region of the flam1 follicle cells, close to specific membrane domains to which the gypsy envelope proteins are targeted, whereas both are absent in the flam+ controls. Low amounts of similar virus-like particles were also observed in flam1 oocytes, but it is not yet known whether they entered passively or as a result of membrane fusion. This is the first report of the beginning of a retrovirus cycle in invertebrates and these observations should be taken into account when explaining the maternal effect of the flamenco gene on the multiplication of gypsy proviruses.