Viral particles of the endogenous retrovirus ZAM from Drosophila melanogasteruse a pre-existing endosome/exosome pathway for transfer to the oocyte

Brasset, Emilie; Taddei, Annarita; Arnaud, Frédérick; Faye, Babacar; Fausto, Anna Maria; Mazzini, Massimo; Giorgi, Franco; Vaury, Chantal

doi:10.1186/1742-4690-3-25

Cited by 53 publications

(33 citation statements)

References 27 publications

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“…Some of these properties are also found for the I factor which is responsible for the occurrence of another system of hybrid dysgenesis (“I-R” system) [45], [46], [71]–. TSE therefore parallels germline regulation of TEs ( P , I ), and does not resemble regulation of TEs in the somatic follicle cells ( gypsy , ZAM , Idefix [19], [20]) for which no epigenetic transmission of repression capacities through meiosis has been described so far. It will be interesting to test if previously described cases of RNA-dependent heterochromatin formation show the reciprocal dependence, thus being able to form a positive loop.…”

Section: Discussionmentioning

confidence: 98%

“…For example in Drosophila , the flam/COM locus, located in pericentromeric heterochromatin, represses various families of “Type I” TEs (retrotransposons which transpose via an RNA intermediate) [12]–[15] and the TAS (Telomeric Associated Sequence) region of sub-telomeric heterochromatin houses strong regulatory P elements (“Type II” TEs whose transposition occurs via a DNA intermediate) [2], [16]–[18]. The flam/COM locus represses expression of gypsy , Zam , and Idefix in somatic follicle cells, thereby preventing transfer of these retrotransposons to the oocyte [19], [20]. By contrast, P element repression by telomeric P copies takes place in the germline of both sexes [17], [18], [21], [22] and it is in this tissue that all P element transposition steps take place [3], [23], [24].…”

Section: Introductionmentioning

confidence: 99%

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The Epigenetic Trans-Silencing Effect in Drosophila Involves Maternally-Transmitted Small RNAs Whose Production Depends on the piRNA Pathway and HP1

et al. 2010

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BackgroundThe study of P transposable element repression in Drosophila melanogaster led to the discovery of the Trans-Silencing Effect (TSE), a homology-dependent repression mechanism by which a P-transgene inserted in subtelomeric heterochromatin (Telomeric Associated Sequences, “TAS”) has the capacity to repress in trans, in the female germline, a homologous P-lacZ transgene located in euchromatin. Phenotypic and genetic analysis have shown that TSE exhibits variegation in ovaries, displays a maternal effect as well as epigenetic transmission through meiosis and involves heterochromatin (including HP1) and RNA silencing.Principal FindingsHere, we show that mutations in squash and zucchini, which are involved in the piwi-interacting RNA (piRNA) silencing pathway, strongly affect TSE. In addition, we carried out a molecular analysis of TSE and show that silencing is correlated to the accumulation of lacZ small RNAs in ovaries. Finally, we show that the production of these small RNAs is sensitive to mutations affecting squash and zucchini, as well as to the dose of HP1.Conclusions and SignificanceThus, our results indicate that the TSE represents a bona fide piRNA-based repression. In addition, the sensitivity of TSE to HP1 dose suggests that in Drosophila, as previously shown in Schizosaccharomyces pombe, a RNA silencing pathway can depend on heterochromatin components.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

The Epigenetic Trans-Silencing Effect in Drosophila Involves Maternally-Transmitted Small RNAs Whose Production Depends on the piRNA Pathway and HP1

et al. 2010

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“…Thus, we predict that Vg may be involved in the ABTM-mediated transport of Pns11 tubules of RGDV between follicular cells or into the oocyte cytoplasm. Previous data has shown that an endogenous retrovirus of D. melanogaster , ZAM, is transmitted from follicular cells to the oocyte by making use of the endogenous endocytic yolk uptake mechanism (Brasset et al, 2006). Similarly, the outer capsid protein of RSV can interact with Vg and use Vg as a vehicle to enter the vector oocyte (Huo et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Virus-Induced Tubules: A Vehicle for Spread of Virions into Ovary Oocyte Cells of an Insect Vector

Liao

Mao

et al. 2017

Front. Microbiol.

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Many arthropod-borne viruses are persistently propagated and transovarially transmitted by female insect vectors through eggs, but the mechanism remains poorly understood. Insect oocytes are surrounded by a layer of follicular cells, which are connected to the oocyte through actin-based microvilli. Here, we demonstrate that a plant reovirus, rice gall dwarf virus (RGDV), exploits virus-containing tubules composed of viral non-structural protein Pns11 to pass through actin-based junctions between follicular cells or through actin-based microvilli from follicular cells into oocyte of its leafhopper vector Recilia dorsalis, thus overcoming transovarial transmission barriers. We further determine that the association of Pns11 tubules with actin-based cellular junctions or microvilli of the ovary is mediated by a specific interaction between Pns11 and actin. Interestingly, RGDV can replicate and assemble progeny virions in the oocyte cytoplasm. The destruction of the tubule assembly by RNA interference with synthesized double-stranded RNA targeting the Pns11 gene strongly inhibits transovarial transmission of RGDV by its vectors. For the first time, we show that a virus can exploit virus-induced tubule as a vehicle to overcome the transovarial transmission barrier by insect vectors.

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“…A study has shown that the endogenous retrovirus of D . melanogaster , ZAM, is transmitted from follicle cells to the oocyte by a mechanism that is linked to endocytic yolk uptake (47). It has also been reported that the vertically transmitted protozoan parasite Babesia exhibits transmission efficiencies that are affected by the rate of tick-host yolk uptake (48).…”

Section: Discussionmentioning

confidence: 99%

Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery

Herren

Paredes

Schüpfer

et al. 2013

mBio

100

101

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Spiroplasma is a diverse bacterial clade that includes many vertically transmitted insect endosymbionts, including Spiroplasma poulsonii, a natural endosymbiont of Drosophila melanogaster. These bacteria persist in the hemolymph of their adult host and exhibit efficient vertical transmission from mother to offspring. In this study, we analyzed the mechanism that underlies their vertical transmission, and here we provide strong evidence that these bacteria use the yolk uptake machinery to colonize the germ line. We show that Spiroplasma reaches the oocyte by passing through the intercellular space surrounding the ovarian follicle cells and is then endocytosed into oocytes within yolk granules during the vitellogenic stages of oogenesis. Mutations that disrupt yolk uptake by oocytes inhibit vertical Spiroplasma transmission and lead to an accumulation of these bacteria outside the oocyte. Impairment of yolk secretion by the fat body results in Spiroplasma not reaching the oocyte and a severe reduction of vertical transmission. We propose a model in which Spiroplasma first interacts with yolk in the hemolymph to gain access to the oocyte and then uses the yolk receptor, Yolkless, to be endocytosed into the oocyte. Cooption of the yolk uptake machinery is a powerful strategy for endosymbionts to target the germ line and achieve vertical transmission. This mechanism may apply to other endosymbionts and provides a possible explanation for endosymbiont host specificity.

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Viral particles of the endogenous retrovirus ZAM from Drosophila melanogasteruse a pre-existing endosome/exosome pathway for transfer to the oocyte

Cited by 53 publications

References 27 publications

The Epigenetic Trans-Silencing Effect in Drosophila Involves Maternally-Transmitted Small RNAs Whose Production Depends on the piRNA Pathway and HP1

The Epigenetic Trans-Silencing Effect in Drosophila Involves Maternally-Transmitted Small RNAs Whose Production Depends on the piRNA Pathway and HP1

Virus-Induced Tubules: A Vehicle for Spread of Virions into Ovary Oocyte Cells of an Insect Vector

Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery

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