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Uncovering the Repertoire of Endogenous Flaviviral Elements in Aedes Mosquito Genomes.

ABSTRACT: Endogenous viral elements derived from nonretroviral RNA viruses have been described in various animal genomes. Whether they have a biological function, such as host immune protection against related viruses, is a field of intense study. Here, we investigated the repertoire of endogenous flaviviral elements (EFVEs) in Aedes mosquitoes, the vectors of arboviruses such as dengue and chikungunya viruses. Previous studies identified three EFVEs from Aedes albopictus cell lines and one from Aedes aegypti cell lines. However, an in-depth characterization of EFVEs in wild-type mosquito populations and individual mosquitoes in vivo has not been performed. We detected the full-length DNA sequence of the previously described EFVEs and their respective transcripts in several A. albopictus and A. aegypti populations from geographically distinct areas. However, EFVE-derived proteins were not detected by mass spectrometry. Using deep sequencing, we detected the production of PIWI-interacting RNA-like small RNAs, in an antisense orientation, targeting the EFVEs and their flanking regions in vivo The EFVEs were integrated in repetitive regions of the mosquito genomes, and their flanking sequences varied among mosquito populations. We bioinformatically predicted several new EFVEs from a Vietnamese A. albopictus population and observed variation in the occurrence of those elements among mosquitoes. Phylogenetic analysis of an A. aegypti EFVE suggested that it integrated prior to the global expansion of the species and subsequently diverged among and within populations. The findings of this study together reveal the substantial structural and nucleotide diversity of flaviviral integrations in Aedes genomes. Unraveling this diversity will help to elucidate the potential biological function of these EFVEs.IMPORTANCE Endogenous viral elements (EVEs) are whole or partial viral sequences integrated in host genomes. Interestingly, some EVEs have important functions for host fitness and antiviral defense. Because mosquitoes also have EVEs in their genomes, characterizing these EVEs is a prerequisite for their potential use to manipulate the mosquito antiviral response. In the study described here, we focused on EVEs related to the Flavivirus genus, to which dengue and Zika viruses belong, in individual Aedes mosquitoes from geographically distinct areas. We show the existence in vivo of flaviviral EVEs previously identified in mosquito cell lines, and we detected new ones. We show that EVEs have evolved differently in each mosquito population. They produce transcripts and small RNAs but not proteins, suggesting a function at the RNA level. Our study uncovers the diverse repertoire of flaviviral EVEs in Aedes mosquito populations and contributes to an understanding of their role in the host antiviral system.

SUBMITTER: Suzuki Y

PROVIDER: S-EPMC5512259 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Uncovering the Repertoire of Endogenous Flaviviral Elements in Aedes Mosquito Genomes.

Suzuki Yasutsugu Y Frangeul Lionel L Dickson Laura B LB Blanc Hervé H Verdier Yann Y Vinh Joelle J Lambrechts Louis L Saleh Maria-Carla MC

Journal of virology 20170712 15

Endogenous viral elements derived from nonretroviral RNA viruses have been described in various animal genomes. Whether they have a biological function, such as host immune protection against related viruses, is a field of intense study. Here, we investigated the repertoire of endogenous flaviviral elements (EFVEs) in <i>Aedes</i> mosquitoes, the vectors of arboviruses such as dengue and chikungunya viruses. Previous studies identified three EFVEs from <i>Aedes albopictus</i> cell lines and one ...[more]

PMID: 28539440

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Project description:BACKGROUND:The Asian tiger mosquito Aedes albopictus is a highly invasive species and competent vector of several arboviruses (e.g. dengue, chikungunya, Zika) and parasites (e.g. dirofilaria) of public health importance. Compared to other mosquito species, Ae. albopictus females exhibit a generalist host seeking as well as a very aggressive biting behaviour that are responsible for its high degree of nuisance. Several complex mosquito behaviours such as host seeking, feeding, mating or oviposition rely on olfactory stimuli that target a range of sensory neurons localized mainly on specialized head appendages such as antennae, maxillary palps and the mouthparts. RESULTS:With the aim to describe the Ae. albopictus olfactory repertoire we have used RNA-seq to reveal the transcriptome profiles of female antennae and maxillary palps. Male heads and whole female bodies were employed as reference for differential expression analysis. The relative transcript abundance within each tissue (TPM, transcripts per kilobase per million) and the pairwise differential abundance in the different tissues (fold change values and false discovery rates) were evaluated. Contigs upregulated in the antennae (620) and maxillary palps (268) were identified and relative GO and PFAM enrichment profiles analysed. Chemosensory genes were described: overall, 77 odorant binding proteins (OBP), 82 odorant receptors (OR), 60 ionotropic receptors (IR) and 30 gustatory receptors (GR) were identified by comparative genomics and transcriptomics. In addition, orthologs of genes expressed in the female/male maxillary palps and/or antennae and involved in thermosensation (e.g. pyrexia and arrestin1), mechanosensation (e.g. piezo and painless) and neuromodulation were classified. CONCLUSIONS:We provide here the first detailed transcriptome of the main Ae. albopictus sensory appendages, i.e. antennae and maxillary palps. A deeper knowledge of the olfactory repertoire of the tiger mosquito will help to better understand its biology and may pave the way to design new attractants/repellents.

Project description:BackgroundMosquitoes are important pathogen vectors affecting human and other animals. Studies on genetic control of mosquito mediated disease transmission gained traction recently due to mosquito transgenesis technology. Active transposons are considered valuable tools to propagate pathogen resistance transgenes among mosquitoes, rendering the whole population recalcitrant to diseases. A major hurdle in this approach is the inefficient remobilization activity after the integration of heterologous transposon vectors bearing transgenes into chromosomes. Therefore, endogenous active transposons in mosquito genomes are highly desirable.ResultsStarting with the transposable element database of the yellow fever mosquito Aedes aegypti genome, detailed analyses of the members of each TE family were performed to identify sequences with multiple identical copies, an indicator of their latest or current transposition activity. Among a dozen of potentially active TE families, two DNA elements (TF000728 and TF000742 in TEfam) are short and nonautonomous. Close inspection of the elements revealed that these two families were previously mis-categorized and, unlike other known TEs, insert specifically at dinucleotide "AT". These two families were therefore designated as ATon-I and ATon-II. ATon-I has a total copy number of 294, among which three elements have more than 10 identical copies (146, 61 and 17). ATon-II has a total copy number of 317, among which three elements have more than 10 identical copies (84, 15 and 12). Genome wide searches revealed additional 24 ATon families in A. aegypti genome with nearly 6500 copies in total. Transposon display analysis of ATon-1 family using different A. aegypti strains suggests that the elements are similarly abundant in the tested mosquito strains.ConclusionATons are novel mobile genetic elements bearing terminal inverted repeats and insert specifically at dinucleotide "AT". Five ATon families contain elements existing at more than 10 identical copies, suggesting very recent or current transposition activity. A total of 24 new TE families with nearly 6000 copies were identified in this study.

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Uncovering the Repertoire of Endogenous Flaviviral Elements in Aedes Mosquito Genomes.

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Uncovering the Repertoire of Endogenous Flaviviral Elements in Aedes Mosquito Genomes.

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