Dataset Information

Wolbachia interferes with the intracellular distribution of Argonaute 1 in the dengue vector Aedes aegypti by manipulating the host microRNAs.

ABSTRACT: Argonaute proteins (AGOs) are vital components of the RNA-induced silencing complex in gene silencing. AGOs are indispensable for microRNA (miRNA) biogenesis as well as function, and are intracellularly localized to both the cytoplasm and the nucleus. Cytoplasmic AGO-miRNA complexes are mainly involved in cleavage or translational repression of target mRNAs while the nuclear ones are engaged in transcriptional gene silencing, methylation, chromatin remodeling, and splicing. In insects, AGO1 and AGO2 are involved in RNA interference and miRNA pathways but the components involved in their trafficking between the nucleus and the cytoplasm are not known. In this study, we found that importin ?-4 facilitates AGO1 distribution to the nucleus, which is regulated by aae-miR-981 miRNA. The results also revealed association of prohibitin with AGO1 that may play an important role in its stability. Importantly, we found that AGO1 distribution to the nucleus is blocked by Wolbachia, an endosymbiotic bacterium introduced into the Dengue vector, Aedes aegypti. Our results provide basic mechanisms on intracellular trafficking of AGO1 in insects and how this may be altered by Wolbachia, which may affect trafficking of miRNAs to the nucleus leading to alteration in epigenetic effects.

SUBMITTER: Hussain M

PROVIDER: S-EPMC3917989 | biostudies-literature | 2013 Dec

REPOSITORIES: biostudies-literature

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Wolbachia interferes with the intracellular distribution of Argonaute 1 in the dengue vector Aedes aegypti by manipulating the host microRNAs.

Hussain Mazhar M O'Neill Scott L SL Asgari Sassan S

RNA biology 20131210 12

Argonaute proteins (AGOs) are vital components of the RNA-induced silencing complex in gene silencing. AGOs are indispensable for microRNA (miRNA) biogenesis as well as function, and are intracellularly localized to both the cytoplasm and the nucleus. Cytoplasmic AGO-miRNA complexes are mainly involved in cleavage or translational repression of target mRNAs while the nuclear ones are engaged in transcriptional gene silencing, methylation, chromatin remodeling, and splicing. In insects, AGO1 and ...[more]

PMID: 24351659

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Project description:BackgroundDengue viruses (DENV) are the causative agents of dengue, the world's most prevalent arthropod-borne disease with around 40% of the world's population at risk of infection annually. Wolbachia pipientis, an obligate intracellular bacterium, is being developed as a biocontrol strategy against dengue because it limits replication of the virus in the mosquito. The Wolbachia strain wMel, which has been introduced into the mosquito vector, Aedes aegypti, has been shown to invade and spread to near fixation in field releases. Standard measures of Wolbachia's efficacy for blocking virus replication focus on the detection and quantification of virus in mosquito tissues. Examining the saliva provides a more accurate measure of transmission potential and can reveal the extrinsic incubation period (EIP), that is, the time it takes virus to arrive in the saliva following the consumption of DENV viremic blood. EIP is a key determinant of a mosquito's ability to transmit DENVs, as the earlier the virus appears in the saliva the more opportunities the mosquito will have to infect humans on subsequent bites.Methodology/principal findingsWe used a non-destructive assay to repeatedly quantify DENV in saliva from wMel-infected and Wolbachia-free wild-type control mosquitoes following the consumption of a DENV-infected blood meal. We show that wMel lengthens the EIP, reduces the frequency at which the virus is expectorated and decreases the dengue copy number in mosquito saliva as compared to wild-type mosquitoes. These observations can at least be partially explained by an overall reduction in saliva produced by wMel mosquitoes. More generally, we found that the concentration of DENV in a blood meal is a determinant of the length of EIP, saliva virus titer and mosquito survival.Conclusions/significanceThe saliva-based traits reported here offer more disease-relevant measures of Wolbachia's effects on the vector and the virus. The lengthening of EIP highlights another means, in addition to the reduction of infection frequencies and DENV titers in mosquitoes, by which Wolbachia should operate to reduce DENV transmission in the field.

Project description:Dengue is the most prevalent arboviral disease world-wide and its primary vector is the mosquito Aedes aegypti. The current lack of commercially-available vaccines makes control of vector populations the only effective strategy to prevent dengue transmission. Aedes aegypti geographic populations exhibit great variability in insecticide resistance and susceptibility to dengue infection. The characterization of single nucleotide polymorphisms (SNPs) as molecular markers to study quantitatively this variation is needed greatly because this species has a low abundance of microsatellite markers and limited known restriction fragments length polymorphisms (RFLPs) and single-strand conformation polymorphism (SSCP) markers.We used RNA-seq to characterize SNPs in three Ae. aegypti strains, including the Liverpool (LVP) strain, from which the current genome annotation is derived. We identified 131,764 unique genome locations with at least one alternative nucleotide to what is reported in the reference annotation. These comprised changes in both open-reading frames (ORFs) and untranslated regions (UTRs) of transcripts. An in depth-look at sequence variation in immunity genes revealed that those associated with autophagy, MD2-like receptors and Peptidoglycan Recognition Proteins had more sequence variation in their 3'UTRs than mutations associated with non-synonymous changes. This supports the conclusion that these genes had maintained their functional specificity while being adapted to different regulatory domains. In contrast, a number of peroxidases, serpins and Clip-domain serine proteases exhibited conservation of putative UTR regulatory sequences while displaying diversification of the ORFs. Transcriptome evidence also was found for ~2500 novel transcriptional units (NTUs) not annotated in the reference genome.The transcriptome-wide assessment of within and inter-strain polymorphisms in Ae. aegypti adds considerably to the number of molecular markers available for genetic studies in this mosquito. Additionally, data supporting NTU discovery emphasizes the need for continuous amendments of the reference genome annotation.

Project description:Globally invasive Aedes aegypti mosquitoes disseminate numerous arboviruses that impact human health. One promising method to control Ae. aegypti populations is transinfection with the intracellular bacterium Wolbachia pipientis, a symbiont that naturally infects ~40-52% of insects but is normally absent from Ae. aegypti. Transinfection of Ae. aegypti with the wMel Wolbachia strain induces cytoplasmic incompatibility (CI), allowing infected individuals to rapidly invade native populations. Further, wMel Wolbachia-infected females display refractoriness to medically relevant arboviruses. Thus, wMel Wolbachia-infected Ae. aegypti are being released in several areas to replace native populations, thereby suppressing disease transmission by this species. Wolbachia is reported to have minimal effects on Ae. aegypti fertility, but its influence on other reproductive processes is unknown. Female insects undergo several post-mating physiological and behavioral changes required for optimal fertility. Post-mating responses (PMRs) in female insects are typically elicited by receipt of male seminal fluid proteins (SFPs) transferred with sperm during mating, but can be modified by other factors, such as adult age, nutritional status, and microbiome composition. To assess how Wolbachia infection influences Ae. aegypti female PMRs, we collected wMel Wolbachia-infected Ae. aegypti from the field in Medellín, Colombia and introduced the bacterium into our laboratory strain. We found that Wolbachia influences female fecundity, fertility, and re-mating incidence. Further, we observed that Wolbachia significantly extends longevity of virgin females. Changes in female PMRs are not due to defects in sperm transfer by infected males, or sperm storage by infected females. Using proteomic methods to examine the seminal proteome of infected males, we found that Wolbachia infection has a moderate effect on SFP composition. However, we identified 125 Wolbachia proteins that are paternally transferred to females by infected males. Surprisingly, the CI factor proteins (Cifs), were not detected in the ejaculates of Wolbachia-infected males. Our findings indicate that Wolbachia infection of Ae. aegypti alters female post-mating responses, potentially influencing control programs that utilize Wolbachia-infected individuals.

Dataset Information

Wolbachia interferes with the intracellular distribution of Argonaute 1 in the dengue vector Aedes aegypti by manipulating the host microRNAs.

Publications

Wolbachia interferes with the intracellular distribution of Argonaute 1 in the dengue vector Aedes aegypti by manipulating the host microRNAs.

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