Differential Small RNA Responses against Co-Infecting Insect-Specific Viruses in Aedes albopictus Mosquitoes

Lionel Frangeul,Yasutsugu Suzuki,Maria-Carla Saleh,Hervé Blanc

doi:10.3390/v12040468

Lionel Frangeul, Yasutsugu Suzuki + Show 2 more

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https://doi.org/10.3390/v12040468

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Abstract

The mosquito antiviral response has mainly been studied in the context of arthropod-borne virus (arbovirus) infection in female mosquitoes. However, in nature, both female and male mosquitoes are frequently infected with insect-specific viruses (ISVs). ISVs are capable of infecting the reproductive organs of both sexes and are primarily maintained by vertical transmission. Since the RNA interference (RNAi)-mediated antiviral response plays an important antiviral role in mosquitoes, ISVs constitute a relevant model to study sex-dependent antiviral responses. Using a naturally generated viral stock containing three distinct ISVs, Aedes flavivirus (AEFV), Menghai rhabdovirus (MERV), and Shinobi tetra virus (SHTV), we infected adult Aedes albopictus females and males and generated small RNA libraries from ovaries, testes, and the remainder of the body. Overall, both female and male mosquitoes showed unique small RNA profiles to each co-infecting ISV regardless of the sex or tissue tested. While all three ISVs generated virus-derived siRNAs, only MERV generated virus-derived piRNAs. We also studied the expression of PIWI genes in reproductive tissues and carcasses. In contrast to Piwi5-9, Piwi1-4 were abundantly expressed in ovaries and testes, suggesting that Piwi5-9 are involved in exogenous viral piRNA production. Together, our results show that ISV-infected Aedes albopictus produce viral small RNAs in a virus-specific manner and that male mosquitoes mount a similar small RNA-mediated antiviral response to that of females.

Highlights

Mosquitoes are efficient vectors for various human pathogens
In contrast to Piwi5-9, Piwi1-4 were abundantly expressed in ovaries and testes, suggesting that Piwi5-9 are involved in exogenous viral piRNA production
Ae. albopictus-Vietnam adult females and males (4–7 days old post-emergence) were intrathoracically injected with a naturally derived viral stock containing a mixture of three insect-specific viruses (ISVs)

Summary

Introduction

Aedes and Culex are two major genera of mosquitoes that transmit medically important arthropod-borne viruses (arboviruses) such as dengue, West Nile and Zika viruses. Recent metagenomics studies have shed light on the virome of these mosquito vectors, revealing diverse virus communities largely composed of insect-specific viruses (ISVs) that infect invertebrates but not vertebrates [1,2,3,4,5,6,7]. ISVs have been shown to negatively regulate some arbovirus infections in mosquito cell cultures and in vivo [8,9,10,11,12,13,14]. It has been suggested that mosquitoes establish a tolerant state to ISVs as well as to arboviruses and that this viral tolerance is one of the critical factors influencing

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