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Antiviral immunity of Anopheles gambiae is highly compartmentalized, with distinct roles for RNA interference and gut microbiota
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Antiviral immunity of Anopheles gambiae is highly compartmentalized, with distinct roles for RNA interference and gut microbiota
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Journal Article
Antiviral immunity of Anopheles gambiae is highly compartmentalized, with distinct roles for RNA interference and gut microbiota
2015
Overview
Significance It is important to understand antiviral mechanisms in potential new arbovirus vectors, such as Anopheles mosquitoes, in order to assess risks associated with arbovirus spread. Using an arbovirus naturally transmitted by Anopheles , we find that important immune mechanisms involved in the first bottleneck to Anopheles infection, the midgut, have distinct effects on arbovirus or malaria. This result is, to our knowledge, the first concrete evidence of protection tradeoffs for different human pathogens in a human disease vector, and it suggests that design of genetically immune-modified mosquitoes could result in unexpected outcomes. These results also indicate that different mosquito tissues display distinct antiviral protection that probably imposes divergent selection pressures upon viral replication during different stages of the infection.
Arboviruses are transmitted by mosquitoes and other arthropods to humans and animals. The risk associated with these viruses is increasing worldwide, including new emergence in Europe and the Americas. Anopheline mosquitoes are vectors of human malaria but are believed to transmit one known arbovirus, o’nyong-nyong virus, whereas Aedes mosquitoes transmit many. Anopheles interactions with viruses have been little studied, and the initial antiviral response in the midgut has not been examined. Here, we determine the antiviral immune pathways of the Anopheles gambiae midgut, the initial site of viral infection after an infective blood meal. We compare them with the responses of the post-midgut systemic compartment, which is the site of the subsequent disseminated viral infection. Normal viral infection of the midgut requires bacterial flora and is inhibited by the activities of immune deficiency (Imd), JAK/STAT, and Leu-rich repeat immune factors. We show that the exogenous siRNA pathway, thought of as the canonical mosquito antiviral pathway, plays no detectable role in antiviral defense in the midgut but only protects later in the systemic compartment. These results alter the prevailing antiviral paradigm by describing distinct protective mechanisms in different body compartments and infection stages. Importantly, the presence of the midgut bacterial flora is required for full viral infectivity to Anopheles , in contrast to malaria infection, where the presence of the midgut bacterial flora is required for protection against infection. Thus, the enteric flora controls a reciprocal protection tradeoff in the vector for resistance to different human pathogens.
Publisher
National Academy of Sciences,National Acad Sciences
Subject
/ Alphavirus Infections - immunology
/ Alphavirus Infections - transmission
/ Animals
/ Arbovirus Infections - immunology
/ Arbovirus Infections - transmission
/ Digestive System - immunology
/ Digestive System - microbiology
/ Female
/ Flora
/ Host-Pathogen Interactions - genetics
/ Host-Pathogen Interactions - immunology
/ Humans
/ immunity
/ Malaria
/ midgut
/ O'nyong-nyong Virus - genetics
/ O'nyong-nyong Virus - immunology
/ O'nyong-nyong Virus - pathogenicity
/ Plasmodium falciparum - immunology
/ Plasmodium falciparum - pathogenicity
/ RNA
/ RNA, Small Interfering - genetics
/ Signal Transduction - immunology
/ STAT Transcription Factors - immunology
/ tissues
