Mosquito gut antiparasitic and antiviral immunity

Saraiva, Raúl G.; Kang, Sang‐Wook; Simões, Maria L.; Angleró-Rodríguez, Yesseinia I.; Dimopoulos, George

doi:10.1016/j.dci.2016.01.015

Cited by 91 publications

(62 citation statements)

References 164 publications

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“…Strategies that target the parasite, including anti-malarial drugs, and those that target the vector, such as insecticides, are encountering resistance of the parasite and vector, respectively [2, 3]. When mosquitoes bite a Plasmodium -infected person, the ingested Plasmodium gametocytes encounter a severe bottleneck in development at the ookinete stage within the midgut, the site where most parasites are killed [4, 5]. During this infection stage, parasites also encounter the mosquito midgut microbiota.…”

Section: Introductionmentioning

confidence: 99%

Functional genomic analyses of Enterobacter, Anopheles and Plasmodium reciprocal interactions that impact vector competence

Dennison

Saraiva

Cirimotich

et al. 2016

Malar J

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BackgroundMalaria exerts a tremendous socioeconomic impact worldwide despite current control efforts, and novel disease transmission-blocking strategies are urgently needed. The Enterobacter bacterium Esp_Z, which is naturally harboured in the mosquito midgut, can inhibit the development of Plasmodium parasites prior to their invasion of the midgut epithelium through a mechanism that involves oxidative stress. Here, a multifaceted approach is used to study the tripartite interactions between the mosquito, Esp_Z and Plasmodium, towards addressing the feasibility of using sugar-baited exposure of mosquitoes to the Esp_Z bacterium for interruption of malaria transmission.MethodsThe ability of Esp_Z to colonize Anopheles gambiae midguts harbouring microbiota derived from wild mosquitoes was determined by qPCR. Upon introduction of Esp_Z via nectar feeding, the permissiveness of colonized mosquitoes to Plasmodium falciparum infection was determined, as well as the impact of Esp_Z on mosquito fitness parameters, such as longevity, number of eggs laid and number of larvae hatched. The genome of Esp_Z was sequenced, and transcriptome analyses were performed to identify bacterial genes that are important for colonization of the mosquito midgut, as well as for ROS-production. A gene expression analysis of members of the oxidative defence pathway of Plasmodium berghei was also conducted to assess the parasite’s oxidative defence response to Esp_Z exposure.ResultsEsp_Z persisted for up to 4 days in the An. gambiae midgut after introduction via nectar feeding, and was able to significantly inhibit Plasmodium sporogonic development. Introduction of this bacterium did not adversely affect mosquito fitness. Candidate genes involved in the selection of a better fit Esp_Z to the mosquito midgut environment and in its ability to condition oxidative status of its surroundings were identified, and parasite expression data indicated that Esp_Z is able to induce a partial and temporary shutdown of the ookinetes antioxidant response.ConclusionsEsp_Z is capable of inhibiting sporogonic development of Plasmodium in the presence of the mosquito’s native microbiota without affecting mosquito fitness. Several candidate bacterial genes are likely mediating midgut colonization and ROS production, and inhibition of Plasmodium development appears to involve a shutdown of the parasite’s oxidative defence system. A better understanding of the complex reciprocal tripartite interactions can facilitate the development and optimization of an Esp_Z-based malaria control strategy.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-016-1468-2) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Functional genomic analyses of Enterobacter, Anopheles and Plasmodium reciprocal interactions that impact vector competence

Dennison

Saraiva

Cirimotich

et al. 2016

Malar J

Self Cite

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“…A number of factors can contribute to the control of virus infection within the mosquito host, which in turn impact virus transmission to the vertebrate host. In addition to the mosquito infection barriers [115,117], the mosquito innate immune system includes the intrinsic RNAi pathway and several inducible systems, including Toll, immune deficiency (IMD) and Janus kinase/signal transducers and activators of transcription (JAK-STAT) pathways [116,118,119]. The Drosophila model system has been used to identify many of these antiviral immune pathways [120,121], but interestingly many of the Drosophila viruses can be highly pathogenic to their host.…”

Section: What Can We Learn From Research On Virus Interactions Witmentioning

confidence: 99%

“…The mosquito gut microbiome is diverse and can influence mosquito vector competence (reviewed in [119,123,124]). Perturbation of the bacterial microbiota can influence virus infection in mosquitoes.…”

Section: What Can We Learn From Research On Virus Interactions Witmentioning

confidence: 99%

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

Dietzgen

Mann

Johnson

2016

Viruses

195

142

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Acquisition and transmission by an insect vector is central to the infection cycle of the majority of plant pathogenic viruses. Plant viruses can interact with their insect host in a variety of ways including both non-persistent and circulative transmission; in some cases, the latter involves virus replication in cells of the insect host. Replicating viruses can also elicit both innate and specific defense responses in the insect host. A consistent feature is that the interaction of the virus with its insect host/vector requires specific molecular interactions between virus and host, commonly via proteins. Understanding the interactions between plant viruses and their insect host can underpin approaches to protect plants from infection by interfering with virus uptake and transmission. Here, we provide a perspective focused on identifying novel approaches and research directions to facilitate control of plant viruses by better understanding and targeting virus–insect molecular interactions. We also draw parallels with molecular interactions in insect vectors of animal viruses, and consider technical advances for their control that may be more broadly applicable to plant virus vectors.

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“…Many studies have demonstrated the influence of the microbiota on vector competence (van Tol and Dimopoulos, ). Some bacteria were shown to inhibit the development of viral pathogens and parasites indirectly by stimulating the mosquito immune system and/or directly by producing antimicrobial peptides (Hegde et al ., ; Saraiva et al ., ). Recent advances have also pointed out a role of the microbiota in many other key mosquito functions (Minard et al ., ; Guégan et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Who is eating fructose within the Aedes albopictus gut microbiota?

Guégan

Van

Martin

et al. 2020

Environmental Microbiology

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Summary The Asian tiger mosquito Aedes albopictus is a major public health concern because of its invasive success and its ability to transmit pathogens. Given the low availability of treatments against mosquito‐borne diseases, vector control remains the most suitable strategy. The methods used thus far are becoming less effective, but recent strategies have emerged from the study of mosquito‐associated microorganisms. Although the role of the microbiota in insect biology does not require further proof, much remains to be deciphered in mosquitoes, especially the contribution of the microbiota to host nutrient metabolism. Mosquitoes feed on plant nectar, composed of mostly fructose. We used stable isotope probing to identify bacteria and fungi assimilating fructose within the gut of Ae. albopictus. Mosquitoes were fed a 13C‐labelled fructose solution for 24 h. Differences in the active microbial community according to the sex of mosquitoes were highlighted. The bacterium Lelliottia and the fungi Cladosporium and Aspergillus dominated the active microbiota in males, whereas the bacterium Ampullimonas and the yeast Cyberlindnera were the most active in females. This study is the first to investigate trophic interactions between Ae. albopictus and its microbiota, thus underscoring the importance of the microbial component in nectar feeding in mosquitoes.

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Mosquito gut antiparasitic and antiviral immunity

Cited by 91 publications

References 164 publications

Functional genomic analyses of Enterobacter, Anopheles and Plasmodium reciprocal interactions that impact vector competence

Functional genomic analyses of Enterobacter, Anopheles and Plasmodium reciprocal interactions that impact vector competence

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

Who is eating fructose within the Aedes albopictus gut microbiota?

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