Wolbachia Do Not Induce Reactive Oxygen Species-Dependent Immune Pathway Activation in Aedes albopictus

Molloy, Jenny; Sinkins, Steven P.

doi:10.3390/v7082836

Cited by 31 publications

(40 citation statements)

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“…However in our experiments, and in w Mel-infected Ae . albopictus , Wolbachia did not affect duox-2 levels, potentially because the gene lacks peroxidase activity, and therefore cannot directly stimulate ROS [43]. As we observed ROS induction without an effect of Wolbachia on duox-2 , this implies that ROS induction occurs via a different process, potentially via the duox-1 gene.…”

Section: Discussionmentioning

confidence: 64%

“…However, it is not universal amongst all host-strain associations where pathogen interference occurs, as is the case for w Mel-infected Ae . albopictus , where there is interference against DENV and Chikungunya virus infection [43, 76, 77]. The fact that ROS induction occurs for w Mel-infected Ae .…”

Section: Discussionmentioning

confidence: 99%

“…The effect has been linked to activation of immune effector genes [22, 23, 38, 39], increased induction of reactive oxygen species (ROS) and related genes, which serve as part of the host defence against pathogens [38, 40], and competition for host cholesterol in Drosophila melanogaster [41]. Critically, none of these effects occur universally amongst the species and Wolbachia strains where pathogen interference has been observed, which suggests that the underlying mechanism may be complex, and that it could potentially be dependent on the length of the host-symbiont relationship [39, 42, 43]. …”

Section: Introductionmentioning

confidence: 99%

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Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti

Caragata¹,

Rezende²,

Simões³

et al. 2016

PLoS Negl Trop Dis

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The pathogen interference phenotype greatly restricts infection with dengue virus (DENV) and other pathogens in Wolbachia-infected Aedes aegypti, and is a vital component of Wolbachia-based mosquito control. Critically, the phenotype’s causal mechanism is complex and poorly understood, with recent evidence suggesting that the cause may be species specific. To better understand this important phenotype, we investigated the role of diet-induced nutritional stress on interference against DENV and the avian malarial parasite Plasmodium gallinaceum in Wolbachia-infected Ae. aegypti, and on physiological processes linked to the phenotype. Wolbachia-infected mosquitoes were fed one of four different concentrations of sucrose, and then challenged with either P. gallinaceum or DENV. Interference against P. gallinaceum was significantly weakened by the change in diet however there was no effect on DENV interference. Immune gene expression and H2O2 levels have previously been linked to pathogen interference. These traits were assayed for mosquitoes on each diet using RT-qPCR and the Amplex Red Hydrogen Peroxide/Peroxidase Assay Kit, and it was observed that the change in diet did not significantly affect immune expression, but low carbohydrate levels led to a loss of ROS induction in Wolbachia-infected mosquitoes. Our data suggest that host nutrition may not influence DENV interference for Wolbachia-infected mosquitoes, but Plasmodium interference may be linked to both nutrition and oxidative stress. This pathogen-specific response to nutritional change highlights the complex nature of interactions between Wolbachia and pathogens in mosquitoes.

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Section: Discussionmentioning

confidence: 64%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti

Caragata¹,

Rezende²,

Simões³

et al. 2016

PLoS Negl Trop Dis

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“…It is therefore unlikely that induction of ROS upon Wolbachia infection correlates with Toll pathway activation in Drosophila. Although the mechanistic involvement of ROS in the insect antiviral response remains to be elucidated, and a recent study has reported that Wolbachia do not induce ROS in Aedes albopictus (Molloy & Sinkins, 2015), ROSrelated responses may constitute a promising area for future research in understanding Wolbachia-mediated antiviral effects (Zug & Hammerstein, 2015).…”

Section: Discussionmentioning

confidence: 99%

Impact of ERK activation on fly survival and Wolbachia-mediated protection during virus infection

Wong

Brownlie

Johnson

2016

Journal of General Virology

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Elevated levels of reactive oxygen species (ROS) provide protection against virus-induced mortality in Drosophila. In addition to contributing to oxidative stress, ROS are known to activate a number of signalling pathways including the extracellular signal-regulated kinases (ERK) signalling cascade. It was recently shown that ERK signalling is important for resistance against viral replication and invasion in cultured Drosophila cells and the gut epithelium of adult flies. Here, using a Drosophila loss-of-function ERK (rolled) mutant we demonstrated that ERK is important for fly survival during virus infection. ERK mutant flies subjected to Drosophila C virus (DCV) oral and systemic infection were more susceptible to virus-induced mortality as compared with wild-type flies. We have demonstrated experimentally that ERK activation is important for fly survival during oral and systemic virus infection. Given that elevated ROS correlates with Wolbachia-mediated antiviral protection, we also investigated the involvement of ERK in antiviral protection in flies infected by Wolbachia. The results indicate that ERK activation is increased in the presence of Wolbachia but this does not appear to influence Wolbachia-mediated antiviral protection, at least during systemic infection.

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“…In contrast to A. albopictus, in which no impact of Wolbachia on immunity has been observed (Bourtzis et al, 2000;Molloy and Sinkins, 2015), wAlbB induces the production of reactive oxygen species and activates the Toll pathway in WB1 strain A. aegypti . In addition, wAlbB has been shown to grow to significantly higher densities in WB1 than in A. albopictus and invade different tissues such as the fat body, midgut, salivary glands, and ovaries .…”

Section: Introductionmentioning

confidence: 93%

The bacteriumWolbachiaexploits host innate immunity to establish a symbiotic relationship with the dengue vector mosquitoAedes aegypti

Pan¹

2016

2016 International Congress of Entomology

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A host's immune system plays a central role in shaping the composition of the microbiota and, in return, resident microbes influence immune responses. Symbiotic associations of the maternally transmitted bacterium Wolbachia occur with a wide range of arthropods. It is, however, absent from the dengue and Zika vector mosquito Aedes aegypti in nature. When Wolbachia is artificially forced to form symbiosis with this new mosquito host, it boosts the basal immune response and enhances the mosquito's resistance to pathogens, including dengue, Zika virus and malaria parasites. The mechanisms involved in establishing a symbiotic relationship between Wolbachia and A. aegypti, and the long-term outcomes of this interaction, are not well understood. Here, we have demonstrated that both the immune deficiency (IMD) and Toll pathways are activated by the Wolbachia strain wAlbB upon its introduction into A. aegypti. Silencing the Toll and IMD pathways via RNA interference reduces the wAlbB load. Notably, wAlbB induces peptidoglycan recognition protein (PGRP)-LE expression in the carcass of A. aegypti, and its silencing results in a reduction of symbiont load. Using transgenic mosquitoes with stage-specific induction of the IMD and Toll pathways, we have shown that elevated wAlbB infection in these mosquitoes is maintained via maternal transmission. These results indicate that host innate immunity is utilized to establish and promote host-microbial symbiosis. Our results will facilitate a long-term projection of the stability of the Wolbachia-A. aegypti mosquito system that is being developed to control dengue and Zika virus transmission to humans.

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Wolbachia Do Not Induce Reactive Oxygen Species-Dependent Immune Pathway Activation in Aedes albopictus

Cited by 31 publications

References 50 publications

Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti

Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti

Impact of ERK activation on fly survival and Wolbachia-mediated protection during virus infection

The bacteriumWolbachiaexploits host innate immunity to establish a symbiotic relationship with the dengue vector mosquitoAedes aegypti

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