Non-retroviral Endogenous Viral Element Limits Cognate Virus Replication in Aedes aegypti Ovaries

Suzuki, Yasutsugu; Baidaliuk, Artem; Miesen, Pascal; Frangeul, Lionel; Crist, Anna B.; Merkling, Sarah H.; Fontaine, Albin; Lequime, Sébastian; Moltini-Conclois, Isabelle; Blanc, Hervé; Rij, Ronald P. van; Lambrechts, Louis; Saleh, Maria-Carla

doi:10.1016/j.cub.2020.06.057

Cited by 87 publications

(83 citation statements)

References 78 publications

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“…More complex interactions between intrinsic ( e . g ., mosquito virome [ 43 ], endogenous non-retroviral elements [ 44 , 45 ], or bacterial microbiome [ 46 ]) or environmental ( e . g ., temperature [ 47 , 48 ], rearing or experimental settings) conditions might further impede comparisons across vector competence studies [ 49 ].…”

Section: Discussionmentioning

confidence: 99%

Modeling intra-mosquito dynamics of Zika virus and its dose-dependence confirms the low epidemic potential of Aedes albopictus

Lequime

Dehecq²,

Matheus

et al. 2020

PLoS Pathog

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Originating from African forests, Zika virus (ZIKV) has now emerged worldwide in urbanized areas, mainly transmitted by Aedes aegypti mosquitoes. Although Aedes albopictus can transmit ZIKV experimentally and was suspected to be a ZIKV vector in Central Africa, the potential of this species to sustain virus transmission was yet to be uncovered until the end of 2019, when several autochthonous transmissions of the virus vectored by Ae. albopictus occurred in France. Aside from these few locally acquired ZIKV infections, most territories colonized by Ae. albopictus have been spared so far. The risk level of ZIKV emergence in these areas remains however an open question. To assess Ae. albopictus’ vector potential for ZIKV and identify key virus outbreak predictors, we built a complete framework using the complementary combination of (i) dose-dependent experimental Ae. albopictus exposure to ZIKV followed by time-dependent assessment of infection and systemic infection rates, (ii) modeling of intra-human ZIKV viremia dynamics, and (iii) in silico epidemiological simulations using an Agent-Based Model. The highest risk of transmission occurred during the pre-symptomatic stage of the disease, at the peak of viremia. At this dose, mosquito infection probability was estimated to be 20%, and 21 days were required to reach the median systemic infection rates. Mosquito population origin, either temperate or tropical, had no impact on infection rates or intra-host virus dynamic. Despite these unfavorable characteristics for transmission, Ae. albopictus was still able to trigger and yield large outbreaks in a simulated environment in the presence of sufficiently high mosquito biting rates. Our results reveal a low but existing epidemic potential of Ae. albopictus for ZIKV, that might explain the absence of large scale ZIKV epidemics so far in territories occupied only by Ae. albopictus. They nevertheless support active surveillance and eradication programs in these territories to maintain the risk of emergence to a low level.

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Section: Discussionmentioning

confidence: 99%

Modeling intra-mosquito dynamics of Zika virus and its dose-dependence confirms the low epidemic potential of Aedes albopictus

Lequime

Dehecq²,

Matheus

et al. 2020

PLoS Pathog

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“…In particular, EREs derived from non-retroviral RNA viruses in insect systems have been actively studied in recent years and are found to provide partial protection against parent viruses. The Saleh group has reported this phenomenon in the form of finding reverse-transcribed viral DNA (from RNA of insect flaviviruses) capable of inducing virus-specific siRNA responses amplification in a range of insect cells [157][158][159][160]. Even when more studies are warranted before a definitive antiviral or proviral role can be ascribed to EREs in mammalian systems during infection, we hypothesize that future studies may show more host nucleic acids can act as agonists for the cGAS/STING pathway during RNA virus infection.…”

Section: Perspectivesmentioning

confidence: 99%

Innate Immune DNA Sensing of Flaviviruses

Zhu

Fernández-Sesma

2020

Viruses

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Flaviviruses are arthropod-borne RNA viruses that have been used extensively to study host antiviral responses. Often selected just to represent standard single-stranded positive-sense RNA viruses in early studies, the Flavivirus genus over time has taught us how truly unique it is in its remarkable ability to target not just the RNA sensory pathways but also the cytosolic DNA sensing system for its successful replication inside the host cell. This review summarizes the main developments on the unexpected antagonistic strategies utilized by different flaviviruses, with RNA genomes, against the host cyclic GAMP synthase (cGAS)/stimulator of interferon genes (STING) cytosolic DNA sensing pathway in mammalian systems. On the basis of the recent advancements on this topic, we hypothesize that the mechanisms of viral sensing and innate immunity are much more fluid than what we had anticipated, and both viral and host factors will continue to be found as important factors contributing to the host innate immune system in the future.

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“…It is therefore valuable to develop our ability to perturb the function of this pathway in vivo , but direct manipulation of endogenous piRNA sequences for direct hypothesis testing is not yet straight-forward in any organism. Although transgenesis and targeted genome editing using Cas9 in mosquitoes were accomplished by 1998 and 2015 respectively, opening up the possibility use genome modifications to explore the piRNA biology, the first report to do so came out this year ( Coates et al, 1998 ; Jasinskiene et al, 1998 ; Basu et al, 2015 ; Dong et al, 2015 ; Kistler et al, 2015 ; Suzuki et al, 2020 ).…”

Section: The Pirna Pathway Exemplifies Basic Biology In Mosquitoes Thmentioning

confidence: 99%

“…A prominent difference is the antiviral activity of the piRNA pathway observed in mosquitoes, but not Drosophila ( Petit et al, 2016 ). piRNAs that may regulate virus replications are generated both from the virus genome ( Hess et al, 2011 ; Morazzani et al, 2012 ; Vodovar et al, 2012 ; Léger et al, 2013 ; Miesen et al, 2015 ; Miesen et al, 2016 ; Göertz et al, 2019 ) and from Endogenous Virus Elements (EVEs) in the mosquito genome, fragments of viruses often integrated into piRNA clusters ( Lequime and Lambrechts, 2017 ; Palatini et al, 2017 ; Suzuki et al, 2017 ; Whitfield et al, 2017 ; ter Horst et al, 2018 ; Aguiar et al, 2020 ; Blair et al, 2020 ; Suzuki et al, 2020 ). Further specialization in mosquitoes is evidenced in both Aedes and Anopheles species: 1) PIWI genes and other piRNA pathway genes have expanded and diverged in Aedes mosquitoes ( Bernhardt et al, 2012 ; Miesen et al, 2015 ; Marconcini et al, 2019 ; Ma et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Leaning Into the Bite: The piRNA Pathway as an Exemplar for the Genetic Engineering Need in Mosquitoes

Macias

Palatini

Bonizzoni

et al. 2021

Front. Cell. Infect. Microbiol.

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The piRNA pathway is a specialized small RNA interference that in mosquitoes is mechanistically distant from analogous biology in the Drosophila model. Current genetic engineering methods, such as targeted genome manipulation, have a high potential to tease out the functional complexity of this intricate molecular pathway. However, progress in utilizing these methods in arthropod vectors has been geared mostly toward the development of new vector control strategies rather than to study cellular functions. Herein we propose that genetic engineering methods will be essential to uncover the full functionality of PIWI/piRNA biology in mosquitoes and that extending the applications of genetic engineering on other aspects of mosquito biology will grant access to a much larger pool of knowledge in disease vectors that is just out of reach. We discuss motivations for and impediments to expanding the utility of genetic engineering to study the underlying biology and disease transmission and describe specific areas where efforts can be placed to achieve the full potential for genetic engineering in basic biology in mosquito vectors. Such efforts will generate a refreshed intellectual source of novel approaches to disease control and strong support for the effective use of approaches currently in development.

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Non-retroviral Endogenous Viral Element Limits Cognate Virus Replication in Aedes aegypti Ovaries

Cited by 87 publications

References 78 publications

Modeling intra-mosquito dynamics of Zika virus and its dose-dependence confirms the low epidemic potential of Aedes albopictus

Modeling intra-mosquito dynamics of Zika virus and its dose-dependence confirms the low epidemic potential of Aedes albopictus

Innate Immune DNA Sensing of Flaviviruses

Leaning Into the Bite: The piRNA Pathway as an Exemplar for the Genetic Engineering Need in Mosquitoes

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