Alphaviruses: Interactions between Arboviruses and Mosquitoes

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: closed (31 May 2020) | Viewed by 30860

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Guest Editor
Florida Medical Entomology Laboratory, University of Florida, Vero Beach, FL, USA
Interests: ecological interactions; arbovirus infection in peri-domestic and invasive mosquitoes
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Mosquito-borne Alphaviruses induce disease in humans and other animals ranging from mild acute febrile illness to severe disease, including life-long neurological complications. Recent outbreaks of chikungunya virus in the Indian Ocean, parts of Europe, and the Americas, and the potential for emergence of other arboviruses such as Mayaro, makes this group of arboviruses an emerging public health threat.  This special issue on Alphaviruses aims to provide a collection of research studies focused on interactions between arboviruses and mosquitoes.  In particular, the objective is to identify potential mosquito vectors for emerging arboviruses, geographic variation and potential determinants of mosquito vector competency, immune responses in mosquitoes in response to infection, and potential remedial techniques to interrupt the infection cycle in mosquitoes.  Identification of weak links between arbovirus replication and mosquito infection may provide an opportunity to inhibit arbovirus proliferation and reduce the risk of disease transmission.

Dr. Barry W. Alto
Guest Editor

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Keywords

  • Chikungunya virus
  • Mayaro virus
  • Mosquito-borne arboviruses
  • Alphavirus vector interactions
  • Immune response
  • Emerging arboviruses

Published Papers (11 papers)

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Research

18 pages, 1011 KiB  
Article
High-Throughput Method for Detection of Arbovirus Infection of Saliva in Mosquitoes Aedes aegypti and Ae. albopictus
by Nildimar Alves Honório, Daniel Cardoso Portela Câmara, Keenan Wiggins, Bradley Eastmond and Barry Wilmer Alto
Viruses 2020, 12(11), 1343; https://doi.org/10.3390/v12111343 - 23 Nov 2020
Cited by 4 | Viewed by 2581
Abstract
Vector competence refers to the ability of a vector to acquire, maintain, and transmit a pathogen. Collecting mosquito saliva in medium-filled capillary tubes has become the standard for approximating arbovirus transmission. However, this method is time-consuming and labor-intensive. Here we compare the capillary [...] Read more.
Vector competence refers to the ability of a vector to acquire, maintain, and transmit a pathogen. Collecting mosquito saliva in medium-filled capillary tubes has become the standard for approximating arbovirus transmission. However, this method is time-consuming and labor-intensive. Here we compare the capillary tube method to an alternative high-throughput detection method the collection of saliva on paper cards saturated with honey, with (FTA card) and without (filter paper) reagents for the preservation of nucleic acid for Aedes aegypti and Aedes albopictus mosquitoes infected with two emerging genotypes of the chikungunya virus (CHIKV). Model results showed that the Asian genotype CHIKV dissemination in the harvested legs of both Ae. aegypti and Ae. albopictus increased the odds of females having a positive salivary infection and higher salivary viral titers, while for the IOL genotype the same effect was observed only for Ae. aegypti. Of the three tested detection methods, the FTA card was significantly more effective at detecting infected saliva of Ae. aegypti and Ae. albopictus females than the capillary tube and filter paper was as effective as the capillary tube for the Asian genotype. We did not find significant effects of the detection method in detecting higher viral titer for both Asian and IOL genotypes. Our results are discussed in light of the limitations of the different tested detection methods. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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18 pages, 2196 KiB  
Article
Effects of Manipulating Fibroblast Growth Factor Expression on Sindbis Virus Replication In Vitro and in Aedes aegypti Mosquitoes
by Wenbi Wu, Cody A. Simmons, Jessica Moffitt, Rollie J. Clem and A. Lorena Passarelli
Viruses 2020, 12(9), 943; https://doi.org/10.3390/v12090943 - 26 Aug 2020
Cited by 2 | Viewed by 2432
Abstract
Fibroblast growth factors (FGFs) are conserved among vertebrate and invertebrate animals and function in cell proliferation, cell differentiation, tissue repair, and embryonic development. A viral fibroblast growth factor (vFGF) homolog encoded by baculoviruses, a group of insect viruses, is involved in escape of [...] Read more.
Fibroblast growth factors (FGFs) are conserved among vertebrate and invertebrate animals and function in cell proliferation, cell differentiation, tissue repair, and embryonic development. A viral fibroblast growth factor (vFGF) homolog encoded by baculoviruses, a group of insect viruses, is involved in escape of baculoviruses from the insect midgut by stimulating basal lamina remodeling. This led us to investigate whether cellular FGF is involved in the escape of an arbovirus from mosquito midgut. In this study, the effects of manipulating FGF expression on Sindbis virus (SINV) replication and escape from the midgut of the mosquito vector Aedes aegypti were examined. RNAi-mediated silencing of either Ae. aegypti FGF (AeFGF) or FGF receptor (AeFGFR) expression reduced SINV replication following oral infection of Ae. aegypti mosquitoes. However, overexpression of baculovirus vFGF using recombinant SINV constructs had no effect on replication of these viruses in cultured mosquito or vertebrate cells, or in orally infected Ae. aegypti mosquitoes. We conclude that reducing FGF signaling decreases the ability of SINV to replicate in mosquitoes, but that overexpression of vFGF has no effect, possibly because endogenous FGF levels are already sufficient for optimal virus replication. These results support the hypothesis that FGF signaling, possibly by inducing remodeling of midgut basal lamina, is involved in arbovirus midgut escape following virus acquisition from a blood meal. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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14 pages, 4835 KiB  
Article
The RNAi Pathway Is Important to Control Mayaro Virus Infection in Aedes aegypti but not for Wolbachia-Mediated Protection
by Pedro H. F. Sucupira, Álvaro G. A. Ferreira, Thiago H. J. F. Leite, Silvana F. de Mendonça, Flávia V. Ferreira, Fernanda O. Rezende, João T. Marques and Luciano A. Moreira
Viruses 2020, 12(8), 871; https://doi.org/10.3390/v12080871 - 10 Aug 2020
Cited by 11 | Viewed by 2829
Abstract
Mayaro virus (MAYV), a sylvatic arbovirus belonging to the Togaviridae family and Alphavirus genus, is responsible for an increasing number of outbreaks in several countries of Central and South America. Despite Haemagogus janthinomys being identified as the main vector of MAYV, laboratory studies [...] Read more.
Mayaro virus (MAYV), a sylvatic arbovirus belonging to the Togaviridae family and Alphavirus genus, is responsible for an increasing number of outbreaks in several countries of Central and South America. Despite Haemagogus janthinomys being identified as the main vector of MAYV, laboratory studies have already demonstrated the competence of Aedes aegypti to transmit MAYV. It has also been demonstrated that the WolbachiawMel strain is able to impair the replication and transmission of MAYV in Ae. aegypti. In Ae. aegypti, the small interfering RNA (siRNA) pathway is an important antiviral mechanism; however, it remains unclear whether siRNA pathway acts against MAYV infection in Ae. aegypti. The main objective of this study was to determine the contribution of the siRNA pathway in the control of MAYV infection. Thus, we silenced the expression of AGO2, an essential component of the siRNA pathway, by injecting dsRNA-targeting AGO2 (dsAGO2). Our results showed that AGO2 is required to control MAYV replication upon oral infection in Wolbachia-free Ae. aegypti. On the other hand, we found that Wolbachia-induced resistance to MAYV in Ae. aegypti is independent of the siRNA pathway. Our study brought new information regarding the mechanism of viral protection, as well as on Wolbachia mediated interference. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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11 pages, 1937 KiB  
Article
Chikungunya virus Detection in Aedes aegypti and Culex quinquefasciatus during an Outbreak in the Amazon Region
by Ana Cecília Ribeiro Cruz, Joaquim Pinto Nunes Neto, Sandro Patroca da Silva, Eliana Vieira Pinto da Silva, Glennda Juscely Galvão Pereira, Maissa Maia Santos, Hamilton Antônio de Oliveira Monteiro, Flavia Barreto dos Santos, Ricardo José de Paula Souza e Guimarães, Carine Fortes Aragão and Lívia Carício Martins
Viruses 2020, 12(8), 853; https://doi.org/10.3390/v12080853 - 04 Aug 2020
Cited by 8 | Viewed by 2935
Abstract
Chikungunya virus (CHIKV) was first reported in Brazil in 2014 and, after it spread countrywide, an outbreak of febrile illness with reports of arthralgia happened in the municipality of Xinguara, Pará, Brazil in 2017, indicating the virus’ circulation. Here, we aimed to investigate [...] Read more.
Chikungunya virus (CHIKV) was first reported in Brazil in 2014 and, after it spread countrywide, an outbreak of febrile illness with reports of arthralgia happened in the municipality of Xinguara, Pará, Brazil in 2017, indicating the virus’ circulation. Here, we aimed to investigate CHIKV in mosquito vectors collected during an active surveillance of virus isolation in cell culture by using molecular detection and viral genome sequencing. A total of 492 Aedes, Culex and Mansonia mosquitoes were collected and separated in 36 pools according to the species and sex, and 22.2% (8/36) were positive. CHIKV was indentified in pools of Ae. aegypti females (n = 5), an Ae. aegypti male (n = 1) and in Culex quinquefasciatus females (n = 2). However, as the mosquitoes’ whole bodies were macerated and used for detection, one cannot suggest the role of the latter in the viral transmission. Despite this, vector competence studies must be carried out in the different species to investigate long-term adaptations. Viral genome sequencing has characterized the East-Central-South-African (ECSA) genotype in all positive pools analyzed, corroborating previous reports for the Amazon region. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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16 pages, 20750 KiB  
Article
The Alphavirus Sindbis Infects Enteroendocrine Cells in the Midgut of Aedes aegypti
by Yani P. Ahearn, Jason J. Saredy and Doria F. Bowers
Viruses 2020, 12(8), 848; https://doi.org/10.3390/v12080848 - 04 Aug 2020
Cited by 2 | Viewed by 2517
Abstract
Transit of the arthropod-borne-virus (arbovirus) Sindbis (SINV) throughout adult female mosquitoes initiates with its attachment to the gut lumen, entry and amplification in midgut cells, followed by dissemination into the hemolymph. Free-mated adult females, aged day 5–7, were proffered a viremic blood suspension [...] Read more.
Transit of the arthropod-borne-virus (arbovirus) Sindbis (SINV) throughout adult female mosquitoes initiates with its attachment to the gut lumen, entry and amplification in midgut cells, followed by dissemination into the hemolymph. Free-mated adult females, aged day 5–7, were proffered a viremic blood suspension via sausage casings containing SINV-TaV-Green Fluorescent Protein (GFP) at a final titer of 106 PFU/mL. Midguts (MGs) from fully engorged mosquitoes were resected on days 5 and 7 post-bloodmeal, and immunolabeled using FMRFamide antibody against enteroendocrine cells (ECs) with a TX-Red secondary antibody. Following immunolabeling, the organs were investigated via laser confocal microscopy to identify the distribution of GFP and TX-Red. Infection using this reporter virus was observed as multiple GFP expression foci along the posterior midgut (PMG) epithelium and ECs were observed as TX-Red labeled cells scattered along the entire length of the MG. Our results demonstrated that SINVGFP did infect ECs, as indicated by the overlapping GFP and TX-Red channels shown as yellow in merged images. We propose that ECs may be involved in the SINV infection pathway in the mosquito MG. Due to the unique role that ECs have in the exocytosis of secretory granules from the MG and the apical-basolateral position of ECs in the PMG monolayer, we speculate that these cells may assist as a mechanism for arboviruses to cross the gut barriers. These findings suggest that MG ECs are involved in arbovirus infection of the invertebrate host. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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22 pages, 1726 KiB  
Article
Effects of Mosquito Biology on Modeled Chikungunya Virus Invasion Potential in Florida
by Cynthia C. Lord, L. Philip Lounibos, Joseph J. Pohedra and Barry W. Alto
Viruses 2020, 12(8), 830; https://doi.org/10.3390/v12080830 - 30 Jul 2020
Cited by 1 | Viewed by 2343
Abstract
Arboviruses transmitted by Aedes aegypti and Aedes albopictus have been introduced to Florida on many occasions. Infrequently, these introductions lead to sporadic local transmission and, more rarely, sustained local transmission. Both mosquito species are present in Florida, with spatio-temporal variation in population composition. [...] Read more.
Arboviruses transmitted by Aedes aegypti and Aedes albopictus have been introduced to Florida on many occasions. Infrequently, these introductions lead to sporadic local transmission and, more rarely, sustained local transmission. Both mosquito species are present in Florida, with spatio-temporal variation in population composition. We developed a two-vector compartmental, deterministic model to investigate factors influencing Chikungunya virus (CHIKV) establishment. The model includes a nonlinear, temperature-dependent mosquito mortality function based on minimum mortality in a central temperature region. Latin Hypercube sampling was used to generate parameter sets used to simulate transmission dynamics, following the introduction of one infected human. The analysis was repeated for three values of the mortality function central temperature. Mean annual temperature was consistently important in the likelihood of epidemics, and epidemics increased as the central temperature increased. Ae. albopictus recruitment was influential at the lowest central temperature while Ae. aegypti recruitment was influential at higher central temperatures. Our results indicate that the likelihood of CHIKV establishment may vary, but overall Florida is permissive for introductions. Model outcomes were sensitive to the specifics of mosquito mortality. Mosquito biology parameters are variable, and improved understanding of this variation will improve our ability to predict the outcome of introductions. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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12 pages, 1518 KiB  
Article
Profiling Transcripts of Vector Competence between Two Different Aedes aegypti Populations in Florida
by Dongyoung Shin, Seokyoung Kang and Chelsea T. Smartt
Viruses 2020, 12(8), 823; https://doi.org/10.3390/v12080823 - 29 Jul 2020
Cited by 3 | Viewed by 2282
Abstract
A Chikungunya virus (CHIKV) outbreak in Italy in 2007 spread to include the islands of the Caribbean and most of the Americas and still circulates in Europe and Africa. Florida being close in distance to the Caribbean islands experienced a CHIKV outbreak in [...] Read more.
A Chikungunya virus (CHIKV) outbreak in Italy in 2007 spread to include the islands of the Caribbean and most of the Americas and still circulates in Europe and Africa. Florida being close in distance to the Caribbean islands experienced a CHIKV outbreak in 2014 and continues to have a few travel-related cases each year. It is known that different environmental conditions in different regions can result in genetic variation that favor changes in competence to arbovirus. We evaluated the vector competence of Florida Aedes aegypti for CHIKV and determined if there is a geographic component that influences genes involved in CHIKV competence. We utilized a genomic approach to identify the candidate genes using RNA sequencing. The infection and dissemination results showed that field populations were more competent vectors for CHIKV than a lab population. The differentially expressed genes in the two field-collected CHIKV-infected populations, compared to the Rockefeller strain, were related to the Wnt/Notch signaling pathway, with similarity to genes scattered throughout the signaling pathway. This result suggested the possibility of identifying genes involved in the determination of vector competence in different gene pools of Ae. aegypti. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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14 pages, 2122 KiB  
Article
aBravo Is a Novel Aedes aegypti Antiviral Protein That Interacts with, but Acts Independently of, the Exogenous siRNA Pathway Effector Dicer 2
by Margus Varjak, Rommel J. Gestuveo, Richard Burchmore, Esther Schnettler and Alain Kohl
Viruses 2020, 12(7), 748; https://doi.org/10.3390/v12070748 - 11 Jul 2020
Cited by 4 | Viewed by 4226
Abstract
Mosquitoes, such as Aedes aegypti, can transmit arboviruses to humans. The exogenous short interfering RNA (exo-siRNA) pathway plays a major antiviral role in controlling virus infection in mosquito cells. The Dicer 2 (Dcr2) nuclease is a key effector protein in this pathway, [...] Read more.
Mosquitoes, such as Aedes aegypti, can transmit arboviruses to humans. The exogenous short interfering RNA (exo-siRNA) pathway plays a major antiviral role in controlling virus infection in mosquito cells. The Dicer 2 (Dcr2) nuclease is a key effector protein in this pathway, which cleaves viral double-stranded RNA into virus-derived siRNAs that are further loaded onto an effector called Argonaute 2 (Ago2), which as part of the multiprotein RNA-induced silencing complex (RISC) targets and cleaves viral RNA. In order to better understand the effector protein Dcr2, proteomics experiments were conducted to identify interacting cellular partners. We identified several known interacting partners including Ago2, as well as two novel and previously uncharacterized Ae. aegypti proteins. The role of these two proteins was further investigated, and their interactions with Dcr2 verified by co-immunoprecipitation. Interestingly, despite their ability to interact with Ago2 and Piwi4, neither of these proteins was found to affect exo-siRNA silencing in a reporter assay. However, one of these proteins, Q0IFK9, subsequently called aBravo (aedine broadly active antiviral protein), was found to mediate antiviral activity against positive strand RNA arboviruses. Intriguingly the presence of Dcr2 was not necessary for this effect, suggesting that this interacting antiviral effector may act as part of protein complexes with potentially separate antiviral activities. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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18 pages, 1349 KiB  
Article
Effect of Oral Infection of Mayaro Virus on Fitness Correlates and Expression of Immune Related Genes in Aedes aegypti
by Barry W. Alto, Ayse Civana, Keenan Wiggins, Bradley Eastmond and Dongyoung Shin
Viruses 2020, 12(7), 719; https://doi.org/10.3390/v12070719 - 02 Jul 2020
Cited by 7 | Viewed by 2214
Abstract
Mayaro virus is a mosquito-borne Alphavirus endemic to forests of tropical South America with a sylvatic cycle involving non-human primates and Haemagogus mosquitoes. Human infection with Mayaro virus causes a febrile illness and long-lasting arthralgia and cases are often associated with exposure to [...] Read more.
Mayaro virus is a mosquito-borne Alphavirus endemic to forests of tropical South America with a sylvatic cycle involving non-human primates and Haemagogus mosquitoes. Human infection with Mayaro virus causes a febrile illness and long-lasting arthralgia and cases are often associated with exposure to tropical forest habitats. Human movement between tropical forest habitats and urban settings may allow for imported cases and subsequent local transmission by domestic mosquito Aedes aegypti. The relative importance of Ae. aegypti as a vector of Mayaro virus may depend on the pathogenic effects of the virus on fitness correlates, especially those entomological parameters that relate to vectorial capacity. We performed mosquito infection studies and compared adult survival and fecundity of females from Brazilian and Floridian populations of Ae. aegypti following oral ingestion of uninfectious (control) and Mayaro virus infectious blood. Mayaro virus infected and refractory mosquitoes had similar or 30–50% lower fecundity than control (unexposed) mosquitoes, suggesting a reproductive cost to mounting an immune response or phenotypic expression of refractoriness. Survival of adult female mosquitoes and targeted gene expression in the Toll and IMD pathways were not altered by Mayaro virus infection. Adult lifespan and fecundity estimates were independent of measured viral titer in the bodies of mosquitoes. The lack of adverse effects of infection status on female survival suggests that Mayaro virus will not alter vectorial capacity mediated by changes in this parameter. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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20 pages, 3823 KiB  
Article
Distinct New York City Aedes albopictus Mosquito Populations Display Differences in Salivary Gland Protein D7 Diversity and Chikungunya Virus Replication
by Maria E. Kaczmarek, Nora L. Herzog, Maria G. Noval, John Zuzworsky, Zahir Shah, Waheed I. Bajwa and Kenneth A. Stapleford
Viruses 2020, 12(7), 698; https://doi.org/10.3390/v12070698 - 28 Jun 2020
Cited by 6 | Viewed by 2223
Abstract
In an increasingly interconnected world, the exposure and subsequent spread of emergent viruses has become inevitable. This is particularly true for Aedes (Ae.) mosquito-vectored viruses, whose range has increased over the past decade from tropical to temperate regions. However, it is [...] Read more.
In an increasingly interconnected world, the exposure and subsequent spread of emergent viruses has become inevitable. This is particularly true for Aedes (Ae.) mosquito-vectored viruses, whose range has increased over the past decade from tropical to temperate regions. However, it is unclear if all populations of Ae. mosquitoes in temperate New York City are able to successfully replicate and transmit arboviruses. To answer this question, we reared Ae. albopictus mosquitoes living in a temperate climate from three locations in New York City. We first sequenced the salivary antiviral protein D7 from individual mosquitoes in each population and found single nucleotide variants that are both shared and unique for each Ae. albopictus population. We then fed each population chikungunya virus (CHIKV) via an artificial blood meal. All three mosquito populations could be infected with CHIKV, yet viral titers differed between populations at 7 days post infection. Moreover, we found that these mosquitoes could transmit CHIKV to mice, and that virus RNA reached the saliva as early as two days post infection. Upon sequencing of the saliva CHIKV genomic RNA, we found mutations at sites correlated with increased transmission and virulence. These studies show that NYC Ae. albopictus populations can be infected with and transmit CHIKV, CHIKV is able to evolve in these mosquitoes, and that host salivary factors display population-specific diversity. Taken together, these studies highlight the need to study how distinct mosquito populations control viral infections, both at the virus and host level. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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23 pages, 5369 KiB  
Article
Ross River Virus Provokes Differentially Expressed MicroRNA and RNA Interference Responses in Aedes aegypti Mosquitoes
by James B. Sinclair and Sassan Asgari
Viruses 2020, 12(7), 695; https://doi.org/10.3390/v12070695 - 27 Jun 2020
Cited by 10 | Viewed by 3270
Abstract
Alphaviruses are globally distributed and predominately transmitted by mosquitoes. Aedes species are common vectors for the clinically important alphaviruses—Chikungunya, Sindbis, and Ross River (RRV) viruses—with Aedes aegypti also being a vector for the flaviviruses dengue, Yellow Fever, and Zika viruses. Ae. aegypti was [...] Read more.
Alphaviruses are globally distributed and predominately transmitted by mosquitoes. Aedes species are common vectors for the clinically important alphaviruses—Chikungunya, Sindbis, and Ross River (RRV) viruses—with Aedes aegypti also being a vector for the flaviviruses dengue, Yellow Fever, and Zika viruses. Ae. aegypti was putatively implicated in the large 1979–1980 South Pacific Islands outbreak of RRV—the leading cause of arboviral disease in Australia today. The RNA interference (RNAi) defense response in mosquitoes involves a number of small RNAs, with their kinetics induced by alphaviruses being poorly understood, particularly at the tissue level. We compared the small RNA profiles between RRV-infected and non-infected Ae. aegypti midgut and fat body tissues at 2, 6, and 12 days post-inoculation (dpi). RRV induced an incremental RNAi response, yielding short interfering and P-element-induced-wimpy-testis (PIWI)-interacting RNAs. Fourteen host microRNAs were differentially expressed due to RRV with the majority in the fat body at 2 dpi. The largely congruent pattern of microRNA regulation with previous reports for alphaviruses and divergence from those for flaviviruses suggests a degree of conservation, whereas patterns of microRNA expression unique to this study provide novel insights into the tissue-specific host-virus attributes of Ae. aegypti responses to this previously unexplored old-world alphavirus. Full article
(This article belongs to the Special Issue Alphaviruses: Interactions between Arboviruses and Mosquitoes)
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