Field-Reassortment of Bluetongue Virus Illustrates Plasticity of Virus Associated Phenotypic Traits in the Arthropod Vector and Mammalian Host
            <i>In Vivo</i>

Sanders, C. J.; Veronesi, Eva; Rajko-Nenow, Paulina; Mertens, Peter P. C.; Batten, Carrie; Gubbins, Simon; Carpenter, Simon; Darpel, Karin E.

doi:10.1128/jvi.00531-22

Cited by 13 publications

(19 citation statements)

References 61 publications

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“…Culicoides with virus-infected cell supernatant has been commonly used (Pages et al, 2014;Sanders et al, 2022). ITI bypasses mesenteron infection (MIB) and escape barriers (MEB) found in the vector and typically results in 100% of surviving individuals being able to transmit the virus (100% vector competence) and hence, it is commonly assumed that ITI would result in the infection of the salivary apparatus of all individuals.…”

Section: Development Of a Protocol For 3d Imaging Of The Salivary App...mentioning

confidence: 99%

“…The bodies of all dissected Culicoides were homogenised, total RNA was extracted and BTV genome detected and quantified using a BTV-specific qRT-PCR (Hofmann et al, 2008). As observed in studies of Culicoides vector competence for BTV (Guimera Ropiak et al, 2021;Sanders et al, 2022), in groups infected by oral feeding, insects separate into three defined populations: those with no viral RNA (vRNA) detected (no Ct); individuals with lower amounts of vRNA (≤ 4.00E+07 genome copies/body, equivalent to a Ct value of ≈25 in our assay) and deemed to not support virus transmission (hence not vector competent), and those with greater quantities of vRNA (≥4.00E+07 genome copies/insect) and deemed vector competent (Figure 6…”

Section: Detection Of Virus In the Salivary Apparatus By Immunolabell...mentioning

confidence: 99%

“…Bluetongue virus (BTV) isolate BTV-4 MOR2009/07 (cell passage KC1), was obtained from the Orbivirus Reference Collection (ORC) at The Pirbright Institute, UK (https://www.reoviridae.org/dsRNA_virus_proteins/ReoID/btv-4.htm#MOR2009/07, accessed on 13 th June 2023) and was previously shown to infect Culicoides sonorensis at high rates (Sanders et al, 2022). Working stocks of the virus were generated by two additional propagations on Culicoidesderived KC cells as previously described (Stevens et al, 2019) and kept at +4 °C.…”

Section: Virusmentioning

confidence: 99%

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Visualisation of bluetongue virus in the salivary apparatus of Culicoides biting midges highlights the accessory glands as a primary arboviral infection site

Busquets

Brown

Carpenter

et al. 2023

Preprint

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Background Arthropods transmit a wide range of pathogens of importance for the global health of humans, animals, and plants. One of these arthropod vectors, Culicoides biting midges (Diptera: Ceratopogonidae), are the biological vectors of several human and animal pathogens, including economically important livestock viruses like bluetongue virus (BTV). Like other arthropods-borne viruses (arboviruses), Culicoides-borne viruses must reach and replicate in the salivary apparatus, from where they can be transmitted to susceptible hosts through the saliva during subsequent blood feeding. Despite the importance of the salivary gland apparatus for pathogen transmission to susceptible animals from the bite of infected Culicoides, these structures have received relatively little attention, perhaps due to the small size and fragility of these vectors. Results In this study, we developed techniques to visualize the infection of the salivary glands and other soft tissues with BTV, in one of the smallest known arbovirus vectors, Culicoides biting midges, using three-dimensional immunofluorescence confocal microscopy. We showed BTV infection of specific structures of the salivary gland apparatus of female Culicoides vectors following oral virus uptake, related visualisation of viral infection in the salivary apparatus to high viral RNA copies in the body, and demonstrated for the first time, that the accessory glands are a primary site for BTV replication within the salivary apparatus. Conclusions Our work has revealed a novel site of virus-vector interactions, and a novel role of the accessory glands of Culicoides in arbovirus amplification and transmission. Our approach would also be applicable to a wide range of arbovirus vector groups including sandflies (Diptera: Psychodidae), as well as provide a powerful tool to investigate arbovirus infection and dissemination, particularly where there are practical challenges in the visualization of small size and delicate tissues of arthropods.

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Section: Development Of a Protocol For 3d Imaging Of The Salivary App...mentioning

confidence: 99%

Section: Detection Of Virus In the Salivary Apparatus By Immunolabell...mentioning

confidence: 99%

Section: Virusmentioning

confidence: 99%

See 1 more Smart Citation

Visualisation of bluetongue virus in the salivary apparatus of Culicoides biting midges highlights the accessory glands as a primary arboviral infection site

Busquets

Brown

Carpenter

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…It important to recognize that while BTV is traditionally classified by serotype, there is additional diversity in the remaining nine genomic segments. As a virus with a segmented genome, reassortment is an important mechanism for BTV evolution [ 23 , 24 ]. Reassortment occurs when two or more parental virus strains exchange genomic segments resulting in progeny with novel segment combinations.…”

Section: Introductionmentioning

confidence: 99%

Evaluating Temperature Effects on Bluetongue Virus Serotype 10 and 17 Coinfection in Culicoides sonorensis

Carpenter,

Kopanke,

Lee

et al. 2024

IJMS

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Bluetongue virus (BTV) is a segmented, double-stranded RNA virus transmitted by Culicoides midges that infects ruminants. As global temperatures increase and geographical ranges of midges expand, there is increased potential for BTV outbreaks from incursions of novel serotypes into endemic regions. However, an understanding of the effect of temperature on reassortment is lacking. The objectives of this study were to compare how temperature affected Culicoides survival, virogenesis, and reassortment in Culicoides sonorensis coinfected with two BTV serotypes. Midges were fed blood meals containing BTV-10, BTV-17, or BTV serotype 10 and 17 and maintained at 20 °C, 25 °C, or 30 °C. Midge survival was assessed, and pools of midges were collected every other day to evaluate virogenesis of BTV via qRT-PCR. Additional pools of coinfected midges were collected for BTV plaque isolation. The genotypes of plaques were determined using next-generation sequencing. Warmer temperatures impacted traits related to vector competence in offsetting ways: BTV replicated faster in midges at warmer temperatures, but midges did not survive as long. Overall, plaques with BTV-17 genotype dominated, but BTV-10 was detected in some plaques, suggesting parental strain fitness may play a role in reassortment outcomes. Temperature adds an important dimension to host–pathogen interactions with implications for transmission and evolution.

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“…A positive BT diagnosis is established based on clinical and pathological anatomical examinations (Bianchi et al 2017;Kang et al 2022;Sanders et al 2022). Viral detection is determined by the presence of either viral mRNA determined by PCR or virus-specific antibodies from whole blood, organ, or tissues samples from suspected, infected animals (Maan et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Improved Efficiency of Bluetongue Viral Antigen Isolation for Successful Immunization

2022

Int J Vet Sci

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Bluetongue (BT) is a viral disease transmitted by Culicoides spp. The clinical presentation of BT varies widely among susceptible sheep, and in most cases results in severe illness and death in the infected animals. The mortality among susceptible sheep ranges from 2-30% but can occasionally be as high as 70%. Therefore, we investigated a new method to increase the purified BTV-antigen. BTV viral suspensions were purified using Freon-113 and ultracentrifugation through 40% sucrose. We obtained 94.5-95.8% purification of the BT-16 viral antigen. Sheep and cows were immunized with the isolated BTV antigen obtained from this method to confirm antibody specificity to BTV. The antibody activity measured by enzyme-linked immunosorbent assay (ELISA) from goat serum was 7.0log2 to 13.0log2 (on average 10.8±2.28log2) relative to that of sheep (P<0.05 to P<0.0001). We show here that this method can successfully purify BTV-16 antigen and could be used for large-scale production and other BTV serotypes.

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Field-Reassortment of Bluetongue Virus Illustrates Plasticity of Virus Associated Phenotypic Traits in the Arthropod Vector and Mammalian Host In Vivo

Cited by 13 publications

References 61 publications

Visualisation of bluetongue virus in the salivary apparatus of Culicoides biting midges highlights the accessory glands as a primary arboviral infection site

Visualisation of bluetongue virus in the salivary apparatus of Culicoides biting midges highlights the accessory glands as a primary arboviral infection site

Evaluating Temperature Effects on Bluetongue Virus Serotype 10 and 17 Coinfection in Culicoides sonorensis

Improved Efficiency of Bluetongue Viral Antigen Isolation for Successful Immunization

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