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Biology subjects

Pompon, J.

Publications and source records attributed to Pompon, J..

11 recordsLinked to original sources

BIRD-Seq: B2 Protein Integrated End-to-End Pipeline for dsRNA Detection and Nanopore Sequencing for Virus Monitoring

Double-stranded RNA (dsRNA) is a near-universal hallmark of active viral infection. Despite its role as a pan-viral replication intermediate, dsRNA-centred technologies for virus monitoring remain scarce and largely rely on monoclonal antibody-based approaches that, while highly sensitive, are costly and difficult to engineer, scale, or integrate with downstream assays. Here, we present a modular and antibody-free pipeline for quantitative and qualitative dsRNA analysis built around an engineered B2 protein from Flock House virus with nanomolar-range binding affinity. The pipeline is compatible with absorbance- or luminescence-based measurement formats. In a sandwich assay configuration (Sand-BIRD), sub-ng mL-1 quantification of dsRNA is achieved, comparable to the gold standard J2 monoclonal antibody, directly from crude biological samples without RNA extraction. Sand-BIRD reliably detects viral infection in both plant samples (Tomato bushy stunt virus and Grapevine fanleaf virus) and mosquitoes (West Nile virus and Dengue virus) with commercial-grade reliability. dsRNA eluted from positive samples were further processed directly by Oxford Nanopore direct sequencing, enabling identification of virus species without prior sequence knowledge or total RNA extraction. Together, this work establishes an end-to-end, sequence-agnostic workflow for direct RNA-duplex quantification and sequencing (BIRD-Seq), which has compelling potential for emerging infectious disease surveillance and next-generation point-of-care (PoC) diagnostics. Technology ReadinessBIRD-Seq is an integrated pipeline for agnostic dsRNA detection and sequencing designed for broad-spectrum virus monitoring. A Technology Readiness Level (TRL) 5 under NASAs classification framework has been reached as BIRD-Seq has been validated in laboratory-relevant environments using real-world samples, including virus-infected plants and mosquitoes. The ELISA-based sensing platform employs engineered variants of the B2 protein (from Flock House virus) in a sandwich assay format for dsRNA capture and detection, achieving sensitivity comparable to the gold-standard J2 monoclonal antibody. Unlike traditional antibody-based methods, the B2 protein offers key practical advantages: straightforward production in bacterial expression systems, high versatility, and reduced manufacturing costs, as well as direct compatibility with crude extract monitoring, eliminating the need for RNA extraction. Captured B2/RNA duplexes can then be directly eluted from the ELISA microplates and subjected to downstream nanopore direct RNA sequencing, providing both quantitative and qualitative information on the underlying virus infection, a capacity enabled by the near-universal nature of dsRNA as a pathogen-associated molecular pattern. That said, further validation on large-scale field-collected and clinical samples will be essential before widespread deployment can be envisioned. While the B2 sandwich assay offers favorable cost-efficiency over antibody-based alternatives, the relatively high cost of Oxford Nanopore direct RNA sequencing remains an important economic constraint. Nevertheless, the growing importance of dsRNA detection across virus sensing, mRNA vaccine development, innate immunity research, and human disease diagnostics, combined with the increasing role of portable long-read sequencing in emerging infectious disease (EIDs) surveillance, positions BIRD-Seq as an innovative and competitive diagnostic platform. Highlights- Double-stranded RNA (dsRNA) is one of the critical pathogen-associated molecular patterns for viral invasion in the host. A protein-based sandwich assay for dsRNA detection in crude biological samples with a sub-ng mL-1 order detection limit was developed, achieving similar sensing efficiency in comparison to expensive and proprietary monoclonal antibody-based ELISA methods. - The quantitative detection of RNA duplex is coupled with an Oxford nanopore direct dsRNA sequencing method for virus species identification and qualitative analysis. - This is one of the very first dsRNA-centered end-to-end workflows for virus monitoring and sequencing, validated for both infected plant and animal samples.

bioengineering↗

Single-cell characterization of skin response to a bite by West Nile virus-infected mosquito reveals fibroblast-mediated barrier to transmission

Cutaneous events at the mosquito bite site that determine orthoflavivirus transmission efficiency remain largely uncharacterized. Here, we report single-cell RNA-sequencing of skin from immunocompetent mice bitten by West Nile virus-infected mosquitoes, capturing early response at a critical transmission bottleneck. Fibroblasts were the dominant cells exposed to infectious saliva. While neutrophils and Folr2+ macrophages diminished, monocyte-derived and antigen-presenting macrophages, and lymphocytes became more abundant. Cell-cell communication analysis revealed the central roles of fibroblasts and myeloid cells in induced immune-related signaling. Transcriptional profiling defined cell type-specific responses to infectious bite integrating immune modulation, skin repair and metabolic remodeling. Using in vivo gene silencing, we demonstrated that fibroblast-expressed LRRC15 (leucine rich repeat-containing 15) functions as a cutaneous restriction factor, limiting viral replication in skin, viral dissemination to draining lymph nodes, and disease severity. Collectively, our analyses provide cellular and molecular understanding of bite-initiated arboviral transmission, establishing skin-resident fibroblasts as frontline defender cells. HIGHLIGHTSO_LISingle-cell profiling captures early cutaneous response to West Nile virus-infected mosquito bites with cell type resolution. C_LIO_LISkin-resident fibroblasts are the dominant frontline cells exposed to infectious mosquito saliva. C_LIO_LIInfectious bite reconfigures cutaneous immune cells, and activates multi-directional signaling between immune and structural skin cell types. C_LIO_LIBite-induced fibroblast-expressed LRRC15 restricts viral transmission and attenuates disease severity. C_LI

zoology↗

Evidence of Human adaptation for cluster 2 TMUV strain despite effective anti-viral responses.

Tembusu virus (TMUV) is an emerging Orthoflavivirus with potential zoonotic importance. To date, the biological differences among TMUV strains remain poorly understood. In this study, we compared the replication of a TMUV strain belonging to the cluster 1 and one belonging to the cluster 2 in human lung epithelial cells and further examined the replication characteristics of TMUV cluster 2 strain in both human and mosquito cell lines. The TMUV cluster 2 strain demonstrated a significant higher replication efficiency than the cluster 1 strain in human cells, indicating stronger adaptation to human-derived cells. Infection of human cells with the cluster 2 strain also induced robust innate immune response, including type I interferon and interferon-stimulated gene expression, associated with activation of the unfolded protein response via the PERK, and IRE1 pathways, reflecting an ER stress engagement. These findings suggest that TMUV cluster 2 strain exhibits enhanced replication capacity and more effectively modulates human host responses at the cellular level, underscoring its potential relevance in human health and the zoonotic risk it represents.

molecular biology↗

Dengue virus harnesses mosquito Syntenin to load and secrete viral RNA into salivary exosomes

Viruses exploit extracellular vesicles (EVs) to transfer infection-enhancing viral RNAs. However, mechanisms underlying viral RNA loading remain elusive. We leveraged our previous discovery that dengue virus secretes transmission-enhancing subgenomic flaviviral RNA (sfRNA) into mosquito salivary EVs to investigate viral RNA loading mechanism. We demonstrate that sfRNA alone promotes the secretion of sfRNA-containing EVs marked by the mosquito EV biogenesis protein AeSyntenin, by applying microscopy and viral genetic editing in in vitro and in vivo models. SfRNA via its stem loop structures interacts intracellularly with mosquito AeSyntenin and this interaction is selectively maintained within EVs as shown by complementary RNA-affinity chromatography and RNA immunoprecipitation, and AI-based prediction. Finally, we used systemic and salivary gland-specific protein depletion to establish a functional role for mosquito AeSyntenin in exosome production and salivary secretion of sfRNA. We propose that sfRNA binds AeSyntenin to drive its selective packaging and release into exosomes, elucidating a mechanism for viral RNA incorporation into EVs. Significance statementViruses hijack extracellular vesicles (EVs) to enhance viral dissemination, but the mechanisms enabling selective viral RNA packaging into EVs remain unclear. Specifically, dengue virus transmission by mosquitoes relies on EV-based delivery of an immune-inhibitory subgenomic flaviviral RNA (sfRNA). Here, we uncover how dengue virus sfRNA is actively sorted into EVs from mosquito saliva. We show that sfRNA alone induces its secretion via EVs. We discover that sfRNA directly interacts with AeSyntenin intracellularly, and that this interaction persists in secreted EVs. Functional depletion studies reveal AeSyntenins role in salivary EV formation and sfRNA secretion. These findings establish a novel paradigm by which viral RNAs exploit vector EV pathways for dissemination.

microbiology↗

Multiple orthoflaviviruses secrete sfRNA in mosquito saliva to promote transmission by inhibiting MDA5-mediated early interferon response

Numerous orthoflaviviruses transmitted through the bites of different mosquito species infect more than 500 million people annually. Skin infection at the bite site represents a critical and conserved step in transmission and a deeper understanding of this process will promote the design of broad-spectrum interventions to address diverse orthoflavivirus health threats. Here, we identify and characterize a transmission-enhancing viral factor in mosquito saliva that is shared across orthoflaviviruses. Saliva from West Nile virus-infected Culex and Zika virus-infected Aedes contains a viral non-coding RNA, subgenomic flaviviral RNA (sfRNA), within lipid vesicles distinct from virions. Higher concentration of sfRNA in infectious saliva positively correlates with infection intensity in human cells and skin explants. Early sfRNA delivery into transmission-relevant skin cell types and human skin explant demonstrate that sfRNA is responsible for the infection enhancement. Co-inoculation of sfRNA in a mouse model of transmission enhanced skin infection and worsened disease severity, supporting the role of salivary sfRNA as a transmission-enhancer. Mechanistically, salivary sfRNA attenuates early interferon response in human skin cells and skin explants by disrupting MDA5 signaling. Our results, derived from two distinct orthoflaviviruses and supported by prior studies, establish salivary sfRNA as a pan-orthoflavivirus transmission-enhancing factor driven by a conserved viral non-coding RNA.

immunology↗

Sphingomyelins in mosquito saliva modify the host lipidome to enhance transmission of flaviviruses by promoting viral protein levels

Mosquito saliva plays a determining role in flavivirus transmission. Here, we discover and elucidate how salivary lipids enhance transmission. Building upon our discovery of salivary extracellular vesicles (EV), we determined that lipids within mosquito EVs, and neither within human EVs nor virions, enhance infection for flaviviruses in primary cell types relevant for transmission. Mechanistically, mosquito EV-lipids specifically promote viral protein levels by reducing ER-associated degradation. Infection enhancement is caused by sphingomyelins within mosquito salivary EVs that elevate sphingomyelin concentration within host cells. Transmission assays showed that mosquito EV-lipids exacerbate disease severity. Our study reveals that EV-associated sphingomyelins within mosquito saliva enhance transmission for multiple flaviviruses by reconfiguring the host lipidome to promote viral protein levels and the resulting skin infection. Our findings open a new dimension centered on lipids in the interplay between hosts, mosquitoes and flaviviruses that determine transmission, unveiling lipids as a new pan-flavivirus target. HighlightsO_LILipids within mosquito extracellular vesicles (EVs) enhance infection in primary skin and immune cells for multiple flaviviruses. C_LIO_LIMosquito EV-lipids increase flaviviral protein levels by dampening ER-associated degradation. C_LIO_LISphingomyelins within salivary EVs are responsible for the infection enhancement by altering host lipidome. C_LIO_LICo-injection of mosquito EV-lipids exacerbate disease severity. C_LI

pathology↗

West Nile virus is transmitted within mosquito populations through infectious mosquito excreta

Understanding transmission routes of arboviruses is key to control their epidemiology and global health burden. Using West Nile virus and Culex mosquitoes, we tested whether arboviruses are transmitted through mosquito excreta. First, we determined the presence of infectious virions in excreta and quantified a high concentration of infectious units per excreta. Second, we showed that virion excretion starts early after oral infection and remains constant for a long period, regardless of mosquito infection level. These results highlight the infectiousness of excreta from infected mosquitoes. Third, we found that both larvae and pupae were susceptible to infection, although pupae were highly permissive. Forth, we established the proof-of-concept that immature mosqui-toes can be infected by infectious excreta, demonstrating a new excreta-mediated mode of transmission. Finally, by mathematically modelling excreta-mediated transmission in the field, we demonstrated its potential impact on arbovirus epidemiology. Our study uncovers a new route of transmission for arboviruses, unveiling mechanisms of viral maintenance in mosquito reservoirs and of vector species shift that contribute to zoonotic emergence.

zoology↗

Characterization of dengue virus 3UTR RNA binding proteins in mosquitoes reveals that AeStaufen reduces subgenomic flaviviral RNA in saliva

Dengue viruses (DENV) are expanding global pathogens that are transmitted through the bite of mosquitoes, mostly Aedes aegypti. As RNA viruses, DENV rely on RNA-binding proteins (RBPs) to complete their life cycle. Alternatively, RBPs can act as restriction factors that prevent DENV multiplication. While the importance of RBPs is well-supported in humans, there is a dearth of information about their influence on DENV transmission by mosquitoes. Such knowledge could be harnessed to design novel, effective interventions against DENV. Here, we successfully adapted RNA-affinity chromatography coupled with mass spectrometry - a technique initially developed in mammalian cells - to identify RBPs in Ae. aegypti cells. We identified fourteen RBPs interacting with DENV serotype 2 3UTR, which is involved in the viral multiplication and produces subgenomic flaviviral RNA (sfRNA). We validated the RNA affinity results for two RBPs by confirming that AePur binds the 3UTR, whereas AeStaufen interacts with both 3UTR and sfRNA. Using in vivo functional evaluation, we determined that RBPs like AeRan, AeExoRNase, and AeRNase have pro-viral functions, whereas AeGTPase, AeAtu, and AePur have anti-viral functions in mosquitoes. Furthermore, we showed that human and mosquito Pur homologs have a shared affinity to DENV2 RNA, although the anti-viral effect is specific to the mosquito protein. Importantly, we revealed that AeStaufen mediates a reduction of gRNA and sfRNA copies in several mosquito tissues, including the salivary glands and that AeStaufen-mediated sfRNA reduction diminishes the concentration of transmission-enhancing sfRNA in saliva, thereby revealing AeStaufens role in DENV transmission. By characterizing the first RBPs that bind to DENV2 3UTR in mosquitoes, our study unravels new pro- and anti-viral targets for the design of novel therapeutic interventions as well as provides foundation for studying the role of RBPs in virus-vector interactions. Author abstractDengue viruses are important human pathogens transmitted by mosquitoes. Currently, there are no effective control measures for dengue. The RNA-binding proteins (RBPs) in mosquitoes, which bind to the dengue virus genome to regulate viral multiplication, could serve as new targets for developing therapeutic interventions. In this study, we pioneered the use of RNA-affinity chromatography - a technique that identifies proteins binding to specific RNA sequences - in mosquito cells. This led to the detection of fourteen RBPs that bind to the 3UTR of dengue virus serotype 2. We validated our results using immunoprecipitation method. Furthermore, we demonstrated that 6 of the 14 RBPs influence viral multiplication in mosquitoes. Among these six RBPs, we showed that the AePur mosquito and human homologs share an affinity to dengue virus RNA, whereas the anti-viral function is specific to the mosquito homolog. Importantly, we revealed that AeStaufen mediates a reduction of genomic and subgenomic flaviviral RNAs in multiple mosquito tissues. We also showed that the reduction of subgenomic flaviviral RNA in salivary glands diminishes the secretion of salivary subgenomic RNA, which facilitates infection at the bite site, thereby unveiling the function of AeStaufen in the virus transmission. By characterizing the first mosquito RBPs that bind to dengue virus genome, our study paves the way for leveraging these proteins as potential targets to block virus transmission.

zoology↗

Y-box binding protein 1 interacts with dengue virus nucleocapsid and mediates viral assembly

Infection with dengue virus (DENV) induces vast rearrangements of the endoplasmic reticulum, which allows the compartmentalization of viral RNA replication and particle assembly. Both processes occur in concert with viral and cellular proteins. Prior studies from our group suggest that the host RNA-binding protein (RBP) Y-box binding protein 1 (YBX1) is required for a late step in the DENV replication cycle. Here we report that YBX1 interacts with the viral nucleocapsid, distributes to DENV assembly sites and is required for efficient assembly of intracellular infectious virions and their secretion. Genetic ablation of YBX1 decreased the spatial proximity between capsid and envelope, increased the susceptibility of envelope to proteinase-K mediated degradation, resulted in the formation of rough empty-looking particles, and decreased the secretion of viral particles. We propose a model wherein YBX1 enables the interaction between the viral nucleocapsid with the structural protein E, which is required for proper assembly of intracellular virus particles and their secretion. ImportanceThe global incidence of dengue virus (DENV) infections has steadily increased over the past decades representing an enormous challenge for public health. During infection, DENV viral RNA interacts with numerous host RNA binding proteins (RBPs) that aid viral replication and thus constitute potential molecular targets to curb infection. We recently reported that Y-box-binding protein 1 (YBX1) interacts with DENV RNA and is required at a late step of the replication cycle. Here we describe the molecular mechanism by which YBX1 mediates DENV infection. We show that YBX1 interacts with the viral nucleocapsid, distributes to DENV assembly sites and is required for efficient assembly of intracellular infectious virions. These results provide important insights into DENV assembly, revealing novel functions of host RBPs during viral infection and opening new avenues for antiviral intervention.

molecular biology↗

The anti-immune dengue subgenomic flaviviral RNA is found in vesicles in mosquito saliva and associated with increased infectivity

Mosquito transmission of dengue viruses to humans starts with infection of skin resident cells at the biting site. There is great interest in identifying transmission-enhancing factors in mosquito saliva in order to counteract them. Here we report the discovery of high levels of subgenomic flaviviral RNA (sfRNA) in dengue virus 2-infected mosquito saliva. We show that salivary sfRNA is protected in detergent-sensitive, protease-resistant compartments. Furthermore, we show that incubation with mosquito saliva containing higher sfRNA levels results in higher virus infectivity in human cells. Since sfRNA potently inhibits innate immunity in human cells, we posit that sfRNA in mosquito saliva is present in extracellular vesicles that deliver it to cells at the biting site to inhibit innate immunity and enhance dengue virus transmission.

physiology↗

JNK pathway restricts DENV, ZIKV and CHIKV infection by activating complement and apoptosis in mosquito salivary glands

Arbovirus infection of Aedes aegypti salivary glands (SGs) determines transmission. However, there is a dearth of knowledge on SG immunity. Here, we characterized SG immune response to dengue, Zika and chikungunya viruses using high-throughput transcriptomics. The three viruses regulate components of Toll, IMD and JNK pathways. However, silencing of Toll and IMD components showed variable effects on SG infection by each virus. In contrast, regulation of JNK pathway produced consistent responses. Virus infection increased with depletion of component Kayak and decreased with depletion of negative regulator Puckered. Virus-induced JNK pathway regulates complement and apoptosis in SGs via TEP20 and Dronc, respectively. Individual and co-silencing of these genes demonstrate their antiviral effects and that both may function together. Co-silencing either TEP20 or Dronc with Puckered annihilates JNK pathway antiviral effect. We identified and characterized the broad antiviral function of JNK pathway in SGs, expanding the immune arsenal that blocks arbovirus transmission.

microbiology↗