Early transcriptomic changes at the skin interface during Powassan virus transmission by Ixodes scapularis ticks
IntroductionPowassan virus (POWV), a vector-borne pathogen transmitted by Ixodes ticks in North America, is the causative agent of Powassan encephalitis. As obligate hematophagous organisms, ticks transmit pathogens like POWV at the tick bite site, specifically during the initial stages of feeding....
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Frontiers Media S.A.
2025-01-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1511132/full |
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| author | Dakota N. Paine Dakota N. Paine Meghan Hermance Saravanan Thangamani Saravanan Thangamani Saravanan Thangamani |
| author_facet | Dakota N. Paine Dakota N. Paine Meghan Hermance Saravanan Thangamani Saravanan Thangamani Saravanan Thangamani |
| author_sort | Dakota N. Paine |
| collection | DOAJ |
| description | IntroductionPowassan virus (POWV), a vector-borne pathogen transmitted by Ixodes ticks in North America, is the causative agent of Powassan encephalitis. As obligate hematophagous organisms, ticks transmit pathogens like POWV at the tick bite site, specifically during the initial stages of feeding. Tick feeding and salivary factors modulate the host’s immunological responses, facilitating blood feeding and pathogen transmission. However, the mechanisms of immunomodulation during POWV transmission remain inadequately understood. In this study, we investigated the global cutaneous transcriptomic changes associated with tick bites during POWV transmission.MethodsWe collected skin biopsies from the tick attachment sites at 1, 3, and 6 h after feeding by POWV-infected and uninfected ticks, followed by RNA sequencing of these samples. Differentially expressed genes were analyzed for pathway enrichment using gene ontology and pathway enrichment analyses.ResultsOur findings reveal that tick feeding alone significantly impacts the skin transcriptome within the first 1 to 3 h of tick attachment. Although early POWV transmission induces minimal changes in the local environment, a pronounced shift toward a proinflammatory state is observed 6 h after tick attachment, characterized by neutrophil recruitment and interleukin signaling.DiscussionThese transcriptomic data elucidate the dynamic changes at the tick bite site, transitioning from changes that assist blood meal acquisition to a proinflammatory phase that may facilitate viral dissemination. |
| format | Article |
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| institution | Kabale University |
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| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
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| spelling | doaj-art-50e1884222a04c23a661e505172ecb562025-01-13T05:10:16ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-01-011510.3389/fimmu.2024.15111321511132Early transcriptomic changes at the skin interface during Powassan virus transmission by Ixodes scapularis ticksDakota N. Paine0Dakota N. Paine1Meghan Hermance2Saravanan Thangamani3Saravanan Thangamani4Saravanan Thangamani5Department of Microbiology and Immunology, State University of New York Upstate Medical University, Syracuse, NY, United StatesState University of New York Center for Vector-Borne Diseases, State University of New York Upstate Medical University, Syracuse, NY, United StatesDepartment of Microbiology and Immunology, University of South Alabama, Mobile, AL, United StatesDepartment of Microbiology and Immunology, State University of New York Upstate Medical University, Syracuse, NY, United StatesState University of New York Center for Vector-Borne Diseases, State University of New York Upstate Medical University, Syracuse, NY, United StatesUpstate Global Health Institute, State University of New York Upstate Medical University, Syracuse, NY, United StatesIntroductionPowassan virus (POWV), a vector-borne pathogen transmitted by Ixodes ticks in North America, is the causative agent of Powassan encephalitis. As obligate hematophagous organisms, ticks transmit pathogens like POWV at the tick bite site, specifically during the initial stages of feeding. Tick feeding and salivary factors modulate the host’s immunological responses, facilitating blood feeding and pathogen transmission. However, the mechanisms of immunomodulation during POWV transmission remain inadequately understood. In this study, we investigated the global cutaneous transcriptomic changes associated with tick bites during POWV transmission.MethodsWe collected skin biopsies from the tick attachment sites at 1, 3, and 6 h after feeding by POWV-infected and uninfected ticks, followed by RNA sequencing of these samples. Differentially expressed genes were analyzed for pathway enrichment using gene ontology and pathway enrichment analyses.ResultsOur findings reveal that tick feeding alone significantly impacts the skin transcriptome within the first 1 to 3 h of tick attachment. Although early POWV transmission induces minimal changes in the local environment, a pronounced shift toward a proinflammatory state is observed 6 h after tick attachment, characterized by neutrophil recruitment and interleukin signaling.DiscussionThese transcriptomic data elucidate the dynamic changes at the tick bite site, transitioning from changes that assist blood meal acquisition to a proinflammatory phase that may facilitate viral dissemination.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1511132/fullPowassan virusIxodesimmunomodulationtransmissionarbovirus |
| spellingShingle | Dakota N. Paine Dakota N. Paine Meghan Hermance Saravanan Thangamani Saravanan Thangamani Saravanan Thangamani Early transcriptomic changes at the skin interface during Powassan virus transmission by Ixodes scapularis ticks Frontiers in Immunology Powassan virus Ixodes immunomodulation transmission arbovirus |
| title | Early transcriptomic changes at the skin interface during Powassan virus transmission by Ixodes scapularis ticks |
| title_full | Early transcriptomic changes at the skin interface during Powassan virus transmission by Ixodes scapularis ticks |
| title_fullStr | Early transcriptomic changes at the skin interface during Powassan virus transmission by Ixodes scapularis ticks |
| title_full_unstemmed | Early transcriptomic changes at the skin interface during Powassan virus transmission by Ixodes scapularis ticks |
| title_short | Early transcriptomic changes at the skin interface during Powassan virus transmission by Ixodes scapularis ticks |
| title_sort | early transcriptomic changes at the skin interface during powassan virus transmission by ixodes scapularis ticks |
| topic | Powassan virus Ixodes immunomodulation transmission arbovirus |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1511132/full |
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