Paine Dakota N, Hermance Meghan, Thangamani Saravanan
Department of Microbiology and Immunology, State University of New York Upstate Medical University, Syracuse, NY, United States.
State University of New York Center for Vector-Borne Diseases, State University of New York Upstate Medical University, Syracuse, NY, United States.
Front Immunol. 2025 Jan 13;15:1511132. doi: 10.3389/fimmu.2024.1511132. eCollection 2024.
Powassan virus (POWV), a vector-borne pathogen transmitted by 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.
We 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.
Our 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.
These 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.
波瓦桑病毒（POWV）是一种由北美蜱传播的媒介传播病原体，是波瓦桑脑炎的病原体。作为专性吸血生物，蜱在蜱叮咬部位传播病原体，如POWV，特别是在进食初期。蜱的进食和唾液因子调节宿主的免疫反应，促进吸血和病原体传播。然而，POWV传播过程中的免疫调节机制仍未得到充分了解。在本研究中，我们调查了POWV传播过程中与蜱叮咬相关的全球皮肤转录组变化。
我们在感染和未感染POWV的蜱进食后1、3和6小时收集蜱附着部位的皮肤活检样本，然后对这些样本进行RNA测序。使用基因本体论和通路富集分析对差异表达基因进行通路富集分析。
我们的研究结果表明，仅蜱进食就在蜱附着后的前1至3小时内显著影响皮肤转录组。尽管早期POWV传播在局部环境中引起的变化最小，但在蜱附着6小时后观察到明显向促炎状态转变，其特征是中性粒细胞募集和白细胞介素信号传导。
这些转录组数据阐明了蜱叮咬部位的动态变化，从有助于获取血餐的变化转变为可能促进病毒传播的促炎阶段。
