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Tick feeding modulates the human skin immune landscape to facilitate tick-borne pathogen transmission
Johanna Strobl, … , Hannes Stockinger, Georg Stary
Johanna Strobl, … , Hannes Stockinger, Georg Stary
Published September 27, 2022
Citation Information: J Clin Invest. 2022;132(21):e161188. https://doi.org/10.1172/JCI161188.
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Research Article Immunology Article has an altmetric score of 268

Tick feeding modulates the human skin immune landscape to facilitate tick-borne pathogen transmission

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Abstract

During cutaneous tick attachment, the feeding cavity becomes a site of transmission for tick salivary compounds and tick-borne pathogens. However, the immunological consequences of tick feeding for human skin remain unclear. Here, we assessed human skin and blood samples upon tick bite and developed a human skin explant model mimicking Ixodes ricinus bites and tick-borne pathogen infection. Following tick attachment, we observed rapidly occurring patterns of immunomodulation, including increases in neutrophils and cutaneous B and T cells. T cells upregulated tissue residency markers, while lymphocytic cytokine production was impaired. In early stages of Borrelia burgdorferi model infections, we detected strain-specific immune responses and close spatial relationships between macrophages and spirochetes. Preincubation of spirochetes with tick salivary gland extracts hampered accumulation of immune cells and increased spirochete loads. Collectively, we showed that tick feeding exerts profound changes on the skin immune network that interfere with the primary response against tick-borne pathogens.

Authors

Johanna Strobl, Verena Mündler, Sophie Müller, Anna Gindl, Sara Berent, Anna-Margarita Schötta, Lisa Kleissl, Clement Staud, Anna Redl, Luisa Unterluggauer, Ana E. Aguilar González, Sophie T. Weninger, Denise Atzmüller, Romana Klasinc, Gerold Stanek, Mateusz Markowicz, Hannes Stockinger, Georg Stary

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Figure 5

Early steps of tick-borne pathogen transmission are mimicked in an ex vivo human skin tick bite model.

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Early steps of tick-borne pathogen transmission are mimicked in an ex vi...
(A) Illustration of the ex vivo TB model in human skin. (B) Representative images of CD3-, CD69-, and CD103-immunolabeled and DAPI-counterstained skin injected with either SGE or PBS control. Scale bar: 20 μm. (C) CD69+ and CD69+CD103+ tissue-resident T cells per mm2 as determined by immunolabeling in skin injected with SGE (n = 8) or PBS (n = 7). (D) Illustration of the ex vivo Bb (Borrelia burgdorferi B31 strain) infection model. (E) Representative image of Bbsl-specific anti-flagellin and DAPI counterstaining in skin 24 hours after injection of Bb or culture media control. Scale bar: 50 μm. (F) Number of Bbsl-specific flagellin+ spirochetes per mm2 in skin cryosections before and after injection of Bb (n = 7) spirochetes or Borrelia afzelii, PKO strain (Ba, n = 7). Number of injected spirochetes: 1 × 105/sample. Data shown as mean spirochete number/mm² at 0, 0.5, 3, 24, and 48 hours after injection. (G) Infection load (spirochetes per mm2) after Bb versus Ba injection. In C, F, and G, data are presented as mean ± SEM. Each dot represents the mean of 2 technical replicates. Statistical analysis was performed by unpaired Student’s t test (C and G) or 1-way ANOVA (F). *P < 0.05; **P < 0.01; ***P < 0.001.

Copyright © 2025 American Society for Clinical Investigation
ISSN: 0021-9738 (print), 1558-8238 (online)

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