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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 6

Early Bb model infection is accompanied by a strain-dependent influx of neutrophils and dDCs.

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Early Bb model infection is accompanied by a strain-dependent influx of ...
(A and B) Percentage of neutrophils (CD11b+CD15+, n = 3), macrophages (CD15–CD11b+CD68+), dDCs (CD15–CD11b–CD11c+), and LCs (CD207+) in explanted abdominal skin after injection of Bbsl culture media (ctrl, n = 2) or Bbsl culture media containing Bb (A, n = 3) or Ba spirochetes (B, n = 3). Data shown as mean cell number/mm² 0.5, 3, 24, and 48 hours after injection and ctrl. Each dot represents the mean of 2 technical replicates. (C) Graphical representation of software-based analysis of cell-cell contact after immunostaining. Spirochetes (red/yellow dots) were analyzed for presence within green ring within 3 μm, indicating direct cell contact. (D and E) Percentages of neutrophils, macrophages, and dDCs colocalizing with spirochetes in skin explants injected with Bb (D, n = 3) or Ba (E, n = 3). Each dot represents the mean of 2 technical replicates. (F) Percentage of dDCs colocalizing with spirochetes after injection of Bb versus Ba. In A–F, data are presented as mean ± SEM. Statistical analysis was performed by 1-way ANOVA (A–E) or unpaired Student’s t test (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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