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Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin

Perforin-2 (P-2) is an antimicrobial protein with unique properties to kill intracellular bacteria. Gamma delta (GD) T cells, as the major T cell population in epithelial tissues, play a central role in protective and pathogenic immune responses in the skin. However, the tissue-specific mechanisms t...

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Autores principales: Pastar, Irena, O’Neill, Katelyn, Padula, Laura, Head, Cheyanne R., Burgess, Jamie L., Chen, Vivien, Garcia, Denisse, Stojadinovic, Olivera, Hower, Suzanne, Plano, Gregory V., Thaller, Seth R., Tomic-Canic, Marjana, Strbo, Natasa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7525037/
https://www.ncbi.nlm.nih.gov/pubmed/33042139
http://dx.doi.org/10.3389/fimmu.2020.550946
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author Pastar, Irena
O’Neill, Katelyn
Padula, Laura
Head, Cheyanne R.
Burgess, Jamie L.
Chen, Vivien
Garcia, Denisse
Stojadinovic, Olivera
Hower, Suzanne
Plano, Gregory V.
Thaller, Seth R.
Tomic-Canic, Marjana
Strbo, Natasa
author_facet Pastar, Irena
O’Neill, Katelyn
Padula, Laura
Head, Cheyanne R.
Burgess, Jamie L.
Chen, Vivien
Garcia, Denisse
Stojadinovic, Olivera
Hower, Suzanne
Plano, Gregory V.
Thaller, Seth R.
Tomic-Canic, Marjana
Strbo, Natasa
author_sort Pastar, Irena
collection PubMed
description Perforin-2 (P-2) is an antimicrobial protein with unique properties to kill intracellular bacteria. Gamma delta (GD) T cells, as the major T cell population in epithelial tissues, play a central role in protective and pathogenic immune responses in the skin. However, the tissue-specific mechanisms that control the innate immune response and the effector functions of GD T cells, especially the cross-talk with commensal organisms, are not very well understood. We hypothesized that the most prevalent skin commensal microorganism, Staphylococcus epidermidis, may play a role in regulating GD T cell-mediated cutaneous responses. We analyzed antimicrobial protein P-2 expression in human skin at a single cell resolution using an amplified fluorescence in situ hybridization approach to detect P-2 mRNA in combination with immunophenotyping. We show that S. epidermidis activates GD T cells and upregulates P-2 in human skin ex vivo in a cell-specific manner. Furthermore, P-2 upregulation following S. epidermidis stimulation correlates with increased ability of skin cells to kill intracellular Staphylococcus aureus. Our findings are the first to reveal that skin commensal bacteria induce P-2 expression, which may be utilized beneficially to modulate host innate immune responses and protect from skin infections.
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spelling pubmed-75250372020-10-09 Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin Pastar, Irena O’Neill, Katelyn Padula, Laura Head, Cheyanne R. Burgess, Jamie L. Chen, Vivien Garcia, Denisse Stojadinovic, Olivera Hower, Suzanne Plano, Gregory V. Thaller, Seth R. Tomic-Canic, Marjana Strbo, Natasa Front Immunol Immunology Perforin-2 (P-2) is an antimicrobial protein with unique properties to kill intracellular bacteria. Gamma delta (GD) T cells, as the major T cell population in epithelial tissues, play a central role in protective and pathogenic immune responses in the skin. However, the tissue-specific mechanisms that control the innate immune response and the effector functions of GD T cells, especially the cross-talk with commensal organisms, are not very well understood. We hypothesized that the most prevalent skin commensal microorganism, Staphylococcus epidermidis, may play a role in regulating GD T cell-mediated cutaneous responses. We analyzed antimicrobial protein P-2 expression in human skin at a single cell resolution using an amplified fluorescence in situ hybridization approach to detect P-2 mRNA in combination with immunophenotyping. We show that S. epidermidis activates GD T cells and upregulates P-2 in human skin ex vivo in a cell-specific manner. Furthermore, P-2 upregulation following S. epidermidis stimulation correlates with increased ability of skin cells to kill intracellular Staphylococcus aureus. Our findings are the first to reveal that skin commensal bacteria induce P-2 expression, which may be utilized beneficially to modulate host innate immune responses and protect from skin infections. Frontiers Media S.A. 2020-09-16 /pmc/articles/PMC7525037/ /pubmed/33042139 http://dx.doi.org/10.3389/fimmu.2020.550946 Text en Copyright © 2020 Pastar, O’Neill, Padula, Head, Burgess, Chen, Garcia, Stojadinovic, Hower, Plano, Thaller, Tomic-Canic and Strbo. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Pastar, Irena
O’Neill, Katelyn
Padula, Laura
Head, Cheyanne R.
Burgess, Jamie L.
Chen, Vivien
Garcia, Denisse
Stojadinovic, Olivera
Hower, Suzanne
Plano, Gregory V.
Thaller, Seth R.
Tomic-Canic, Marjana
Strbo, Natasa
Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin
title Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin
title_full Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin
title_fullStr Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin
title_full_unstemmed Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin
title_short Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin
title_sort staphylococcus epidermidis boosts innate immune response by activation of gamma delta t cells and induction of perforin-2 in human skin
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7525037/
https://www.ncbi.nlm.nih.gov/pubmed/33042139
http://dx.doi.org/10.3389/fimmu.2020.550946
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