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Calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory T cell biased agonist

Interleukin-2 is a pleiotropic cytokine that mediates both pro- and anti-inflammatory functions. Immune cells naturally differ in their sensitivity to IL-2 due to cell type and activation state-dependent expression of receptors and signaling pathway components. To probe differences in IL-2 signaling...

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Autores principales: Glassman, Caleb R, Su, Leon, Majri-Morrison, Sonia S, Winkelmann, Hauke, Mo, Fei, Li, Peng, Pérez-Cruz, Magdiel, Ho, Peggy P, Koliesnik, Ievgen, Nagy, Nadine, Hnizdilova, Tereza, Picton, Lora K, Kovar, Marek, Bollyky, Paul, Steinman, Lawrence, Meyer, Everett, Piehler, Jacob, Leonard, Warren J, Garcia, K Christopher
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8131104/
https://www.ncbi.nlm.nih.gov/pubmed/34003116
http://dx.doi.org/10.7554/eLife.65777
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author Glassman, Caleb R
Su, Leon
Majri-Morrison, Sonia S
Winkelmann, Hauke
Mo, Fei
Li, Peng
Pérez-Cruz, Magdiel
Ho, Peggy P
Koliesnik, Ievgen
Nagy, Nadine
Hnizdilova, Tereza
Picton, Lora K
Kovar, Marek
Bollyky, Paul
Steinman, Lawrence
Meyer, Everett
Piehler, Jacob
Leonard, Warren J
Garcia, K Christopher
author_facet Glassman, Caleb R
Su, Leon
Majri-Morrison, Sonia S
Winkelmann, Hauke
Mo, Fei
Li, Peng
Pérez-Cruz, Magdiel
Ho, Peggy P
Koliesnik, Ievgen
Nagy, Nadine
Hnizdilova, Tereza
Picton, Lora K
Kovar, Marek
Bollyky, Paul
Steinman, Lawrence
Meyer, Everett
Piehler, Jacob
Leonard, Warren J
Garcia, K Christopher
author_sort Glassman, Caleb R
collection PubMed
description Interleukin-2 is a pleiotropic cytokine that mediates both pro- and anti-inflammatory functions. Immune cells naturally differ in their sensitivity to IL-2 due to cell type and activation state-dependent expression of receptors and signaling pathway components. To probe differences in IL-2 signaling across cell types, we used structure-based design to create and profile a series of IL-2 variants with the capacity to titrate maximum signal strength in fine increments. One of these partial agonists, IL-2-REH, specifically expanded Foxp3+ regulatory T cells with reduced activity on CD8+ T cells due to cell type-intrinsic differences in IL-2 signaling. IL-2-REH elicited cell type-dependent differences in gene expression and provided mixed therapeutic results: showing benefit in the in vivo mouse dextran sulfate sodium (DSS) model of colitis, but no therapeutic efficacy in a transfer colitis model. Our findings show that cytokine partial agonists can be used to calibrate intrinsic differences in response thresholds across responding cell types to narrow pleiotropic actions, which may be generalizable to other cytokine and growth factor systems.
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spelling pubmed-81311042021-05-19 Calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory T cell biased agonist Glassman, Caleb R Su, Leon Majri-Morrison, Sonia S Winkelmann, Hauke Mo, Fei Li, Peng Pérez-Cruz, Magdiel Ho, Peggy P Koliesnik, Ievgen Nagy, Nadine Hnizdilova, Tereza Picton, Lora K Kovar, Marek Bollyky, Paul Steinman, Lawrence Meyer, Everett Piehler, Jacob Leonard, Warren J Garcia, K Christopher eLife Biochemistry and Chemical Biology Interleukin-2 is a pleiotropic cytokine that mediates both pro- and anti-inflammatory functions. Immune cells naturally differ in their sensitivity to IL-2 due to cell type and activation state-dependent expression of receptors and signaling pathway components. To probe differences in IL-2 signaling across cell types, we used structure-based design to create and profile a series of IL-2 variants with the capacity to titrate maximum signal strength in fine increments. One of these partial agonists, IL-2-REH, specifically expanded Foxp3+ regulatory T cells with reduced activity on CD8+ T cells due to cell type-intrinsic differences in IL-2 signaling. IL-2-REH elicited cell type-dependent differences in gene expression and provided mixed therapeutic results: showing benefit in the in vivo mouse dextran sulfate sodium (DSS) model of colitis, but no therapeutic efficacy in a transfer colitis model. Our findings show that cytokine partial agonists can be used to calibrate intrinsic differences in response thresholds across responding cell types to narrow pleiotropic actions, which may be generalizable to other cytokine and growth factor systems. eLife Sciences Publications, Ltd 2021-05-18 /pmc/articles/PMC8131104/ /pubmed/34003116 http://dx.doi.org/10.7554/eLife.65777 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication (https://creativecommons.org/publicdomain/zero/1.0/) .
spellingShingle Biochemistry and Chemical Biology
Glassman, Caleb R
Su, Leon
Majri-Morrison, Sonia S
Winkelmann, Hauke
Mo, Fei
Li, Peng
Pérez-Cruz, Magdiel
Ho, Peggy P
Koliesnik, Ievgen
Nagy, Nadine
Hnizdilova, Tereza
Picton, Lora K
Kovar, Marek
Bollyky, Paul
Steinman, Lawrence
Meyer, Everett
Piehler, Jacob
Leonard, Warren J
Garcia, K Christopher
Calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory T cell biased agonist
title Calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory T cell biased agonist
title_full Calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory T cell biased agonist
title_fullStr Calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory T cell biased agonist
title_full_unstemmed Calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory T cell biased agonist
title_short Calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory T cell biased agonist
title_sort calibration of cell-intrinsic interleukin-2 response thresholds guides design of a regulatory t cell biased agonist
topic Biochemistry and Chemical Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8131104/
https://www.ncbi.nlm.nih.gov/pubmed/34003116
http://dx.doi.org/10.7554/eLife.65777
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