PIM kinase control of CD8 T cell protein synthesis and cell trafficking

Integration of kinase signalling networks co-ordinates the transcriptional, translational, and metabolic changes required for T cell activation and differentiation. This study explores the role of the Serine/Threonine kinases PIM1 and PIM2 in controlling mouse CD8 T lymphocyte antigen receptor-media...

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Main Authors: Julia M Marchingo, Laura Spinelli, Shalini Pathak, Doreen A Cantrell
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-05-01
Series:eLife
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Online Access:https://elifesciences.org/articles/98622
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author Julia M Marchingo
Laura Spinelli
Shalini Pathak
Doreen A Cantrell
author_facet Julia M Marchingo
Laura Spinelli
Shalini Pathak
Doreen A Cantrell
author_sort Julia M Marchingo
collection DOAJ
description Integration of kinase signalling networks co-ordinates the transcriptional, translational, and metabolic changes required for T cell activation and differentiation. This study explores the role of the Serine/Threonine kinases PIM1 and PIM2 in controlling mouse CD8 T lymphocyte antigen receptor-mediated activation and differentiation in response to the cytokines Interleukin-2 (IL-2) or IL-15. We show that the PIM kinases are dispensable for antigen-receptor and IL-15 controlled differentiation programs, but that they play a selective role in IL-2 regulated CD8 T cell fate. One key insight was that PIM kinases controlled the migratory capabilities of effector CD8 T cells, with Pim1/Pim2-deficient CD8 T cells unable to fully switch off the naive T cell chemokine and adhesion receptor program during effector differentiation. PIM kinases were also needed for IL-2 to sustain high expression of the glucose transporters SLC2A1 and SLC2A3 and to maintain activity of the nutrient-sensing kinase mTORc1. Strikingly, PIM kinases did not have a dominant impact on IL-2-driven transcriptional programs but rather selectively modulated protein synthesis to shape cytotoxic T cell proteomes. This study reveals a selective role of PIM kinases in IL-2 control of CD8 T cells and highlights how regulated changes in protein synthesis can impact T cell phenotypes.
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spelling doaj-art-5312bc3dc9be456f91063ca26347a3a92025-08-20T03:52:57ZengeLife Sciences Publications LtdeLife2050-084X2025-05-011310.7554/eLife.98622PIM kinase control of CD8 T cell protein synthesis and cell traffickingJulia M Marchingo0https://orcid.org/0000-0001-8823-9718Laura Spinelli1https://orcid.org/0000-0002-5801-6297Shalini Pathak2Doreen A Cantrell3https://orcid.org/0000-0001-7525-3350Cell Signalling and Immunology Division, School of Life Sciences, University of Dundee, Dundee, United KingdomCell Signalling and Immunology Division, School of Life Sciences, University of Dundee, Dundee, United Kingdom; Molecular Cell and Developmental Biology Division, School of Life Sciences, University of Dundee, Dundee, United KingdomCell Signalling and Immunology Division, School of Life Sciences, University of Dundee, Dundee, United KingdomCell Signalling and Immunology Division, School of Life Sciences, University of Dundee, Dundee, United KingdomIntegration of kinase signalling networks co-ordinates the transcriptional, translational, and metabolic changes required for T cell activation and differentiation. This study explores the role of the Serine/Threonine kinases PIM1 and PIM2 in controlling mouse CD8 T lymphocyte antigen receptor-mediated activation and differentiation in response to the cytokines Interleukin-2 (IL-2) or IL-15. We show that the PIM kinases are dispensable for antigen-receptor and IL-15 controlled differentiation programs, but that they play a selective role in IL-2 regulated CD8 T cell fate. One key insight was that PIM kinases controlled the migratory capabilities of effector CD8 T cells, with Pim1/Pim2-deficient CD8 T cells unable to fully switch off the naive T cell chemokine and adhesion receptor program during effector differentiation. PIM kinases were also needed for IL-2 to sustain high expression of the glucose transporters SLC2A1 and SLC2A3 and to maintain activity of the nutrient-sensing kinase mTORc1. Strikingly, PIM kinases did not have a dominant impact on IL-2-driven transcriptional programs but rather selectively modulated protein synthesis to shape cytotoxic T cell proteomes. This study reveals a selective role of PIM kinases in IL-2 control of CD8 T cells and highlights how regulated changes in protein synthesis can impact T cell phenotypes.https://elifesciences.org/articles/98622T cellPIM kinaseproteomicsprotein translationIL-2IL-15
spellingShingle Julia M Marchingo
Laura Spinelli
Shalini Pathak
Doreen A Cantrell
PIM kinase control of CD8 T cell protein synthesis and cell trafficking
eLife
T cell
PIM kinase
proteomics
protein translation
IL-2
IL-15
title PIM kinase control of CD8 T cell protein synthesis and cell trafficking
title_full PIM kinase control of CD8 T cell protein synthesis and cell trafficking
title_fullStr PIM kinase control of CD8 T cell protein synthesis and cell trafficking
title_full_unstemmed PIM kinase control of CD8 T cell protein synthesis and cell trafficking
title_short PIM kinase control of CD8 T cell protein synthesis and cell trafficking
title_sort pim kinase control of cd8 t cell protein synthesis and cell trafficking
topic T cell
PIM kinase
proteomics
protein translation
IL-2
IL-15
url https://elifesciences.org/articles/98622
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AT lauraspinelli pimkinasecontrolofcd8tcellproteinsynthesisandcelltrafficking
AT shalinipathak pimkinasecontrolofcd8tcellproteinsynthesisandcelltrafficking
AT doreenacantrell pimkinasecontrolofcd8tcellproteinsynthesisandcelltrafficking