Single cell immune profiling in ankylosing spondylitis reveals resistance of CD8+ T cells to immune exhaustion

Summary: Persistent chronic inflammation is a hallmark of ankylosing spondylitis (AS), with cytotoxic T cells (CTLs) increasingly implicated in its pathogenesis. Ordinarily, T cell exhaustion follows sustained, persistent T cell activation to limit collateral tissue damage. Using mass cytometry and...

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Main Authors: Michael Tang, Zoya Qaiyum, Melissa Lim, Robert D. Inman
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225009769
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author Michael Tang
Zoya Qaiyum
Melissa Lim
Robert D. Inman
author_facet Michael Tang
Zoya Qaiyum
Melissa Lim
Robert D. Inman
author_sort Michael Tang
collection DOAJ
description Summary: Persistent chronic inflammation is a hallmark of ankylosing spondylitis (AS), with cytotoxic T cells (CTLs) increasingly implicated in its pathogenesis. Ordinarily, T cell exhaustion follows sustained, persistent T cell activation to limit collateral tissue damage. Using mass cytometry and single-cell RNA sequencing (scRNA-seq), we identified a clonally expanded CTL subset in AS synovial fluid that expresses inhibitory receptors (PD-1, TIGIT, LAG-3) yet retains its effector capacity to express granzymes, perforin, TNF-α, and IFN-γ. Gene expression profile of this CTL subset shows the downregulation of canonical exhaustion markers. At the protein level, TOX, a critical transcription factor regulating CTL exhaustion, is downregulated in PD-1+TIGIT+LAG-3+CTLs. In-silico trajectory analyses suggest that these cells may differentiate into other effector CTL subsets. Our findings reveal a checkpoint-expressing CTL population in AS that resists exhaustion and retains an activated, effector phenotype. We propose that failure to undergo exhaustion may be a fundamental mechanism sustaining AS chronic inflammation.
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spelling doaj-art-a8bf741fc8f94164a26ee84fa05a3e972025-08-20T02:42:37ZengElsevieriScience2589-00422025-07-0128711271510.1016/j.isci.2025.112715Single cell immune profiling in ankylosing spondylitis reveals resistance of CD8+ T cells to immune exhaustionMichael Tang0Zoya Qaiyum1Melissa Lim2Robert D. Inman3Spondylitis Program, Schroeder Arthritis Institute, University Health Network, Toronto, ON M5T0S8, CanadaSpondylitis Program, Schroeder Arthritis Institute, University Health Network, Toronto, ON M5T0S8, CanadaSpondylitis Program, Schroeder Arthritis Institute, University Health Network, Toronto, ON M5T0S8, CanadaSpondylitis Program, Schroeder Arthritis Institute, University Health Network, Toronto, ON M5T0S8, Canada; Department of Immunology, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S1A8Canada; Division of Rheumatology, Department of Medicine, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S3H2, Canada; Corresponding authorSummary: Persistent chronic inflammation is a hallmark of ankylosing spondylitis (AS), with cytotoxic T cells (CTLs) increasingly implicated in its pathogenesis. Ordinarily, T cell exhaustion follows sustained, persistent T cell activation to limit collateral tissue damage. Using mass cytometry and single-cell RNA sequencing (scRNA-seq), we identified a clonally expanded CTL subset in AS synovial fluid that expresses inhibitory receptors (PD-1, TIGIT, LAG-3) yet retains its effector capacity to express granzymes, perforin, TNF-α, and IFN-γ. Gene expression profile of this CTL subset shows the downregulation of canonical exhaustion markers. At the protein level, TOX, a critical transcription factor regulating CTL exhaustion, is downregulated in PD-1+TIGIT+LAG-3+CTLs. In-silico trajectory analyses suggest that these cells may differentiate into other effector CTL subsets. Our findings reveal a checkpoint-expressing CTL population in AS that resists exhaustion and retains an activated, effector phenotype. We propose that failure to undergo exhaustion may be a fundamental mechanism sustaining AS chronic inflammation.http://www.sciencedirect.com/science/article/pii/S2589004225009769ImmunologyImmune responseTranscriptomics
spellingShingle Michael Tang
Zoya Qaiyum
Melissa Lim
Robert D. Inman
Single cell immune profiling in ankylosing spondylitis reveals resistance of CD8+ T cells to immune exhaustion
iScience
Immunology
Immune response
Transcriptomics
title Single cell immune profiling in ankylosing spondylitis reveals resistance of CD8+ T cells to immune exhaustion
title_full Single cell immune profiling in ankylosing spondylitis reveals resistance of CD8+ T cells to immune exhaustion
title_fullStr Single cell immune profiling in ankylosing spondylitis reveals resistance of CD8+ T cells to immune exhaustion
title_full_unstemmed Single cell immune profiling in ankylosing spondylitis reveals resistance of CD8+ T cells to immune exhaustion
title_short Single cell immune profiling in ankylosing spondylitis reveals resistance of CD8+ T cells to immune exhaustion
title_sort single cell immune profiling in ankylosing spondylitis reveals resistance of cd8 t cells to immune exhaustion
topic Immunology
Immune response
Transcriptomics
url http://www.sciencedirect.com/science/article/pii/S2589004225009769
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