Integrated single-cell transcriptome and T cell receptor profiling reveals defects of T cell exhaustion in pulmonary tuberculosis
Tuberculosis-affected lungs with chronic inflammation harbor abundant immunosuppressive immune cells but the nature of such inflammation is unclear. Dysfunction in T cell exhaustion, while implicated in chronic inflammatory diseases, remains unexplored in tuberculosis. Given that immunotherapy targe...
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Published in | The Journal of infection Vol. 88; no. 6; p. 106158 |
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Main Authors | , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Ltd
01.06.2024
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Abstract | Tuberculosis-affected lungs with chronic inflammation harbor abundant immunosuppressive immune cells but the nature of such inflammation is unclear. Dysfunction in T cell exhaustion, while implicated in chronic inflammatory diseases, remains unexplored in tuberculosis. Given that immunotherapy targeting exhaustion checkpoints exacerbates tuberculosis, we speculate that T cell exhaustion is dysfunctional in tuberculosis. Using integrated single-cell RNA sequencing and T cell receptor profiling we reported defects in exhaustion responses within inflamed tuberculosis-affected lungs. Tuberculosis lungs demonstrated significantly reduced levels of exhausted CD8+ T cells and exhibited diminished expression of exhaustion-related transcripts among clonally expanded CD4+ and CD8+ T cells. Additionally, clonal expansion of CD4+ and CD8+ T cells bearing T cell receptors specific for CMV was observed. Expanded CD8+ T cells expressed the cytolytic marker GZMK. Hence, inflamed tuberculosis-affected lungs displayed dysfunction in T cell exhaustion. Our findings likely hold implications for understanding the reactivation of tuberculosis observed in patients undergoing immunotherapy targeting the exhaustion checkpoint.
•Single-cell analysis revealed defective T cell exhaustion in TB lungs.•Clonal expansion of T cells in TB linked to diminished exhaustion responses.•CMV-reactive clonally expanded T cells were enriched in TB lungs.•Upregulated GZMK, IFNγ in precursor of exhausted CD8+ T cells in TB lungs.•Dysfunctional T cell exhaustion may contribute to TB immunopathology. |
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AbstractList | Tuberculosis-affected lungs with chronic inflammation harbor abundant immunosuppressive immune cells but the nature of such inflammation is unclear. Dysfunction in T cell exhaustion, while implicated in chronic inflammatory diseases, remains unexplored in tuberculosis. Given that immunotherapy targeting exhaustion checkpoints exacerbates tuberculosis, we speculate that T cell exhaustion is dysfunctional in tuberculosis. Using integrated single-cell RNA sequencing and T cell receptor profiling we reported defects in exhaustion responses within inflamed tuberculosis-affected lungs. Tuberculosis lungs demonstrated significantly reduced levels of exhausted CD8+ T cells and exhibited diminished expression of exhaustion-related transcripts among clonally expanded CD4+ and CD8+ T cells. Additionally, clonal expansion of CD4+ and CD8+ T cells bearing T cell receptors specific for CMV was observed. Expanded CD8+ T cells expressed the cytolytic marker GZMK. Hence, inflamed tuberculosis-affected lungs displayed dysfunction in T cell exhaustion. Our findings likely hold implications for understanding the reactivation of tuberculosis observed in patients undergoing immunotherapy targeting the exhaustion checkpoint.
•Single-cell analysis revealed defective T cell exhaustion in TB lungs.•Clonal expansion of T cells in TB linked to diminished exhaustion responses.•CMV-reactive clonally expanded T cells were enriched in TB lungs.•Upregulated GZMK, IFNγ in precursor of exhausted CD8+ T cells in TB lungs.•Dysfunctional T cell exhaustion may contribute to TB immunopathology. Tuberculosis-affected lungs with chronic inflammation harbor abundant immunosuppressive immune cells but the nature of such inflammation is unclear. Dysfunction in T cell exhaustion, while implicated in chronic inflammatory diseases, remains unexplored in tuberculosis. Given that immunotherapy targeting exhaustion checkpoints exacerbates tuberculosis, we speculate that T cell exhaustion is dysfunctional in tuberculosis. Using integrated single-cell RNA sequencing and T cell receptor profiling we reported defects in exhaustion responses within inflamed tuberculosis-affected lungs. Tuberculosis lungs demonstrated significantly reduced levels of exhausted CD8+ T cells and exhibited diminished expression of exhaustion-related transcripts among clonally expanded CD4+ and CD8+ T cells. Additionally, clonal expansion of CD4+ and CD8+ T cells bearing T cell receptors specific for CMV was observed. Expanded CD8+ T cells expressed the cytolytic marker GZMK. Hence, inflamed tuberculosis-affected lungs displayed dysfunction in T cell exhaustion. Our findings likely hold implications for understanding the reactivation of tuberculosis observed in patients undergoing immunotherapy targeting the exhaustion checkpoint. |
ArticleNumber | 106158 |
Author | Wan, Laiyi Wen, Zilu Li, Feng Song, Shu Hao, Wentao Chen, Hui Song, Yanzheng Ma, Hui Zhang, Shulin Wong, Ka-Wing Wang, Lin Li, Leilei Shi, Lei Wei, Yutong Xue, Qinghua Li, Hongwei Xu, Jianqing |
Author_xml | – sequence: 1 givenname: Zilu surname: Wen fullname: Wen, Zilu organization: Department of Scientific Research, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 2 givenname: Lin surname: Wang fullname: Wang, Lin organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 3 givenname: Hui surname: Ma fullname: Ma, Hui organization: Department of Scientific Research, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 4 givenname: Leilei surname: Li fullname: Li, Leilei organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 5 givenname: Laiyi surname: Wan fullname: Wan, Laiyi organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 6 givenname: Lei surname: Shi fullname: Shi, Lei organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 7 givenname: Hongwei surname: Li fullname: Li, Hongwei organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 8 givenname: Hui surname: Chen fullname: Chen, Hui organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 9 givenname: Wentao surname: Hao fullname: Hao, Wentao organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 10 givenname: Shu surname: Song fullname: Song, Shu organization: Department of Pathology, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 11 givenname: Qinghua surname: Xue fullname: Xue, Qinghua organization: Department of Scientific Research, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 12 givenname: Yutong surname: Wei fullname: Wei, Yutong organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 13 givenname: Feng surname: Li fullname: Li, Feng organization: Department of Respiratory Diseases, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 14 givenname: Jianqing surname: Xu fullname: Xu, Jianqing organization: Department of Scientific Research, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 15 givenname: Shulin surname: Zhang fullname: Zhang, Shulin organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 16 givenname: Ka-Wing orcidid: 0000-0001-8356-5880 surname: Wong fullname: Wong, Ka-Wing email: kwwong@gmail.com organization: Department of Scientific Research, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China – sequence: 17 givenname: Yanzheng surname: Song fullname: Song, Yanzheng email: yanzhengsong@163.com organization: Department of Thoracic Surgery, Shanghai Public Health Clinical Center, Fudan University, Shanghai, China |
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Keywords | T cell exhaustion Tuberculosis Chronic inflammation Single-cell RNA sequencing Immunotherapy |
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SubjectTerms | Chronic inflammation Immunotherapy Single-cell RNA sequencing T cell exhaustion Tuberculosis |
Title | Integrated single-cell transcriptome and T cell receptor profiling reveals defects of T cell exhaustion in pulmonary tuberculosis |
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