Single-cell profiling reveals distinct immune response landscapes in tuberculous pleural effusion and non-TPE.

Yang, X; Yan, J; Xue, Y; Sun, Q; Zhang, Y; Guo, R; Wang, C; Li, X; Liang, Q; Wu, H; Wang, C; Liao, X; Long, S; Zheng, M; Wei, R; Zhang, H; Liu, Y; Che, N; Luu, LDW; Pan, J; Wang, G; Wang, Y

Single-cell profiling reveals distinct immune response landscapes in tuberculous pleural effusion and non-TPE.

Yang, X Yan, J Xue, Y Sun, Q Zhang, Y Guo, R Wang, C Li, X Liang, Q Wu, H Wang, C Liao, X Long, S Zheng, M Wei, R Zhang, H Liu, Y Che, N Luu, LDW Pan, J Wang, G Wang, Y

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Publisher:: FRONTIERS MEDIA SA
Publication Type:: Journal Article
Citation:: Front Immunol, 2023, 14, pp. 1191357
Issue Date:: 2023

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Field	Value	Language
dc.contributor.author	Yang, X
dc.contributor.author	Yan, J
dc.contributor.author	Xue, Y
dc.contributor.author	Sun, Q
dc.contributor.author	Zhang, Y
dc.contributor.author	Guo, R
dc.contributor.author	Wang, C
dc.contributor.author	Li, X
dc.contributor.author	Liang, Q
dc.contributor.author	Wu, H
dc.contributor.author	Wang, C
dc.contributor.author	Liao, X
dc.contributor.author	Long, S
dc.contributor.author	Zheng, M
dc.contributor.author	Wei, R
dc.contributor.author	Zhang, H
dc.contributor.author	Liu, Y
dc.contributor.author	Che, N
dc.contributor.author	Luu, LDW
dc.contributor.author	Pan, J
dc.contributor.author	Wang, G
dc.contributor.author	Wang, Y
dc.date.accessioned	2024-01-08T06:22:37Z
dc.date.available	2023-05-30
dc.date.available	2024-01-08T06:22:37Z
dc.date.issued	2023
dc.identifier.citation	Front Immunol, 2023, 14, pp. 1191357
dc.identifier.issn	1664-3224
dc.identifier.issn	1664-3224
dc.identifier.uri	http://hdl.handle.net/10453/174102
dc.description.abstract	BACKGROUND: Tuberculosis (TB) is caused by Mycobacterium tuberculosis (Mtb) and remains a major health threat worldwide. However, a detailed understanding of the immune cells and inflammatory mediators in Mtb-infected tissues is still lacking. Tuberculous pleural effusion (TPE), which is characterized by an influx of immune cells to the pleural space, is thus a suitable platform for dissecting complex tissue responses to Mtb infection. METHODS: We employed singe-cell RNA sequencing to 10 pleural fluid (PF) samples from 6 patients with TPE and 4 non-TPEs including 2 samples from patients with TSPE (transudative pleural effusion) and 2 samples with MPE (malignant pleural effusion). RESULT: Compared to TSPE and MPE, TPE displayed obvious difference in the abundance of major cell types (e.g., NK, CD4+T, Macrophages), which showed notable associations with disease type. Further analyses revealed that the CD4 lymphocyte population in TPE favored a Th1 and Th17 response. Tumor necrosis factors (TNF)-, and XIAP related factor 1 (XAF1)-pathways induced T cell apoptosis in patients with TPE. Immune exhaustion in NK cells was an important feature in TPE. Myeloid cells in TPE displayed stronger functional capacity for phagocytosis, antigen presentation and IFN-γ response, than TSPE and MPE. Systemic elevation of inflammatory response genes and pro-inflammatory cytokines were mainly driven by macrophages in patients with TPE. CONCLUSION: We provide a tissue immune landscape of PF immune cells, and revealed a distinct local immune response in TPE and non-TPE (TSPE and MPE). These findings will improve our understanding of local TB immunopathogenesis and provide potential targets for TB therapy.
dc.format	Electronic-eCollection
dc.language	eng
dc.publisher	FRONTIERS MEDIA SA
dc.relation.ispartof	Front Immunol
dc.relation.isbasedon	10.3389/fimmu.2023.1191357
dc.rights	info:eu-repo/semantics/openAccess
dc.subject	1107 Immunology, 1108 Medical Microbiology
dc.subject.classification	3101 Biochemistry and cell biology
dc.subject.classification	3105 Genetics
dc.subject.classification	3204 Immunology
dc.subject.mesh	Humans
dc.subject.mesh	Pleural Effusion
dc.subject.mesh	Tuberculosis
dc.subject.mesh	Antigen Presentation
dc.subject.mesh	Mycobacterium tuberculosis
dc.subject.mesh	Pleural Cavity
dc.subject.mesh	Pleural Cavity
dc.subject.mesh	Humans
dc.subject.mesh	Mycobacterium tuberculosis
dc.subject.mesh	Tuberculosis
dc.subject.mesh	Pleural Effusion
dc.subject.mesh	Antigen Presentation
dc.subject.mesh	Humans
dc.subject.mesh	Pleural Effusion
dc.subject.mesh	Tuberculosis
dc.subject.mesh	Antigen Presentation
dc.subject.mesh	Mycobacterium tuberculosis
dc.subject.mesh	Pleural Cavity
dc.title	Single-cell profiling reveals distinct immune response landscapes in tuberculous pleural effusion and non-TPE.
dc.type	Journal Article
utslib.citation.volume	14
utslib.location.activity	Switzerland
utslib.for	1107 Immunology
utslib.for	1108 Medical Microbiology
pubs.organisational-group	/University of Technology Sydney
pubs.organisational-group	/University of Technology Sydney/Faculty of Science
pubs.organisational-group	/University of Technology Sydney/Faculty of Science/School of Life Sciences
utslib.copyright.status	open_access	*
dc.date.updated	2024-01-08T06:22:31Z
pubs.publication-status	Published online
pubs.volume	14

Abstract:

BACKGROUND: Tuberculosis (TB) is caused by Mycobacterium tuberculosis (Mtb) and remains a major health threat worldwide. However, a detailed understanding of the immune cells and inflammatory mediators in Mtb-infected tissues is still lacking. Tuberculous pleural effusion (TPE), which is characterized by an influx of immune cells to the pleural space, is thus a suitable platform for dissecting complex tissue responses to Mtb infection. METHODS: We employed singe-cell RNA sequencing to 10 pleural fluid (PF) samples from 6 patients with TPE and 4 non-TPEs including 2 samples from patients with TSPE (transudative pleural effusion) and 2 samples with MPE (malignant pleural effusion). RESULT: Compared to TSPE and MPE, TPE displayed obvious difference in the abundance of major cell types (e.g., NK, CD4+T, Macrophages), which showed notable associations with disease type. Further analyses revealed that the CD4 lymphocyte population in TPE favored a Th1 and Th17 response. Tumor necrosis factors (TNF)-, and XIAP related factor 1 (XAF1)-pathways induced T cell apoptosis in patients with TPE. Immune exhaustion in NK cells was an important feature in TPE. Myeloid cells in TPE displayed stronger functional capacity for phagocytosis, antigen presentation and IFN-γ response, than TSPE and MPE. Systemic elevation of inflammatory response genes and pro-inflammatory cytokines were mainly driven by macrophages in patients with TPE. CONCLUSION: We provide a tissue immune landscape of PF immune cells, and revealed a distinct local immune response in TPE and non-TPE (TSPE and MPE). These findings will improve our understanding of local TB immunopathogenesis and provide potential targets for TB therapy.

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http://hdl.handle.net/10453/174102