A single-cell transcriptional landscape of immune cells shows disease-specific changes of T cell and macrophage populations in human achalasia

Zu-Qiang Liu, Hao Dai, Lu Yao, Wei-Feng Chen, Yun Wang, Li-Yun Ma, Xiao-Qing Li, Sheng-Li Lin, Meng-Jiang He, Ping-Ting Gao, Xin-Yang Liu, Jia-Xin Xu, Xiao-Yue Xu, Ke-Hao Wang, Li Wang, Luonan Chen (), Ping-Hong Zhou () and Quan-Lin Li ()
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Zu-Qiang Liu: Fudan University
Hao Dai: Chinese Academy of Sciences
Lu Yao: Fudan University
Wei-Feng Chen: Fudan University
Yun Wang: Fudan University
Li-Yun Ma: Fudan University
Xiao-Qing Li: Fudan University
Sheng-Li Lin: Fudan University
Meng-Jiang He: Fudan University
Ping-Ting Gao: Fudan University
Xin-Yang Liu: Fudan University
Jia-Xin Xu: Fudan University
Xiao-Yue Xu: Fudan University
Ke-Hao Wang: Fudan University
Li Wang: Fudan University
Luonan Chen: Chinese Academy of Sciences
Ping-Hong Zhou: Fudan University
Quan-Lin Li: Fudan University

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: Abstract Achalasia is a rare motility disorder of the esophagus caused by the gradual degeneration of myenteric neurons. Immune-mediated ganglionitis has been proposed to underlie the loss of myenteric neurons. Here, we measure the immune cell transcriptional profile of paired lower esophageal sphincter (LES) tissue and blood samples in achalasia and controls using single-cell RNA sequencing (scRNA-seq). In achalasia, we identify a pattern of expanded immune cells and a specific transcriptional phenotype, especially in LES tissue. We show C1QC+ macrophages and tissue-resident memory T cells (TRM), especially ZNF683+ CD8+ TRM and XCL1+ CD4+ TRM, are significantly expanded and localized surrounding the myenteric plexus in the LES tissue of achalasia. C1QC+ macrophages are transcriptionally similar to microglia of the central nervous system and have a neurodegenerative dysfunctional phenotype in achalasia. TRM also expresses transcripts of dysregulated immune responses in achalasia. Moreover, inflammation increases with disease progression since immune cells are more activated in type I compared with type II achalasia. Thus, we profile the immune cell transcriptional landscape and identify C1QC+ macrophages and TRM as disease-associated immune cell subsets in achalasia.

Date: 2023
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DOI: 10.1038/s41467-023-39750-5

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