Reciprocal costimulatory molecules control the activation of mucosal type 3 innate lymphoid cells during engagement with B cells

Xinping Lv; Shan Zhu; Jing Wu; Jinfeng Shi; Qiuyu Wei; Tete Li; Ning Yang; Chunyan Liu; Lingli Qi; Guoxia Zang; Hang Cheng; Zhiguang Yang; Chengyan Jin; Yusheng Wang; Jiuwei Cui; Hideki Ueno; Yong-Jun Liu; Jingtao Chen

doi:10.1038/s41423-023-01041-w

Reciprocal costimulatory molecules control the activation of mucosal type 3 innate lymphoid cells during engagement with B cells

Cell Mol Immunol. 2023 Jul;20(7):808-819. doi: 10.1038/s41423-023-01041-w. Epub 2023 May 25.

Authors

Xinping Lv^{1

2}, Shan Zhu^{1

2}, Jing Wu^{1

2}, Jinfeng Shi³, Qiuyu Wei², Tete Li^{2

4}, Ning Yang², Chunyan Liu^{2

5}, Lingli Qi^{2

6}, Guoxia Zang², Hang Cheng^{2

7}, Zhiguang Yang⁸, Chengyan Jin⁹, Yusheng Wang³, Jiuwei Cui¹, Hideki Ueno^{10

11}, Yong-Jun Liu¹², Jingtao Chen^{13

14}

Affiliations

¹ Cancer Center, First Hospital of Jilin University, Changchun, Jilin, 130021, China.
² Laboratory for Tumor Immunology, First Hospital of Jilin University, Changchun, Jilin, 130061, China.
³ Department of Otolaryngology Head and Neck Surgery, First Hospital of Jilin University, Changchun, Jilin, 130021, China.
⁴ Department of Translational Medicine, Changchun GeneScience Pharmaceuticals Co., Ltd., Changchun, Jilin, 130012, China.
⁵ Department of Gynecology, First Hospital of Jilin University, Changchun, Jilin, 130021, China.
⁶ Department of Pediatric Gastroenterology, First Hospital of Jilin University, Changchun, Jilin, 130021, China.
⁷ Department of Pediatrics, First Hospital of Jilin University, Changchun, Jilin, 130021, China.
⁸ Department of Thoracic Surgery, First Hospital of Jilin University, Changchun, Jilin, 130021, China.
⁹ Department of Thoracic Surgery, Second Hospital of Jilin University, Changchun, Jilin, 130041, China.
¹⁰ Department of Immunology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
¹¹ ASHBi Institute for the Advanced Study of Human Biology, Kyoto University, Kyoto, Japan.
¹² Laboratory for Tumor Immunology, First Hospital of Jilin University, Changchun, Jilin, 130061, China. yjliuanderson@jlu.edu.cn.
¹³ Cancer Center, First Hospital of Jilin University, Changchun, Jilin, 130021, China. jtchen@jlu.edu.cn.
¹⁴ Laboratory for Tumor Immunology, First Hospital of Jilin University, Changchun, Jilin, 130061, China. jtchen@jlu.edu.cn.

Abstract

Innate lymphoid cells (ILCs) are the counterpart of T helper cells in the innate immune system and share multiple phenotypes with T helper cells. Inducible T-cell costimulator (ICOS) is recognized on T cells and participates in T-cell activation and T and B-cell engagement in lymphoid tissues. However, the role of ICOS in ILC3s and ILC3-involved interactions with the immune microenvironment remains unclear. Here, we found that ICOS expression on human ILC3s was correlated with the activated state of ILC3s. ICOS costimulation enhanced the survival, proliferation, and capacity of ILC3s to produce cytokines (IL-22, IL-17A, IFN-γ, TNF, and GM-CSF). Via synergistic effects of ICOS and CD40 signaling, B cells promoted ILC3 functions, and ILC3-induced T-cell-independent B-cell IgA and IgM secretion primarily required CD40 signaling. Hence, ICOS is essential for the nonredundant role of ILC3s and their interaction with adjacent B cells.

Keywords: B cell; Costimulatory molecule; ICOS; Innate lymphoid cell; Tonsil.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

B-Lymphocytes
Cytokines
Humans
Immunity, Innate*
Inducible T-Cell Co-Stimulator Protein
Lymphocytes*
Lymphoid Tissue

Substances

Cytokines
Inducible T-Cell Co-Stimulator Protein

Abstract

Publication types

MeSH terms

Substances

Grants and funding