Transcription factor TCF-1 regulates the functions, but not the development, of lymphoid tissue inducer subsets in different tissues

Mingzhu Zheng; Chen Yao; Gang Ren; Kairui Mao; Hyunwoo Chung; Xi Chen; Gangqing Hu; Lei Wang; Xuemei Luan; Difeng Fang; Dan Li; Chao Zhong; Xiaoxiao Lu; Nikki Cannon; Mingxu Zhang; Avinash Bhandoola; Keji Zhao; John J O'Shea; Jinfang Zhu

doi:10.1016/j.celrep.2023.112924

Transcription factor TCF-1 regulates the functions, but not the development, of lymphoid tissue inducer subsets in different tissues

Cell Rep. 2023 Aug 29;42(8):112924. doi: 10.1016/j.celrep.2023.112924. Epub 2023 Aug 3.

Authors

Mingzhu Zheng¹, Chen Yao², Gang Ren³, Kairui Mao⁴, Hyunwoo Chung⁵, Xi Chen⁵, Gangqing Hu⁶, Lei Wang⁷, Xuemei Luan⁸, Difeng Fang⁵, Dan Li⁹, Chao Zhong¹⁰, Xiaoxiao Lu¹¹, Nikki Cannon⁷, Mingxu Zhang¹², Avinash Bhandoola¹¹, Keji Zhao¹³, John J O'Shea¹⁴, Jinfang Zhu¹⁵

Affiliations

¹ Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA; Department of Microbiology and Immunology School of Medicine, Jiangsu Provincial Key Laboratory of Critical Care Medicine, Southeast University, Nanjing, Jiangsu 210009, China. Electronic address: zhengmz@zju.edu.cn.
² Molecular Immunology and Inflammation Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD 20892, USA; Department of Immunology & Kidney Cancer Program, Harold C. Simmons Comprehensive Cancer Center, The University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.
³ Laboratory of Epigenome Biology, Systems Biology Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; College of Animal Science and Technology, Northwest A&F University, Shannxi 712100, China.
⁴ Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA; State Key Laboratory of Cellular Stress Biology, Innovation Center for Cell Signaling Network, School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, China.
⁵ Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
⁶ Laboratory of Epigenome Biology, Systems Biology Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; Bioinformatics Core, West Virginia University, Morgantown, WV 26506, USA; Department of Microbiology, Immunology, and Cell Biology, School of Medicine, West Virginia University, Morgantown, WV 26506, USA.
⁷ Bioinformatics Core, West Virginia University, Morgantown, WV 26506, USA.
⁸ State Key Laboratory of Cellular Stress Biology, Innovation Center for Cell Signaling Network, School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, China.
⁹ Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA; Institute of Immunology, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310058, China; Department of Clinical Laboratory, the Second Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215004, China.
¹⁰ Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA; Institute of Systems Biomedicine, School of Basic Medical Sciences, Peking University Health Science Center, Beijing 100191, China.
¹¹ Laboratory of Genome Integrity, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
¹² Zhejiang University-University of Edinburgh Institute, Zhejiang University School of Medicine, Haining 314400, China.
¹³ Laboratory of Epigenome Biology, Systems Biology Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁴ Molecular Immunology and Inflammation Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁵ Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: jfzhu@niaid.nih.gov.

Abstract

Lymphoid tissue inducer (LTi) cells, a subset of innate lymphoid cells (ILCs), play an essential role in the formation of secondary lymphoid tissues. However, the regulation of the development and functions of this ILC subset is still elusive. In this study, we report that the transcription factor T cell factor 1 (TCF-1), just as GATA3, is indispensable for the development of non-LTi ILC subsets. While LTi cells are still present in TCF-1-deficient mice, the organogenesis of Peyer's patches (PPs), but not of lymph nodes, is impaired in these mice. LTi cells from different tissues have distinct gene expression patterns, and TCF-1 regulates the expression of lymphotoxin specifically in PP LTi cells. Mechanistically, TCF-1 may directly and/or indirectly regulate Lta, including through promoting the expression of GATA3. Thus, the TCF-1-GATA3 axis, which plays an important role during T cell development, also critically regulates the development of non-LTi cells and tissue-specific functions of LTi cells.

Keywords: CP: Immunology; Peyer’s patches; TCF-1; lymphoid tissue inducer; lymphotoxin.

Published by Elsevier Inc.

Publication types

Research Support, N.I.H., Extramural
Research Support, N.I.H., Intramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Immunity, Innate*
Lymphocytes
Lymphoid Tissue / metabolism
Mice
T Cell Transcription Factor 1* / metabolism

Substances

T Cell Transcription Factor 1
Hnf1a protein, mouse

Abstract

Publication types

MeSH terms

Substances

Grants and funding