Adipose stem cells control obesity-induced T cell infiltration into adipose tissue

Xiyan Liao; Qin Zeng; Limin Xie; Haowei Zhang; Wanyu Hu; Liuling Xiao; Hui Zhou; Fanqi Wang; Wanqin Xie; Jianfeng Song; Xiaoxiao Sun; Dandan Wang; Yujin Ding; Yayi Jiao; Wuqian Mai; Wufuer Aini; Xiaoyan Hui; Wei Liu; Willa A Hsueh; Tuo Deng

doi:10.1016/j.celrep.2024.113963

Adipose stem cells control obesity-induced T cell infiltration into adipose tissue

Cell Rep. 2024 Mar 26;43(3):113963. doi: 10.1016/j.celrep.2024.113963. Epub 2024 Mar 15.

Authors

Xiyan Liao¹, Qin Zeng¹, Limin Xie¹, Haowei Zhang², Wanyu Hu¹, Liuling Xiao³, Hui Zhou¹, Fanqi Wang¹, Wanqin Xie⁴, Jianfeng Song¹, Xiaoxiao Sun¹, Dandan Wang¹, Yujin Ding¹, Yayi Jiao¹, Wuqian Mai¹, Wufuer Aini¹, Xiaoyan Hui⁵, Wei Liu⁶, Willa A Hsueh⁷, Tuo Deng⁸

Affiliations

¹ National Clinical Research Center for Metabolic Diseases and Department of Metabolism and Endocrinology, The Second Xiangya Hospital of Central South University, Changsha, Hunan 410011, China; Key Laboratory of Diabetes Immunology, Ministry of Education, and Metabolic Syndrome Research Center, The Second Xiangya Hospital of Central South University, Changsha, Hunan 410011, China.
² The First Affiliated Hospital, Department of Orthopedics, Hengyang Medical School, University of South China, Hengyang, Hunan 421001, China.
³ Center for Translational Research in Hematological Malignancies, Neal Cancer Center, Houston Methodist Research Institute, Houston, TX 77080, USA.
⁴ NHC Key Laboratory of Birth Defects for Research and Prevention, Hunan Provincial Maternal and Child Health Care Hospital, 53 Xiangchun Road, Changsha, Hunan 410028, China.
⁵ School of Biomedical Sciences, The Chinese University of Hong Kong, Hong Kong 999077, China.
⁶ Department of Biliopancreatic Surgery and Bariatric Surgery, The Second Xiangya Hospital, Central South University, Changsha, Hunan 410011, China.
⁷ The Diabetes and Metabolism Research Center, Division of Endocrinology, Diabetes, and Metabolism, Department of Medicine, The Ohio State University, Columbus, OH 43210, USA.
⁸ National Clinical Research Center for Metabolic Diseases and Department of Metabolism and Endocrinology, The Second Xiangya Hospital of Central South University, Changsha, Hunan 410011, China; Key Laboratory of Diabetes Immunology, Ministry of Education, and Metabolic Syndrome Research Center, The Second Xiangya Hospital of Central South University, Changsha, Hunan 410011, China; Clinical Immunology Center, The Second Xiangya Hospital of Central South University, Changsha, Hunan 410011, China. Electronic address: dengtuo@csu.edu.cn.

PMID: 38492218
DOI: 10.1016/j.celrep.2024.113963

Abstract

T cell infiltration into white adipose tissue (WAT) drives obesity-induced adipose inflammation, but the mechanisms of obesity-induced T cell infiltration into WAT remain unclear. Our single-cell RNA sequencing reveals a significant impact of adipose stem cells (ASCs) on T cells. Transplanting ASCs from obese mice into WAT enhances T cell accumulation. C-C motif chemokine ligand 5 (CCL5) is upregulated in ASCs as early as 4 weeks of high-fat diet feeding, coinciding with the onset of T cell infiltration into WAT during obesity. ASCs and bone marrow transplantation experiments demonstrate that CCL5 from ASCs plays a crucial role in T cell accumulation during obesity. The production of CCL5 in ASCs is induced by tumor necrosis factor alpha via the nuclear factor κB pathway. Overall, our findings underscore the pivotal role of ASCs in regulating T cell accumulation in WAT during the early phases of obesity, emphasizing their importance in modulating adaptive immunity in obesity-induced adipose inflammation.

Keywords: ASCs; CCL5; CP: Metabolism; CP: Stem cell research; T cells; adipose tissue inflammation; obesity.

MeSH terms

Adipose Tissue* / metabolism
Animals
Inflammation / pathology
Mice
Obesity / metabolism
Stem Cells / metabolism
T-Lymphocytes* / metabolism