Setdb1 ablation in macrophages attenuates fibrosis in heart allografts

Z Zhibo Ma (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) X Xi Zhou W Wenlong Jia (Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) X Xiaosheng Tan (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) X Xia Huang (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) J Jingzeng Wang (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) L Lingjuan Sun (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) Q Qingwen Li (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) X Xiangli Zhao (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) N Naonao Yuan (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) P Ping Liu (Chemistry Department) J Jing Liu Z Zhishui Chen (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology) P Peixiang Lan (Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology)

Abstract

Tissue fibrosis is commonly associated with organ malfunction and is strongly associated with the development of chronic rejection, cardiovascular diseases, and other chronic diseases. Fibrosis also contributes to immune exclusion in tumor tissues. Targeting fibrosis might be a strategy for prolonging allograft survival while suppressing cancer development. Here, single-cell transcriptomes of human and mouse heart allografts showed that macrophages accumulated in grafts with fibrosis were reprogrammed via histone methylation regulated by Setdb1, an H3K9 methyltransferase. Myeloid-specific deletion of Setdb1 prolonged heart allograft survival but reversed immune exclusion in tumor tissues. Interestingly, myeloid-specific Setdb1-knockout led to lower fibrosis in heart allografts and tumor tissues in mice. Our single-cell sequencing data showed that Setdb1 ablation impaired Fn1 + and SPP1 + profibrogenic macrophage reprogramming. Mechanistically, Fn1, which was induced by the CCR2-Creb/Setdb1 axis, upregulated the expression of genes related to fibrosis in fibroblasts and macrophages via ITGA5 and PIRA receptors. Blocking the interaction between FN1 and these receptors inhibited fibrosis in allograft and tumor tissues. Our results reveal a target, histone methylation in macrophages, for the treatment of fibrosis-related disease.

Article Details

Volume / Issue Vol. 122, Issue 26
Published July 01, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (14)

Z

Zhibo Ma

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

X

Xi Zhou

W

Wenlong Jia

Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

X

Xiaosheng Tan

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

X

Xia Huang

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

J

Jingzeng Wang

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

L

Lingjuan Sun

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

Q

Qingwen Li

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

X

Xiangli Zhao

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

N

Naonao Yuan

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

P

Ping Liu

Chemistry Department

J

Jing Liu

Z

Zhishui Chen

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology

P

Peixiang Lan

Institute of Organ Transplantation, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology