Cell Discovery (Aug 2023)
The TRIM37 variants in Mulibrey nanism patients paralyze follicular helper T cell differentiation
- Wangpeng Gu,
- Jia Zhang,
- Qing Li,
- Yaguang Zhang,
- Xuan Lin,
- Bingbing Wu,
- Qi Yin,
- Jinqiao Sun,
- Yulan Lu,
- Xiaoyu Sun,
- Caiwei Jia,
- Chuanyin Li,
- Yu Zhang,
- Meng Wang,
- Xidi Yin,
- Su Wang,
- Jiefang Xu,
- Ran Wang,
- Songling Zhu,
- Shipeng Cheng,
- Shuangfeng Chen,
- Lian Liu,
- Lin Zhu,
- Chenghua Yan,
- Chunyan Yi,
- Xuezhen Li,
- Qiaoshi Lian,
- Guomei Lin,
- Zhiyang Ling,
- Liyan Ma,
- Min Zhou,
- Kuanlin Xiao,
- Haiming Wei,
- Ronggui Hu,
- Wenhao Zhou,
- Lilin Ye,
- Haikun Wang,
- Jinsong Li,
- Bing Sun
Affiliations
- Wangpeng Gu
- Division of Life Sciences and Medicine, University of Science and Technology of China
- Jia Zhang
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Qing Li
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Yaguang Zhang
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Xuan Lin
- Institute of Pasteur of Shanghai
- Bingbing Wu
- Center for Molecular Medicine, Children’s Hospital of Fudan University, National Children’s Medical Center
- Qi Yin
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Jinqiao Sun
- Department of Allergy and Clinical Immunology, Children’s Hospital of Fudan University, National Children’s Medical Center
- Yulan Lu
- Center for Molecular Medicine, Children’s Hospital of Fudan University, National Children’s Medical Center
- Xiaoyu Sun
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Caiwei Jia
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Chuanyin Li
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Yu Zhang
- Institute of Pasteur of Shanghai
- Meng Wang
- Institute of Pasteur of Shanghai
- Xidi Yin
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Su Wang
- Division of Life Sciences and Medicine, University of Science and Technology of China
- Jiefang Xu
- Division of Life Sciences and Medicine, University of Science and Technology of China
- Ran Wang
- Division of Life Sciences and Medicine, University of Science and Technology of China
- Songling Zhu
- Division of Life Sciences and Medicine, University of Science and Technology of China
- Shipeng Cheng
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Shuangfeng Chen
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Lian Liu
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Lin Zhu
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Chenghua Yan
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Chunyan Yi
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Xuezhen Li
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Qiaoshi Lian
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Guomei Lin
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Zhiyang Ling
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Liyan Ma
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Min Zhou
- Department of Ophthalmology, Eye and ENT Hospital of Fudan University
- Kuanlin Xiao
- Department of Ophthalmology, Eye and ENT Hospital of Fudan University
- Haiming Wei
- Division of Life Sciences and Medicine, University of Science and Technology of China
- Ronggui Hu
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Wenhao Zhou
- Center for Molecular Medicine, Children’s Hospital of Fudan University, National Children’s Medical Center
- Lilin Ye
- Institute of Immunology, Third Military Medical University
- Haikun Wang
- Institute of Pasteur of Shanghai
- Jinsong Li
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- Bing Sun
- State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences
- DOI
- https://doi.org/10.1038/s41421-023-00561-z
- Journal volume & issue
-
Vol. 9,
no. 1
pp. 1 – 18
Abstract
Abstract The Mulibrey (Muscle–liver–brain–eye) nanism caused by loss-of-function variants in TRIM37 gene is an autosomal recessive disorder characterized by severe growth failure and constrictive pericarditis. These patients also suffer from severe respiratory infections, co-incident with an increased mortality rate. Here, we revealed that TRIM37 variants were associated with recurrent infection. Trim37 FIN major (a representative variant of Mulibrey nanism patients) and Trim37 knockout mice were susceptible to influenza virus infection. These mice showed defects in follicular helper T (TFH) cell development and antibody production. The effects of Trim37 on TFH cell differentiation relied on its E3 ligase activity catalyzing the K27/29-linked polyubiquitination of Bcl6 and its MATH domain-mediated interactions with Bcl6, thereby protecting Bcl6 from proteasome-mediated degradation. Collectively, these findings highlight the importance of the Trim37-Bcl6 axis in controlling the development of TFH cells and the production of high-affinity antibodies, and further unveil the immunologic mechanism underlying recurrent respiratory infection in Mulibrey nanism.