CBX2 suppresses interferon signaling to diminish tumor immunogenicity via a noncanonical corepressor complex

Y Yanxun Lin H Huan Jin Y Yong She (State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center) Y Yiqun Zhang (Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University) L Lei Cui C Chunyuan Xie Y Yongxiang Liu (Wuya College of Innovation) H Huanling Zhang (State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center) H Hui Guo J Jiaxin Wu L Lin Li Z Zixuan Guo X Xiaojuan Wang (Department of Endocrinology, Genetics and Metabolism, National Center for Children’s Health, Beijing Children’s Hospital Capital Medical University) W Wu Jiang (State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center) X Xu Chen (Jinan University , , , ,) S Shuai He (State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center) P Penghui Zhou (State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center) J Jing Tan J Jin-Xin Bei J Jinyun Liu (State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center) Y Yan-Xing Chen (State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center) Q Qi Zhao X Xiaojun Xia Z Zining Wang

Abstract

Chromobox 2 (CBX2), a crucial component of the polycomb repressive complex (PRC), has been implicated in the development of various human cancers. However, its role in the regulation of tumor immunogenicity and immune evasion remains inadequately understood. In this study, we found that ablation of CBX2 led to tumor growth inhibition, activation of the tumor immune microenvironment, and enhanced therapeutic efficacy of anti-PD1 or adoptive T cell therapies by using murine syngeneic tumor models. By analysis of the CBX2-regulated transcriptional program coupled with mass spectrometry screening of CBX2-interacting proteins, we found that CBX2 suppresses interferon signaling independent of its function in the canonical PRC. Mechanistically, CBX2 directly interacts with RACK1 and facilitates the recruitment of HDAC1, which attenuates the H3K27ac modification on the promoter regions of interferon-stimulated genes, thereby suppressing interferon signaling. Consequently, CBX2 reduces tumor immunogenicity and enables immune evasion. Moreover, a high expression level of CBX2 is associated with immune suppressive tumor microenvironment and reduced efficacy of immunotherapy across various human cancer types. Our study identifies a noncanonical CBX2–RACK1–HDAC1 corepressor complex in suppression of tumor immunogenicity, thereby presenting a potential target and biomarker for tumor immunotherapy.

Article Details

Volume / Issue Vol. 122, Issue 5
Published February 04, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (24)

Y

Yanxun Lin

H

Huan Jin

Y

Yong She

State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center

Y

Yiqun Zhang

Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University

L

Lei Cui

C

Chunyuan Xie

Y

Yongxiang Liu

Wuya College of Innovation

H

Huanling Zhang

State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center

H

Hui Guo

J

Jiaxin Wu

L

Lin Li

Z

Zixuan Guo

X

Xiaojuan Wang

Department of Endocrinology, Genetics and Metabolism, National Center for Children’s Health, Beijing Children’s Hospital Capital Medical University

W

Wu Jiang

State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center

X

Xu Chen

Jinan University , , , ,

S

Shuai He

State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center

P

Penghui Zhou

State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center

J

Jing Tan

J

Jin-Xin Bei

J

Jinyun Liu

State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center

Y

Yan-Xing Chen

State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center

Q

Qi Zhao

X

Xiaojun Xia

Z

Zining Wang