Carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancer

Abstract Impressive clinical benefit is seen in clinic with PD‐1 inhibitors on portion of cancer patients. Yet, there remains an urgent need to develop effective synergizers to expand their clinical application. Tumor‐associated macrophage (TAM), a type of M2‐polarized macrophage, eliminates or supp...

Full description

Saved in:
Bibliographic Details
Main Authors: Qian Zhou, Jinxia Liang, Tong Yang, Jin Liu, Bo Li, Yingchang Li, Zhenzhen Fan, Weida Wang, Wensheng Chen, Sujing Yuan, Meng Xu, Qigui Xu, Zhidong Luan, Zhongjun Xia, Penghui Zhou, Yadong Huang, Liang Chen
Format: Article
Language:English
Published: Springer Nature 2021-12-01
Series:EMBO Molecular Medicine
Subjects:
Online Access:https://doi.org/10.15252/emmm.202114502
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849761554504876032
author Qian Zhou
Jinxia Liang
Tong Yang
Jin Liu
Bo Li
Yingchang Li
Zhenzhen Fan
Weida Wang
Wensheng Chen
Sujing Yuan
Meng Xu
Qigui Xu
Zhidong Luan
Zhongjun Xia
Penghui Zhou
Yadong Huang
Liang Chen
author_facet Qian Zhou
Jinxia Liang
Tong Yang
Jin Liu
Bo Li
Yingchang Li
Zhenzhen Fan
Weida Wang
Wensheng Chen
Sujing Yuan
Meng Xu
Qigui Xu
Zhidong Luan
Zhongjun Xia
Penghui Zhou
Yadong Huang
Liang Chen
author_sort Qian Zhou
collection DOAJ
description Abstract Impressive clinical benefit is seen in clinic with PD‐1 inhibitors on portion of cancer patients. Yet, there remains an urgent need to develop effective synergizers to expand their clinical application. Tumor‐associated macrophage (TAM), a type of M2‐polarized macrophage, eliminates or suppresses T‐cell‐mediated anti‐tumor responses. Transforming TAMs into M1 macrophages is an attractive strategy of anti‐tumor therapy. Here, we conducted a high‐throughput screening and found that Carfilzomib potently drove M2 macrophages to express M1 cytokines, phagocytose tumor cells, and present antigens to T cells. Mechanistically, Carfilzomib elicited unfolded protein response (UPR), activated IRE1α to recruit TRAF2, and activated NF‐κB to transcribe genes encoding M1 markers in M2 macrophages. In vivo, Carfilzomib effectively rewired tumor microenvironment through reprogramming TAMs into M1‐like macrophages and shrank autochthonous lung cancers in transgenic mouse model. More importantly, Carfilzomib synergized with PD‐1 antibody to almost completely regress autochthonous lung cancers. Given the safety profiles of Carfilzomib in clinic, our work suggested a potentially immediate application of combinational treatment with Carfilzomib and PD‐1 inhibitors for patients with solid tumors.
format Article
id doaj-art-a5e0e58dd2f14cd383c1a32c658a93a5
institution DOAJ
issn 1757-4676
1757-4684
language English
publishDate 2021-12-01
publisher Springer Nature
record_format Article
series EMBO Molecular Medicine
spelling doaj-art-a5e0e58dd2f14cd383c1a32c658a93a52025-08-20T03:06:00ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842021-12-0114112010.15252/emmm.202114502Carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancerQian Zhou0Jinxia Liang1Tong Yang2Jin Liu3Bo Li4Yingchang Li5Zhenzhen Fan6Weida Wang7Wensheng Chen8Sujing Yuan9Meng Xu10Qigui Xu11Zhidong Luan12Zhongjun Xia13Penghui Zhou14Yadong Huang15Liang Chen16Key Laboratory of Functional Protein Research of Guangdong Higher Education Institutes and MOE Key Laboratory of Tumor Molecular Biology, Institute of Life and Health Engineering, College of Life Science and Technology, Jinan UniversityKey Laboratory of Functional Protein Research of Guangdong Higher Education Institutes and MOE Key Laboratory of Tumor Molecular Biology, Institute of Life and Health Engineering, College of Life Science and Technology, Jinan UniversityKey Laboratory of Functional Protein Research of Guangdong Higher Education Institutes and MOE Key Laboratory of Tumor Molecular Biology, Institute of Life and Health Engineering, College of Life Science and Technology, Jinan UniversityKey Laboratory of Functional Protein Research of Guangdong Higher Education Institutes and MOE Key Laboratory of Tumor Molecular Biology, Institute of Life and Health Engineering, College of Life Science and Technology, Jinan UniversityKey Laboratory of Functional Protein Research of Guangdong Higher Education Institutes and MOE Key Laboratory of Tumor Molecular Biology, Institute of Life and Health Engineering, College of Life Science and Technology, Jinan UniversityKey Laboratory of Functional Protein Research of Guangdong Higher Education Institutes and MOE Key Laboratory of Tumor Molecular Biology, Institute of Life and Health Engineering, College of Life Science and Technology, Jinan UniversityKey Laboratory of Functional Protein Research of Guangdong Higher Education Institutes and MOE Key Laboratory of Tumor Molecular Biology, Institute of Life and Health Engineering, College of Life Science and Technology, Jinan UniversityState Key Laboratory of Oncology in Southern China, Collaborative Innovation Center for Cancer Medicine, Sun Yat‐sen University Cancer CenterKey Laboratory of Functional Protein Research of Guangdong Higher Education Institutes and MOE Key Laboratory of Tumor Molecular Biology, Institute of Life and Health Engineering, College of Life Science and Technology, Jinan UniversityState Key Laboratory of Oncology in Southern China, Collaborative Innovation Center for Cancer Medicine, Sun Yat‐sen University Cancer CenterDepartment of Oncology, The First Affiliated Hospital, Jinan UniversityTranslational medicine laboratory, People’s Hospital of Yangjiang CityTranslational medicine laboratory, People’s Hospital of Yangjiang CityState Key Laboratory of Oncology in Southern China, Collaborative Innovation Center for Cancer Medicine, Sun Yat‐sen University Cancer CenterState Key Laboratory of Oncology in Southern China, Collaborative Innovation Center for Cancer Medicine, Sun Yat‐sen University Cancer CenterGuangdong Province Key Laboratory of Bioengineering Medicine, Jinan UniversityDepartment of Oncology, The First Affiliated Hospital, Jinan UniversityAbstract Impressive clinical benefit is seen in clinic with PD‐1 inhibitors on portion of cancer patients. Yet, there remains an urgent need to develop effective synergizers to expand their clinical application. Tumor‐associated macrophage (TAM), a type of M2‐polarized macrophage, eliminates or suppresses T‐cell‐mediated anti‐tumor responses. Transforming TAMs into M1 macrophages is an attractive strategy of anti‐tumor therapy. Here, we conducted a high‐throughput screening and found that Carfilzomib potently drove M2 macrophages to express M1 cytokines, phagocytose tumor cells, and present antigens to T cells. Mechanistically, Carfilzomib elicited unfolded protein response (UPR), activated IRE1α to recruit TRAF2, and activated NF‐κB to transcribe genes encoding M1 markers in M2 macrophages. In vivo, Carfilzomib effectively rewired tumor microenvironment through reprogramming TAMs into M1‐like macrophages and shrank autochthonous lung cancers in transgenic mouse model. More importantly, Carfilzomib synergized with PD‐1 antibody to almost completely regress autochthonous lung cancers. Given the safety profiles of Carfilzomib in clinic, our work suggested a potentially immediate application of combinational treatment with Carfilzomib and PD‐1 inhibitors for patients with solid tumors.https://doi.org/10.15252/emmm.202114502immunotherapyM1 macrophageM2 macrophagetumor microenvironmenttumor‐associated macrophage
spellingShingle Qian Zhou
Jinxia Liang
Tong Yang
Jin Liu
Bo Li
Yingchang Li
Zhenzhen Fan
Weida Wang
Wensheng Chen
Sujing Yuan
Meng Xu
Qigui Xu
Zhidong Luan
Zhongjun Xia
Penghui Zhou
Yadong Huang
Liang Chen
Carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancer
EMBO Molecular Medicine
immunotherapy
M1 macrophage
M2 macrophage
tumor microenvironment
tumor‐associated macrophage
title Carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancer
title_full Carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancer
title_fullStr Carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancer
title_full_unstemmed Carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancer
title_short Carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancer
title_sort carfilzomib modulates tumor microenvironment to potentiate immune checkpoint therapy for cancer
topic immunotherapy
M1 macrophage
M2 macrophage
tumor microenvironment
tumor‐associated macrophage
url https://doi.org/10.15252/emmm.202114502
work_keys_str_mv AT qianzhou carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT jinxialiang carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT tongyang carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT jinliu carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT boli carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT yingchangli carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT zhenzhenfan carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT weidawang carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT wenshengchen carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT sujingyuan carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT mengxu carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT qiguixu carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT zhidongluan carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT zhongjunxia carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT penghuizhou carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT yadonghuang carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer
AT liangchen carfilzomibmodulatestumormicroenvironmenttopotentiateimmunecheckpointtherapyforcancer