Systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironment

The composition of the tumor immune microenvironment has become a major determinant of response to therapy, particularly immunotherapy. Clinically, a tumor microenvironment lacking lymphocytes, so-called ''cold'' tumors, are considered poor candidates for immune checkpoint inhibi...

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Main Authors: Lin Ma, Jian-Hua Mao, Mary Helen Barcellos-Hoff
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Neoplasia: An International Journal for Oncology Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S1476558625000430
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author Lin Ma
Jian-Hua Mao
Mary Helen Barcellos-Hoff
author_facet Lin Ma
Jian-Hua Mao
Mary Helen Barcellos-Hoff
author_sort Lin Ma
collection DOAJ
description The composition of the tumor immune microenvironment has become a major determinant of response to therapy, particularly immunotherapy. Clinically, a tumor microenvironment lacking lymphocytes, so-called ''cold'' tumors, are considered poor candidates for immune checkpoint inhibition. In this review, we describe the diversity of the tumor immune microenvironment in breast cancer and how radiation exposure alters carcinogenesis. We review the development and use of a radiation-genetic mammary chimera model to clarify the mechanism by which radiation acts. Using the chimera model, we demonstrate that systemic inflammation elicited by a low dose of radiation is key to the construction of an immunosuppressive tumor microenvironment, resulting in aggressive, rapidly growing tumors lacking lymphocytes. Our experimental studies inform the non-mutagenic mechanisms by which radiation affects cancer and provide insight into the genesis of cold tumors.
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series Neoplasia: An International Journal for Oncology Research
spelling doaj-art-e868adf53ee04729893bef08004f3a062025-08-20T02:24:45ZengElsevierNeoplasia: An International Journal for Oncology Research1476-55862025-06-016410116410.1016/j.neo.2025.101164Systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironmentLin Ma0Jian-Hua Mao1Mary Helen Barcellos-Hoff2Department of Stomatology, Shenzhen University General Hospital, Shenzhen University, Shenzhen, 518055, ChinaBiological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USADepartment of Radiation Oncology, School of Medicine, Helen Diller Comprehensive Cancer Center, University of California, San Francisco, CA 94143 USA; Corresponding author.The composition of the tumor immune microenvironment has become a major determinant of response to therapy, particularly immunotherapy. Clinically, a tumor microenvironment lacking lymphocytes, so-called ''cold'' tumors, are considered poor candidates for immune checkpoint inhibition. In this review, we describe the diversity of the tumor immune microenvironment in breast cancer and how radiation exposure alters carcinogenesis. We review the development and use of a radiation-genetic mammary chimera model to clarify the mechanism by which radiation acts. Using the chimera model, we demonstrate that systemic inflammation elicited by a low dose of radiation is key to the construction of an immunosuppressive tumor microenvironment, resulting in aggressive, rapidly growing tumors lacking lymphocytes. Our experimental studies inform the non-mutagenic mechanisms by which radiation affects cancer and provide insight into the genesis of cold tumors.http://www.sciencedirect.com/science/article/pii/S1476558625000430Tumor microenvironmentRadiation carcinogenesisTGFβDNA damage responseImmunophenotypeEvolution
spellingShingle Lin Ma
Jian-Hua Mao
Mary Helen Barcellos-Hoff
Systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironment
Neoplasia: An International Journal for Oncology Research
Tumor microenvironment
Radiation carcinogenesis
TGFβ
DNA damage response
Immunophenotype
Evolution
title Systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironment
title_full Systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironment
title_fullStr Systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironment
title_full_unstemmed Systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironment
title_short Systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironment
title_sort systemic inflammation in response to radiation drives the genesis of an immunosuppressed tumor microenvironment
topic Tumor microenvironment
Radiation carcinogenesis
TGFβ
DNA damage response
Immunophenotype
Evolution
url http://www.sciencedirect.com/science/article/pii/S1476558625000430
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