Low-dose radiotherapy promotes the formation of tertiary lymphoid structures in lung adenocarcinoma

A tertiary lymphoid structure (TLS) refers to an organized infiltration of immune cells that is linked to a positive prognosis and improved response to immunotherapy. However, methods that promote TLS formation are limited and challenging to implement in clinical settings. In this study, we aimed to...

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Published in:	Frontiers in immunology Vol. 14; p. 1334408
Main Authors:	Wang, Duo, Huang, Liuying, Qian, Danqi, Cao, Yulin, Wu, Xiaohan, Xu, Peiwen, Ming, Liang, Tang, Junhui, Huang, Zhaohui, Yin, Yuan, Zhou, Leyuan
Format:	Journal Article
Language:	English
Published:	Switzerland Frontiers Media SA 08.01.2024 Frontiers Media S.A
Subjects:	Adenocarcinoma Adenocarcinoma - radiotherapy Adenocarcinoma of Lung - radiotherapy Alcohol Animals Antibodies Antigens Antitumor activity Cancer therapies CD8 antigen Dendritic cells Disease Models, Animal Humans Immunology Immunotherapy low dose radiotherapy Lung cancer Lung Neoplasms - radiotherapy Lymphocytes T Maturation Medical prognosis Medical research Mice Optimization techniques Patients PD-1 protein Prognosis Proto-Oncogene Proteins p21(ras) - genetics Radiation therapy Risk factors Tertiary Lymphoid Structures tumor microenvironment Tumors lung cancer low dose radiotherapy tumor microenvironment immunotherapy tertiary lymphoid structures
ISSN:	1664-3224, 1664-3224
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Abstract	A tertiary lymphoid structure (TLS) refers to an organized infiltration of immune cells that is linked to a positive prognosis and improved response to immunotherapy. However, methods that promote TLS formation are limited and challenging to implement in clinical settings. In this study, we aimed to promote the formation and maturation of TLSs in lung adenocarcinoma (LUAD) by combining low-dose radiotherapy (LDRT) with immunotherapy. Tissue sections from 198 patients who had undergone surgery were examined. Risk factors for patient survival were assessed, and the relationship between TLSs and five-year survival was analyzed. The Kras-LSL-G12D spontaneous lung cancer mouse model was used to screen the optimal irradiation dose (0/1/2 Gy whole lung irradiation) for promoting TLS formation. LDRT combined with anti-PD-1 was used to promote the formation and maturation of TLSs. TLS+, TLS , TLS+GC+ and CD8 within TLS+ were associated with a favorable prognosis. LDRT increased the formation of early TLSs in the Kras-LSL-G12D lung cancer mouse model. In addition, LDRT combined with anti-PD-1 treatment can significantly improve the maturity of TLSs in mouse LUAD, resulting in greater antitumor effects. This antitumor effect was strongly associated with the number of CD8+ T cells within the TLSs. We successfully applied LDRT combined with PD-1 inhibitor therapy for the first time, which increased both the quantity and maturity of TLSs in lung cancer. This approach achieved a promising antitumor effect.
AbstractList	PurposeA tertiary lymphoid structure (TLS) refers to an organized infiltration of immune cells that is linked to a positive prognosis and improved response to immunotherapy. However, methods that promote TLS formation are limited and challenging to implement in clinical settings. In this study, we aimed to promote the formation and maturation of TLSs in lung adenocarcinoma (LUAD) by combining low-dose radiotherapy (LDRT) with immunotherapy.MethodsTissue sections from 198 patients who had undergone surgery were examined. Risk factors for patient survival were assessed, and the relationship between TLSs and five-year survival was analyzed. The Kras-LSL-G12D spontaneous lung cancer mouse model was used to screen the optimal irradiation dose (0/1/2 Gy whole lung irradiation) for promoting TLS formation. LDRT combined with anti-PD-1 was used to promote the formation and maturation of TLSs.ResultsTLS+, TLSHigh, TLS+GC+ and CD8High within TLS+ were associated with a favorable prognosis. LDRT increased the formation of early TLSs in the Kras-LSL-G12D lung cancer mouse model. In addition, LDRT combined with anti-PD-1 treatment can significantly improve the maturity of TLSs in mouse LUAD, resulting in greater antitumor effects. This antitumor effect was strongly associated with the number of CD8+ T cells within the TLSs.ConclusionWe successfully applied LDRT combined with PD-1 inhibitor therapy for the first time, which increased both the quantity and maturity of TLSs in lung cancer. This approach achieved a promising antitumor effect. A tertiary lymphoid structure (TLS) refers to an organized infiltration of immune cells that is linked to a positive prognosis and improved response to immunotherapy. However, methods that promote TLS formation are limited and challenging to implement in clinical settings. In this study, we aimed to promote the formation and maturation of TLSs in lung adenocarcinoma (LUAD) by combining low-dose radiotherapy (LDRT) with immunotherapy.PurposeA tertiary lymphoid structure (TLS) refers to an organized infiltration of immune cells that is linked to a positive prognosis and improved response to immunotherapy. However, methods that promote TLS formation are limited and challenging to implement in clinical settings. In this study, we aimed to promote the formation and maturation of TLSs in lung adenocarcinoma (LUAD) by combining low-dose radiotherapy (LDRT) with immunotherapy.Tissue sections from 198 patients who had undergone surgery were examined. Risk factors for patient survival were assessed, and the relationship between TLSs and five-year survival was analyzed. The Kras-LSL-G12D spontaneous lung cancer mouse model was used to screen the optimal irradiation dose (0/1/2 Gy whole lung irradiation) for promoting TLS formation. LDRT combined with anti-PD-1 was used to promote the formation and maturation of TLSs.MethodsTissue sections from 198 patients who had undergone surgery were examined. Risk factors for patient survival were assessed, and the relationship between TLSs and five-year survival was analyzed. The Kras-LSL-G12D spontaneous lung cancer mouse model was used to screen the optimal irradiation dose (0/1/2 Gy whole lung irradiation) for promoting TLS formation. LDRT combined with anti-PD-1 was used to promote the formation and maturation of TLSs.TLS+, TLSHigh, TLS+GC+ and CD8High within TLS+ were associated with a favorable prognosis. LDRT increased the formation of early TLSs in the Kras-LSL-G12D lung cancer mouse model. In addition, LDRT combined with anti-PD-1 treatment can significantly improve the maturity of TLSs in mouse LUAD, resulting in greater antitumor effects. This antitumor effect was strongly associated with the number of CD8+ T cells within the TLSs.ResultsTLS+, TLSHigh, TLS+GC+ and CD8High within TLS+ were associated with a favorable prognosis. LDRT increased the formation of early TLSs in the Kras-LSL-G12D lung cancer mouse model. In addition, LDRT combined with anti-PD-1 treatment can significantly improve the maturity of TLSs in mouse LUAD, resulting in greater antitumor effects. This antitumor effect was strongly associated with the number of CD8+ T cells within the TLSs.We successfully applied LDRT combined with PD-1 inhibitor therapy for the first time, which increased both the quantity and maturity of TLSs in lung cancer. This approach achieved a promising antitumor effect.ConclusionWe successfully applied LDRT combined with PD-1 inhibitor therapy for the first time, which increased both the quantity and maturity of TLSs in lung cancer. This approach achieved a promising antitumor effect. A tertiary lymphoid structure (TLS) refers to an organized infiltration of immune cells that is linked to a positive prognosis and improved response to immunotherapy. However, methods that promote TLS formation are limited and challenging to implement in clinical settings. In this study, we aimed to promote the formation and maturation of TLSs in lung adenocarcinoma (LUAD) by combining low-dose radiotherapy (LDRT) with immunotherapy. Tissue sections from 198 patients who had undergone surgery were examined. Risk factors for patient survival were assessed, and the relationship between TLSs and five-year survival was analyzed. The Kras-LSL-G12D spontaneous lung cancer mouse model was used to screen the optimal irradiation dose (0/1/2 Gy whole lung irradiation) for promoting TLS formation. LDRT combined with anti-PD-1 was used to promote the formation and maturation of TLSs. TLS+, TLS , TLS+GC+ and CD8 within TLS+ were associated with a favorable prognosis. LDRT increased the formation of early TLSs in the Kras-LSL-G12D lung cancer mouse model. In addition, LDRT combined with anti-PD-1 treatment can significantly improve the maturity of TLSs in mouse LUAD, resulting in greater antitumor effects. This antitumor effect was strongly associated with the number of CD8+ T cells within the TLSs. We successfully applied LDRT combined with PD-1 inhibitor therapy for the first time, which increased both the quantity and maturity of TLSs in lung cancer. This approach achieved a promising antitumor effect.
Author	Cao, Yulin Ming, Liang Qian, Danqi Zhou, Leyuan Wang, Duo Xu, Peiwen Wu, Xiaohan Huang, Liuying Tang, Junhui Yin, Yuan Huang, Zhaohui
AuthorAffiliation	2 Department of Radiation Oncology, Affiliated Hospital of Jiangnan University , Wuxi , China 4 State Key Laboratory of Radiation Medicine and Protection, Soochow University , Suzhou , China 3 Department of Radiation Oncology, Dushu Lake Hospital Affiliated to Soochow University , Suzhou , China 1 Wuxi Cancer Institute, Affiliated Hospital of Jiangnan University , Wuxi , China
AuthorAffiliation_xml	– name: 3 Department of Radiation Oncology, Dushu Lake Hospital Affiliated to Soochow University , Suzhou , China – name: 2 Department of Radiation Oncology, Affiliated Hospital of Jiangnan University , Wuxi , China – name: 1 Wuxi Cancer Institute, Affiliated Hospital of Jiangnan University , Wuxi , China – name: 4 State Key Laboratory of Radiation Medicine and Protection, Soochow University , Suzhou , China
Author_xml	– sequence: 1 givenname: Duo surname: Wang fullname: Wang, Duo – sequence: 2 givenname: Liuying surname: Huang fullname: Huang, Liuying – sequence: 3 givenname: Danqi surname: Qian fullname: Qian, Danqi – sequence: 4 givenname: Yulin surname: Cao fullname: Cao, Yulin – sequence: 5 givenname: Xiaohan surname: Wu fullname: Wu, Xiaohan – sequence: 6 givenname: Peiwen surname: Xu fullname: Xu, Peiwen – sequence: 7 givenname: Liang surname: Ming fullname: Ming, Liang – sequence: 8 givenname: Junhui surname: Tang fullname: Tang, Junhui – sequence: 9 givenname: Zhaohui surname: Huang fullname: Huang, Zhaohui – sequence: 10 givenname: Yuan surname: Yin fullname: Yin, Yuan – sequence: 11 givenname: Leyuan surname: Zhou fullname: Zhou, Leyuan
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Keywords	lung cancer low dose radiotherapy tumor microenvironment immunotherapy tertiary lymphoid structures
Language	English
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Edited by: Tiezheng Hou, University College London, United Kingdom Shisuo Du, Fudan University, China Minghui Cao, University of California, San Diego, United States Reviewed by: Lei Dong, Nanjing University, China Xu Zhang, Jiangsu University, China
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10.1158/1078-0432.ccr-13-2590
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Snippet	A tertiary lymphoid structure (TLS) refers to an organized infiltration of immune cells that is linked to a positive prognosis and improved response to... PurposeA tertiary lymphoid structure (TLS) refers to an organized infiltration of immune cells that is linked to a positive prognosis and improved response to...
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SubjectTerms	Adenocarcinoma Adenocarcinoma - radiotherapy Adenocarcinoma of Lung - radiotherapy Alcohol Animals Antibodies Antigens Antitumor activity Cancer therapies CD8 antigen Dendritic cells Disease Models, Animal Humans Immunology Immunotherapy low dose radiotherapy Lung cancer Lung Neoplasms - radiotherapy Lymphocytes T Maturation Medical prognosis Medical research Mice Optimization techniques Patients PD-1 protein Prognosis Proto-Oncogene Proteins p21(ras) - genetics Radiation therapy Risk factors Tertiary Lymphoid Structures tumor microenvironment Tumors
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Title	Low-dose radiotherapy promotes the formation of tertiary lymphoid structures in lung adenocarcinoma
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