Heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neck
IntroductionRecurrent or metastatic adenoid cystic carcinoma (ACC) of the head and neck is rare and highly aggressive. Due to the ineffectiveness of immune checkpoint therapies, this study aims to investigate the tumor immune microenvironment of primary tumor tissues and lung metastatic tissues and...
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Frontiers Media S.A.
2024-12-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1483887/full |
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| author | Xuelian Wang Xuelian Wang Tingyao Ma Hongfei Liu Shujing Zhang Guoliang Yang Yue Zhao Lu Kong Ran Gao Xiaohong Chen |
| author_facet | Xuelian Wang Xuelian Wang Tingyao Ma Hongfei Liu Shujing Zhang Guoliang Yang Yue Zhao Lu Kong Ran Gao Xiaohong Chen |
| author_sort | Xuelian Wang |
| collection | DOAJ |
| description | IntroductionRecurrent or metastatic adenoid cystic carcinoma (ACC) of the head and neck is rare and highly aggressive. Due to the ineffectiveness of immune checkpoint therapies, this study aims to investigate the tumor immune microenvironment of primary tumor tissues and lung metastatic tissues and to comprehend the challenges of immunotherapy.MethodsWe analyzed RNA sequencing data and constructed immune landscapes from 25 primary tumors and 34 lung metastases. The data were then validated by immunohistochemistry and single-cell sequencing analysis.ResultsCompared to adjacent normal tissues, both primary and lung metastatic ACC showed low immune infiltration. Lung metastases had higher immune infiltration levels and antigen presentation scores but also higher T cell exclusion and dysfunction scores. Single-cell sequencing data and immunohistochemistry revealed abundant immunosuppressive tumor-associated macrophages in lung metastases. Patients with high M2 macrophage infiltration had shorter lung metastasis-free survival. DiscussionPrimary and lung metastatic ACC exhibit heterogeneous tumor immune microenvironments. Higher immune cell infiltration in lung metastases is countered by the presence of suppressive tumor-associated macrophages, which may limit effective anti-tumor responses. |
| format | Article |
| id | doaj-art-69d8349fd46448cfa4d1fd0eff5b6996 |
| institution | OA Journals |
| issn | 1664-3224 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj-art-69d8349fd46448cfa4d1fd0eff5b69962025-08-20T02:36:03ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-12-011510.3389/fimmu.2024.14838871483887Heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neckXuelian Wang0Xuelian Wang1Tingyao Ma2Hongfei Liu3Shujing Zhang4Guoliang Yang5Yue Zhao6Lu Kong7Ran Gao8Xiaohong Chen9Department of Otolaryngology, Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, ChinaNational Human Diseases Animal Model Resource Center; State Key Laboratory of Respiratory Health and Multimorbidity, National Health Commission (NHC) Key Laboratory of Comparative Medicine, Institute of Laboratory Animal Science, Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC), Beijing, ChinaDepartment of Otolaryngology, Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, ChinaDepartment of Otolaryngology, Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, ChinaDepartment of Otolaryngology, Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, ChinaDepartment of Otolaryngology, Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, ChinaDepartment of Otolaryngology, Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, ChinaDepartment of Biochemistry and Molecular Biology, Capital Medical University, Beijing, ChinaNational Human Diseases Animal Model Resource Center; State Key Laboratory of Respiratory Health and Multimorbidity, National Health Commission (NHC) Key Laboratory of Comparative Medicine, Institute of Laboratory Animal Science, Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC), Beijing, ChinaDepartment of Otolaryngology, Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, ChinaIntroductionRecurrent or metastatic adenoid cystic carcinoma (ACC) of the head and neck is rare and highly aggressive. Due to the ineffectiveness of immune checkpoint therapies, this study aims to investigate the tumor immune microenvironment of primary tumor tissues and lung metastatic tissues and to comprehend the challenges of immunotherapy.MethodsWe analyzed RNA sequencing data and constructed immune landscapes from 25 primary tumors and 34 lung metastases. The data were then validated by immunohistochemistry and single-cell sequencing analysis.ResultsCompared to adjacent normal tissues, both primary and lung metastatic ACC showed low immune infiltration. Lung metastases had higher immune infiltration levels and antigen presentation scores but also higher T cell exclusion and dysfunction scores. Single-cell sequencing data and immunohistochemistry revealed abundant immunosuppressive tumor-associated macrophages in lung metastases. Patients with high M2 macrophage infiltration had shorter lung metastasis-free survival. DiscussionPrimary and lung metastatic ACC exhibit heterogeneous tumor immune microenvironments. Higher immune cell infiltration in lung metastases is countered by the presence of suppressive tumor-associated macrophages, which may limit effective anti-tumor responses.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1483887/fulladenoid cystic carcinomalung metastasistumor immune microenvironmenttumor-associated macrophageimmune evasion |
| spellingShingle | Xuelian Wang Xuelian Wang Tingyao Ma Hongfei Liu Shujing Zhang Guoliang Yang Yue Zhao Lu Kong Ran Gao Xiaohong Chen Heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neck Frontiers in Immunology adenoid cystic carcinoma lung metastasis tumor immune microenvironment tumor-associated macrophage immune evasion |
| title | Heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neck |
| title_full | Heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neck |
| title_fullStr | Heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neck |
| title_full_unstemmed | Heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neck |
| title_short | Heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neck |
| title_sort | heterogeneous immune landscapes and macrophage dynamics in primary and lung metastatic adenoid cystic carcinoma of the head and neck |
| topic | adenoid cystic carcinoma lung metastasis tumor immune microenvironment tumor-associated macrophage immune evasion |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1483887/full |
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