CD47-mediated immune evasion in early-stage lung cancer progression
Alveolar and interstitial macrophages play crucial roles in eradicating pathogens and transformed cells in the lungs. The immune checkpoint CD47, found on normal and malignant cells, interacts with the SIRPα ligand on macrophages, inhibiting phagocytosis, antigen presentation, and promoting immune e...
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| Published in | Biochemical and biophysical research communications Vol. 720; p. 150066 |
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| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
06.08.2024
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Alveolar and interstitial macrophages play crucial roles in eradicating pathogens and transformed cells in the lungs. The immune checkpoint CD47, found on normal and malignant cells, interacts with the SIRPα ligand on macrophages, inhibiting phagocytosis, antigen presentation, and promoting immune evasion. In this study, we demonstrated that CD47 is not only a transmembrane protein, but that it is also highly concentrated in extracellular vesicles from lung cancer cell lines and patient plasma. Abundant CD47 was observed in the cytoplasm of lung cancer cells, aligning with our finding that it was packed into extracellular vesicles for physiological and pathological functions. In our clinical cohort, extracellular vesicle CD47 was significantly higher in the patients with early-stage lung cancer, emphasizing innate immunity inactivation in early tumor progression. To validate our hypothesis, we established an orthotopic xenograft model mimicking lung cancer development, which showed increased serum soluble CD47 and elevated IL-10/TNF-α ratio, indicating an immune-suppressive tumor microenvironment. CD47 expression led to reduced tumor-infiltrating macrophages during progression, while there was a post-xenograft increase in tumor-associated macrophages. In conclusion, CD47 is pivotal in early lung cancer progression, with soluble CD47 emerging as a key pathological effector.
•The CD47 immune checkpoint plays a critical role in immune evasion during the early stages of lung cancer.•CD47 exhibits high concentrations in extracellular vesicles, both in vitro and in vivo.•Elevated ratios of serum IL-10 to TNF-α and increased CD47 expression, identified in our orthotopic xenograft animal model, contribute to the promotion of tumor growth.•The interplay with CD47 in vivo is recognized to suppress tumor-infiltrating macrophages while concurrently increasing tumor-associated macrophages. |
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| AbstractList | Alveolar and interstitial macrophages play crucial roles in eradicating pathogens and transformed cells in the lungs. The immune checkpoint CD47, found on normal and malignant cells, interacts with the SIRPα ligand on macrophages, inhibiting phagocytosis, antigen presentation, and promoting immune evasion. In this study, we demonstrated that CD47 is not only a transmembrane protein, but that it is also highly concentrated in extracellular vesicles from lung cancer cell lines and patient plasma. Abundant CD47 was observed in the cytoplasm of lung cancer cells, aligning with our finding that it was packed into extracellular vesicles for physiological and pathological functions. In our clinical cohort, extracellular vesicle CD47 was significantly higher in the patients with early-stage lung cancer, emphasizing innate immunity inactivation in early tumor progression. To validate our hypothesis, we established an orthotopic xenograft model mimicking lung cancer development, which showed increased serum soluble CD47 and elevated IL-10/TNF-α ratio, indicating an immune-suppressive tumor microenvironment. CD47 expression led to reduced tumor-infiltrating macrophages during progression, while there was a post-xenograft increase in tumor-associated macrophages. In conclusion, CD47 is pivotal in early lung cancer progression, with soluble CD47 emerging as a key pathological effector.
•The CD47 immune checkpoint plays a critical role in immune evasion during the early stages of lung cancer.•CD47 exhibits high concentrations in extracellular vesicles, both in vitro and in vivo.•Elevated ratios of serum IL-10 to TNF-α and increased CD47 expression, identified in our orthotopic xenograft animal model, contribute to the promotion of tumor growth.•The interplay with CD47 in vivo is recognized to suppress tumor-infiltrating macrophages while concurrently increasing tumor-associated macrophages. Alveolar and interstitial macrophages play crucial roles in eradicating pathogens and transformed cells in the lungs. The immune checkpoint CD47, found on normal and malignant cells, interacts with the SIRPα ligand on macrophages, inhibiting phagocytosis, antigen presentation, and promoting immune evasion. In this study, we demonstrated that CD47 is not only a transmembrane protein, but that it is also highly concentrated in extracellular vesicles from lung cancer cell lines and patient plasma. Abundant CD47 was observed in the cytoplasm of lung cancer cells, aligning with our finding that it was packed into extracellular vesicles for physiological and pathological functions. In our clinical cohort, extracellular vesicle CD47 was significantly higher in the patients with early-stage lung cancer, emphasizing innate immunity inactivation in early tumor progression. To validate our hypothesis, we established an orthotopic xenograft model mimicking lung cancer development, which showed increased serum soluble CD47 and elevated IL-10/TNF-α ratio, indicating an immune-suppressive tumor microenvironment. CD47 expression led to reduced tumor-infiltrating macrophages during progression, while there was a post-xenograft increase in tumor-associated macrophages. In conclusion, CD47 is pivotal in early lung cancer progression, with soluble CD47 emerging as a key pathological effector. Alveolar and interstitial macrophages play crucial roles in eradicating pathogens and transformed cells in the lungs. The immune checkpoint CD47, found on normal and malignant cells, interacts with the SIRPα ligand on macrophages, inhibiting phagocytosis, antigen presentation, and promoting immune evasion. In this study, we demonstrated that CD47 is not only a transmembrane protein, but that it is also highly concentrated in extracellular vesicles from lung cancer cell lines and patient plasma. Abundant CD47 was observed in the cytoplasm of lung cancer cells, aligning with our finding that it was packed into extracellular vesicles for physiological and pathological functions. In our clinical cohort, extracellular vesicle CD47 was significantly higher in the patients with early-stage lung cancer, emphasizing innate immunity inactivation in early tumor progression. To validate our hypothesis, we established an orthotopic xenograft model mimicking lung cancer development, which showed increased serum soluble CD47 and elevated IL-10/TNF-α ratio, indicating an immune-suppressive tumor microenvironment. CD47 expression led to reduced tumor-infiltrating macrophages during progression, while there was a post-xenograft increase in tumor-associated macrophages. In conclusion, CD47 is pivotal in early lung cancer progression, with soluble CD47 emerging as a key pathological effector.Alveolar and interstitial macrophages play crucial roles in eradicating pathogens and transformed cells in the lungs. The immune checkpoint CD47, found on normal and malignant cells, interacts with the SIRPα ligand on macrophages, inhibiting phagocytosis, antigen presentation, and promoting immune evasion. In this study, we demonstrated that CD47 is not only a transmembrane protein, but that it is also highly concentrated in extracellular vesicles from lung cancer cell lines and patient plasma. Abundant CD47 was observed in the cytoplasm of lung cancer cells, aligning with our finding that it was packed into extracellular vesicles for physiological and pathological functions. In our clinical cohort, extracellular vesicle CD47 was significantly higher in the patients with early-stage lung cancer, emphasizing innate immunity inactivation in early tumor progression. To validate our hypothesis, we established an orthotopic xenograft model mimicking lung cancer development, which showed increased serum soluble CD47 and elevated IL-10/TNF-α ratio, indicating an immune-suppressive tumor microenvironment. CD47 expression led to reduced tumor-infiltrating macrophages during progression, while there was a post-xenograft increase in tumor-associated macrophages. In conclusion, CD47 is pivotal in early lung cancer progression, with soluble CD47 emerging as a key pathological effector. |
| ArticleNumber | 150066 |
| Author | Chang, Yu-Chan Wu, Chun-Chieh Hung, Huei-Yang Yang, Chih-Jen Huang, Chi-Ying F. Lee, Tai-Huang Huang, Ming-Shyan Hsiao, Michael Wang, Pei-Hui Lee, Ying-Ray Ma, Juei-Yang Zhen, Yen-Yi Huang, Ching-Tang Chuang, Cheng-Hao |
| Author_xml | – sequence: 1 givenname: Cheng-Hao orcidid: 0000-0003-4239-4012 surname: Chuang fullname: Chuang, Cheng-Hao organization: Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan – sequence: 2 givenname: Yen-Yi surname: Zhen fullname: Zhen, Yen-Yi organization: Division of Nephrology, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan – sequence: 3 givenname: Juei-Yang surname: Ma fullname: Ma, Juei-Yang organization: Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan – sequence: 4 givenname: Tai-Huang surname: Lee fullname: Lee, Tai-Huang organization: Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan – sequence: 5 givenname: Huei-Yang surname: Hung fullname: Hung, Huei-Yang organization: Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan – sequence: 6 givenname: Chun-Chieh surname: Wu fullname: Wu, Chun-Chieh organization: Department of Pathology, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan – sequence: 7 givenname: Pei-Hui surname: Wang fullname: Wang, Pei-Hui organization: Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan – sequence: 8 givenname: Ching-Tang surname: Huang fullname: Huang, Ching-Tang organization: Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan – sequence: 9 givenname: Ming-Shyan surname: Huang fullname: Huang, Ming-Shyan organization: Department of Internal Medicine, E-Da Cancer Hospital, School of Medicine, I-Shou University, Kaohsiung, 82445, Taiwan – sequence: 10 givenname: Michael surname: Hsiao fullname: Hsiao, Michael organization: Genomics Research Center, Academia Sinica, Taiwan – sequence: 11 givenname: Ying-Ray surname: Lee fullname: Lee, Ying-Ray organization: Department of Microbiology and Immunology, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan – sequence: 12 givenname: Chi-Ying F. orcidid: 0000-0003-4898-4937 surname: Huang fullname: Huang, Chi-Ying F. organization: Institute of Biopharmaceutical Sciences, National Yang Ming Chiao Tung University, Taipei, Taiwan – sequence: 13 givenname: Yu-Chan surname: Chang fullname: Chang, Yu-Chan organization: Department of Biomedical Imaging and Radiological Sciences, National Yang Ming Chiao Tung University, Taipei, Taiwan – sequence: 14 givenname: Chih-Jen surname: Yang fullname: Yang, Chih-Jen email: chjeya@cc.kmu.edu.tw organization: Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan |
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| Keywords | Extracellular vesicles Immune checkpoint Immune evasion Tumor microenvironment Macrophage |
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| SubjectTerms | Animals antigen presentation blood serum carcinogenesis CD47 Antigen - immunology CD47 Antigen - metabolism Cell Line, Tumor cytoplasm Disease Progression Extracellular vesicles Extracellular Vesicles - immunology Extracellular Vesicles - metabolism Female Humans Immune checkpoint Immune Evasion ligands lung neoplasms Lung Neoplasms - immunology Lung Neoplasms - pathology Macrophage macrophages Macrophages - immunology Macrophages - metabolism Mice neoplasm cells neoplasm progression Neoplasm Staging patients phagocytosis transmembrane proteins Tumor Escape Tumor microenvironment Tumor Microenvironment - immunology xenotransplantation |
| Title | CD47-mediated immune evasion in early-stage lung cancer progression |
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