Mass cytometry analysis reveals a cross-tissue immune landscape in Actinobacillus pleuropneumoniae-induced pneumonia
ABSTRACT Porcine contagious pleuropneumonia caused by Actinobacillus pleuropneumoniae (APP) is a fatal respiratory disease that threatens the worldwide farming industry’s health. The immune responses of extrapulmonary tissues play an important role in developing porcine contagious pleuropneumonia; h...
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| Language: | English |
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American Society for Microbiology
2025-06-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02665-24 |
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| author | Yanyan Tian Xuan Jiang Chuntong Bao Tamin Abdelaal Dexi Chen Wenjing Wang Fengyang Li Liancheng Lei Na Li |
| author_facet | Yanyan Tian Xuan Jiang Chuntong Bao Tamin Abdelaal Dexi Chen Wenjing Wang Fengyang Li Liancheng Lei Na Li |
| author_sort | Yanyan Tian |
| collection | DOAJ |
| description | ABSTRACT Porcine contagious pleuropneumonia caused by Actinobacillus pleuropneumoniae (APP) is a fatal respiratory disease that threatens the worldwide farming industry’s health. The immune responses of extrapulmonary tissues play an important role in developing porcine contagious pleuropneumonia; however, the immune responses of extrapulmonary tissues induced by APP are rarely uncovered. Here, we used high-dimensional mass cytometry to investigate the immune cell response in the spleen and peripheral blood during APP infection in mice. We found that the immune response triggered by APP was highly tissue-specific. Numerous infection time- or tissue-specific immune cell clusters, including previously unrecognized ones, were also identified in the spleen and peripheral blood. Integrative analysis of splenic lymphoid and myeloid cell clusters maps the dynamic immune response cellular network during APP infection. Surprisingly, during the early stages of APP infection, the majority of the top 6 cell clusters contributing to the infection time-specificity in the spleen were adaptive immune cell clusters rather than innate immune cell clusters, among which CD24hiMHCII+CD8+TEM cells exhibited a stronger expression of IFN-γ, IL-17A, and IL-10 compared to the CD24lo compartment. In peripheral blood, there was unprecedented heterogeneity in the immune cell composition. Also, peripheral immune cell clusters closely related to the severity of APP infection were identified. In summary, our data provide a systemic and comprehensive overview of the immune responses to APP infection in the spleen and peripheral blood. This provides a foundation for understanding the immune pathogenesis of APP and identifying potential diagnostic biomarkers and therapeutic targets.IMPORTANCEThis study explored the cross-tissue immune dynamic landscape in the APP-induced pneumonia model by utilizing high-dimensional mass cytometry. We discovered that APP-induced immune responses are tissue-specific. Key infection-specific clusters in the spleen and peripheral blood were identified, some of which were previously unrecognized. Meanwhile, the specific functions of APP infection-related immune subsets were explored. The research systematically outlined an overview of immune responses in these tissues, deepening the understanding of APP pathogenesis and laying the foundation for the search for diagnostic and therapeutic targets. |
| format | Article |
| id | doaj-art-d515acd0bfa84255b2bd0d27dadceea9 |
| institution | OA Journals |
| issn | 2165-0497 |
| language | English |
| publishDate | 2025-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj-art-d515acd0bfa84255b2bd0d27dadceea92025-08-20T02:05:20ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-06-0113610.1128/spectrum.02665-24Mass cytometry analysis reveals a cross-tissue immune landscape in Actinobacillus pleuropneumoniae-induced pneumoniaYanyan Tian0Xuan Jiang1Chuntong Bao2Tamin Abdelaal3Dexi Chen4Wenjing Wang5Fengyang Li6Liancheng Lei7Na Li8Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education, Institute of Zoonosis, and College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education, Institute of Zoonosis, and College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education, Institute of Zoonosis, and College of Veterinary Medicine, Jilin University, Changchun, ChinaLeiden Computational Biology Center, Leiden University Medical Center, Leiden, NetherlandsBeijing Institute of Hepatology, Beijing Youan Hospital, Capital Medical University, Beijing, Beijing, ChinaBeijing Institute of Hepatology, Beijing Youan Hospital, Capital Medical University, Beijing, Beijing, ChinaKey Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education, Institute of Zoonosis, and College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education, Institute of Zoonosis, and College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education, Institute of Zoonosis, and College of Veterinary Medicine, Jilin University, Changchun, ChinaABSTRACT Porcine contagious pleuropneumonia caused by Actinobacillus pleuropneumoniae (APP) is a fatal respiratory disease that threatens the worldwide farming industry’s health. The immune responses of extrapulmonary tissues play an important role in developing porcine contagious pleuropneumonia; however, the immune responses of extrapulmonary tissues induced by APP are rarely uncovered. Here, we used high-dimensional mass cytometry to investigate the immune cell response in the spleen and peripheral blood during APP infection in mice. We found that the immune response triggered by APP was highly tissue-specific. Numerous infection time- or tissue-specific immune cell clusters, including previously unrecognized ones, were also identified in the spleen and peripheral blood. Integrative analysis of splenic lymphoid and myeloid cell clusters maps the dynamic immune response cellular network during APP infection. Surprisingly, during the early stages of APP infection, the majority of the top 6 cell clusters contributing to the infection time-specificity in the spleen were adaptive immune cell clusters rather than innate immune cell clusters, among which CD24hiMHCII+CD8+TEM cells exhibited a stronger expression of IFN-γ, IL-17A, and IL-10 compared to the CD24lo compartment. In peripheral blood, there was unprecedented heterogeneity in the immune cell composition. Also, peripheral immune cell clusters closely related to the severity of APP infection were identified. In summary, our data provide a systemic and comprehensive overview of the immune responses to APP infection in the spleen and peripheral blood. This provides a foundation for understanding the immune pathogenesis of APP and identifying potential diagnostic biomarkers and therapeutic targets.IMPORTANCEThis study explored the cross-tissue immune dynamic landscape in the APP-induced pneumonia model by utilizing high-dimensional mass cytometry. We discovered that APP-induced immune responses are tissue-specific. Key infection-specific clusters in the spleen and peripheral blood were identified, some of which were previously unrecognized. Meanwhile, the specific functions of APP infection-related immune subsets were explored. The research systematically outlined an overview of immune responses in these tissues, deepening the understanding of APP pathogenesis and laying the foundation for the search for diagnostic and therapeutic targets.https://journals.asm.org/doi/10.1128/spectrum.02665-24Actinobacillus pleuropneumoniaeimmune cell clustersmass cytometryimmune response |
| spellingShingle | Yanyan Tian Xuan Jiang Chuntong Bao Tamin Abdelaal Dexi Chen Wenjing Wang Fengyang Li Liancheng Lei Na Li Mass cytometry analysis reveals a cross-tissue immune landscape in Actinobacillus pleuropneumoniae-induced pneumonia Microbiology Spectrum Actinobacillus pleuropneumoniae immune cell clusters mass cytometry immune response |
| title | Mass cytometry analysis reveals a cross-tissue immune landscape in Actinobacillus pleuropneumoniae-induced pneumonia |
| title_full | Mass cytometry analysis reveals a cross-tissue immune landscape in Actinobacillus pleuropneumoniae-induced pneumonia |
| title_fullStr | Mass cytometry analysis reveals a cross-tissue immune landscape in Actinobacillus pleuropneumoniae-induced pneumonia |
| title_full_unstemmed | Mass cytometry analysis reveals a cross-tissue immune landscape in Actinobacillus pleuropneumoniae-induced pneumonia |
| title_short | Mass cytometry analysis reveals a cross-tissue immune landscape in Actinobacillus pleuropneumoniae-induced pneumonia |
| title_sort | mass cytometry analysis reveals a cross tissue immune landscape in actinobacillus pleuropneumoniae induced pneumonia |
| topic | Actinobacillus pleuropneumoniae immune cell clusters mass cytometry immune response |
| url | https://journals.asm.org/doi/10.1128/spectrum.02665-24 |
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