Extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammation
Abstract Extracellular vesicles (EVs) are single‐membrane vesicles that play an essential role in long‐range intercellular communications. EV investigation has been explored largely through cell‐culture systems, but it remains unclear how physiological EVs exert homeostatic or pathological functions...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Wiley
2022-05-01
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| Series: | Journal of Extracellular Vesicles |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/jev2.12223 |
| _version_ | 1818240896817168384 |
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| author | Bowen Liu Yuan Jin Jingyi Yang Yue Han Hui Shan Mantang Qiu Xuyang Zhao Anhang Liu Yan Jin Yuxin Yin |
| author_facet | Bowen Liu Yuan Jin Jingyi Yang Yue Han Hui Shan Mantang Qiu Xuyang Zhao Anhang Liu Yan Jin Yuxin Yin |
| author_sort | Bowen Liu |
| collection | DOAJ |
| description | Abstract Extracellular vesicles (EVs) are single‐membrane vesicles that play an essential role in long‐range intercellular communications. EV investigation has been explored largely through cell‐culture systems, but it remains unclear how physiological EVs exert homeostatic or pathological functions in vivo. Here, we report that lung EVs promote chemotaxis of neutrophils in bone marrow through delivery of double stranded DNA (dsDNA). We have identified and characterized EVs containing dsDNA collected from both human and murine lung tissues using newly developed approaches. Our analysis of EV proteomics together with single‐cell RNA sequencing data reveals that type II alveolar epithelial cells are the main source of the lung EVs. Furthermore, we demonstrate that the lung EVs accumulate in bone marrow and enhance neutrophil recruitment under inflammation conditions. Moreover, lung EV‐DNA stimulates neutrophils to release the chemokines CXCL1 and CXCL2 via DNA‐TLR9 signalling. Our findings establish a molecular basis of lung EVs in enhancement of host immune response to bacterial infection and provide new insights into understanding of vesicle‐mediated systematic communications. |
| first_indexed | 2024-12-12T13:20:44Z |
| format | Article |
| id | doaj.art-2cbb456d81cd4dc6bd0c9b274ed7a48b |
| institution | Directory Open Access Journal |
| issn | 2001-3078 |
| language | English |
| last_indexed | 2024-12-12T13:20:44Z |
| publishDate | 2022-05-01 |
| publisher | Wiley |
| record_format | Article |
| series | Journal of Extracellular Vesicles |
| spelling | doaj.art-2cbb456d81cd4dc6bd0c9b274ed7a48b2022-12-22T00:23:18ZengWileyJournal of Extracellular Vesicles2001-30782022-05-01115n/an/a10.1002/jev2.12223Extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammationBowen Liu0Yuan Jin1Jingyi Yang2Yue Han3Hui Shan4Mantang Qiu5Xuyang Zhao6Anhang Liu7Yan Jin8Yuxin Yin9Institute of Systems Biomedicine Department of Pathology Beijing Key Laboratory of Tumour Systems Biology School of Basic Medical Sciences Peking‐Tsinghua Center for Life Sciences Peking University Health Science Center Beijing ChinaInstitute of Systems Biomedicine Department of Pathology Beijing Key Laboratory of Tumour Systems Biology School of Basic Medical Sciences Peking‐Tsinghua Center for Life Sciences Peking University Health Science Center Beijing ChinaInstitute of Systems Biomedicine Department of Pathology Beijing Key Laboratory of Tumour Systems Biology School of Basic Medical Sciences Peking‐Tsinghua Center for Life Sciences Peking University Health Science Center Beijing ChinaInstitute of Systems Biomedicine Department of Pathology Beijing Key Laboratory of Tumour Systems Biology School of Basic Medical Sciences Peking‐Tsinghua Center for Life Sciences Peking University Health Science Center Beijing ChinaInstitute of Precision Medicine Peking University Shenzhen Hospital Shenzhen ChinaDepartment of Thoracic Surgery Peking University People's Hospital Beijing ChinaInstitute of Systems Biomedicine Department of Pathology Beijing Key Laboratory of Tumour Systems Biology School of Basic Medical Sciences Peking‐Tsinghua Center for Life Sciences Peking University Health Science Center Beijing ChinaInstitute of Systems Biomedicine Department of Pathology Beijing Key Laboratory of Tumour Systems Biology School of Basic Medical Sciences Peking‐Tsinghua Center for Life Sciences Peking University Health Science Center Beijing ChinaInstitute of Systems Biomedicine Department of Pathology Beijing Key Laboratory of Tumour Systems Biology School of Basic Medical Sciences Peking‐Tsinghua Center for Life Sciences Peking University Health Science Center Beijing ChinaInstitute of Systems Biomedicine Department of Pathology Beijing Key Laboratory of Tumour Systems Biology School of Basic Medical Sciences Peking‐Tsinghua Center for Life Sciences Peking University Health Science Center Beijing ChinaAbstract Extracellular vesicles (EVs) are single‐membrane vesicles that play an essential role in long‐range intercellular communications. EV investigation has been explored largely through cell‐culture systems, but it remains unclear how physiological EVs exert homeostatic or pathological functions in vivo. Here, we report that lung EVs promote chemotaxis of neutrophils in bone marrow through delivery of double stranded DNA (dsDNA). We have identified and characterized EVs containing dsDNA collected from both human and murine lung tissues using newly developed approaches. Our analysis of EV proteomics together with single‐cell RNA sequencing data reveals that type II alveolar epithelial cells are the main source of the lung EVs. Furthermore, we demonstrate that the lung EVs accumulate in bone marrow and enhance neutrophil recruitment under inflammation conditions. Moreover, lung EV‐DNA stimulates neutrophils to release the chemokines CXCL1 and CXCL2 via DNA‐TLR9 signalling. Our findings establish a molecular basis of lung EVs in enhancement of host immune response to bacterial infection and provide new insights into understanding of vesicle‐mediated systematic communications.https://doi.org/10.1002/jev2.12223dsDNAlung EVsneutrophil chemotaxis |
| spellingShingle | Bowen Liu Yuan Jin Jingyi Yang Yue Han Hui Shan Mantang Qiu Xuyang Zhao Anhang Liu Yan Jin Yuxin Yin Extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammation Journal of Extracellular Vesicles dsDNA lung EVs neutrophil chemotaxis |
| title | Extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammation |
| title_full | Extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammation |
| title_fullStr | Extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammation |
| title_full_unstemmed | Extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammation |
| title_short | Extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammation |
| title_sort | extracellular vesicles from lung tissue drive bone marrow neutrophil recruitment in inflammation |
| topic | dsDNA lung EVs neutrophil chemotaxis |
| url | https://doi.org/10.1002/jev2.12223 |
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