Comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin CD11b as a regulatory hub during pneumococcal pneumonia infection
IntroductionStreptococcus pneumoniae is one of the main causes of community-acquired infections in the lung alveoli in children and the elderly. Alveolar macrophages (AM) patrol alveoli in homeostasis and under infectious conditions. However, the molecular adaptations of AM upon infections with Stre...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1227191/full |
| _version_ | 1797681844279312384 |
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| author | Kristina Zec Kristina Zec Stephanie Thiebes Jenny Bottek Devon Siemes Philippa Spangenberg Duc Viet Trieu Nils Kirstein Nirojah Subramaniam Robin Christ Diana Klein Verena Jendrossek Maria Loose Florian Wagenlehner Jadwiga Jablonska Thilo Bracht Thilo Bracht Barbara Sitek Barbara Sitek Bettina Budeus Ludger Klein-Hitpass Dirk Theegarten Olga Shevchuk Daniel R. Engel |
| author_facet | Kristina Zec Kristina Zec Stephanie Thiebes Jenny Bottek Devon Siemes Philippa Spangenberg Duc Viet Trieu Nils Kirstein Nirojah Subramaniam Robin Christ Diana Klein Verena Jendrossek Maria Loose Florian Wagenlehner Jadwiga Jablonska Thilo Bracht Thilo Bracht Barbara Sitek Barbara Sitek Bettina Budeus Ludger Klein-Hitpass Dirk Theegarten Olga Shevchuk Daniel R. Engel |
| author_sort | Kristina Zec |
| collection | DOAJ |
| description | IntroductionStreptococcus pneumoniae is one of the main causes of community-acquired infections in the lung alveoli in children and the elderly. Alveolar macrophages (AM) patrol alveoli in homeostasis and under infectious conditions. However, the molecular adaptations of AM upon infections with Streptococcus pneumoniae are incompletely resolved.MethodsWe used a comparative transcriptomic and proteomic approach to provide novel insights into the cellular mechanism that changes the molecular signature of AM during lung infections. Using a tandem mass spectrometry approach to murine cell-sorted AM, we revealed significant proteomic changes upon lung infection with Streptococcus pneumoniae.ResultsAM showed a strong neutrophil-associated proteomic signature, such as expression of CD11b, MPO, neutrophil gelatinases, and elastases, which was associated with phagocytosis of recruited neutrophils. Transcriptomic analysis indicated intrinsic expression of CD11b by AM. Moreover, comparative transcriptomic and proteomic profiling identified CD11b as the central molecular hub in AM, which influenced neutrophil recruitment, activation, and migration.DiscussionIn conclusion, our study provides novel insights into the intrinsic molecular adaptations of AM upon lung infection with Streptococcus pneumoniae and reveals profound alterations critical for effective antimicrobial immunity. |
| first_indexed | 2024-03-11T23:50:54Z |
| format | Article |
| id | doaj.art-23d3fe4f1c024fdb82b614f980d5c4d4 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-11T23:50:54Z |
| publishDate | 2023-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-23d3fe4f1c024fdb82b614f980d5c4d42023-09-19T07:08:08ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-09-011410.3389/fimmu.2023.12271911227191Comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin CD11b as a regulatory hub during pneumococcal pneumonia infectionKristina Zec0Kristina Zec1Stephanie Thiebes2Jenny Bottek3Devon Siemes4Philippa Spangenberg5Duc Viet Trieu6Nils Kirstein7Nirojah Subramaniam8Robin Christ9Diana Klein10Verena Jendrossek11Maria Loose12Florian Wagenlehner13Jadwiga Jablonska14Thilo Bracht15Thilo Bracht16Barbara Sitek17Barbara Sitek18Bettina Budeus19Ludger Klein-Hitpass20Dirk Theegarten21Olga Shevchuk22Daniel R. Engel23Institute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyKennedy Institute of Rheumatology, University of Oxford, Oxford, United KingdomInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Cell Biology (Cancer Research), University Hospital Essen, Essen, GermanyInstitute for Cell Biology (Cancer Research), University Hospital Essen, Essen, GermanyClinic for Urology, Paediatric Urology and Andrology, Justus-Liebig University of Giessen, Giessen, GermanyClinic for Urology, Paediatric Urology and Andrology, Justus-Liebig University of Giessen, Giessen, GermanyDepartment of Otorhinolaryngology, University Hospital Essen, University Duisburg-Essen, Essen, GermanyMedical Faculty, Medizinisches Proteom‐Center, Ruhr‐University Bochum, Bochum, GermanyClinic for Anesthesiology, Intensive Care Medicine and Pain Therapy, University Hospital Knappschafts-krankenhaus Bochum, Bochum, GermanyMedical Faculty, Medizinisches Proteom‐Center, Ruhr‐University Bochum, Bochum, GermanyClinic for Anesthesiology, Intensive Care Medicine and Pain Therapy, University Hospital Knappschafts-krankenhaus Bochum, Bochum, GermanyInstitute of Cell Biology (Cancer Research), Faculty of Medicine, University of Duisburg-Essen, Essen, GermanyInstitute of Cell Biology (Cancer Research), Faculty of Medicine, University of Duisburg-Essen, Essen, GermanyInstitute of Pathology, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyInstitute for Experimental Immunology and Imaging, Department of Immunodynamics, University Hospital Essen, Essen, GermanyIntroductionStreptococcus pneumoniae is one of the main causes of community-acquired infections in the lung alveoli in children and the elderly. Alveolar macrophages (AM) patrol alveoli in homeostasis and under infectious conditions. However, the molecular adaptations of AM upon infections with Streptococcus pneumoniae are incompletely resolved.MethodsWe used a comparative transcriptomic and proteomic approach to provide novel insights into the cellular mechanism that changes the molecular signature of AM during lung infections. Using a tandem mass spectrometry approach to murine cell-sorted AM, we revealed significant proteomic changes upon lung infection with Streptococcus pneumoniae.ResultsAM showed a strong neutrophil-associated proteomic signature, such as expression of CD11b, MPO, neutrophil gelatinases, and elastases, which was associated with phagocytosis of recruited neutrophils. Transcriptomic analysis indicated intrinsic expression of CD11b by AM. Moreover, comparative transcriptomic and proteomic profiling identified CD11b as the central molecular hub in AM, which influenced neutrophil recruitment, activation, and migration.DiscussionIn conclusion, our study provides novel insights into the intrinsic molecular adaptations of AM upon lung infection with Streptococcus pneumoniae and reveals profound alterations critical for effective antimicrobial immunity.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1227191/fullalveolar macrophageproteomicsbioinformaticstranscriptomicsinfection |
| spellingShingle | Kristina Zec Kristina Zec Stephanie Thiebes Jenny Bottek Devon Siemes Philippa Spangenberg Duc Viet Trieu Nils Kirstein Nirojah Subramaniam Robin Christ Diana Klein Verena Jendrossek Maria Loose Florian Wagenlehner Jadwiga Jablonska Thilo Bracht Thilo Bracht Barbara Sitek Barbara Sitek Bettina Budeus Ludger Klein-Hitpass Dirk Theegarten Olga Shevchuk Daniel R. Engel Comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin CD11b as a regulatory hub during pneumococcal pneumonia infection Frontiers in Immunology alveolar macrophage proteomics bioinformatics transcriptomics infection |
| title | Comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin CD11b as a regulatory hub during pneumococcal pneumonia infection |
| title_full | Comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin CD11b as a regulatory hub during pneumococcal pneumonia infection |
| title_fullStr | Comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin CD11b as a regulatory hub during pneumococcal pneumonia infection |
| title_full_unstemmed | Comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin CD11b as a regulatory hub during pneumococcal pneumonia infection |
| title_short | Comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin CD11b as a regulatory hub during pneumococcal pneumonia infection |
| title_sort | comparative transcriptomic and proteomic signature of lung alveolar macrophages reveals the integrin cd11b as a regulatory hub during pneumococcal pneumonia infection |
| topic | alveolar macrophage proteomics bioinformatics transcriptomics infection |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1227191/full |
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