Impact of bronchoalveolar lavage from influenza A virus diseased pigs on neutrophil functions and growth of co-infecting pathogenic bacteria
IntroductionInfluenza A viruses (IAVs) infect the respiratory tract of mainly humans, poultry, and pigs. Co-infections with pathogenic lung bacteria are a common event and contribute to the severity of disease progression. Neutrophils are a major cell type of the innate immune system and are rapidly...
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| Format: | Article |
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Frontiers Media S.A.
2024-02-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1325269/full |
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| author | Simon Lassnig Simon Lassnig Isabel Hennig-Pauka Isabel Hennig-Pauka Marta C. Bonilla Marta C. Bonilla Matthias Mörgelin Rabea Imker Rabea Imker Maren von Köckritz-Blickwede Maren von Köckritz-Blickwede Nicole de Buhr Nicole de Buhr |
| author_facet | Simon Lassnig Simon Lassnig Isabel Hennig-Pauka Isabel Hennig-Pauka Marta C. Bonilla Marta C. Bonilla Matthias Mörgelin Rabea Imker Rabea Imker Maren von Köckritz-Blickwede Maren von Köckritz-Blickwede Nicole de Buhr Nicole de Buhr |
| author_sort | Simon Lassnig |
| collection | DOAJ |
| description | IntroductionInfluenza A viruses (IAVs) infect the respiratory tract of mainly humans, poultry, and pigs. Co-infections with pathogenic lung bacteria are a common event and contribute to the severity of disease progression. Neutrophils are a major cell type of the innate immune system and are rapidly recruited to the site of infection. They have several effector functions to fight invading pathogens such as the secretion of reactive oxygen species (ROS) or the release of neutrophil extracellular traps (NETs). NETs are known to promote the growth of Pasteurellaceae bacteria, especially if degraded by nucleases.MethodsIn this study, bronchoalveolar lavage fluid (BALF) from 45 field-infected pigs was analyzed for 1) NET markers, 2) influence on growth of lung bacteria, and 3) impact on neutrophil functions. BALF samples from 21 IAV-positive pigs and 24 lung diseased but IAV-negative pigs were compared.ResultsHere, we show that neutrophils in the lungs of IAV-positive pigs release vesicular NETs. Several NET markers were increased in the BALF of IAV-positive pigs compared with the BALF from IAV-negative pigs. The amount of NET markers positively correlated with the viral load of the IAV infection. Interestingly, the BALF of IAV-positive pigs enhanced the growth of bacteria belonging to the family of Pasteurellaceae as potential coinfecting bacteria. These effects were weaker with the BALF derived from IAV-negative pigs with other lung infections. The intensity of oxidative burst in neutrophils was significantly decreased by BALF from IAVpositive pigs, indicating impaired antimicrobial activity of neutrophils. Finally, the lung milieu reflected by IAV-positive BALF does not enable neutrophils to kill Actinobacillus pleuropneumoniae but rather enhances its growth.DiscussionIn summary, our data show that an IAV infection is affecting neutrophil functions, in particular the release of NETs and ROS. Furthermore, IAV infection seems to provide growth-enhancing factors for especially coinfecting Pasteurellaceae and reduces the killing efficiency of neutrophils. |
| first_indexed | 2024-03-07T23:26:09Z |
| format | Article |
| id | doaj.art-d81fb64c6feb458184c9dd54d4c7dcbb |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-07T23:26:09Z |
| publishDate | 2024-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj.art-d81fb64c6feb458184c9dd54d4c7dcbb2024-02-21T04:32:49ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-02-011510.3389/fimmu.2024.13252691325269Impact of bronchoalveolar lavage from influenza A virus diseased pigs on neutrophil functions and growth of co-infecting pathogenic bacteriaSimon Lassnig0Simon Lassnig1Isabel Hennig-Pauka2Isabel Hennig-Pauka3Marta C. Bonilla4Marta C. Bonilla5Matthias Mörgelin6Rabea Imker7Rabea Imker8Maren von Köckritz-Blickwede9Maren von Köckritz-Blickwede10Nicole de Buhr11Nicole de Buhr12Institute of Biochemistry, University of Veterinary Medicine Hannover, Hannover, GermanyResearch Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, GermanyClinic for Swine, Small Ruminants, Forensic Medicine and Ambulatory Service, University of Veterinary Medicine Hannover, Hannover, GermanyField Station for Epidemiology, University of Veterinary Medicine Hannover, Bakum, GermanyInstitute of Biochemistry, University of Veterinary Medicine Hannover, Hannover, GermanyResearch Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, GermanyColzyx AB, Medicon Village, Lund, SwedenInstitute of Biochemistry, University of Veterinary Medicine Hannover, Hannover, GermanyResearch Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, GermanyInstitute of Biochemistry, University of Veterinary Medicine Hannover, Hannover, GermanyResearch Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, GermanyInstitute of Biochemistry, University of Veterinary Medicine Hannover, Hannover, GermanyResearch Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, GermanyIntroductionInfluenza A viruses (IAVs) infect the respiratory tract of mainly humans, poultry, and pigs. Co-infections with pathogenic lung bacteria are a common event and contribute to the severity of disease progression. Neutrophils are a major cell type of the innate immune system and are rapidly recruited to the site of infection. They have several effector functions to fight invading pathogens such as the secretion of reactive oxygen species (ROS) or the release of neutrophil extracellular traps (NETs). NETs are known to promote the growth of Pasteurellaceae bacteria, especially if degraded by nucleases.MethodsIn this study, bronchoalveolar lavage fluid (BALF) from 45 field-infected pigs was analyzed for 1) NET markers, 2) influence on growth of lung bacteria, and 3) impact on neutrophil functions. BALF samples from 21 IAV-positive pigs and 24 lung diseased but IAV-negative pigs were compared.ResultsHere, we show that neutrophils in the lungs of IAV-positive pigs release vesicular NETs. Several NET markers were increased in the BALF of IAV-positive pigs compared with the BALF from IAV-negative pigs. The amount of NET markers positively correlated with the viral load of the IAV infection. Interestingly, the BALF of IAV-positive pigs enhanced the growth of bacteria belonging to the family of Pasteurellaceae as potential coinfecting bacteria. These effects were weaker with the BALF derived from IAV-negative pigs with other lung infections. The intensity of oxidative burst in neutrophils was significantly decreased by BALF from IAVpositive pigs, indicating impaired antimicrobial activity of neutrophils. Finally, the lung milieu reflected by IAV-positive BALF does not enable neutrophils to kill Actinobacillus pleuropneumoniae but rather enhances its growth.DiscussionIn summary, our data show that an IAV infection is affecting neutrophil functions, in particular the release of NETs and ROS. Furthermore, IAV infection seems to provide growth-enhancing factors for especially coinfecting Pasteurellaceae and reduces the killing efficiency of neutrophils.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1325269/fullinfluenza A virusPasteurellaceaeneutrophil extracellular trapspigsco-infectionlung |
| spellingShingle | Simon Lassnig Simon Lassnig Isabel Hennig-Pauka Isabel Hennig-Pauka Marta C. Bonilla Marta C. Bonilla Matthias Mörgelin Rabea Imker Rabea Imker Maren von Köckritz-Blickwede Maren von Köckritz-Blickwede Nicole de Buhr Nicole de Buhr Impact of bronchoalveolar lavage from influenza A virus diseased pigs on neutrophil functions and growth of co-infecting pathogenic bacteria Frontiers in Immunology influenza A virus Pasteurellaceae neutrophil extracellular traps pigs co-infection lung |
| title | Impact of bronchoalveolar lavage from influenza A virus diseased pigs on neutrophil functions and growth of co-infecting pathogenic bacteria |
| title_full | Impact of bronchoalveolar lavage from influenza A virus diseased pigs on neutrophil functions and growth of co-infecting pathogenic bacteria |
| title_fullStr | Impact of bronchoalveolar lavage from influenza A virus diseased pigs on neutrophil functions and growth of co-infecting pathogenic bacteria |
| title_full_unstemmed | Impact of bronchoalveolar lavage from influenza A virus diseased pigs on neutrophil functions and growth of co-infecting pathogenic bacteria |
| title_short | Impact of bronchoalveolar lavage from influenza A virus diseased pigs on neutrophil functions and growth of co-infecting pathogenic bacteria |
| title_sort | impact of bronchoalveolar lavage from influenza a virus diseased pigs on neutrophil functions and growth of co infecting pathogenic bacteria |
| topic | influenza A virus Pasteurellaceae neutrophil extracellular traps pigs co-infection lung |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1325269/full |
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