Microbiota Promotes Chronic Pulmonary Inflammation by Enhancing IL-17A and Autoantibodies

Changes in the pulmonary microbiota are associated with progressive respiratory diseases including chronic obstructive pulmonary disease (COPD). Whether there is a causal relationship between these changes and disease progression remains unknown. To investigate the link between an altered microbiota...

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Vydané v:	American journal of respiratory and critical care medicine Ročník 193; číslo 9; s. 975 - 987
Hlavní autori:	Yadava, Koshika, Pattaroni, Céline, Sichelstiel, Anke K., Trompette, Aurélien, Gollwitzer, Eva S., Salami, Olawale, von Garnier, Christophe, Nicod, Laurent P., Marsland, Benjamin J.
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States American Thoracic Society 01.05.2016
Predmet:	Animals Autoantibodies - immunology Disease Models, Animal Inflammation - complications Inflammation - immunology Inflammation - physiopathology Interleukin-17 - immunology Lung - immunology Lung - physiopathology Mice Mice, Inbred BALB C Microbiota Pulmonary Disease, Chronic Obstructive - complications Pulmonary Disease, Chronic Obstructive - immunology Pulmonary Disease, Chronic Obstructive - physiopathology microbiome; COPD; autoimmunity; IL-17
ISSN:	1073-449X, 1535-4970
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Abstract	Changes in the pulmonary microbiota are associated with progressive respiratory diseases including chronic obstructive pulmonary disease (COPD). Whether there is a causal relationship between these changes and disease progression remains unknown. To investigate the link between an altered microbiota and disease, we used a murine model of chronic lung inflammation that is characterized by key pathological features found in COPD and compared responses in specific pathogen-free (SPF) mice and mice depleted of microbiota by antibiotic treatment or devoid of a microbiota (axenic). Mice were challenged with LPS/elastase intranasally over 4 weeks, resulting in a chronically inflamed and damaged lung. The ensuing cellular infiltration, histological damage, and decline in lung function were quantified. Similar to human disease, the composition of the pulmonary microbiota was altered in diseased animals. We found that the microbiota richness and diversity were decreased in LPS/elastase-treated mice, with an increased representation of the genera Pseudomonas and Lactobacillus and a reduction in Prevotella. Moreover, the microbiota was implicated in disease development as mice depleted, or devoid, of microbiota exhibited an improvement in lung function, reduced inflammation, and lymphoid neogenesis. The absence of microbial cues markedly decreased the production of IL-17A, whereas intranasal transfer of fluid enriched with the pulmonary microbiota isolated from diseased mice enhanced IL-17A production in the lungs of antibiotic-treated or axenic recipients. Finally, in mice harboring a microbiota, neutralizing IL-17A dampened inflammation and restored lung function. Collectively, our data indicate that host-microbial cross-talk promotes inflammation and could underlie the chronicity of inflammatory lung diseases.
AbstractList	RATIONALEChanges in the pulmonary microbiota are associated with progressive respiratory diseases including chronic obstructive pulmonary disease (COPD). Whether there is a causal relationship between these changes and disease progression remains unknown.OBJECTIVESTo investigate the link between an altered microbiota and disease, we used a murine model of chronic lung inflammation that is characterized by key pathological features found in COPD and compared responses in specific pathogen-free (SPF) mice and mice depleted of microbiota by antibiotic treatment or devoid of a microbiota (axenic).METHODSMice were challenged with LPS/elastase intranasally over 4 weeks, resulting in a chronically inflamed and damaged lung. The ensuing cellular infiltration, histological damage, and decline in lung function were quantified.MEASUREMENTS AND MAIN RESULTSSimilar to human disease, the composition of the pulmonary microbiota was altered in diseased animals. We found that the microbiota richness and diversity were decreased in LPS/elastase-treated mice, with an increased representation of the genera Pseudomonas and Lactobacillus and a reduction in Prevotella. Moreover, the microbiota was implicated in disease development as mice depleted, or devoid, of microbiota exhibited an improvement in lung function, reduced inflammation, and lymphoid neogenesis. The absence of microbial cues markedly decreased the production of IL-17A, whereas intranasal transfer of fluid enriched with the pulmonary microbiota isolated from diseased mice enhanced IL-17A production in the lungs of antibiotic-treated or axenic recipients. Finally, in mice harboring a microbiota, neutralizing IL-17A dampened inflammation and restored lung function.CONCLUSIONSCollectively, our data indicate that host-microbial cross-talk promotes inflammation and could underlie the chronicity of inflammatory lung diseases. Changes in the pulmonary microbiota are associated with progressive respiratory diseases including chronic obstructive pulmonary disease (COPD). Whether there is a causal relationship between these changes and disease progression remains unknown. To investigate the link between an altered microbiota and disease, we used a murine model of chronic lung inflammation that is characterized by key pathological features found in COPD and compared responses in specific pathogen-free (SPF) mice and mice depleted of microbiota by antibiotic treatment or devoid of a microbiota (axenic). Mice were challenged with LPS/elastase intranasally over 4 weeks, resulting in a chronically inflamed and damaged lung. The ensuing cellular infiltration, histological damage, and decline in lung function were quantified. Similar to human disease, the composition of the pulmonary microbiota was altered in diseased animals. We found that the microbiota richness and diversity were decreased in LPS/elastase-treated mice, with an increased representation of the genera Pseudomonas and Lactobacillus and a reduction in Prevotella. Moreover, the microbiota was implicated in disease development as mice depleted, or devoid, of microbiota exhibited an improvement in lung function, reduced inflammation, and lymphoid neogenesis. The absence of microbial cues markedly decreased the production of IL-17A, whereas intranasal transfer of fluid enriched with the pulmonary microbiota isolated from diseased mice enhanced IL-17A production in the lungs of antibiotic-treated or axenic recipients. Finally, in mice harboring a microbiota, neutralizing IL-17A dampened inflammation and restored lung function. Collectively, our data indicate that host-microbial cross-talk promotes inflammation and could underlie the chronicity of inflammatory lung diseases.
Author	Pattaroni, Céline Trompette, Aurélien Salami, Olawale Sichelstiel, Anke K. Nicod, Laurent P. Marsland, Benjamin J. Yadava, Koshika Gollwitzer, Eva S. von Garnier, Christophe
Author_xml	– sequence: 1 givenname: Koshika surname: Yadava fullname: Yadava, Koshika organization: Service de Pneumologie, Faculté de Biologie et de Médecine, Centre Hospitalier Universitaire Vaudoise–Université Lausanne Lausanne, Switzerland, Division of Infectious Diseases, Department of Medicine, Stanford University School of Medicine, Stanford, California – sequence: 2 givenname: Céline surname: Pattaroni fullname: Pattaroni, Céline organization: Service de Pneumologie, Faculté de Biologie et de Médecine, Centre Hospitalier Universitaire Vaudoise–Université Lausanne Lausanne, Switzerland – sequence: 3 givenname: Anke K. surname: Sichelstiel fullname: Sichelstiel, Anke K. organization: Service de Pneumologie, Faculté de Biologie et de Médecine, Centre Hospitalier Universitaire Vaudoise–Université Lausanne Lausanne, Switzerland – sequence: 4 givenname: Aurélien surname: Trompette fullname: Trompette, Aurélien organization: Service de Pneumologie, Faculté de Biologie et de Médecine, Centre Hospitalier Universitaire Vaudoise–Université Lausanne Lausanne, Switzerland – sequence: 5 givenname: Eva S. surname: Gollwitzer fullname: Gollwitzer, Eva S. organization: Service de Pneumologie, Faculté de Biologie et de Médecine, Centre Hospitalier Universitaire Vaudoise–Université Lausanne Lausanne, Switzerland – sequence: 6 givenname: Olawale surname: Salami fullname: Salami, Olawale organization: Service de Pneumologie, Faculté de Biologie et de Médecine, Centre Hospitalier Universitaire Vaudoise–Université Lausanne Lausanne, Switzerland – sequence: 7 givenname: Christophe surname: von Garnier fullname: von Garnier, Christophe organization: Department of Respiratory Medicine, Inselspital, Bern University Hospital, Bern, Switzerland; and, Department of Clinical Research, University of Bern, Bern, Switzerland – sequence: 8 givenname: Laurent P. surname: Nicod fullname: Nicod, Laurent P. organization: Service de Pneumologie, Faculté de Biologie et de Médecine, Centre Hospitalier Universitaire Vaudoise–Université Lausanne Lausanne, Switzerland – sequence: 9 givenname: Benjamin J. surname: Marsland fullname: Marsland, Benjamin J. organization: Service de Pneumologie, Faculté de Biologie et de Médecine, Centre Hospitalier Universitaire Vaudoise–Université Lausanne Lausanne, Switzerland
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Snippet	Changes in the pulmonary microbiota are associated with progressive respiratory diseases including chronic obstructive pulmonary disease (COPD). Whether there... RATIONALEChanges in the pulmonary microbiota are associated with progressive respiratory diseases including chronic obstructive pulmonary disease (COPD)....
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SubjectTerms	Animals Autoantibodies - immunology Disease Models, Animal Inflammation - complications Inflammation - immunology Inflammation - physiopathology Interleukin-17 - immunology Lung - immunology Lung - physiopathology Mice Mice, Inbred BALB C Microbiota Pulmonary Disease, Chronic Obstructive - complications Pulmonary Disease, Chronic Obstructive - immunology Pulmonary Disease, Chronic Obstructive - physiopathology
Title	Microbiota Promotes Chronic Pulmonary Inflammation by Enhancing IL-17A and Autoantibodies
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