Protein tyrosine phosphatase 1B negatively regulates S100A9-mediated lung damage during respiratory syncytial virus exacerbations

Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure. Here we investigate whether PTP1B expression affects lung disease severity during respiratory syncytial viral (RSV) exacerbations of chronic...

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Published inMucosal immunology Vol. 9; no. 5; pp. 1317 - 1329
Main Authors Foronjy, R.F., Ochieng, P.O., Salathe, M.A., Dabo, A.J., Eden, E., Baumlin, N., Cummins, N., Barik, S., Campos, M., Thorp, E.B., Geraghty, P.
Format Journal Article
LanguageEnglish
Published New York Elsevier Inc 01.09.2016
Nature Publishing Group US
Elsevier Limited
Subjects
631/250/255/2514
631/250/347
631/80/86
692/699/1785
Allergology
Animals
Antibodies
Antibodies, Neutralizing - pharmacology
Biomedical and Life Sciences
Biomedicine
Bronchoalveolar Lavage Fluid - chemistry
Bronchoalveolar Lavage Fluid - cytology
Calgranulin B - genetics
Calgranulin B - immunology
Case-Control Studies
Disease Models, Animal
Female
Gastroenterology
Gene Expression Regulation
Humans
Immunology
Macrophages, Alveolar - immunology
Macrophages, Alveolar - pathology
Mice
Mice, Knockout
Primary Cell Culture
Protein Tyrosine Phosphatase, Non-Receptor Type 1 - deficiency
Protein Tyrosine Phosphatase, Non-Receptor Type 1 - genetics
Protein Tyrosine Phosphatase, Non-Receptor Type 1 - immunology
Pulmonary Disease, Chronic Obstructive - complications
Pulmonary Disease, Chronic Obstructive - genetics
Pulmonary Disease, Chronic Obstructive - immunology
Pulmonary Disease, Chronic Obstructive - virology
Respiratory Syncytial Virus Infections - complications
Respiratory Syncytial Virus Infections - genetics
Respiratory Syncytial Virus Infections - immunology
Respiratory Syncytial Virus Infections - virology
Respiratory Syncytial Viruses - growth & development
Respiratory Syncytial Viruses - immunology
Signal Transduction
Smoking - genetics
Smoking - immunology
Smoking - pathology
Tobacco Smoke Pollution
Online AccessGet full text
ISSN1933-0219
1935-3456
1935-3456
DOI10.1038/mi.2015.138

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Abstract Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure. Here we investigate whether PTP1B expression affects lung disease severity during respiratory syncytial viral (RSV) exacerbations of chronic obstructive pulmonary disease (COPD). Ptp1b−/− mice infected with RSV exhibit exaggerated immune cell infiltration, damaged epithelial cell barriers, cytokine production, and increased apoptosis. Elevated expression of S100A9, a damage-associated molecular pattern molecule, was observed in the lungs of Ptp1b−/− mice during RSV infection. Utilizing a neutralizing anti-S100A9 IgG antibody, it was determined that extracellular S100A9 signaling significantly affects lung damage during RSV infection. Preexposure to cigarette smoke desensitized PTP1B activity that coincided with enhanced S100A9 secretion and inflammation in wild-type animals during RSV infection. S100A9 levels in human bronchoalveolar lavage fluid had an inverse relationship with lung function in healthy subjects, smokers, and COPD subjects. Fully differentiated human bronchial epithelial cells isolated from COPD donors cultured at the air liquid interface secreted more S100A9 than cells from healthy donors or smokers following RSV infection. Together, these findings show that reduced PTP1B responses contribute to disease symptoms in part by enhancing S100A9 expression during viral-associated COPD exacerbations.
AbstractList Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure. Here we investigate whether PTP1B expression affects lung disease severity during respiratory syncytial viral (RSV) exacerbations of chronic obstructive pulmonary disease (COPD). Ptp1b −/− mice infected with RSV exhibit exaggerated immune cell infiltration, damaged epithelial cell barriers, cytokine production, and increased apoptosis. Elevated expression of S100A9, a damage-associated molecular pattern molecule, was observed in the lungs of Ptp1b −/− mice during RSV infection. Utilizing a neutralizing anti-S100A9 IgG antibody, it was determined that extracellular S100A9 signaling significantly affects lung damage during RSV infection. Preexposure to cigarette smoke desensitized PTP1B activity that coincided with enhanced S100A9 secretion and inflammation in wild-type animals during RSV infection. S100A9 levels in human bronchoalveolar lavage fluid had an inverse relationship with lung function in healthy subjects, smokers, and COPD subjects. Fully differentiated human bronchial epithelial cells isolated from COPD donors cultured at the air liquid interface secreted more S100A9 than cells from healthy donors or smokers following RSV infection. Together, these findings show that reduced PTP1B responses contribute to disease symptoms in part by enhancing S100A9 expression during viral-associated COPD exacerbations.
Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure. Here we investigate whether PTP1B expression affects lung disease severity during respiratory syncytial viral (RSV) exacerbations of chronic obstructive pulmonary disease (COPD). Ptp1b -/- mice infected with RSV exhibit exaggerated immune cell infiltration, damaged epithelial cell barriers, cytokine production, and increased apoptosis. Elevated expression of S100A9, a damage-associated molecular pattern molecule, was observed in the lungs of Ptp1b -/- mice during RSV infection. Utilizing a neutralizing anti-S100A9 IgG antibody, it was determined that extracellular S100A9 signaling significantly affects lung damage during RSV infection. Preexposure to cigarette smoke desensitized PTP1B activity that coincided with enhanced S100A9 secretion and inflammation in wild-type animals during RSV infection. S100A9 levels in human bronchoalveolar lavage fluid had an inverse relationship with lung function in healthy subjects, smokers, and COPD subjects. Fully differentiated human bronchial epithelial cells isolated from COPD donors cultured at the air liquid interface secreted more S100A9 than cells from healthy donors or smokers following RSV infection. Together, these findings show that reduced PTP1B responses contribute to disease symptoms in part by enhancing S100A9 expression during viral-associated COPD exacerbations.
Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure. Here we investigate whether PTP1B expression affects lung disease severity during respiratory syncytial viral (RSV) exacerbations of chronic obstructive pulmonary disease (COPD). Ptp1b−/− mice infected with RSV exhibit exaggerated immune cell infiltration, damaged epithelial cell barriers, cytokine production, and increased apoptosis. Elevated expression of S100A9, a damage-associated molecular pattern molecule, was observed in the lungs of Ptp1b−/− mice during RSV infection. Utilizing a neutralizing anti-S100A9 IgG antibody, it was determined that extracellular S100A9 signaling significantly affects lung damage during RSV infection. Preexposure to cigarette smoke desensitized PTP1B activity that coincided with enhanced S100A9 secretion and inflammation in wild-type animals during RSV infection. S100A9 levels in human bronchoalveolar lavage fluid had an inverse relationship with lung function in healthy subjects, smokers, and COPD subjects. Fully differentiated human bronchial epithelial cells isolated from COPD donors cultured at the air liquid interface secreted more S100A9 than cells from healthy donors or smokers following RSV infection. Together, these findings show that reduced PTP1B responses contribute to disease symptoms in part by enhancing S100A9 expression during viral-associated COPD exacerbations.
Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure. Here we investigate whether PTP1B expression affects lung disease severity during respiratory syncytial viral (RSV) exacerbations of chronic obstructive pulmonary disease (COPD). Ptp1b(-/-) mice infected with RSV exhibit exaggerated immune cell infiltration, damaged epithelial cell barriers, cytokine production, and increased apoptosis. Elevated expression of S100A9, a damage-associated molecular pattern molecule, was observed in the lungs of Ptp1b(-/-) mice during RSV infection. Utilizing a neutralizing anti-S100A9 IgG antibody, it was determined that extracellular S100A9 signaling significantly affects lung damage during RSV infection. Preexposure to cigarette smoke desensitized PTP1B activity that coincided with enhanced S100A9 secretion and inflammation in wild-type animals during RSV infection. S100A9 levels in human bronchoalveolar lavage fluid had an inverse relationship with lung function in healthy subjects, smokers, and COPD subjects. Fully differentiated human bronchial epithelial cells isolated from COPD donors cultured at the air liquid interface secreted more S100A9 than cells from healthy donors or smokers following RSV infection. Together, these findings show that reduced PTP1B responses contribute to disease symptoms in part by enhancing S100A9 expression during viral-associated COPD exacerbations.Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure. Here we investigate whether PTP1B expression affects lung disease severity during respiratory syncytial viral (RSV) exacerbations of chronic obstructive pulmonary disease (COPD). Ptp1b(-/-) mice infected with RSV exhibit exaggerated immune cell infiltration, damaged epithelial cell barriers, cytokine production, and increased apoptosis. Elevated expression of S100A9, a damage-associated molecular pattern molecule, was observed in the lungs of Ptp1b(-/-) mice during RSV infection. Utilizing a neutralizing anti-S100A9 IgG antibody, it was determined that extracellular S100A9 signaling significantly affects lung damage during RSV infection. Preexposure to cigarette smoke desensitized PTP1B activity that coincided with enhanced S100A9 secretion and inflammation in wild-type animals during RSV infection. S100A9 levels in human bronchoalveolar lavage fluid had an inverse relationship with lung function in healthy subjects, smokers, and COPD subjects. Fully differentiated human bronchial epithelial cells isolated from COPD donors cultured at the air liquid interface secreted more S100A9 than cells from healthy donors or smokers following RSV infection. Together, these findings show that reduced PTP1B responses contribute to disease symptoms in part by enhancing S100A9 expression during viral-associated COPD exacerbations.
Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure. Here we investigate whether PTP1B expression impacts lung disease severity during respiratory syncytial viral (RSV) exacerbations of chronic obstructive pulmonary disease (COPD). Ptp1b -/- mice infected with RSV exhibit exaggerated immune cell infiltration, damaged epithelial cell barriers, cytokine production and increased apoptosis. Elevated expression of S100A9, a damage-associated molecular pattern molecule, was observed in the lungs of Ptp1b -/- mice during RSV infection. Utilizing a neutralizing anti-S100A9 IgG antibody, it was determined that extracellular S100A9 signaling significantly impacts lung damage during RSV infection. Pre-exposure to cigarette smoke desensitized PTP1B activity, which coincided with enhanced S100A9 secretion and inflammation in wild type animals during RSV infection. S100A9 levels in human bronchoalveolar lavage fluid had an inverse relationship with lung function in healthy subjects, smokers and COPD subjects. Fully differentiated human bronchial epithelial cells isolated from COPD donors cultured at the air liquid interface secreted more S100A9 than cells from healthy donors or smokers following RSV infection. Together, these findings show that reduced PTP1B responses contribute to disease symptoms in part by enhancing S100A9 expression during viral-associated COPD exacerbations.
Author Ochieng, P.O.
Foronjy, R.F.
Dabo, A.J.
Barik, S.
Thorp, E.B.
Salathe, M.A.
Geraghty, P.
Eden, E.
Campos, M.
Cummins, N.
Baumlin, N.
AuthorAffiliation 2 Division of Pulmonary and Critical Care Medicine, Mount Sinai Roosevelt, Mount Sinai Health System, New York, NY, USA
3 Division of Pulmonary, Allergy, Critical Care, and Sleep Medicine, University of Miami, Miami, Florida, USA
1 Division of Pulmonary & Critical Care Medicine, SUNY Downstate Medical Center, Brooklyn, NY, USA
4 Center for Gene Regulation in Health and Disease, and Department of Biological, Geological and Environmental Sciences, Cleveland State University, Cleveland, Ohio, USA
5 Department of Pathology and Feinberg Cardiovascular Research Institute, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
AuthorAffiliation_xml – name: 5 Department of Pathology and Feinberg Cardiovascular Research Institute, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
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PublicationSubtitle The official publication of the Society for Mucosal Immunology
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Nature Publishing Group US
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Snippet Protein tyrosine phosphatase 1B (PTP1B) has anti-inflammatory potential but PTP1B responses are desensitized in the lung by prolonged cigarette smoke exposure....
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SubjectTerms 631/250/255/2514
631/250/347
631/80/86
692/699/1785
Allergology
Animals
Antibodies
Antibodies, Neutralizing - pharmacology
Biomedical and Life Sciences
Biomedicine
Bronchoalveolar Lavage Fluid - chemistry
Bronchoalveolar Lavage Fluid - cytology
Calgranulin B - genetics
Calgranulin B - immunology
Case-Control Studies
Disease Models, Animal
Female
Gastroenterology
Gene Expression Regulation
Humans
Immunology
Macrophages, Alveolar - immunology
Macrophages, Alveolar - pathology
Mice
Mice, Knockout
Primary Cell Culture
Protein Tyrosine Phosphatase, Non-Receptor Type 1 - deficiency
Protein Tyrosine Phosphatase, Non-Receptor Type 1 - genetics
Protein Tyrosine Phosphatase, Non-Receptor Type 1 - immunology
Pulmonary Disease, Chronic Obstructive - complications
Pulmonary Disease, Chronic Obstructive - genetics
Pulmonary Disease, Chronic Obstructive - immunology
Pulmonary Disease, Chronic Obstructive - virology
Respiratory Syncytial Virus Infections - complications
Respiratory Syncytial Virus Infections - genetics
Respiratory Syncytial Virus Infections - immunology
Respiratory Syncytial Virus Infections - virology
Respiratory Syncytial Viruses - growth & development
Respiratory Syncytial Viruses - immunology
Signal Transduction
Smoking - genetics
Smoking - immunology
Smoking - pathology
Tobacco Smoke Pollution
Title Protein tyrosine phosphatase 1B negatively regulates S100A9-mediated lung damage during respiratory syncytial virus exacerbations
URI https://www.clinicalkey.com/#!/content/1-s2.0-S1933021922007759
https://link.springer.com/article/10.1038/mi.2015.138
https://www.ncbi.nlm.nih.gov/pubmed/26813343
https://www.proquest.com/docview/1811360896
https://www.proquest.com/docview/1812227752
https://pubmed.ncbi.nlm.nih.gov/PMC4963308
Volume 9
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