Decreased surfactant lipids correlate with lung function in chronic obstructive pulmonary disease (COPD)

Smoke exposure is known to decrease total pulmonary surfactant and alter its composition, but the role of surfactant in chronic obstructive pulmonary disease (COPD) remains unknown. We aimed to analyze the compositional changes in the surfactant lipidome in COPD and identify specific lipids associat...

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Published inPloS one Vol. 15; no. 2; p. e0228279
Main Authors Agudelo, Christina W., Kumley, Britta K., Area-Gomez, Estela, Xu, Yimeng, Dabo, Abdoulaye J., Geraghty, Patrick, Campos, Michael, Foronjy, Robert, Garcia-Arcos, Itsaso
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 06.02.2020
Public Library of Science (PLoS)
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ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0228279

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Abstract Smoke exposure is known to decrease total pulmonary surfactant and alter its composition, but the role of surfactant in chronic obstructive pulmonary disease (COPD) remains unknown. We aimed to analyze the compositional changes in the surfactant lipidome in COPD and identify specific lipids associated with pulmonary function decline. Bronchoalveolar lavage (BAL) fluid was obtained from 12 former smokers with COPD and 5 non-smoking, non-asthmatic healthy control volunteers. Lipids were extracted and analyzed by liquid chromatography and mass spectrometry. Pulmonary function data were obtained by spirometry, and correlations of lung function with lipid species were determined. Wild-type C57BL/6 mice were exposed to 6 months of second-hand smoke in a full-body chamber. Surfactant lipids were decreased by 60% in subjects with COPD. All phospholipid classes were dramatically decreased, including ether phospholipids, which have not been studied in pulmonary surfactant. Availability of phospholipid, cholesterol, and sphingomyelin in BAL strongly correlated with pulmonary function and this was attributable to specific lipid species of phosphatidylcholine with surface tension reducing properties, and of phosphatidylglycerol with antimicrobial roles, as well as to other less studied lipid species. Mice exposed to smoke for six months recapitulated surfactant lipidomic changes observed in human subjects with COPD. In summary, we show that the surfactant lipidome is substantially altered in subjects with COPD, and decreased availability of phospholipids correlated with decreased pulmonary function. Further investigation of surfactant alterations in COPD would improve our understanding of its physiopathology and reveal new potential therapeutic targets.
AbstractList Smoke exposure is known to decrease total pulmonary surfactant and alter its composition, but the role of surfactant in chronic obstructive pulmonary disease (COPD) remains unknown. We aimed to analyze the compositional changes in the surfactant lipidome in COPD and identify specific lipids associated with pulmonary function decline. Bronchoalveolar lavage (BAL) fluid was obtained from 12 former smokers with COPD and 5 non-smoking, non-asthmatic healthy control volunteers. Lipids were extracted and analyzed by liquid chromatography and mass spectrometry. Pulmonary function data were obtained by spirometry, and correlations of lung function with lipid species were determined. Wild-type C57BL/6 mice were exposed to 6 months of second-hand smoke in a full-body chamber. Surfactant lipids were decreased by 60% in subjects with COPD. All phospholipid classes were dramatically decreased, including ether phospholipids, which have not been studied in pulmonary surfactant. Availability of phospholipid, cholesterol, and sphingomyelin in BAL strongly correlated with pulmonary function and this was attributable to specific lipid species of phosphatidylcholine with surface tension reducing properties, and of phosphatidylglycerol with antimicrobial roles, as well as to other less studied lipid species. Mice exposed to smoke for six months recapitulated surfactant lipidomic changes observed in human subjects with COPD. In summary, we show that the surfactant lipidome is substantially altered in subjects with COPD, and decreased availability of phospholipids correlated with decreased pulmonary function. Further investigation of surfactant alterations in COPD would improve our understanding of its physiopathology and reveal new potential therapeutic targets.
Smoke exposure is known to decrease total pulmonary surfactant and alter its composition, but the role of surfactant in chronic obstructive pulmonary disease (COPD) remains unknown. We aimed to analyze the compositional changes in the surfactant lipidome in COPD and identify specific lipids associated with pulmonary function decline. Bronchoalveolar lavage (BAL) fluid was obtained from 12 former smokers with COPD and 5 non-smoking, non-asthmatic healthy control volunteers. Lipids were extracted and analyzed by liquid chromatography and mass spectrometry. Pulmonary function data were obtained by spirometry, and correlations of lung function with lipid species were determined. Wild-type C57BL/6 mice were exposed to 6 months of second-hand smoke in a full-body chamber. Surfactant lipids were decreased by 60% in subjects with COPD. All phospholipid classes were dramatically decreased, including ether phospholipids, which have not been studied in pulmonary surfactant. Availability of phospholipid, cholesterol, and sphingomyelin in BAL strongly correlated with pulmonary function and this was attributable to specific lipid species of phosphatidylcholine with surface tension reducing properties, and of phosphatidylglycerol with antimicrobial roles, as well as to other less studied lipid species. Mice exposed to smoke for six months recapitulated surfactant lipidomic changes observed in human subjects with COPD. In summary, we show that the surfactant lipidome is substantially altered in subjects with COPD, and decreased availability of phospholipids correlated with decreased pulmonary function. Further investigation of surfactant alterations in COPD would improve our understanding of its physiopathology and reveal new potential therapeutic targets.Smoke exposure is known to decrease total pulmonary surfactant and alter its composition, but the role of surfactant in chronic obstructive pulmonary disease (COPD) remains unknown. We aimed to analyze the compositional changes in the surfactant lipidome in COPD and identify specific lipids associated with pulmonary function decline. Bronchoalveolar lavage (BAL) fluid was obtained from 12 former smokers with COPD and 5 non-smoking, non-asthmatic healthy control volunteers. Lipids were extracted and analyzed by liquid chromatography and mass spectrometry. Pulmonary function data were obtained by spirometry, and correlations of lung function with lipid species were determined. Wild-type C57BL/6 mice were exposed to 6 months of second-hand smoke in a full-body chamber. Surfactant lipids were decreased by 60% in subjects with COPD. All phospholipid classes were dramatically decreased, including ether phospholipids, which have not been studied in pulmonary surfactant. Availability of phospholipid, cholesterol, and sphingomyelin in BAL strongly correlated with pulmonary function and this was attributable to specific lipid species of phosphatidylcholine with surface tension reducing properties, and of phosphatidylglycerol with antimicrobial roles, as well as to other less studied lipid species. Mice exposed to smoke for six months recapitulated surfactant lipidomic changes observed in human subjects with COPD. In summary, we show that the surfactant lipidome is substantially altered in subjects with COPD, and decreased availability of phospholipids correlated with decreased pulmonary function. Further investigation of surfactant alterations in COPD would improve our understanding of its physiopathology and reveal new potential therapeutic targets.
Audience Academic
Author Geraghty, Patrick
Kumley, Britta K.
Area-Gomez, Estela
Agudelo, Christina W.
Campos, Michael
Xu, Yimeng
Dabo, Abdoulaye J.
Foronjy, Robert
Garcia-Arcos, Itsaso
AuthorAffiliation University of Alberta, CANADA
3 Department of Cell Biology, SUNY Downstate Medical Center, New York, New York, United States of America
2 Department of Neurology, Columbia University, New York, New York, United States of America
1 Department of Medicine, SUNY Downstate Medical Center, New York, New York, United States of America
4 Division of Pulmonary, Allergy, Critical Care and Sleep Medicine, University of Miami Miller School of Medicine, Miami, Florida, United States of America
AuthorAffiliation_xml – name: 1 Department of Medicine, SUNY Downstate Medical Center, New York, New York, United States of America
– name: 4 Division of Pulmonary, Allergy, Critical Care and Sleep Medicine, University of Miami Miller School of Medicine, Miami, Florida, United States of America
– name: 3 Department of Cell Biology, SUNY Downstate Medical Center, New York, New York, United States of America
– name: University of Alberta, CANADA
– name: 2 Department of Neurology, Columbia University, New York, New York, United States of America
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  givenname: Christina W.
  orcidid: 0000-0002-9633-0308
  surname: Agudelo
  fullname: Agudelo, Christina W.
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  surname: Kumley
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  surname: Garcia-Arcos
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32027677$$D View this record in MEDLINE/PubMed
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2020 Agudelo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Competing Interests: The authors have declared that no competing interests exist.
ORCID 0000-0003-1647-5505
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Snippet Smoke exposure is known to decrease total pulmonary surfactant and alter its composition, but the role of surfactant in chronic obstructive pulmonary disease...
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StartPage e0228279
SubjectTerms Adults
Aged
Alveoli
Analysis
Animals
Asthma
Biology
Biology and Life Sciences
Blood lipids
Bronchoalveolar Lavage Fluid - chemistry
Bronchus
Case-Control Studies
Cholesterol
Chromatography
Chromatography, High Pressure Liquid
Chronic obstructive lung disease
Chronic obstructive pulmonary disease
Correlation
Cytokines
Demographics
Disease Models, Animal
Diseases
Exposure
House mouse
Humans
Lecithin
Lipids
Lipids - analysis
Liquid chromatography
Lung - metabolism
Lung diseases
Lungs
Mass Spectrometry
Mass spectroscopy
Medicine
Medicine and Health Sciences
Membrane lipids
Mice
Mice, Inbred C57BL
Middle Aged
Obstructive lung disease
Passive smoking
Patients
Phosphatidylcholine
Phosphatidylcholines - chemistry
Phosphatidylcholines - metabolism
Phosphatidylglycerol
Phospholipids
Phospholipids - chemistry
Phospholipids - metabolism
Physical Sciences
Plant lipids
Pulmonary Disease, Chronic Obstructive - physiopathology
Pulmonary functions
Pulmonary Surfactants - metabolism
Research and Analysis Methods
Respiratory distress syndrome
Respiratory function
Scientific imaging
Smoke
Smokers
Smoking
Smoking cessation
Species
Spectroscopy
Sphingomyelin
Spirometry
Surface active agents
Surface tension
Surfactants
Therapeutic applications
Tobacco Smoke Pollution
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Title Decreased surfactant lipids correlate with lung function in chronic obstructive pulmonary disease (COPD)
URI https://www.ncbi.nlm.nih.gov/pubmed/32027677
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