MMP-1 activation contributes to airway smooth muscle growth and asthma severity

Introduction: Matrix metalloproteinase-1 and mast cells are present in the airways of people with asthma. We hypothesised that matrix metalloproteinase-1 could be activated by mast cells and increase asthma severity. Methods: Patients with stable asthma and healthy controls underwent spirometry, met...

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Main Authors: Naveed, Shams-un-nisa, Clements, Debbie, Jackson, David J., Philp, Christopher, Billington, Charlotte K., Soomro, Irshad N., Reynolds, Catherine, Harrison, Timothy W., Johnston, Sebastian L., Shaw, Dominick E., Johnson, Simon R.
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Published: American Thoracic Society 2017
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Online Access:https://eprints.nottingham.ac.uk/40029/
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author Naveed, Shams-un-nisa
Clements, Debbie
Jackson, David J.
Philp, Christopher
Billington, Charlotte K.
Soomro, Irshad N.
Reynolds, Catherine
Harrison, Timothy W.
Johnston, Sebastian L.
Shaw, Dominick E.
Johnson, Simon R.
author_facet Naveed, Shams-un-nisa
Clements, Debbie
Jackson, David J.
Philp, Christopher
Billington, Charlotte K.
Soomro, Irshad N.
Reynolds, Catherine
Harrison, Timothy W.
Johnston, Sebastian L.
Shaw, Dominick E.
Johnson, Simon R.
author_sort Naveed, Shams-un-nisa
building Nottingham Research Data Repository
collection Online Access
description Introduction: Matrix metalloproteinase-1 and mast cells are present in the airways of people with asthma. We hypothesised that matrix metalloproteinase-1 could be activated by mast cells and increase asthma severity. Methods: Patients with stable asthma and healthy controls underwent spirometry, methacholine challenge, bronchoscopy and their airway smooth muscle cells were grown in culture. A second asthma group and controls had symptom scores, spirometry and bronchoalveolar lavage before and after rhinovirus-induced asthma exacerbations. Extra-cellular matrix was prepared from decellularised airway smooth muscle cultures. Matrix metalloproteinase-1 protein and activity were assessed. Results: Airway smooth muscle cells generated pro-matrix metalloproteinase-1 which was proteolytically activated by mast cell tryptase. Airway smooth muscle treated with activated mast cell supernatants produced extra-cellular matrix which enhanced subsequent airway smooth muscle growth by 1.5 fold (p<0.05) which was dependent on matrix metalloproteinase-1 activation. In asthma, airway pro-matrix metalloproteinase-1 was 5.4 fold higher than control subjects (p=0.002). Mast cell numbers were associated with airway smooth muscle proliferation and matrix metalloproteinase-1 protein associated with bronchial hyper-responsiveness. During exacerbations, matrix metalloproteinase-1 activity increased and was associated with fall in FEV1 and worsening asthma symptoms. Conclusions: Matrix metalloproteinase-1 is activated by mast cell tryptase resulting in a pro-proliferative extra-cellular matrix. In asthma, mast cells are associated with airway smooth muscle growth, matrix metalloproteinase-1 levels are associated with bronchial hyper-responsiveness and matrix metalloproteinase-1 activation with exacerbation severity. Our findings suggest that airway smooth muscle/mast cell interactions contribute to asthma severity by transiently increasing matrix metalloproteinase activation, airway smooth muscle growth and airway responsiveness.
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spelling nottingham-400292024-08-15T15:22:25Z https://eprints.nottingham.ac.uk/40029/ MMP-1 activation contributes to airway smooth muscle growth and asthma severity Naveed, Shams-un-nisa Clements, Debbie Jackson, David J. Philp, Christopher Billington, Charlotte K. Soomro, Irshad N. Reynolds, Catherine Harrison, Timothy W. Johnston, Sebastian L. Shaw, Dominick E. Johnson, Simon R. Introduction: Matrix metalloproteinase-1 and mast cells are present in the airways of people with asthma. We hypothesised that matrix metalloproteinase-1 could be activated by mast cells and increase asthma severity. Methods: Patients with stable asthma and healthy controls underwent spirometry, methacholine challenge, bronchoscopy and their airway smooth muscle cells were grown in culture. A second asthma group and controls had symptom scores, spirometry and bronchoalveolar lavage before and after rhinovirus-induced asthma exacerbations. Extra-cellular matrix was prepared from decellularised airway smooth muscle cultures. Matrix metalloproteinase-1 protein and activity were assessed. Results: Airway smooth muscle cells generated pro-matrix metalloproteinase-1 which was proteolytically activated by mast cell tryptase. Airway smooth muscle treated with activated mast cell supernatants produced extra-cellular matrix which enhanced subsequent airway smooth muscle growth by 1.5 fold (p<0.05) which was dependent on matrix metalloproteinase-1 activation. In asthma, airway pro-matrix metalloproteinase-1 was 5.4 fold higher than control subjects (p=0.002). Mast cell numbers were associated with airway smooth muscle proliferation and matrix metalloproteinase-1 protein associated with bronchial hyper-responsiveness. During exacerbations, matrix metalloproteinase-1 activity increased and was associated with fall in FEV1 and worsening asthma symptoms. Conclusions: Matrix metalloproteinase-1 is activated by mast cell tryptase resulting in a pro-proliferative extra-cellular matrix. In asthma, mast cells are associated with airway smooth muscle growth, matrix metalloproteinase-1 levels are associated with bronchial hyper-responsiveness and matrix metalloproteinase-1 activation with exacerbation severity. Our findings suggest that airway smooth muscle/mast cell interactions contribute to asthma severity by transiently increasing matrix metalloproteinase activation, airway smooth muscle growth and airway responsiveness. American Thoracic Society 2017-04-15 Article PeerReviewed Naveed, Shams-un-nisa, Clements, Debbie, Jackson, David J., Philp, Christopher, Billington, Charlotte K., Soomro, Irshad N., Reynolds, Catherine, Harrison, Timothy W., Johnston, Sebastian L., Shaw, Dominick E. and Johnson, Simon R. (2017) MMP-1 activation contributes to airway smooth muscle growth and asthma severity. American Journal of Respiratory and Critical Care Medicine, 195 (8). pp. 1000-1009. ISSN 1535-4970 Asthma Extracellular matrix Airway remodeling Airway smooth muscle Mast cells http://www.atsjournals.org/doi/abs/10.1164/rccm.201604-0822OC?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub%3dpubmed doi:10.1164/rccm.201604-0822OC doi:10.1164/rccm.201604-0822OC
spellingShingle Asthma
Extracellular matrix
Airway remodeling
Airway smooth muscle
Mast cells
Naveed, Shams-un-nisa
Clements, Debbie
Jackson, David J.
Philp, Christopher
Billington, Charlotte K.
Soomro, Irshad N.
Reynolds, Catherine
Harrison, Timothy W.
Johnston, Sebastian L.
Shaw, Dominick E.
Johnson, Simon R.
MMP-1 activation contributes to airway smooth muscle growth and asthma severity
title MMP-1 activation contributes to airway smooth muscle growth and asthma severity
title_full MMP-1 activation contributes to airway smooth muscle growth and asthma severity
title_fullStr MMP-1 activation contributes to airway smooth muscle growth and asthma severity
title_full_unstemmed MMP-1 activation contributes to airway smooth muscle growth and asthma severity
title_short MMP-1 activation contributes to airway smooth muscle growth and asthma severity
title_sort mmp-1 activation contributes to airway smooth muscle growth and asthma severity
topic Asthma
Extracellular matrix
Airway remodeling
Airway smooth muscle
Mast cells
url https://eprints.nottingham.ac.uk/40029/
https://eprints.nottingham.ac.uk/40029/
https://eprints.nottingham.ac.uk/40029/