Roles of epithelial cell-derived periostin in TGF-β activation, collagen production, and collagen gel elasticity in asthma

Periostin is considered to be a matricellular protein with expression typically confined to cells of mesenchymal origin. Here, by using in situ hybridization, we show that periostin is specifically up-regulated in bronchial epithelial cells of asthmatic subjects, and in vitro, we show that periostin...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 107; no. 32; pp. 14170 - 14175
Main Authors Sidhu, Sukhvinder S., Yuan, Shaopeng, Innes, Anh L., Kerr, Sheena, Woodruff, Prescott G., Hou, Lydia, Muller, Susan J., Fahy, John V., Yamamoto, Keith R.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 10.08.2010
National Acad Sciences
Subjects
Online AccessGet full text
ISSN0027-8424
1091-6490
1091-6490
DOI10.1073/pnas.1009426107

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Abstract Periostin is considered to be a matricellular protein with expression typically confined to cells of mesenchymal origin. Here, by using in situ hybridization, we show that periostin is specifically up-regulated in bronchial epithelial cells of asthmatic subjects, and in vitro, we show that periostin protein is basally secreted by airway epithelial cells in response to IL-13 to influence epithelial cell function, epithelial–mesenchymal interactions, and extracellular matrix organization. In primary human bronchial epithelial cells stimulated with periostin and epithelial cells overexpressing periostin, we reveal a function for periostin in stimulating the TGF-β signaling pathway in a mechanism involving matrix metalloproteinases 2 and 9. Furthermore, conditioned medium from the epithelial cells overexpressing periostin caused TGF-β–dependent secretion of type 1 collagen by airway fibroblasts. In addition, mixing recombinant periostin with type 1 collagen in solution caused a dramatic increase in the elastic modulus of the collagen gel, indicating that periostin alters collagen fibrillogenesis or cross-linking and leads to stiffening of the matrix. Epithelial cell-derived periostin in asthma has roles in TGF-β activation and collagen gel elasticity in asthma.
AbstractList Periostin is considered to be a matricellular protein with expression typically confined to cells of mesenchymal origin. Here, by using in situ hybridization, we show that periostin is specifically up-regulated in bronchial epithelial cells of asthmatic subjects, and in vitro, we show that periostin protein is basally secreted by airway epithelial cells in response to IL-13 to influence epithelial cell function, epithelial–mesenchymal interactions, and extracellular matrix organization. In primary human bronchial epithelial cells stimulated with periostin and epithelial cells overexpressing periostin, we reveal a function for periostin in stimulating the TGF-β signaling pathway in a mechanism involving matrix metalloproteinases 2 and 9. Furthermore, conditioned medium from the epithelial cells overexpressing periostin caused TGF-β–dependent secretion of type 1 collagen by airway fibroblasts. In addition, mixing recombinant periostin with type 1 collagen in solution caused a dramatic increase in the elastic modulus of the collagen gel, indicating that periostin alters collagen fibrillogenesis or cross-linking and leads to stiffening of the matrix. Epithelial cell-derived periostin in asthma has roles in TGF-β activation and collagen gel elasticity in asthma.
Periostin is considered to be a matricellular protein with expression typically confined to cells of mesenchymal origin. Here, by using in situ hybridization, we show that periostin is specifically up-regulated in bronchial epithelial cells of asthmatic subjects, and in vitro, we show that periostin protein is basally secreted by airway epithelial cells in response to IL-13 to influence epithelial cell function, epithelial-mesenchymal interactions, and extracellular matrix organization. In primary human bronchial epithelial cells stimulated with periostin and epithelial cells overexpressing periostin, we reveal a function for periostin in stimulating the TGF-beta signaling pathway in a mechanism involving matrix metalloproteinases 2 and 9. Furthermore, conditioned medium from the epithelial cells overexpressing periostin caused TGF-beta-dependent secretion of type 1 collagen by airway fibroblasts. In addition, mixing recombinant periostin with type 1 collagen in solution caused a dramatic increase in the elastic modulus of the collagen gel, indicating that periostin alters collagen fibrillogenesis or cross-linking and leads to stiffening of the matrix. Epithelial cell-derived periostin in asthma has roles in TGF-beta activation and collagen gel elasticity in asthma.Periostin is considered to be a matricellular protein with expression typically confined to cells of mesenchymal origin. Here, by using in situ hybridization, we show that periostin is specifically up-regulated in bronchial epithelial cells of asthmatic subjects, and in vitro, we show that periostin protein is basally secreted by airway epithelial cells in response to IL-13 to influence epithelial cell function, epithelial-mesenchymal interactions, and extracellular matrix organization. In primary human bronchial epithelial cells stimulated with periostin and epithelial cells overexpressing periostin, we reveal a function for periostin in stimulating the TGF-beta signaling pathway in a mechanism involving matrix metalloproteinases 2 and 9. Furthermore, conditioned medium from the epithelial cells overexpressing periostin caused TGF-beta-dependent secretion of type 1 collagen by airway fibroblasts. In addition, mixing recombinant periostin with type 1 collagen in solution caused a dramatic increase in the elastic modulus of the collagen gel, indicating that periostin alters collagen fibrillogenesis or cross-linking and leads to stiffening of the matrix. Epithelial cell-derived periostin in asthma has roles in TGF-beta activation and collagen gel elasticity in asthma.
Periostin is considered to be a matricellular protein with expression typically confined to cells of mesenchymal origin. Here, by using in situ hybridization, we show that periostin is specifically up-regulated in bronchial epithelial cells of asthmatic subjects, and in vitro, we show that periostin protein is basally secreted by airway epithelial cells in response to IL-13 to influence epithelial cell function, epithelial-mesenchymal interactions, and extracellular matrix organization. In primary human bronchial epithelial cells stimulated with periostin and epithelial cells overexpressing periostin, we reveal a function for periostin in stimulating the TGF-beta signaling pathway in a mechanism involving matrix metalloproteinases 2 and 9. Furthermore, conditioned medium from the epithelial cells overexpressing periostin caused TGF-beta-dependent secretion of type 1 collagen by airway fibroblasts. In addition, mixing recombinant periostin with type 1 collagen in solution caused a dramatic increase in the elastic modulus of the collagen gel, indicating that periostin alters collagen fibrillogenesis or cross-linking and leads to stiffening of the matrix. Epithelial cell-derived periostin in asthma has roles in TGF-beta activation and collagen gel elasticity in asthma.
Author Sidhu, Sukhvinder S.
Innes, Anh L.
Yuan, Shaopeng
Woodruff, Prescott G.
Yamamoto, Keith R.
Fahy, John V.
Muller, Susan J.
Kerr, Sheena
Hou, Lydia
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  givenname: Sukhvinder S.
  surname: Sidhu
  fullname: Sidhu, Sukhvinder S.
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  givenname: Shaopeng
  surname: Yuan
  fullname: Yuan, Shaopeng
– sequence: 3
  givenname: Anh L.
  surname: Innes
  fullname: Innes, Anh L.
– sequence: 4
  givenname: Sheena
  surname: Kerr
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  givenname: Prescott G.
  surname: Woodruff
  fullname: Woodruff, Prescott G.
– sequence: 6
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– sequence: 7
  givenname: Susan J.
  surname: Muller
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  surname: Fahy
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  givenname: Keith R.
  surname: Yamamoto
  fullname: Yamamoto, Keith R.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/20660732$$D View this record in MEDLINE/PubMed
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Author contributions: S.S.S., S.K., P.G.W., and J.V.F. designed research; S.S.S., S.Y., A.L.I., S.K., L.H., M.S., and J.V.F. performed research; S.S.S., A.L.I., S.K., P.G.W., S.J.M., and J.V.F. analyzed data; and S.S.S. and J.V.F. wrote the paper.
Communicated by Keith R. Yamamoto, University of California, San Francisco, CA, June 30, 2010 (received for review January 11, 2010)
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Snippet Periostin is considered to be a matricellular protein with expression typically confined to cells of mesenchymal origin. Here, by using in situ hybridization,...
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SourceType Open Access Repository
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Enrichment Source
Publisher
StartPage 14170
SubjectTerms Asthma
Asthma - metabolism
Asthma - pathology
Biological Sciences
Bronchi - cytology
Bronchi - pathology
Business to business
Cell Adhesion Molecules - physiology
Cells, Cultured
collagen
Collagen Type I - biosynthesis
Collagen Type I - chemistry
Collagen Type I - secretion
Collagens
crosslinking
Elasticity
Epithelial cells
Epithelial Cells - metabolism
epithelium
extracellular matrix
Fibroblasts
Fibrosis
Gels
Gene expression
gene expression regulation
Humans
in situ hybridization
interleukin-13
Matrix Metalloproteinases
metalloproteinases
mixing
Moduli of elasticity
modulus of elasticity
protein synthesis
secretion
signal transduction
transforming growth factor beta
Transforming Growth Factor beta - metabolism
Up regulation
Title Roles of epithelial cell-derived periostin in TGF-β activation, collagen production, and collagen gel elasticity in asthma
URI https://www.jstor.org/stable/25708874
http://www.pnas.org/content/107/32/14170.abstract
https://www.ncbi.nlm.nih.gov/pubmed/20660732
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