Quantitative proteomic profiling of extracellular matrix and site-specific collagen post-translational modifications in an in vitro model of lung fibrosis

Lung fibrosis is characterized by excessive deposition of extracellular matrix (ECM), in particular collagens, by fibroblasts in the interstitium. Transforming growth factor-β1 (TGF-β1) alters the expression of many extracellular matrix (ECM) components produced by fibroblasts, but such changes in E...

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Vydáno v:Matrix biology plus Ročník 1; s. 100005
Hlavní autoři: Merl-Pham, Juliane, Basak, Trayambak, Knüppel, Larissa, Ramanujam, Deepak, Athanason, Mark, Behr, Jürgen, Engelhardt, Stefan, Eickelberg, Oliver, Hauck, Stefanie M., Vanacore, Roberto, Staab-Weijnitz, Claudia A.
Médium: Journal Article
Jazyk:angličtina
Vydáno: Elsevier 01.02.2019
Témata:
PTM, post-translational modification
LH, lysyl hydroxylase
DCN, decorin
FN1, fibronectin 1
Collagen post-translational modifications
ECM, extracellular matrix
3-HyP, 3-hydroxyproline
TGF-β, transforming growth factor β
P3H, prolyl-3-hydroxylase
PCA, principal component analysis
LOX(L), lysyl oxidase(-like)
TGM2, transglutaminase 1
Lysyl glycosylation
Prolyl hydroxylation
Extracellular matrix
PAI1, plasminogen activator inhibitor 1
G-HyK, galactosylhydroxylysine
SEMA7A, semaphorin 7a
AGC, automatic gain control
HyP, hydroxyproline
Lysyl hydroxylation
4-HyP, 4-hydroxyproline
PLOD (LH), procollagen-lysine,2-oxoglutarate 5-dioxygenases (lysyl hydroxylases)
GG-HyK, glucosylgalactosylhydroxylysine
ILD, interstitial lung disease
P4H, prolyl-4-hydroxylase
α-SMA, α-smooth muscle actin
ANXA11, annexin A11
HyK, hydroxylysine
IPF, idiopathic pulmonary fibrosis
Pulmonary fibrosis
VCAN, versican
Collagen
Transforming growth factor-β
BGN, biglycan
COL1A1, collagen-I alpha 1 chain
LTBP2, latent-transforming growth factor β -binding protein 2
Xaa, Xaa position in the Gly-Xaa-Yaa repeat in triple-helical collagen
Yaa, Yaa position in the Gly-Xaa-Yaa repeat in triple-helical collagen
ISSN:2590-0285, 2590-0285
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Abstract Lung fibrosis is characterized by excessive deposition of extracellular matrix (ECM), in particular collagens, by fibroblasts in the interstitium. Transforming growth factor-β1 (TGF-β1) alters the expression of many extracellular matrix (ECM) components produced by fibroblasts, but such changes in ECM composition as well as modulation of collagen post-translational modification (PTM) levels have not been comprehensively investigated. Here, we performed mass spectrometry (MS)-based proteomics analyses to assess changes in the ECM deposited by cultured lung fibroblasts from idiopathic pulmonary fibrosis (IPF) patients upon stimulation with transforming growth factor β1 (TGF-β1). In addition to the ECM changes commonly associated with lung fibrosis, MS-based label-free quantification revealed profound effects on enzymes involved in ECM crosslinking and turnover as well as multiple positive and negative feedback mechanisms of TGF-β1 signaling. Notably, the ECM changes observed in this model correlated significantly with ECM changes observed in patient samples. Because collagens are subject to multiple PTMs with major implications in disease, we implemented a new bioinformatic platform to analyze MS data that allows for the comprehensive mapping and site-specific quantitation of collagen PTMs in crude ECM preparations. These analyses yielded a comprehensive map of prolyl and lysyl hydroxylations as well as lysyl glycosylations for 15 collagen chains. In addition, site-specific PTM analysis revealed novel sites of prolyl-3-hydroxylation and lysyl glycosylation in type I collagen. Interestingly, the results show, for the first time, that TGF-β1 can modulate prolyl-3-hydroxylation and glycosylation in a site-specific manner. Taken together, this proof of concept study not only reveals unanticipated TGF-β1 mediated regulation of collagen PTMs and other ECM components but also lays the foundation for dissecting their key roles in health and disease. The proteomic data has been deposited to the ProteomeXchange Consortium the MassIVE partner repository with the data set identifier MSV000082958.
AbstractList Lung fibrosis is characterized by excessive deposition of extracellular matrix (ECM), in particular collagens, by fibroblasts in the interstitium. Transforming growth factor-β1 (TGF-β1) alters the expression of many extracellular matrix (ECM) components produced by fibroblasts, but such changes in ECM composition as well as modulation of collagen post-translational modification (PTM) levels have not been comprehensively investigated. Here, we performed mass spectrometry (MS)-based proteomics analyses to assess changes in the ECM deposited by cultured lung fibroblasts from idiopathic pulmonary fibrosis (IPF) patients upon stimulation with transforming growth factor β1 (TGF-β1). In addition to the ECM changes commonly associated with lung fibrosis, MS-based label-free quantification revealed profound effects on enzymes involved in ECM crosslinking and turnover as well as multiple positive and negative feedback mechanisms of TGF-β1 signaling. Notably, the ECM changes observed in this in vitro model correlated significantly with ECM changes observed in patient samples. Because collagens are subject to multiple PTMs with major implications in disease, we implemented a new bioinformatic platform to analyze MS data that allows for the comprehensive mapping and site-specific quantitation of collagen PTMs in crude ECM preparations. These analyses yielded a comprehensive map of prolyl and lysyl hydroxylations as well as lysyl glycosylations for 15 collagen chains. In addition, site-specific PTM analysis revealed novel sites of prolyl-3-hydroxylation and lysyl glycosylation in type I collagen. Interestingly, the results show, for the first time, that TGF-β1 can modulate prolyl-3-hydroxylation and glycosylation in a site-specific manner. Taken together, this proof of concept study not only reveals unanticipated TGF-β1 mediated regulation of collagen PTMs and other ECM components but also lays the foundation for dissecting their key roles in health and disease. The proteomic data has been deposited to the ProteomeXchange Consortium via the MassIVE partner repository with the data set identifier MSV000082958.Lung fibrosis is characterized by excessive deposition of extracellular matrix (ECM), in particular collagens, by fibroblasts in the interstitium. Transforming growth factor-β1 (TGF-β1) alters the expression of many extracellular matrix (ECM) components produced by fibroblasts, but such changes in ECM composition as well as modulation of collagen post-translational modification (PTM) levels have not been comprehensively investigated. Here, we performed mass spectrometry (MS)-based proteomics analyses to assess changes in the ECM deposited by cultured lung fibroblasts from idiopathic pulmonary fibrosis (IPF) patients upon stimulation with transforming growth factor β1 (TGF-β1). In addition to the ECM changes commonly associated with lung fibrosis, MS-based label-free quantification revealed profound effects on enzymes involved in ECM crosslinking and turnover as well as multiple positive and negative feedback mechanisms of TGF-β1 signaling. Notably, the ECM changes observed in this in vitro model correlated significantly with ECM changes observed in patient samples. Because collagens are subject to multiple PTMs with major implications in disease, we implemented a new bioinformatic platform to analyze MS data that allows for the comprehensive mapping and site-specific quantitation of collagen PTMs in crude ECM preparations. These analyses yielded a comprehensive map of prolyl and lysyl hydroxylations as well as lysyl glycosylations for 15 collagen chains. In addition, site-specific PTM analysis revealed novel sites of prolyl-3-hydroxylation and lysyl glycosylation in type I collagen. Interestingly, the results show, for the first time, that TGF-β1 can modulate prolyl-3-hydroxylation and glycosylation in a site-specific manner. Taken together, this proof of concept study not only reveals unanticipated TGF-β1 mediated regulation of collagen PTMs and other ECM components but also lays the foundation for dissecting their key roles in health and disease. The proteomic data has been deposited to the ProteomeXchange Consortium via the MassIVE partner repository with the data set identifier MSV000082958.
Lung fibrosis is characterized by excessive deposition of extracellular matrix (ECM), in particular collagens, by fibroblasts in the interstitium. Transforming growth factor-β1 (TGF-β1) alters the expression of many extracellular matrix (ECM) components produced by fibroblasts, but such changes in ECM composition as well as modulation of collagen post-translational modification (PTM) levels have not been comprehensively investigated. Here, we performed mass spectrometry (MS)-based proteomics analyses to assess changes in the ECM deposited by cultured lung fibroblasts from idiopathic pulmonary fibrosis (IPF) patients upon stimulation with transforming growth factor β1 (TGF-β1). In addition to the ECM changes commonly associated with lung fibrosis, MS-based label-free quantification revealed profound effects on enzymes involved in ECM crosslinking and turnover as well as multiple positive and negative feedback mechanisms of TGF-β1 signaling. Notably, the ECM changes observed in this in vitro model correlated significantly with ECM changes observed in patient samples. Because collagens are subject to multiple PTMs with major implications in disease, we implemented a new bioinformatic platform to analyze MS data that allows for the comprehensive mapping and site-specific quantitation of collagen PTMs in crude ECM preparations. These analyses yielded a comprehensive map of prolyl and lysyl hydroxylations as well as lysyl glycosylations for 15 collagen chains. In addition, site-specific PTM analysis revealed novel sites of prolyl-3-hydroxylation and lysyl glycosylation in type I collagen. Interestingly, the results show, for the first time, that TGF-β1 can modulate prolyl-3-hydroxylation and glycosylation in a site-specific manner. Taken together, this proof of concept study not only reveals unanticipated TGF-β1 mediated regulation of collagen PTMs and other ECM components but also lays the foundation for dissecting their key roles in health and disease. The proteomic data has been deposited to the ProteomeXchange Consortium via the MassIVE partner repository with the data set identifier MSV000082958. • Quantitative proteomics of TGF-β-induced changes in ECM composition and collagen PTM in pulmonary fibroblasts • TGF-β promotes crosslinking and turnover as well as complex feedback mechanisms that alter fibroblast ECM homeostasis. • A novel bioinformatic workflow for MS data analysis enabled global mapping and quantitation of known and novel collagen PTMs • Quantitative assessment of prolyl-3-hydroxylation site occupancy and lysine-O-glycosylation microheterogeneity • TGF-β1 modulates collagen PTMs in a site-specific manner that may favor collagen accumulation in lung fibrosis
Lung fibrosis is characterized by excessive deposition of extracellular matrix (ECM), in particular collagens, by fibroblasts in the interstitium. Transforming growth factor-β1 (TGF-β1) alters the expression of many extracellular matrix (ECM) components produced by fibroblasts, but such changes in ECM composition as well as modulation of collagen post-translational modification (PTM) levels have not been comprehensively investigated. Here, we performed mass spectrometry (MS)-based proteomics analyses to assess changes in the ECM deposited by cultured lung fibroblasts from idiopathic pulmonary fibrosis (IPF) patients upon stimulation with transforming growth factor β1 (TGF-β1). In addition to the ECM changes commonly associated with lung fibrosis, MS-based label-free quantification revealed profound effects on enzymes involved in ECM crosslinking and turnover as well as multiple positive and negative feedback mechanisms of TGF-β1 signaling. Notably, the ECM changes observed in this in vitro model correlated significantly with ECM changes observed in patient samples. Because collagens are subject to multiple PTMs with major implications in disease, we implemented a new bioinformatic platform to analyze MS data that allows for the comprehensive mapping and site-specific quantitation of collagen PTMs in crude ECM preparations. These analyses yielded a comprehensive map of prolyl and lysyl hydroxylations as well as lysyl glycosylations for 15 collagen chains. In addition, site-specific PTM analysis revealed novel sites of prolyl-3-hydroxylation and lysyl glycosylation in type I collagen. Interestingly, the results show, for the first time, that TGF-β1 can modulate prolyl-3-hydroxylation and glycosylation in a site-specific manner. Taken together, this proof of concept study not only reveals unanticipated TGF-β1 mediated regulation of collagen PTMs and other ECM components but also lays the foundation for dissecting their key roles in health and disease.The proteomic data has been deposited to the ProteomeXchange Consortium via the MassIVE partner repository with the data set identifier MSV000082958. Keywords: Pulmonary fibrosis, Collagen, Extracellular matrix, Transforming growth factor-β, Collagen post-translational modifications, Prolyl hydroxylation, Lysyl hydroxylation, Lysyl glycosylation
Lung fibrosis is characterized by excessive deposition of extracellular matrix (ECM), in particular collagens, by fibroblasts in the interstitium. Transforming growth factor-β1 (TGF-β1) alters the expression of many extracellular matrix (ECM) components produced by fibroblasts, but such changes in ECM composition as well as modulation of collagen post-translational modification (PTM) levels have not been comprehensively investigated. Here, we performed mass spectrometry (MS)-based proteomics analyses to assess changes in the ECM deposited by cultured lung fibroblasts from idiopathic pulmonary fibrosis (IPF) patients upon stimulation with transforming growth factor β1 (TGF-β1). In addition to the ECM changes commonly associated with lung fibrosis, MS-based label-free quantification revealed profound effects on enzymes involved in ECM crosslinking and turnover as well as multiple positive and negative feedback mechanisms of TGF-β1 signaling. Notably, the ECM changes observed in this model correlated significantly with ECM changes observed in patient samples. Because collagens are subject to multiple PTMs with major implications in disease, we implemented a new bioinformatic platform to analyze MS data that allows for the comprehensive mapping and site-specific quantitation of collagen PTMs in crude ECM preparations. These analyses yielded a comprehensive map of prolyl and lysyl hydroxylations as well as lysyl glycosylations for 15 collagen chains. In addition, site-specific PTM analysis revealed novel sites of prolyl-3-hydroxylation and lysyl glycosylation in type I collagen. Interestingly, the results show, for the first time, that TGF-β1 can modulate prolyl-3-hydroxylation and glycosylation in a site-specific manner. Taken together, this proof of concept study not only reveals unanticipated TGF-β1 mediated regulation of collagen PTMs and other ECM components but also lays the foundation for dissecting their key roles in health and disease. The proteomic data has been deposited to the ProteomeXchange Consortium the MassIVE partner repository with the data set identifier MSV000082958.
ArticleNumber 100005
Author Engelhardt, Stefan
Staab-Weijnitz, Claudia A.
Basak, Trayambak
Knüppel, Larissa
Athanason, Mark
Ramanujam, Deepak
Merl-Pham, Juliane
Hauck, Stefanie M.
Vanacore, Roberto
Behr, Jürgen
Eickelberg, Oliver
Author_xml – sequence: 1
  givenname: Juliane
  surname: Merl-Pham
  fullname: Merl-Pham, Juliane
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  surname: Basak
  fullname: Basak, Trayambak
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  givenname: Larissa
  surname: Knüppel
  fullname: Knüppel, Larissa
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  givenname: Deepak
  surname: Ramanujam
  fullname: Ramanujam, Deepak
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  givenname: Mark
  surname: Athanason
  fullname: Athanason, Mark
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  givenname: Jürgen
  surname: Behr
  fullname: Behr, Jürgen
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  givenname: Stefan
  surname: Engelhardt
  fullname: Engelhardt, Stefan
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  orcidid: 0000-0001-7170-0360
  surname: Eickelberg
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  surname: Hauck
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  surname: Vanacore
  fullname: Vanacore, Roberto
– sequence: 11
  givenname: Claudia A.
  orcidid: 0000-0002-1211-7834
  surname: Staab-Weijnitz
  fullname: Staab-Weijnitz, Claudia A.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33543004$$D View this record in MEDLINE/PubMed
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Keywords PTM, post-translational modification
LH, lysyl hydroxylase
DCN, decorin
FN1, fibronectin 1
Collagen post-translational modifications
ECM, extracellular matrix
3-HyP, 3-hydroxyproline
TGF-β, transforming growth factor β
P3H, prolyl-3-hydroxylase
PCA, principal component analysis
LOX(L), lysyl oxidase(-like)
TGM2, transglutaminase 1
Lysyl glycosylation
Prolyl hydroxylation
Extracellular matrix
PAI1, plasminogen activator inhibitor 1
G-HyK, galactosylhydroxylysine
SEMA7A, semaphorin 7a
AGC, automatic gain control
HyP, hydroxyproline
Lysyl hydroxylation
4-HyP, 4-hydroxyproline
PLOD (LH), procollagen-lysine,2-oxoglutarate 5-dioxygenases (lysyl hydroxylases)
GG-HyK, glucosylgalactosylhydroxylysine
ILD, interstitial lung disease
P4H, prolyl-4-hydroxylase
α-SMA, α-smooth muscle actin
ANXA11, annexin A11
HyK, hydroxylysine
IPF, idiopathic pulmonary fibrosis
Pulmonary fibrosis
VCAN, versican
Collagen
Transforming growth factor-β
BGN, biglycan
COL1A1, collagen-I alpha 1 chain
LTBP2, latent-transforming growth factor β -binding protein 2
Xaa, Xaa position in the Gly-Xaa-Yaa repeat in triple-helical collagen
Yaa, Yaa position in the Gly-Xaa-Yaa repeat in triple-helical collagen
Language English
License 2019 Published by Elsevier B.V.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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content type line 23
JM-P and TB contributed equally to this work.
Member of the German Center for Lung Research.
Member of the German Center of Lung Research (DZL).
DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany.
Present address: Pulmonary and Critical Care Medicine University, Colorado Anschutz Medical Campus, Denver, CO, United States of America.
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0000-0001-7170-0360
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Publisher Elsevier
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Snippet Lung fibrosis is characterized by excessive deposition of extracellular matrix (ECM), in particular collagens, by fibroblasts in the interstitium. Transforming...
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