Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation

Cyclooxygenase-2 (COX-2), with its main antifibrotic metabolite PGE, is regarded as an antifibrotic gene. Repressed COX-2 expression and deficient PGE have been shown to contribute to the activation of lung fibroblasts and excessive deposition of collagen in pulmonary fibrosis. We have previously de...

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Main Authors: Pasini, Alice, Brand, Oliver J., Jenkins, Gisli, Knox, Alan J., Pang, Linhua
Format: Article
Published: Elsevier 2018
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Online Access:https://eprints.nottingham.ac.uk/51701/
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author Pasini, Alice
Brand, Oliver J.
Jenkins, Gisli
Knox, Alan J.
Pang, Linhua
author_facet Pasini, Alice
Brand, Oliver J.
Jenkins, Gisli
Knox, Alan J.
Pang, Linhua
author_sort Pasini, Alice
building Nottingham Research Data Repository
collection Online Access
description Cyclooxygenase-2 (COX-2), with its main antifibrotic metabolite PGE, is regarded as an antifibrotic gene. Repressed COX-2 expression and deficient PGE have been shown to contribute to the activation of lung fibroblasts and excessive deposition of collagen in pulmonary fibrosis. We have previously demonstrated that COX-2 expression in lung fibroblasts from patients with idiopathic pulmonary fibrosis (IPF) is epigenetically silenced and can be restored by epigenetic inhibitors. This study aimed to investigate whether COX-2 downregulation induced by the profibrotic cytokine transforming growth factor-β1 (TGF-β1) in normal lung fibroblasts could be prevented by epigenetic inhibitors. We found that COX-2 protein expression and PGE production were markedly reduced by TGF-β1 and this was prevented by the pan-histone deacetylase inhibitor suberanilohydroxamic acid (SAHA) and to a lesser extent by the DNA demethylating agent Decitabine (DAC), but not by the G9a histone methyltransferase (HMT) inhibitor BIX01294 or the EZH2 HMT inhibitor 3-deazaneplanocin A (DZNep). However, chromatin immunoprecipitation assay revealed that the effect of SAHA was unlikely mediated by histone modifications. Instead 3'-untranslated region (3'-UTR) luciferase reporter assay indicated the involvement of post-transcriptional mechanisms. This was supported by the downregulation by SAHA of the 3'-UTR mRNA binding protein TIA-1 (T-cell intracellular antigen-1), a negative regulator of COX-2 translation. Furthermore, TIA-1 knockdown by siRNA mimicked the effect of SAHA on COX-2 expression. These findings suggest SAHA can prevent TGF-β1-induced COX-2 repression in lung fibroblasts post-transcriptionally through a novel TIA-1-dependent mechanism and provide new insights into the mechanisms underlying its potential antifibrotic activity.
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spelling nottingham-517012020-05-04T19:38:09Z https://eprints.nottingham.ac.uk/51701/ Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation Pasini, Alice Brand, Oliver J. Jenkins, Gisli Knox, Alan J. Pang, Linhua Cyclooxygenase-2 (COX-2), with its main antifibrotic metabolite PGE, is regarded as an antifibrotic gene. Repressed COX-2 expression and deficient PGE have been shown to contribute to the activation of lung fibroblasts and excessive deposition of collagen in pulmonary fibrosis. We have previously demonstrated that COX-2 expression in lung fibroblasts from patients with idiopathic pulmonary fibrosis (IPF) is epigenetically silenced and can be restored by epigenetic inhibitors. This study aimed to investigate whether COX-2 downregulation induced by the profibrotic cytokine transforming growth factor-β1 (TGF-β1) in normal lung fibroblasts could be prevented by epigenetic inhibitors. We found that COX-2 protein expression and PGE production were markedly reduced by TGF-β1 and this was prevented by the pan-histone deacetylase inhibitor suberanilohydroxamic acid (SAHA) and to a lesser extent by the DNA demethylating agent Decitabine (DAC), but not by the G9a histone methyltransferase (HMT) inhibitor BIX01294 or the EZH2 HMT inhibitor 3-deazaneplanocin A (DZNep). However, chromatin immunoprecipitation assay revealed that the effect of SAHA was unlikely mediated by histone modifications. Instead 3'-untranslated region (3'-UTR) luciferase reporter assay indicated the involvement of post-transcriptional mechanisms. This was supported by the downregulation by SAHA of the 3'-UTR mRNA binding protein TIA-1 (T-cell intracellular antigen-1), a negative regulator of COX-2 translation. Furthermore, TIA-1 knockdown by siRNA mimicked the effect of SAHA on COX-2 expression. These findings suggest SAHA can prevent TGF-β1-induced COX-2 repression in lung fibroblasts post-transcriptionally through a novel TIA-1-dependent mechanism and provide new insights into the mechanisms underlying its potential antifibrotic activity. Elsevier 2018-05-30 Article PeerReviewed Pasini, Alice, Brand, Oliver J., Jenkins, Gisli, Knox, Alan J. and Pang, Linhua (2018) Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 1861 (5). pp. 463-472. ISSN 0006-3002 Pulmonary fibrosis ; Cyclooxygenase 2 (COX-2) ; Post-transcriptional regulation ; epigenetics ; Histone deacetylase inhibitor ; Transforming growth factor β1 (TGF-β1) https://www.sciencedirect.com/science/article/pii/S1874939917303383 doi:10.1016/j.bbagrm.2018.03.007 doi:10.1016/j.bbagrm.2018.03.007
spellingShingle Pulmonary fibrosis ; Cyclooxygenase 2 (COX-2) ; Post-transcriptional regulation ; epigenetics ; Histone deacetylase inhibitor ; Transforming growth factor β1 (TGF-β1)
Pasini, Alice
Brand, Oliver J.
Jenkins, Gisli
Knox, Alan J.
Pang, Linhua
Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation
title Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation
title_full Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation
title_fullStr Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation
title_full_unstemmed Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation
title_short Suberanilohydroxamic acid prevents TGF-β1-induced COX-2 repression in human lung fibroblasts post-transcriptionally by TIA-1 downregulation
title_sort suberanilohydroxamic acid prevents tgf-β1-induced cox-2 repression in human lung fibroblasts post-transcriptionally by tia-1 downregulation
topic Pulmonary fibrosis ; Cyclooxygenase 2 (COX-2) ; Post-transcriptional regulation ; epigenetics ; Histone deacetylase inhibitor ; Transforming growth factor β1 (TGF-β1)
url https://eprints.nottingham.ac.uk/51701/
https://eprints.nottingham.ac.uk/51701/
https://eprints.nottingham.ac.uk/51701/