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Published in: Respiratory Research 1/2018

Open Access 01-12-2018 | Research

Transforming growth factor beta1 targets estrogen receptor signaling in bronchial epithelial cells

Authors: L. Cody Smith, Santiago Moreno, Lauren Robertson, Sarah Robinson, Kristal Gant, Andrew J. Bryant, Tara Sabo-Attwood

Published in: Respiratory Research | Issue 1/2018

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Abstract

Background

Sex differences in idiopathic pulmonary fibrosis (IPF) suggest a protective role for estrogen (E2); however, mechanistic studies in animal models have produced mixed results. Reports using cell lines have investigated molecular interactions between transforming growth factor beta1 (TGF-β1) and estrogen receptor (ESR) pathways in breast, prostate, and skin cells, but no such interactions have been described in human lung cells. To address this gap in the literature, we investigated a role for E2 in modulating TGF-β1-induced signaling mechanisms and identified novel pathways impacted by estrogen in bronchial epithelial cells.

Methods

We investigated a role for E2 in modulating TGF-β1-induced epithelial to mesenchymal transition (EMT) in bronchial epithelial cells (BEAS-2Bs) and characterized the effect of TGF-β1 on ESR mRNA and protein expression in BEAS-2Bs. We also quantified mRNA expression of ESRs in lung tissue from individuals with IPF and identified potential downstream targets of E2 signaling in BEAS-2Bs using RNA-Seq and gene set enrichment analysis.

Results

E2 negligibly modulated TGF-β1-induced EMT; however, we report the novel observation that TGF-β1 repressed ESR expression, most notably estrogen receptor alpha (ESR1). Results of the RNA-Seq analysis showed that TGF-β1 and E2 inversely modulated the expression of several genes involved in processes such as extracellular matrix (ECM) turnover, airway smooth muscle cell contraction, and calcium flux regulation. We also report that E2 specifically modulated the expression of genes involved in chromatin remodeling pathways and that this regulation was absent in the presence of TGF-β1.

Conclusions

Collectively, these results suggest that E2 influences unexplored pathways that may be relevant to pulmonary disease and highlights potential roles for E2 in the lung that may contribute to sex-specific differences.
Appendix
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Literature
1.
go back to reference Han MK, Murray S, Fell CD, Flaherty KR, Toews GB, Myers J, Colby TV, Travis WD, Kazerooni EA, Gross BH, Martinez FJ. Sex differences in physiological progression of idiopathic pulmonary fibrosis. Eur Respir J. 2008;31:1183–8.CrossRefPubMed Han MK, Murray S, Fell CD, Flaherty KR, Toews GB, Myers J, Colby TV, Travis WD, Kazerooni EA, Gross BH, Martinez FJ. Sex differences in physiological progression of idiopathic pulmonary fibrosis. Eur Respir J. 2008;31:1183–8.CrossRefPubMed
2.
go back to reference Gribbin J, Hubbard RB, Le Jeune I, Smith CJ, West J, Tata LJ. Incidence and mortality of idiopathic pulmonary fibrosis and sarcoidosis in the UK. Thorax. 2006;61:980–5.CrossRefPubMedPubMedCentral Gribbin J, Hubbard RB, Le Jeune I, Smith CJ, West J, Tata LJ. Incidence and mortality of idiopathic pulmonary fibrosis and sarcoidosis in the UK. Thorax. 2006;61:980–5.CrossRefPubMedPubMedCentral
3.
go back to reference Olson AL, Swigris JJ, Lezotte DC, Norris JM, Wilson CG, Brown KK. Mortality from pulmonary fibrosis increased in the United States from 1992 to 2003. Am J Respir Crit Care Med. 2007;176:277–84.CrossRefPubMed Olson AL, Swigris JJ, Lezotte DC, Norris JM, Wilson CG, Brown KK. Mortality from pulmonary fibrosis increased in the United States from 1992 to 2003. Am J Respir Crit Care Med. 2007;176:277–84.CrossRefPubMed
4.
go back to reference Raghu G, Weycker D, Edelsberg J, Bradford WZ, Oster G. Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2006;174:810–6.CrossRefPubMed Raghu G, Weycker D, Edelsberg J, Bradford WZ, Oster G. Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2006;174:810–6.CrossRefPubMed
5.
go back to reference Raghu G, Chen SY, Hou Q, Yeh WS, Collard HR. Incidence and prevalence of idiopathic pulmonary fibrosis in US adults 18–64 years old. Eur Respir J. 2016;48:179–86.CrossRefPubMed Raghu G, Chen SY, Hou Q, Yeh WS, Collard HR. Incidence and prevalence of idiopathic pulmonary fibrosis in US adults 18–64 years old. Eur Respir J. 2016;48:179–86.CrossRefPubMed
6.
go back to reference McGee SP, Zhang H, Karmaus W, Sabo-Attwood T. Influence of sex and disease severity on gene expression profiles in individuals with idiopathic pulmonary fibrosis. Int J Mol Epidemiol Genet. 2014;5:71–86.PubMedPubMedCentral McGee SP, Zhang H, Karmaus W, Sabo-Attwood T. Influence of sex and disease severity on gene expression profiles in individuals with idiopathic pulmonary fibrosis. Int J Mol Epidemiol Genet. 2014;5:71–86.PubMedPubMedCentral
7.
go back to reference Redente EF, Jacobsen KM, Solomon JJ, Lara AR, Faubel S, Keith RC, Henson PM, Downey GP, Riches DW. Age and sex dimorphisms contribute to the severity of bleomycin-induced lung injury and fibrosis. Am J Physiol Lung Cell Mol Physiol. 2011;301:L510–8.CrossRefPubMedPubMedCentral Redente EF, Jacobsen KM, Solomon JJ, Lara AR, Faubel S, Keith RC, Henson PM, Downey GP, Riches DW. Age and sex dimorphisms contribute to the severity of bleomycin-induced lung injury and fibrosis. Am J Physiol Lung Cell Mol Physiol. 2011;301:L510–8.CrossRefPubMedPubMedCentral
8.
go back to reference Voltz JW, Card JW, Carey MA, LM DG, Ferguson CD, Flake GP, Bonner JC, Korach KS, Zeldin DC. Male sex hormones exacerbate lung function impairment after bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol. 2008;39:45–52.CrossRefPubMedPubMedCentral Voltz JW, Card JW, Carey MA, LM DG, Ferguson CD, Flake GP, Bonner JC, Korach KS, Zeldin DC. Male sex hormones exacerbate lung function impairment after bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol. 2008;39:45–52.CrossRefPubMedPubMedCentral
9.
go back to reference Valera IC, Kafaja S, Pham B, Fishbein M, Singh RR. Investigating mechanisms of sex bias in lung fibrosis using mice with sex chromosome complement. J Immunol. 2016;196:197–8. Valera IC, Kafaja S, Pham B, Fishbein M, Singh RR. Investigating mechanisms of sex bias in lung fibrosis using mice with sex chromosome complement. J Immunol. 2016;196:197–8.
10.
11.
go back to reference Haston CK, Wang M, Dejournett RE, Zhou X, Ni D, Gu X, King TM, Weil MM, Newman RA, Amos CI, Travis EL. Bleomycin hydrolase and a genetic locus within the MHC affect risk for pulmonary fibrosis in mice. Hum Mol Gen. 2002;11:1855–63.CrossRefPubMed Haston CK, Wang M, Dejournett RE, Zhou X, Ni D, Gu X, King TM, Weil MM, Newman RA, Amos CI, Travis EL. Bleomycin hydrolase and a genetic locus within the MHC affect risk for pulmonary fibrosis in mice. Hum Mol Gen. 2002;11:1855–63.CrossRefPubMed
12.
go back to reference Lekgabe ED, Royce SG, Hewitson TD, MLK T, Zhao C, Moore XL, Tregear GW, Bathgate RA, Du XJ SCS. The effects of relaxin and estrogen deficiency on collagen deposition and hypertrophy of nonreproductive organs. Endocrinology. 2006;147:5575–83.CrossRefPubMed Lekgabe ED, Royce SG, Hewitson TD, MLK T, Zhao C, Moore XL, Tregear GW, Bathgate RA, Du XJ SCS. The effects of relaxin and estrogen deficiency on collagen deposition and hypertrophy of nonreproductive organs. Endocrinology. 2006;147:5575–83.CrossRefPubMed
13.
go back to reference Chang EC, Frasor J, Komm B, Katzenellenbogen BS. Impact of estrogen receptor β on gene networks regulated by estrogen receptor α in breast cancer cells. Endocrinology. 2006;147:4831–42.CrossRefPubMed Chang EC, Frasor J, Komm B, Katzenellenbogen BS. Impact of estrogen receptor β on gene networks regulated by estrogen receptor α in breast cancer cells. Endocrinology. 2006;147:4831–42.CrossRefPubMed
14.
go back to reference Ito I, Hanyu A, Wayama M, Goto N, Katsuno Y, Kawasaki S, Nakajima Y, Kajiro M, Komatsu Y, Fujimura A. Estrogen inhibits transforming growth factor β signaling by promoting Smad2/3 degradation. J Biol Chem. 2010;285:14747–55.CrossRefPubMedPubMedCentral Ito I, Hanyu A, Wayama M, Goto N, Katsuno Y, Kawasaki S, Nakajima Y, Kajiro M, Komatsu Y, Fujimura A. Estrogen inhibits transforming growth factor β signaling by promoting Smad2/3 degradation. J Biol Chem. 2010;285:14747–55.CrossRefPubMedPubMedCentral
15.
go back to reference Goto N, Hiyoshi H, Ito I, Tsuchiya M, Nakajima Y, Yanagisawa J. Estrogen and antiestrogens alter breast cancer invasiveness by modulating the transforming growth factor-β signaling pathway. Cancer Sci. 2011;102:1501–8.CrossRefPubMed Goto N, Hiyoshi H, Ito I, Tsuchiya M, Nakajima Y, Yanagisawa J. Estrogen and antiestrogens alter breast cancer invasiveness by modulating the transforming growth factor-β signaling pathway. Cancer Sci. 2011;102:1501–8.CrossRefPubMed
16.
go back to reference Ashcroft GS, Dodsworth J, Van Boxtel E, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson MWJ. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-b1 levels. Nat Med. 1997;3:1209–15.CrossRefPubMed Ashcroft GS, Dodsworth J, Van Boxtel E, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson MWJ. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-b1 levels. Nat Med. 1997;3:1209–15.CrossRefPubMed
17.
go back to reference Lovegrove AS, Sun J, Gould KA, Lubahn DB, Korach KS, Lane PH. Estrogen receptor α-mediated events promote sex-specific diabetic glomerular hypertrophy. Am J Physiol Renal Physiol. 2004;287:F586–91.CrossRefPubMed Lovegrove AS, Sun J, Gould KA, Lubahn DB, Korach KS, Lane PH. Estrogen receptor α-mediated events promote sex-specific diabetic glomerular hypertrophy. Am J Physiol Renal Physiol. 2004;287:F586–91.CrossRefPubMed
18.
go back to reference Stope MB, Popp SL, Knabbe C, Buck MB. Estrogen receptor α attenuates transforming growth factor-β signaling in breast cancer cells independent from agonistic and antagonistic ligands. Breast Cancer Res Treat. 2010;120:357–67.CrossRefPubMed Stope MB, Popp SL, Knabbe C, Buck MB. Estrogen receptor α attenuates transforming growth factor-β signaling in breast cancer cells independent from agonistic and antagonistic ligands. Breast Cancer Res Treat. 2010;120:357–67.CrossRefPubMed
19.
go back to reference Yamamoto T, Saatcioglu F, Matsuda T. Cross-talk between bone morphogenic proteins and estrogen receptor signaling. Endocrinology. 2002;143:2635–42.CrossRefPubMed Yamamoto T, Saatcioglu F, Matsuda T. Cross-talk between bone morphogenic proteins and estrogen receptor signaling. Endocrinology. 2002;143:2635–42.CrossRefPubMed
20.
go back to reference Matsuda T, Yamamoto T, Muraguchi A, Saatcioglu F. Cross-talk between transforming growth factor-β and estrogen receptor signaling through Smad3. J Biol Chem. 2001;276:42908–14.CrossRefPubMed Matsuda T, Yamamoto T, Muraguchi A, Saatcioglu F. Cross-talk between transforming growth factor-β and estrogen receptor signaling through Smad3. J Biol Chem. 2001;276:42908–14.CrossRefPubMed
21.
go back to reference Kleuser B, Malek D, Gust R, Pertz HH, Potteck H. 17-β-estradiol inhibits transforming growth factor-β signaling and function in breast cancer cells via activation of extracellular signal-regulated kinase through the G protein-coupled receptor 30. Mol Pharmacol. 2008;74:1533–43.CrossRefPubMed Kleuser B, Malek D, Gust R, Pertz HH, Potteck H. 17-β-estradiol inhibits transforming growth factor-β signaling and function in breast cancer cells via activation of extracellular signal-regulated kinase through the G protein-coupled receptor 30. Mol Pharmacol. 2008;74:1533–43.CrossRefPubMed
22.
go back to reference Li YC, Ding XS, Li HM, Zhang Y, Bao J. Role of G protein-coupled estrogen receptor 1 in modulating transforming growth factor-β stimulated mesangial cell extracellular matrix synthesis and migration. Mol Cell Endocrinol. 2014;391:50–9.CrossRefPubMed Li YC, Ding XS, Li HM, Zhang Y, Bao J. Role of G protein-coupled estrogen receptor 1 in modulating transforming growth factor-β stimulated mesangial cell extracellular matrix synthesis and migration. Mol Cell Endocrinol. 2014;391:50–9.CrossRefPubMed
23.
go back to reference Society AT. Idiopathic pulmonary fibrosis, diagnosis and treatment. (International consensus statement). Am J Respir Crit Care Med. 2000;161:646–64.CrossRef Society AT. Idiopathic pulmonary fibrosis, diagnosis and treatment. (International consensus statement). Am J Respir Crit Care Med. 2000;161:646–64.CrossRef
24.
go back to reference Travis WD, King TE, Bateman ED, Lynch DA, Capron F, Center D, Colby TV, Cordier JF, DuBois RM, Galvin J. American Thoracic Society/European Respiratory Society international multidisciplinary consensus classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med. 2002;165:277–304.CrossRef Travis WD, King TE, Bateman ED, Lynch DA, Capron F, Center D, Colby TV, Cordier JF, DuBois RM, Galvin J. American Thoracic Society/European Respiratory Society international multidisciplinary consensus classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med. 2002;165:277–304.CrossRef
25.
go back to reference Bryant AJ, Carrick RP, McConaha ME, Jones BR, Shay SD, Moore CS, Blackwell TR, Gladson S, Penner NL, Burman A. Endothelial HIF signaling regulates pulmonary fibrosis-associated pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2016;310:L249–62.CrossRefPubMed Bryant AJ, Carrick RP, McConaha ME, Jones BR, Shay SD, Moore CS, Blackwell TR, Gladson S, Penner NL, Burman A. Endothelial HIF signaling regulates pulmonary fibrosis-associated pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2016;310:L249–62.CrossRefPubMed
26.
go back to reference Smith LC, Ralston-Hooper KJ, Ferguson PL, Sabo-Attwood T. The G protein-coupled estrogen receptor agonist G-1 inhibits nuclear estrogen receptor activity and stimulates novel phosphoproteomic signatures. Toxicol Sci. 2016;151:434–46.CrossRefPubMedPubMedCentral Smith LC, Ralston-Hooper KJ, Ferguson PL, Sabo-Attwood T. The G protein-coupled estrogen receptor agonist G-1 inhibits nuclear estrogen receptor activity and stimulates novel phosphoproteomic signatures. Toxicol Sci. 2016;151:434–46.CrossRefPubMedPubMedCentral
27.
go back to reference Smith LC, Clark JC, Bisesi JH, Ferguson PL, Sabo-Attwood T. Differential recruitment of co-regulatory proteins to the human estrogen receptor 1 in response to xenoestrogens. Comp Biochem Physiol Part D Genomics Proteomics. 2016;19:159–73.CrossRefPubMedPubMedCentral Smith LC, Clark JC, Bisesi JH, Ferguson PL, Sabo-Attwood T. Differential recruitment of co-regulatory proteins to the human estrogen receptor 1 in response to xenoestrogens. Comp Biochem Physiol Part D Genomics Proteomics. 2016;19:159–73.CrossRefPubMedPubMedCentral
28.
go back to reference Kamitani S, Yamauchi Y, Kawasaki S, Takami K, Takizawa H, Nagase T, Kohyama T. Simultaneous stimulation with TGF-β1 and TNF-α induces epithelial mesenchymal transition in bronchial epithelial cells. Int Arch Allergy Immunol. 2011;155:119–28.CrossRefPubMed Kamitani S, Yamauchi Y, Kawasaki S, Takami K, Takizawa H, Nagase T, Kohyama T. Simultaneous stimulation with TGF-β1 and TNF-α induces epithelial mesenchymal transition in bronchial epithelial cells. Int Arch Allergy Immunol. 2011;155:119–28.CrossRefPubMed
29.
go back to reference Doerner AM, Zuraw BL. TGF-β1 induced epithelial to mesenchymal transition (EMT) in human bronchial epithelial cells is enhanced by IL-1β but not abrogated by corticosteroids. Respir Res. 2009;10:100.CrossRefPubMedPubMedCentral Doerner AM, Zuraw BL. TGF-β1 induced epithelial to mesenchymal transition (EMT) in human bronchial epithelial cells is enhanced by IL-1β but not abrogated by corticosteroids. Respir Res. 2009;10:100.CrossRefPubMedPubMedCentral
30.
go back to reference Hosper NA, van den Berg PP, de Rond S, Popa ER, Wilmer MJ, Masereeuw R, Bank RA. Epithelial-to-mesenchymal transition in fibrosis: collagen type I expression is highly upregulated after EMT, but does not contribute to collagen deposition. Exp Cell Res. 2013;319:3000–9.CrossRefPubMed Hosper NA, van den Berg PP, de Rond S, Popa ER, Wilmer MJ, Masereeuw R, Bank RA. Epithelial-to-mesenchymal transition in fibrosis: collagen type I expression is highly upregulated after EMT, but does not contribute to collagen deposition. Exp Cell Res. 2013;319:3000–9.CrossRefPubMed
31.
go back to reference Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M. A practical approach to RT-qPCR—publishing data that conform to the MIQE guidelines. Methods. 2010;50:S1–5.CrossRefPubMed Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M. A practical approach to RT-qPCR—publishing data that conform to the MIQE guidelines. Methods. 2010;50:S1–5.CrossRefPubMed
32.
go back to reference Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007;8:R19.CrossRefPubMedPubMedCentral Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007;8:R19.CrossRefPubMedPubMedCentral
35.
go back to reference Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30:207–10.CrossRefPubMedPubMedCentral Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30:207–10.CrossRefPubMedPubMedCentral
36.
go back to reference Alhamad EH, Cal JG, Shakoor Z, Almogren A, AlBoukai AA. Cytokine gene polymorphisms and serum cytokine levels in patients with idiopathic pulmonary fibrosis. BMC Med Genet. 2013;14:66.CrossRefPubMedPubMedCentral Alhamad EH, Cal JG, Shakoor Z, Almogren A, AlBoukai AA. Cytokine gene polymorphisms and serum cytokine levels in patients with idiopathic pulmonary fibrosis. BMC Med Genet. 2013;14:66.CrossRefPubMedPubMedCentral
37.
go back to reference Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102:15545–50.CrossRefPubMed Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102:15545–50.CrossRefPubMed
38.
go back to reference Stabile LP, Davis ALG, Gubish CT, Hopkins TM, Luketich JD, Christie N, Finkelstein S, Siegfried JM. Human non-small cell lung tumors and cells derived from normal lung express both estrogen receptor α and β and show biological responses to estrogen. Cancer Res. 2002;62:2141–50.PubMed Stabile LP, Davis ALG, Gubish CT, Hopkins TM, Luketich JD, Christie N, Finkelstein S, Siegfried JM. Human non-small cell lung tumors and cells derived from normal lung express both estrogen receptor α and β and show biological responses to estrogen. Cancer Res. 2002;62:2141–50.PubMed
39.
go back to reference Mollerup S, Jørgensen K, Berge G, Haugen A. Expression of estrogen receptors α and β in human lung tissue and cell lines. Lung Cancer. 2002;37:153–9.CrossRefPubMed Mollerup S, Jørgensen K, Berge G, Haugen A. Expression of estrogen receptors α and β in human lung tissue and cell lines. Lung Cancer. 2002;37:153–9.CrossRefPubMed
40.
go back to reference Couse JF, Lindzey J, Grandien K, Gustafsson J, Korach KS. Tissue distribution and quantitative analysis of estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) messenger ribonucleic acid in the wild-type and ERα-knockout mouse. Endocrinology. 1997;138:4613–21.CrossRefPubMed Couse JF, Lindzey J, Grandien K, Gustafsson J, Korach KS. Tissue distribution and quantitative analysis of estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) messenger ribonucleic acid in the wild-type and ERα-knockout mouse. Endocrinology. 1997;138:4613–21.CrossRefPubMed
41.
go back to reference Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D, Chapman HA. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA. 2006;103:13180–5.CrossRefPubMed Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D, Chapman HA. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA. 2006;103:13180–5.CrossRefPubMed
42.
go back to reference Willis BC, Borok Z. TGF-b-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol. 2007;293:L525–34.CrossRefPubMed Willis BC, Borok Z. TGF-b-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol. 2007;293:L525–34.CrossRefPubMed
43.
44.
go back to reference Bartis D, Mise N, Mahida RY, Eickelberg O, Thickett DR. Epithelial-mesenchymal transition in lung development and disease: does it exist and is it important? Thorax. 2014;69:760–5.CrossRefPubMed Bartis D, Mise N, Mahida RY, Eickelberg O, Thickett DR. Epithelial-mesenchymal transition in lung development and disease: does it exist and is it important? Thorax. 2014;69:760–5.CrossRefPubMed
45.
go back to reference Kasai H, Allen JT, Mason RM, Kamimura T, Zhang Z. TGF-b1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res. 2005;6:56.CrossRefPubMedPubMedCentral Kasai H, Allen JT, Mason RM, Kamimura T, Zhang Z. TGF-b1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res. 2005;6:56.CrossRefPubMedPubMedCentral
47.
go back to reference Wik E, Ræder MB, Krakstad C, Trovik J, Birkeland E, Hoivik EA, Mjos S, Werner HM, Mannelqvist M, Stefansson IM. Lack of estrogen receptor-α is associated with epithelial–mesenchymal transition and PI3K alterations in endometrial carcinoma. Clin Cancer Res. 2013;19:1094–105.CrossRefPubMed Wik E, Ræder MB, Krakstad C, Trovik J, Birkeland E, Hoivik EA, Mjos S, Werner HM, Mannelqvist M, Stefansson IM. Lack of estrogen receptor-α is associated with epithelial–mesenchymal transition and PI3K alterations in endometrial carcinoma. Clin Cancer Res. 2013;19:1094–105.CrossRefPubMed
48.
go back to reference Dhasarathy A, Kajita M, Wade PA. The transcription factor snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-α. Mol Endocrinol. 2007;21:2907–18.CrossRefPubMedPubMedCentral Dhasarathy A, Kajita M, Wade PA. The transcription factor snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-α. Mol Endocrinol. 2007;21:2907–18.CrossRefPubMedPubMedCentral
49.
go back to reference Guttilla IK, Adams BD, White BA. ERα, microRNAs, and the epithelial–mesenchymal transition in breast cancer. Trends Endocrinol Metab. 2012;23:73–82.CrossRefPubMed Guttilla IK, Adams BD, White BA. ERα, microRNAs, and the epithelial–mesenchymal transition in breast cancer. Trends Endocrinol Metab. 2012;23:73–82.CrossRefPubMed
50.
go back to reference Ye Y, Xiao Y, Wang W, Yearsley K, Gao J, Shetuni B, Barsky S. ERα signaling through slug regulates E-cadherin and EMT. Oncogene. 2010;29:1451–62.CrossRefPubMed Ye Y, Xiao Y, Wang W, Yearsley K, Gao J, Shetuni B, Barsky S. ERα signaling through slug regulates E-cadherin and EMT. Oncogene. 2010;29:1451–62.CrossRefPubMed
51.
go back to reference Mak P, Leav I, Pursell B, Bae D, Yang X, Taglienti CA, Gouvin LM, Sharma VM, Mercurio AM. ERβ impedes prostate cancer EMT by destabilizing HIF-1α and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell. 2010;17:319–32.CrossRefPubMedPubMedCentral Mak P, Leav I, Pursell B, Bae D, Yang X, Taglienti CA, Gouvin LM, Sharma VM, Mercurio AM. ERβ impedes prostate cancer EMT by destabilizing HIF-1α and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell. 2010;17:319–32.CrossRefPubMedPubMedCentral
52.
go back to reference Planas-Silva MD, Waltz PK. Estrogen promotes reversible epithelial-to-mesenchymal-like transition and collective motility in MCF-7 breast cancer cells. J Steroid Biochem Mol Biol. 2007;104:11–21.CrossRefPubMed Planas-Silva MD, Waltz PK. Estrogen promotes reversible epithelial-to-mesenchymal-like transition and collective motility in MCF-7 breast cancer cells. J Steroid Biochem Mol Biol. 2007;104:11–21.CrossRefPubMed
53.
go back to reference Fridriksdottir AJ, Kim J, Villadsen R, Klitgaard MC, Hopkinson BM, Petersen OW, Rønnov-Jessen L. Propagation of oestrogen receptor-positive and oestrogen-responsive normal human breast cells in culture. Nature communications. 2015;6:8786.CrossRefPubMedPubMedCentral Fridriksdottir AJ, Kim J, Villadsen R, Klitgaard MC, Hopkinson BM, Petersen OW, Rønnov-Jessen L. Propagation of oestrogen receptor-positive and oestrogen-responsive normal human breast cells in culture. Nature communications. 2015;6:8786.CrossRefPubMedPubMedCentral
54.
go back to reference Stoica A, Saceda M, Fakhro A, Solomon HB, Fenster BD, Martin MB. The role of transforming growth factor-β in the regulation of estrogen receptor expression in the MCF-7 breast cancer cell line. Endocrinology. 1997;138:1498–505.CrossRefPubMed Stoica A, Saceda M, Fakhro A, Solomon HB, Fenster BD, Martin MB. The role of transforming growth factor-β in the regulation of estrogen receptor expression in the MCF-7 breast cancer cell line. Endocrinology. 1997;138:1498–505.CrossRefPubMed
55.
go back to reference Petrel TA, Brueggemeier RW. Increased proteasome-dependent degradation of estrogen receptor-alpha by TGF-β1 in breast cancer cell lines. J Cell Biochem. 2003;88:181–90.CrossRefPubMedPubMedCentral Petrel TA, Brueggemeier RW. Increased proteasome-dependent degradation of estrogen receptor-alpha by TGF-β1 in breast cancer cell lines. J Cell Biochem. 2003;88:181–90.CrossRefPubMedPubMedCentral
56.
go back to reference Sonnylal S, Xu S, Jones H, Tam A, Sreeram VR, Ponticos M, Norman J, Agrawal P, Abraham D, de Crombrugghe B. Connective tissue growth factor causes EMT-like cell fate changes in vivo and in vitro. J Cell Sci. 2013;126:2164–75.CrossRefPubMedPubMedCentral Sonnylal S, Xu S, Jones H, Tam A, Sreeram VR, Ponticos M, Norman J, Agrawal P, Abraham D, de Crombrugghe B. Connective tissue growth factor causes EMT-like cell fate changes in vivo and in vitro. J Cell Sci. 2013;126:2164–75.CrossRefPubMedPubMedCentral
57.
go back to reference Leask A, Abraham DJ. The role of connective tissue growth factor, a multifunctional matricellular protein, in fibroblast biology. Biochem Cell Biol. 2003;81:355–63.CrossRefPubMed Leask A, Abraham DJ. The role of connective tissue growth factor, a multifunctional matricellular protein, in fibroblast biology. Biochem Cell Biol. 2003;81:355–63.CrossRefPubMed
58.
go back to reference Mäkelä M, Larjava H, Pirilä E, Maisi P, Salo T, Sorsa T, Uitto V-J. Matrix metalloproteinase 2 (gelatinase A) is related to migration of keratinocytes. Exp Cell Res. 1999;251:67–78.CrossRefPubMed Mäkelä M, Larjava H, Pirilä E, Maisi P, Salo T, Sorsa T, Uitto V-J. Matrix metalloproteinase 2 (gelatinase A) is related to migration of keratinocytes. Exp Cell Res. 1999;251:67–78.CrossRefPubMed
59.
go back to reference Kim ES, Sohn YW, Moon A. TGF-β-induced transcriptional activation of MMP-2 is mediated by activating transcription factor (ATF) 2 in human breast epithelial cells. Cancer Lett. 2007;252:147–56.CrossRefPubMed Kim ES, Sohn YW, Moon A. TGF-β-induced transcriptional activation of MMP-2 is mediated by activating transcription factor (ATF) 2 in human breast epithelial cells. Cancer Lett. 2007;252:147–56.CrossRefPubMed
60.
go back to reference Seomun Y, Kim J, Choun-Ki J. Overexpression of matrix metalloproteinase-2 mediates phenotypic transformation of lens epithelial cells. Biochem J. 2001;358:41–8.CrossRefPubMedPubMedCentral Seomun Y, Kim J, Choun-Ki J. Overexpression of matrix metalloproteinase-2 mediates phenotypic transformation of lens epithelial cells. Biochem J. 2001;358:41–8.CrossRefPubMedPubMedCentral
61.
go back to reference Kheradmand F, Rishi K, Werb Z. Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2. J Cell Sci. 2002;115:839–48.PubMedPubMedCentral Kheradmand F, Rishi K, Werb Z. Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2. J Cell Sci. 2002;115:839–48.PubMedPubMedCentral
62.
go back to reference Ravanti L, Kahari V. Matrix metalloproteinases in wound repair. Int J Mol Med. 2000;6:391–407.PubMed Ravanti L, Kahari V. Matrix metalloproteinases in wound repair. Int J Mol Med. 2000;6:391–407.PubMed
63.
go back to reference García-Alvarez J, Ramirez R, Sampieri CL, Nuttall RK, Edwards DR, Selman M, Pardo A. Membrane type-matrix metalloproteinases in idiopathic pulmonary fibrosis. Sarcoidosis Vasc Diffuse Lung Dis. 2006;23:13–21.PubMed García-Alvarez J, Ramirez R, Sampieri CL, Nuttall RK, Edwards DR, Selman M, Pardo A. Membrane type-matrix metalloproteinases in idiopathic pulmonary fibrosis. Sarcoidosis Vasc Diffuse Lung Dis. 2006;23:13–21.PubMed
64.
go back to reference Craig VJ, Zhang L, Hagood JS, Owen CA. Matrix metalloproteinases as therapeutic targets for idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol. 2015;53:585–600.CrossRefPubMedPubMedCentral Craig VJ, Zhang L, Hagood JS, Owen CA. Matrix metalloproteinases as therapeutic targets for idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol. 2015;53:585–600.CrossRefPubMedPubMedCentral
65.
go back to reference Dozynkiewicz MA, Jamieson NB, MacPherson I, Grindlay J, van den Berghe PV, von Thun A, Morton JP, Gourley C, Timpson P, Nixon C. Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev Cell. 2012;22:131–45.CrossRefPubMedPubMedCentral Dozynkiewicz MA, Jamieson NB, MacPherson I, Grindlay J, van den Berghe PV, von Thun A, Morton JP, Gourley C, Timpson P, Nixon C. Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev Cell. 2012;22:131–45.CrossRefPubMedPubMedCentral
66.
go back to reference Macpherson IR, Rainero E, Mitchell LE, Van Den Berghe PV, Speirs C, Dozynkiewicz MA, Chaudhary S, Kalna G, Edwards J, Timpson P. CLIC3 controls recycling of late endosomal MT1-MMP and dictates invasion and metastasis in breast cancer. J Cell Sci. 2014;127:3893–901.CrossRefPubMed Macpherson IR, Rainero E, Mitchell LE, Van Den Berghe PV, Speirs C, Dozynkiewicz MA, Chaudhary S, Kalna G, Edwards J, Timpson P. CLIC3 controls recycling of late endosomal MT1-MMP and dictates invasion and metastasis in breast cancer. J Cell Sci. 2014;127:3893–901.CrossRefPubMed
67.
go back to reference Koenig GC, Rowe RG, Day SM, Sabeh F, Atkinson JJ, Cooke KR, Weiss SJ. MT1-MMP–dependent remodeling of cardiac extracellular matrix structure and function following myocardial infarction. Am J Pathol. 2012;180:1863–78.CrossRefPubMedPubMedCentral Koenig GC, Rowe RG, Day SM, Sabeh F, Atkinson JJ, Cooke KR, Weiss SJ. MT1-MMP–dependent remodeling of cardiac extracellular matrix structure and function following myocardial infarction. Am J Pathol. 2012;180:1863–78.CrossRefPubMedPubMedCentral
68.
go back to reference Karow M, Popp T, Egea V, Ries C, Jochum M, Neth P. Wnt signalling in mouse mesenchymal stem cells: impact on proliferation, invasion and MMP expression. J Cell Mol Med. 2009;13:2506–20.CrossRefPubMed Karow M, Popp T, Egea V, Ries C, Jochum M, Neth P. Wnt signalling in mouse mesenchymal stem cells: impact on proliferation, invasion and MMP expression. J Cell Mol Med. 2009;13:2506–20.CrossRefPubMed
69.
go back to reference Mu D, Cambier S, Fjellbirkeland L, Baron JL, Munger JS, Kawakatsu H, Sheppard D, Broaddus VC, Nishimura SL. The integrin αvβ8 mediates epithelial homeostasis through MT1-MMP–dependent activation of TGF-β1. J Cell Biol. 2002;157:493–507.CrossRefPubMedPubMedCentral Mu D, Cambier S, Fjellbirkeland L, Baron JL, Munger JS, Kawakatsu H, Sheppard D, Broaddus VC, Nishimura SL. The integrin αvβ8 mediates epithelial homeostasis through MT1-MMP–dependent activation of TGF-β1. J Cell Biol. 2002;157:493–507.CrossRefPubMedPubMedCentral
70.
go back to reference Folli C, Calderone V, Ramazzina I, Zanotti G, Berni R. Ligand binding and structural analysis of a human putative cellular retinol-binding protein. J Biol Chem. 2002;277:41970–7.CrossRefPubMed Folli C, Calderone V, Ramazzina I, Zanotti G, Berni R. Ligand binding and structural analysis of a human putative cellular retinol-binding protein. J Biol Chem. 2002;277:41970–7.CrossRefPubMed
71.
go back to reference Molyneaux PL, Willis Owen SA, Cox MJ, James P, Cowman S, Loebinger M, Blanchard A, Edwards LM, Stock C, Daccord C. Host-microbial interactions in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2017;195(12):1640–50.CrossRefPubMedPubMedCentral Molyneaux PL, Willis Owen SA, Cox MJ, James P, Cowman S, Loebinger M, Blanchard A, Edwards LM, Stock C, Daccord C. Host-microbial interactions in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2017;195(12):1640–50.CrossRefPubMedPubMedCentral
72.
go back to reference Soulet F, Kilarski WW, Antczak P, Herbert J, Bicknell R, Falciani F, Bikfalvi A. Gene signatures in wound tissue as evidenced by molecular profiling in the chick embryo model. BMC Genomics. 2010;11:495.CrossRefPubMedPubMedCentral Soulet F, Kilarski WW, Antczak P, Herbert J, Bicknell R, Falciani F, Bikfalvi A. Gene signatures in wound tissue as evidenced by molecular profiling in the chick embryo model. BMC Genomics. 2010;11:495.CrossRefPubMedPubMedCentral
73.
go back to reference Kinyamu HK, Collins JB, Grissom SF, Hebbar PB, Archer TK. Genome wide transcriptional profiling in breast cancer cells reveals distinct changes in hormone receptor target genes and chromatin modifying enzymes after proteasome inhibition. Mol Carcinog. 2008;47:845–85.CrossRefPubMedPubMedCentral Kinyamu HK, Collins JB, Grissom SF, Hebbar PB, Archer TK. Genome wide transcriptional profiling in breast cancer cells reveals distinct changes in hormone receptor target genes and chromatin modifying enzymes after proteasome inhibition. Mol Carcinog. 2008;47:845–85.CrossRefPubMedPubMedCentral
74.
go back to reference Calvo E, Belleau P, Martel C, Labrie F. Specific transcriptional response of four blockers of estrogen receptors on estradiol-modulated genes in the mouse mammary gland. Breast Cancer Res Treat. 2012;134:625–47.CrossRefPubMed Calvo E, Belleau P, Martel C, Labrie F. Specific transcriptional response of four blockers of estrogen receptors on estradiol-modulated genes in the mouse mammary gland. Breast Cancer Res Treat. 2012;134:625–47.CrossRefPubMed
75.
go back to reference Blobe GC, Schiemann WP, Lodish HF. Role of transforming growth factor β in human disease. New Engl J Med. 2000;342:1350–8.CrossRefPubMed Blobe GC, Schiemann WP, Lodish HF. Role of transforming growth factor β in human disease. New Engl J Med. 2000;342:1350–8.CrossRefPubMed
76.
go back to reference Parekh T, Saxena B, Reibman J, Cronstein BN, Gold LI. Neutrophil chemotaxis in response to TGF-beta isoforms (TGF-beta 1, TGF-beta 2, TGF-beta 3) is mediated by fibronectin. J Immunol. 1994;152:2456–66.PubMed Parekh T, Saxena B, Reibman J, Cronstein BN, Gold LI. Neutrophil chemotaxis in response to TGF-beta isoforms (TGF-beta 1, TGF-beta 2, TGF-beta 3) is mediated by fibronectin. J Immunol. 1994;152:2456–66.PubMed
77.
go back to reference Fernandez IE, Eickelberg O. The impact of TGF-β on lung fibrosis: from targeting to biomarkers. Proc Am Thorac Soc. 2012;9:111–6.CrossRefPubMed Fernandez IE, Eickelberg O. The impact of TGF-β on lung fibrosis: from targeting to biomarkers. Proc Am Thorac Soc. 2012;9:111–6.CrossRefPubMed
78.
go back to reference Border WA, Noble NA. Transforming growth factor β in tissue fibrosis. New Engl J Med. 1994;331:1286–92.CrossRefPubMed Border WA, Noble NA. Transforming growth factor β in tissue fibrosis. New Engl J Med. 1994;331:1286–92.CrossRefPubMed
79.
go back to reference Lai J-C, Cheng Y-W, Chiou H-L, Wu M-F, Chen C-Y, Lee H. Gender difference in estrogen receptor alpha promoter hypermethylation and its prognostic value in non-small cell lung cancer. Int J Cancer. 2005;117:974–80.CrossRefPubMed Lai J-C, Cheng Y-W, Chiou H-L, Wu M-F, Chen C-Y, Lee H. Gender difference in estrogen receptor alpha promoter hypermethylation and its prognostic value in non-small cell lung cancer. Int J Cancer. 2005;117:974–80.CrossRefPubMed
80.
go back to reference Coward WR, Saini G, Jenkins G. The pathogenesis of idiopathic pulmonary fibrosis. Ther Adv Respir Dis. 2010;4:367–88.CrossRefPubMed Coward WR, Saini G, Jenkins G. The pathogenesis of idiopathic pulmonary fibrosis. Ther Adv Respir Dis. 2010;4:367–88.CrossRefPubMed
81.
go back to reference Coward WR, Watts K, Feghali-Bostwick CA, Jenkins G, Pang L. Repression of IP-10 by interactions between histone deacetylation and hypermethylation in idiopathic pulmonary fibrosis. Mol Cell Biol. 2010;30:2874–86.CrossRefPubMedPubMedCentral Coward WR, Watts K, Feghali-Bostwick CA, Jenkins G, Pang L. Repression of IP-10 by interactions between histone deacetylation and hypermethylation in idiopathic pulmonary fibrosis. Mol Cell Biol. 2010;30:2874–86.CrossRefPubMedPubMedCentral
82.
go back to reference Coward WR, Watts K, Feghali-Bostwick CA, Knox A, Pang L. Defective histone acetylation is responsible for the diminished expression of cyclooxygenase 2 in idiopathic pulmonary fibrosis. Mol Cell Biol. 2009;29:4325–39.CrossRefPubMedPubMedCentral Coward WR, Watts K, Feghali-Bostwick CA, Knox A, Pang L. Defective histone acetylation is responsible for the diminished expression of cyclooxygenase 2 in idiopathic pulmonary fibrosis. Mol Cell Biol. 2009;29:4325–39.CrossRefPubMedPubMedCentral
83.
go back to reference Rabinovich EI, Kapetanaki MG, Steinfeld I, Gibson KF, Pandit KV, Yu G, Yakhini Z, Kaminski N. Global methylation patterns in idiopathic pulmonary fibrosis. PLoS One. 2012;7:e33770.CrossRefPubMedPubMedCentral Rabinovich EI, Kapetanaki MG, Steinfeld I, Gibson KF, Pandit KV, Yu G, Yakhini Z, Kaminski N. Global methylation patterns in idiopathic pulmonary fibrosis. PLoS One. 2012;7:e33770.CrossRefPubMedPubMedCentral
84.
go back to reference Sanders YY, Ambalavanan N, Halloran B, Zhang X, Liu H, Crossman DK, Bray M, Zhang K, Thannickal VJ, Hagood JS. Altered DNA methylation profile in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2012;186:525–35.CrossRefPubMedPubMedCentral Sanders YY, Ambalavanan N, Halloran B, Zhang X, Liu H, Crossman DK, Bray M, Zhang K, Thannickal VJ, Hagood JS. Altered DNA methylation profile in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2012;186:525–35.CrossRefPubMedPubMedCentral
85.
go back to reference Yang IV, Schwartz DA. Epigenetics of idiopathic pulmonary fibrosis. Transl Res. 2014;165.1(2015):48–60. Yang IV, Schwartz DA. Epigenetics of idiopathic pulmonary fibrosis. Transl Res. 2014;165.1(2015):48–60.
86.
go back to reference Wang Z, Chen C, Finger S, Jung M, Schwarz H, Swanson N, Lareu R, Raghunath M. Suberoylanilide hydroxamic acid: a potential epigenetic therapeutic agent for lung fibrosis? Eur Respir J. 2009;34:145–55.CrossRefPubMed Wang Z, Chen C, Finger S, Jung M, Schwarz H, Swanson N, Lareu R, Raghunath M. Suberoylanilide hydroxamic acid: a potential epigenetic therapeutic agent for lung fibrosis? Eur Respir J. 2009;34:145–55.CrossRefPubMed
87.
go back to reference Noh H, Oh EY, Seo JY, Yu MR, Kim YO, Ha H, Lee HB. Histone deacetylase-2 is a key regulator of diabetes-and transforming growth factor-β1-induced renal injury. Am J Physiol Renal Physiol. 2009;297:F729–39.CrossRefPubMed Noh H, Oh EY, Seo JY, Yu MR, Kim YO, Ha H, Lee HB. Histone deacetylase-2 is a key regulator of diabetes-and transforming growth factor-β1-induced renal injury. Am J Physiol Renal Physiol. 2009;297:F729–39.CrossRefPubMed
88.
go back to reference Cox DA, Helvering LM. Extracellular matrix integrity: a possible mechanism for differential clinical effects among selective estrogen receptor modulators and estrogens? Mol Cell Endocrinol. 2006;247:53–9.CrossRefPubMed Cox DA, Helvering LM. Extracellular matrix integrity: a possible mechanism for differential clinical effects among selective estrogen receptor modulators and estrogens? Mol Cell Endocrinol. 2006;247:53–9.CrossRefPubMed
89.
go back to reference Komm BS, Terpening CM, Benz DJ, Graeme KA, Gallegos A. Estrogen binding, receptor mRNA, and biologic response in osteoblast-like osteosarcoma cells. Science. 1988;241:81.CrossRefPubMed Komm BS, Terpening CM, Benz DJ, Graeme KA, Gallegos A. Estrogen binding, receptor mRNA, and biologic response in osteoblast-like osteosarcoma cells. Science. 1988;241:81.CrossRefPubMed
90.
go back to reference Son ED, Lee JY, Lee S, Kim MS, Lee BG, Chang IS, Chung JH. Topical application of 17β-estradiol increases extracellular matrix protein synthesis by stimulating TGF-β signaling in aged human skin in vivo. J Invest Dermatol. 2005;124:1149–61.CrossRefPubMed Son ED, Lee JY, Lee S, Kim MS, Lee BG, Chang IS, Chung JH. Topical application of 17β-estradiol increases extracellular matrix protein synthesis by stimulating TGF-β signaling in aged human skin in vivo. J Invest Dermatol. 2005;124:1149–61.CrossRefPubMed
91.
go back to reference Pincus DJ, Kassira N, Gombosh M, Berho M, Glassberg M, Karl M, Elliot SJ, Thaller S. 17β-Estradiol modifies diabetic wound healing by decreasing matrix metalloproteinase activity. Wounds. 2010;22:171–8.PubMed Pincus DJ, Kassira N, Gombosh M, Berho M, Glassberg M, Karl M, Elliot SJ, Thaller S. 17β-Estradiol modifies diabetic wound healing by decreasing matrix metalloproteinase activity. Wounds. 2010;22:171–8.PubMed
92.
go back to reference Beck LA, Tancowny B, Brummet ME, Asaki SY, Curry SL, Penno MB, Foster M, Bahl A, Stellato C. Functional analysis of the chemokine receptor CCR3 on airway epithelial cells. J Immunol. 2006;177:3344–54.CrossRefPubMed Beck LA, Tancowny B, Brummet ME, Asaki SY, Curry SL, Penno MB, Foster M, Bahl A, Stellato C. Functional analysis of the chemokine receptor CCR3 on airway epithelial cells. J Immunol. 2006;177:3344–54.CrossRefPubMed
93.
go back to reference Spizzo R, Nicoloso M, Lupini L, Lu Y, Fogarty J, Rossi S, Zagatti B, Fabbri M, Veronese A, Liu X. miR-145 participates with TP53 in a death-promoting regulatory loop and targets estrogen receptor-α in human breast cancer cells. Cell Death Differ. 2010;17:246–54.CrossRefPubMed Spizzo R, Nicoloso M, Lupini L, Lu Y, Fogarty J, Rossi S, Zagatti B, Fabbri M, Veronese A, Liu X. miR-145 participates with TP53 in a death-promoting regulatory loop and targets estrogen receptor-α in human breast cancer cells. Cell Death Differ. 2010;17:246–54.CrossRefPubMed
94.
go back to reference Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics. 2012;13:134.CrossRefPubMedPubMedCentral Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics. 2012;13:134.CrossRefPubMedPubMedCentral
95.
go back to reference Tanaka KI, Tanaka Y, Namba T, Azuma A, Mizushima T. Heat shock protein 70 protects against bleomycin-induced pulmonary fibrosis in mice. Biochem Pharmacol. 2010;80:920–31.CrossRefPubMed Tanaka KI, Tanaka Y, Namba T, Azuma A, Mizushima T. Heat shock protein 70 protects against bleomycin-induced pulmonary fibrosis in mice. Biochem Pharmacol. 2010;80:920–31.CrossRefPubMed
96.
go back to reference Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3—new capabilities and interfaces. Nucleic Acids Res. 2012;40:e115.CrossRefPubMedPubMedCentral Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3—new capabilities and interfaces. Nucleic Acids Res. 2012;40:e115.CrossRefPubMedPubMedCentral
97.
go back to reference Nagaraja T, Chen L, Balasubramanian A, Groopman JE, Ghoshal K, Jacob ST, Leask A, Brigstock DR, Anand AR, Ganju RK. Activation of the connective tissue growth factor (CTGF)-transforming growth factor β 1 (TGF-β 1) axis in hepatitis C virus-expressing hepatocytes. PLoS One. 2012;7:e46526.CrossRefPubMedPubMedCentral Nagaraja T, Chen L, Balasubramanian A, Groopman JE, Ghoshal K, Jacob ST, Leask A, Brigstock DR, Anand AR, Ganju RK. Activation of the connective tissue growth factor (CTGF)-transforming growth factor β 1 (TGF-β 1) axis in hepatitis C virus-expressing hepatocytes. PLoS One. 2012;7:e46526.CrossRefPubMedPubMedCentral
Metadata
Title
Transforming growth factor beta1 targets estrogen receptor signaling in bronchial epithelial cells
Authors
L. Cody Smith
Santiago Moreno
Lauren Robertson
Sarah Robinson
Kristal Gant
Andrew J. Bryant
Tara Sabo-Attwood
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2018
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-018-0861-5

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