PPARγ/ETV2 axis regulates endothelial‐to‐mesenchymal transition in pulmonary hypertension

Abstract Endothelial‐to‐mesenchymal transition (EndoMT) plays an important role in pulmonary hypertension (PH) but the molecular mechanisms regulating EndoMT remain to be defined. We demonstrate that the axis of the transcription factors PPARγ (Peroxisome Proliferator‐Activated Receptor gamma) and E...

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Main Authors: Dong Hun Lee, Minseong Kim, Sarah S. Chang, Raham Lee, Andrew J. Jang, Juyoung Kim, Jing Ma, Michael J. Passineau, Raymond L. Benza, Harry Karmouty‐Quintana, Wilbur A. Lam, Benjamin T. Kopp, Roy L. Sutliff, C. Michael Hart, Changwon Park, Bum‐Yong Kang
Format: Article
Language:English
Published: Wiley 2024-10-01
Series:Pulmonary Circulation
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Online Access:https://doi.org/10.1002/pul2.12448
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author Dong Hun Lee
Minseong Kim
Sarah S. Chang
Raham Lee
Andrew J. Jang
Juyoung Kim
Jing Ma
Michael J. Passineau
Raymond L. Benza
Harry Karmouty‐Quintana
Wilbur A. Lam
Benjamin T. Kopp
Roy L. Sutliff
C. Michael Hart
Changwon Park
Bum‐Yong Kang
author_facet Dong Hun Lee
Minseong Kim
Sarah S. Chang
Raham Lee
Andrew J. Jang
Juyoung Kim
Jing Ma
Michael J. Passineau
Raymond L. Benza
Harry Karmouty‐Quintana
Wilbur A. Lam
Benjamin T. Kopp
Roy L. Sutliff
C. Michael Hart
Changwon Park
Bum‐Yong Kang
author_sort Dong Hun Lee
collection DOAJ
description Abstract Endothelial‐to‐mesenchymal transition (EndoMT) plays an important role in pulmonary hypertension (PH) but the molecular mechanisms regulating EndoMT remain to be defined. We demonstrate that the axis of the transcription factors PPARγ (Peroxisome Proliferator‐Activated Receptor gamma) and ETV2 (ETS variant 2) play important roles in the pathogenesis of PH. Decreased levels of the expression of PPARγ and ETV2 along with reduced endothelial and increased EndoMT markers are consistently observed in lungs and pulmonary artery endothelial cells (PAECs) of idiopathic pulmonary arterial hypertension patients, in hypoxia‐exposed mouse lungs, human PAECs, and in induced‐EndoMT cells. Etv2+/− mice spontaneously developed PH and right ventricular hypertrophy (RVH), associated with increased EndoMT markers and decreased EC markers. Interestingly, chronic hypoxia exacerbated right ventricular systolic pressure and RVH in Etv2+/− mice. PPARγ transcriptionally activates the ETV2 promoter. Consistently, while mice overexpressing endothelial PPARγ increases the expression of ETV2 and endothelial markers with reduced EndoMT markers, endothelial PPARγ KO mice show decreased ETV2 expression and enhanced EndoMT markers. Inducible overexpression of ETV2 under induced‐EndoMT cell model reduces number of cells with mesenchymal morphology and decreases expression of mesenchymal markers with increased EC makers, compared to control. Therefore, our study suggests that PPARγ‐ETV2 signaling regulates PH pathogenesis through EndoMT.
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spelling doaj-art-facc4024f56944e0ae62c125adb62cf42024-12-27T05:54:34ZengWileyPulmonary Circulation2045-89402024-10-01144n/an/a10.1002/pul2.12448PPARγ/ETV2 axis regulates endothelial‐to‐mesenchymal transition in pulmonary hypertensionDong Hun Lee0Minseong Kim1Sarah S. Chang2Raham Lee3Andrew J. Jang4Juyoung Kim5Jing Ma6Michael J. Passineau7Raymond L. Benza8Harry Karmouty‐Quintana9Wilbur A. Lam10Benjamin T. Kopp11Roy L. Sutliff12C. Michael Hart13Changwon Park14Bum‐Yong Kang15Department of Pediatrics Emory University School of Medicine Atlanta Georgia USADepartment of Pediatrics Emory University School of Medicine Atlanta Georgia USADepartment of Medicine Emory University School of Medicine Atlanta Georgia USADepartment of Molecular and Cellular Physiology Louisiana State University Health Science Center Shreveport Louisiana USADepartment of Medicine, Allegheny Health Network Cardiovascular Institute Pittsburgh Pennsylvania USADepartment of Pediatrics Emory University School of Medicine Atlanta Georgia USADepartment of Medicine Emory University School of Medicine Atlanta Georgia USADepartment of Medicine, Allegheny Health Network Cardiovascular Institute Pittsburgh Pennsylvania USADivision of Cardiology Icahn School of Medicine at Mount Sinai New York New York USADepartment of Biochemistry and Molecular Biology University of Texas Health Science Center Houston Texas USADepartment of Pediatrics Emory University School of Medicine Atlanta Georgia USADepartment of Pediatrics Emory University School of Medicine Atlanta Georgia USADepartment of Medicine Emory University School of Medicine Atlanta Georgia USADepartment of Medicine Emory University School of Medicine Atlanta Georgia USADepartment of Pediatrics Emory University School of Medicine Atlanta Georgia USADepartment of Pediatrics Emory University School of Medicine Atlanta Georgia USAAbstract Endothelial‐to‐mesenchymal transition (EndoMT) plays an important role in pulmonary hypertension (PH) but the molecular mechanisms regulating EndoMT remain to be defined. We demonstrate that the axis of the transcription factors PPARγ (Peroxisome Proliferator‐Activated Receptor gamma) and ETV2 (ETS variant 2) play important roles in the pathogenesis of PH. Decreased levels of the expression of PPARγ and ETV2 along with reduced endothelial and increased EndoMT markers are consistently observed in lungs and pulmonary artery endothelial cells (PAECs) of idiopathic pulmonary arterial hypertension patients, in hypoxia‐exposed mouse lungs, human PAECs, and in induced‐EndoMT cells. Etv2+/− mice spontaneously developed PH and right ventricular hypertrophy (RVH), associated with increased EndoMT markers and decreased EC markers. Interestingly, chronic hypoxia exacerbated right ventricular systolic pressure and RVH in Etv2+/− mice. PPARγ transcriptionally activates the ETV2 promoter. Consistently, while mice overexpressing endothelial PPARγ increases the expression of ETV2 and endothelial markers with reduced EndoMT markers, endothelial PPARγ KO mice show decreased ETV2 expression and enhanced EndoMT markers. Inducible overexpression of ETV2 under induced‐EndoMT cell model reduces number of cells with mesenchymal morphology and decreases expression of mesenchymal markers with increased EC makers, compared to control. Therefore, our study suggests that PPARγ‐ETV2 signaling regulates PH pathogenesis through EndoMT.https://doi.org/10.1002/pul2.12448endothelial‐to‐mesenchymal transitionETV2hypoxiaPPARγpulmonary hypertension
spellingShingle Dong Hun Lee
Minseong Kim
Sarah S. Chang
Raham Lee
Andrew J. Jang
Juyoung Kim
Jing Ma
Michael J. Passineau
Raymond L. Benza
Harry Karmouty‐Quintana
Wilbur A. Lam
Benjamin T. Kopp
Roy L. Sutliff
C. Michael Hart
Changwon Park
Bum‐Yong Kang
PPARγ/ETV2 axis regulates endothelial‐to‐mesenchymal transition in pulmonary hypertension
Pulmonary Circulation
endothelial‐to‐mesenchymal transition
ETV2
hypoxia
PPARγ
pulmonary hypertension
title PPARγ/ETV2 axis regulates endothelial‐to‐mesenchymal transition in pulmonary hypertension
title_full PPARγ/ETV2 axis regulates endothelial‐to‐mesenchymal transition in pulmonary hypertension
title_fullStr PPARγ/ETV2 axis regulates endothelial‐to‐mesenchymal transition in pulmonary hypertension
title_full_unstemmed PPARγ/ETV2 axis regulates endothelial‐to‐mesenchymal transition in pulmonary hypertension
title_short PPARγ/ETV2 axis regulates endothelial‐to‐mesenchymal transition in pulmonary hypertension
title_sort pparγ etv2 axis regulates endothelial to mesenchymal transition in pulmonary hypertension
topic endothelial‐to‐mesenchymal transition
ETV2
hypoxia
PPARγ
pulmonary hypertension
url https://doi.org/10.1002/pul2.12448
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