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Citations to this article

Disruption of PPARγ/β-catenin–mediated regulation of apelin impairs BMP-induced mouse and human pulmonary arterial EC survival
Tero-Pekka Alastalo, … , Howard Y. Chang, Marlene Rabinovitch
Tero-Pekka Alastalo, … , Howard Y. Chang, Marlene Rabinovitch
Published August 8, 2011
Citation Information: J Clin Invest. 2011;121(9):3735-3746. https://doi.org/10.1172/JCI43382.
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Research Article Pulmonology

Disruption of PPARγ/β-catenin–mediated regulation of apelin impairs BMP-induced mouse and human pulmonary arterial EC survival

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Abstract

Reduced bone morphogenetic protein receptor 2 (BMPR2) expression in patients with pulmonary arterial hypertension (PAH) can impair pulmonary arterial EC (PAEC) function. This can adversely affect EC survival and promote SMC proliferation. We hypothesized that interventions to normalize expression of genes that are targets of BMPR2 signaling could restore PAEC function and prevent or reverse PAH. Here we have characterized, in human PAECs, a BMPR2-mediated transcriptional complex between PPARγ and β-catenin and shown that disruption of this complex impaired BMP-mediated PAEC survival. Using whole genome-wide ChIP-Chip promoter analysis and gene expression microarrays, we delineated PPARγ/β-catenin–dependent transcription of target genes including APLN, which encodes apelin. We documented reduced PAEC expression of apelin in PAH patients versus controls. In cell culture experiments, we showed that apelin-deficient PAECs were prone to apoptosis and promoted pulmonary arterial SMC (PASMC) proliferation. Conversely, we established that apelin, like BMPR2 ligands, suppressed proliferation and induced apoptosis of PASMCs. Consistent with these functions, administration of apelin reversed PAH in mice with reduced production of apelin resulting from deletion of PPARγ in ECs. Taken together, our findings suggest that apelin could be effective in treating PAH by rescuing BMPR2 and PAEC dysfunction.

Authors

Tero-Pekka Alastalo, Molong Li, Vinicio de Jesus Perez, David Pham, Hirofumi Sawada, Jordon K. Wang, Minna Koskenvuo, Lingli Wang, Bruce A. Freeman, Howard Y. Chang, Marlene Rabinovitch

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Year: 2024 2023 2022 2021 2020 2019 2018 2017 2016 2015 2014 2013 2012 2011 2009 Total
Citations: 9 13 9 14 14 11 10 8 9 12 13 12 5 2 1 142
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Cell Metabolism 2015
Elafin Reverses Pulmonary Hypertension via Caveolin-1–Dependent Bone Morphogenetic Protein Signaling
NP Nickel, E Spiekerkoetter, M Gu, CG Li, H Li, M Kaschwich, I Diebold, JK Hennigs, KY Kim, K Miyagawa, L Wang, A Cao, S Sa, X Jiang, RW Stockstill, MR Nicolls, RT Zamanian, RD Bland, M Rabinovitch
American journal of respiratory and critical care medicine 2015
PPARγ Ligands Attenuate Hypoxia-Induced Proliferation in Human Pulmonary Artery Smooth Muscle Cells through Modulation of MicroRNA-21
DE Green, TC Murphy, BY Kang, CD Searles, CM Hart, J West
PloS one 2015
Raf/ERK drives the proliferative and invasive phenotype of BMPR2-silenced pulmonary artery endothelial cells
KS Awad, JM Elinoff, S Wang, S Gairhe, GA Ferreyra, R Cai, J Sun, MA Solomon, RL Danner
American journal of physiology. Lung cellular and molecular physiology 2015
Effects of apelin on the cardiovascular system
A Folino, PG Montarolo, M Samaja, R Rastaldo
Heart Failure Reviews 2015
Apelin, Elabela/Toddler, and biased agonists as novel therapeutic agents in the cardiovascular system
P Yang, JJ Maguire, AP Davenport
Trends in Pharmacological Sciences 2015
The Endothelial Transcription Factor ERG Promotes Vascular Stability and Growth through Wnt/β-Catenin Signaling
GM Birdsey, AV Shah, N Dufton, LE Reynolds, L Osuna Almagro, Y Yang, IM Aspalter, ST Khan, JC Mason, E Dejana, B Göttgens, K Hodivala-Dilke, H Gerhardt, RH Adams, AM Randi
Developmental Cell 2015
Design, Characterization, and First-In-Human Study of the Vascular Actions of a Novel Biased Apelin Receptor Agonist
AL Brame, JJ Maguire, P Yang, A Dyson, R Torella, J Cheriyan, M Singer, RC Glen, IB Wilkinson, AP Davenport
Hypertension 2015
Elafin in Pulmonary Arterial Hypertension. Beyond Targeting Elastases
HJ Chun, PB Yu
American journal of respiratory and critical care medicine 2015
RNA Sequencing Analysis Detection of a Novel Pathway of Endothelial Dysfunction in Pulmonary Arterial Hypertension
CJ Rhodes, H Im, A Cao, JK Hennigs, L Wang, S Sa, PI Chen, NP Nickel, K Miyagawa, RK Hopper, NF Tojais, CG Li, M Gu, E Spiekerkoetter, Z Xian, R Chen, M Zhao, M Kaschwich, PA Rosario, D Bernstein, RT Zamanian, JC Wu, MP Snyder, M Rabinovitch
American journal of respiratory and critical care medicine 2015
Systems-level regulation of microRNA networks by miR-130/301 promotes pulmonary hypertension
Thomas Bertero, Yu Lu, Sofia Annis, Andrew Hale, Balkrishen Bhat, Rajan Saggar, Rajeev Saggar, W. Dean Wallace, David J. Ross, Sara O. Vargas, Brian B. Graham, Rahul Kumar, Stephen M. Black, Sohrab Fratz, Jeffrey R. Fineman, James D. West, Kathleen J. Haley, Aaron B. Waxman, B. Nelson Chau, Katherine A. Cottrill, Stephen Y. Chan
Journal of Clinical Investigation 2014
Restoration of Impaired Endothelial MEF2 Function Rescues Pulmonary Arterial Hypertension
J Kim, C Hwangbo, X Hu, Y Kang, I Papangeli, D Mehrotra, H Park, DL McLean, H Ju, SA Comhair, SC Erzurum, HJ Chun
Circulation 2014
Reduced BMPR2 expression induces GM-CSF translation and macrophage recruitment in humans and mice to exacerbate pulmonary hypertension
H Sawada, T Saito, NP Nickel, TP Alastalo, JP Glotzbach, R Chan, L Haghighat, G Fuchs, M Januszyk, A Cao, YJ Lai, VJ Perez, YM Kim, L Wang, PI Chen, E Spiekerkoetter, Y Mitani, GC Gurtner, P Sarnow, M Rabinovitch
Journal of Experimental Medicine 2014
The myriad essential roles of microRNAs in cardiovascular homeostasis and disease
RL Neppl, DZ Wang
Genes & Diseases 2014
Endothelium as a gatekeeper of fatty acid transport
D Mehrotra, J Wu, I Papangeli, HJ Chun
Trends in Endocrinology & Metabolism 2014
Inflammation and Immunity in the Pathogenesis of Pulmonary Arterial Hypertension
M Rabinovitch, C Guignabert, M Humbert, MR Nicolls
Circulation research 2014
Targeting the Wnt signaling pathways in pulmonary arterial hypertension
VJ Perez, K Yuan, TP Alastalo, E Spiekerkoetter, M Rabinovitch
Drug Discovery Today 2014
The MicroRNA-130/301 Family Controls Vasoconstriction in Pulmonary Hypertension
T Bertero, K Cottrill, A Krauszman, Y Lu, S Annis, A Hale, B Bhat, AB Waxman, BN Chau, WM Kuebler, SY Chan
The Journal of biological chemistry 2014
Apelin-APJ Signaling: a Potential Therapeutic Target for Pulmonary Arterial Hypertension
J Kim
Molecules and Cells 2014
ERG-APLNR Axis Controls Pulmonary Venule Endothelial Proliferation in Pulmonary Veno-Occlusive Disease
C Lathen, Y Zhang, J Chow, M Singh, G Lin, V Nigam, YA Ashraf, JX Yuan, IM Robbins, PA Thistlethwaite
Circulation 2014
Apelin inhibits the proliferation and migration of rat PASMCs via the activation of PI3K/Akt/mTOR signal and the inhibition of autophagy under hypoxia
H Zhang, Y Gong, Z Wang, L Jiang, R Chen, X Fan, H Zhu, L Han, X Li, J Xiao, X Kong
Journal of Cellular and Molecular Medicine 2014
The role of BMPs in endothelial cell function and dysfunction
LA Dyer, X Pi, C Patterson
Trends in Endocrinology & Metabolism 2014
Diversity Is in My Veins: Role of Bone Morphogenetic Protein Signaling During Venous Morphogenesis in Zebrafish Illustrates the Heterogeneity Within Endothelial Cells
JD Kim, HW Lee, SW Jin
Arteriosclerosis, thrombosis, and vascular biology 2014
FK506 Activates BMPR2 Signaling, Rescues Endothelial Dysfunction, Reverses Pulmonary Hypertension
Edda Spiekerkoetter, Xuefei Tian, Jie Cai, Rachel Hopper, Deepti Sudheendra, Caiyun Grace Li, Nesrine El-Bizri, Hirofumi Sawada, Roxanna Haghighat, Roshelle Chan, Leila Haghighat, Vinicio de Jesus Perez, Lingli Wang, Sushma Reddy, Mingming Zhao, Daniel Bernstein, David Solow-Cordero, Philip A. Beachy, Thomas Wandless, Peter Ten Dijke, Marlene Rabinovitch
Journal of Clinical Investigation 2013
Loss of Apelin exacerbates myocardial infarction adverse remodeling and ischemia-reperfusion injury: therapeutic potential of synthetic Apelin analogues
W Wang, SM McKinnie, VB Patel, G Haddad, Z Wang, P Zhabyeyev, SK Das, R Basu, B McLean, V Kandalam, JM Penninger, Z Kassiri, JC Vederas, AG Murray, GY Oudit
Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease 2013
Blocking Macrophage Leukotriene B4 Prevents Endothelial Injury and Reverses Pulmonary Hypertension
W Tian, X Jiang, R Tamosiuniene, YK Sung, J Qian, G Dhillon, L Gera, L Farkas, M Rabinovitch, RT Zamanian, M Inayathullah, M Fridlib, J Rajadas, M Peters-Golden, NF Voelkel, MR Nicolls
Science Translational Medicine 2013
Anticipated classes of new medications and molecular targets for pulmonary arterial hypertension
NW Morrell, SL Archer, A Defelice, S Evans, M Fiszman, T Martin, M Saulnier, M Rabinovitch, R Schermuly, D Stewart, H Truebel, G Walker, KR Stenmark
Pulmonary circulation 2013
Molecular mechanisms of mesenchymal stem cell differentiation towards osteoblasts
M Fakhry, E Hamade, B Badran, R Buchet, D Magne
World journal of stem cells 2013
Endothelial Indoleamine 2,3-Dioxygenase Protects against Development of Pulmonary Hypertension
Y Xiao, H Christou, L Liu, G Visner, SA Mitsialis, S Kourembanas, H Liu
American journal of respiratory and critical care medicine 2013
Signal transduction in the development of pulmonary arterial hypertension
S Malenfant, AS Neyron, R Paulin, F Potus, J Meloche, S Provencher, S Bonnet
Pulmonary circulation 2013
Hypoxia mediates mutual repression between microRNA-27a and PPARγ in the pulmonary vasculature
BY Kang, KK Park, DE Green, KM Bijli, CD Searles, RL Sutliff, CM Hart
PloS one 2013
Decreased apelin and apelin-receptor expression in the pulmonary vasculature of nitrofen-induced congenital diaphragmatic hernia
AD Hofmann, F Friedmacher, H Takahashi, M Hunziker, JH Gosemann, P Puri
Pediatric Surgery International 2013
Effects of PPAR γ Agonist Pioglitazone on Redox-Sensitive Cellular Signaling in Young Spontaneously Hypertensive Rats
I Dovinová, M Barancik, M Majzunova, S Zorad, L Gajdosechová, L Gresová, S Cacanyiova, F Kristek, P Balis, JY Chan
PPAR Research 2013
Integrating molecular genetics and systems approaches to pulmonary vascular diseases
MW Geraci
Pulmonary circulation 2013
New horizons in pulmonary arterial hypertension therapies
Galiè N, Ghofrani AH
European Respiratory Review 2013
Molecular pathogenesis of pulmonary arterial hypertension
Marlene Rabinovitch
Journal of Clinical Investigation 2012
A process-based review of mouse models of pulmonary hypertension
M Das, J Fessel, H Tang, J West
Pulmonary circulation 2012
Loss of Adenomatous Poliposis Coli-α3 Integrin Interaction Promotes Endothelial Apoptosis in Mice and Humans
VA de Jesus Perez, K Yuan, ME Orcholski, H Sawada, M Zhao, CG Li, NF Tojais, N Nickel, V Rajagopalan, E Spiekerkoetter, L Wang, R Dutta, D Bernstein, M Rabinovitch
Circulation research 2012
Targeting the ACE2 and Apelin Pathways Are Novel Therapies for Heart Failure: Opportunities and Challenges
SM Kazemi-Bajestani, VB Patel, W Wang, GY Oudit
Cardiology Research and Practice 2012
An endothelial apelin-FGF link mediated by miR-424 and miR-503 is disrupted in pulmonary arterial hypertension
J Kim, Y Kang, Y Kojima, JK Lighthouse, X Hu, MA Aldred, DL McLean, H Park, SA Comhair, DM Greif, SC Erzurum, HJ Chun
Nature Medicine 2012
Comprehensive Physiology
R Terjung
Comprehensive Physiology 2011
Apelin and pulmonary hypertension
CU Andersen, O Hilberg, S Mellemkjær, JE Nielsen-Kudsk, U Simonsen
Pulmonary circulation 2011
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009

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