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Novel TNIP2 and TRAF2 Variants Are Implicated in the Pathogenesis of Pulmonary Arterial Hypertension

Background: Pulmonary arterial hypertension (PAH) is a rare disease characterized by pulmonary vascular remodeling and right heart failure. Specific genetic variants increase the incidence of PAH in carriers with a family history of PAH, those who suffer from certain medical conditions, and even tho...

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Autores principales: Pienkos, Shaun, Gallego, Natalia, Condon, David F., Cruz-Utrilla, Alejandro, Ochoa, Nuria, Nevado, Julián, Arias, Pedro, Agarwal, Stuti, Patel, Hiral, Chakraborty, Ananya, Lapunzina, Pablo, Escribano, Pilar, Tenorio-Castaño, Jair, de Jesús Pérez, Vinicio A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8119639/
https://www.ncbi.nlm.nih.gov/pubmed/33996849
http://dx.doi.org/10.3389/fmed.2021.625763
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author Pienkos, Shaun
Gallego, Natalia
Condon, David F.
Cruz-Utrilla, Alejandro
Ochoa, Nuria
Nevado, Julián
Arias, Pedro
Agarwal, Stuti
Patel, Hiral
Chakraborty, Ananya
Lapunzina, Pablo
Escribano, Pilar
Tenorio-Castaño, Jair
de Jesús Pérez, Vinicio A.
author_facet Pienkos, Shaun
Gallego, Natalia
Condon, David F.
Cruz-Utrilla, Alejandro
Ochoa, Nuria
Nevado, Julián
Arias, Pedro
Agarwal, Stuti
Patel, Hiral
Chakraborty, Ananya
Lapunzina, Pablo
Escribano, Pilar
Tenorio-Castaño, Jair
de Jesús Pérez, Vinicio A.
author_sort Pienkos, Shaun
collection PubMed
description Background: Pulmonary arterial hypertension (PAH) is a rare disease characterized by pulmonary vascular remodeling and right heart failure. Specific genetic variants increase the incidence of PAH in carriers with a family history of PAH, those who suffer from certain medical conditions, and even those with no apparent risk factors. Inflammation and immune dysregulation are related to vascular remodeling in PAH, but whether genetic susceptibility modifies the PAH immune response is unclear. TNIP2 and TRAF2 encode for immunomodulatory proteins that regulate NF-κB activation, a transcription factor complex associated with inflammation and vascular remodeling in PAH. Methods: Two unrelated families with PAH cases underwent whole-exome sequencing (WES). A custom pipeline for variant prioritization was carried out to obtain candidate variants. To determine the impact of TNIP2 and TRAF2 in cell proliferation, we performed an MTS [3-(4,5-dimethylthiazol-2-yl)-5-(3-carboxymethoxyphenyl)-2-(4-sulfophenyl)-2H-tetrazolium] assay on healthy lung pericytes transfected with siRNA specific for each gene. To measure the effect of loss of TNIP2 and TRAF2 on NF-kappa-beta (NF-κB) activity, we measured levels of Phospho-p65-NF-κB in siRNA-transfected pericytes using western immunoblotting. Results: We discovered a novel missense variant in the TNIP2 gene in two affected individuals from the same family. The two patients had a complex form of PAH with interatrial communication and scleroderma. In the second family, WES of the proband with PAH and primary biliary cirrhosis revealed a de novo protein-truncating variant in the TRAF2. The knockdown of TNIP2 and TRAF2 increased NF-κB activity in healthy lung pericytes, which correlated with a significant increase in proliferation over 24 h. Conclusions: We have identified two rare novel variants in TNIP2 and TRAF2 using WES. We speculate that loss of function in these genes promotes pulmonary vascular remodeling by allowing overactivation of the NF-κB signaling activity. Our findings support a role for WES in helping identify novel genetic variants associated with dysfunctional immune response in PAH.
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spelling pubmed-81196392021-05-15 Novel TNIP2 and TRAF2 Variants Are Implicated in the Pathogenesis of Pulmonary Arterial Hypertension Pienkos, Shaun Gallego, Natalia Condon, David F. Cruz-Utrilla, Alejandro Ochoa, Nuria Nevado, Julián Arias, Pedro Agarwal, Stuti Patel, Hiral Chakraborty, Ananya Lapunzina, Pablo Escribano, Pilar Tenorio-Castaño, Jair de Jesús Pérez, Vinicio A. Front Med (Lausanne) Medicine Background: Pulmonary arterial hypertension (PAH) is a rare disease characterized by pulmonary vascular remodeling and right heart failure. Specific genetic variants increase the incidence of PAH in carriers with a family history of PAH, those who suffer from certain medical conditions, and even those with no apparent risk factors. Inflammation and immune dysregulation are related to vascular remodeling in PAH, but whether genetic susceptibility modifies the PAH immune response is unclear. TNIP2 and TRAF2 encode for immunomodulatory proteins that regulate NF-κB activation, a transcription factor complex associated with inflammation and vascular remodeling in PAH. Methods: Two unrelated families with PAH cases underwent whole-exome sequencing (WES). A custom pipeline for variant prioritization was carried out to obtain candidate variants. To determine the impact of TNIP2 and TRAF2 in cell proliferation, we performed an MTS [3-(4,5-dimethylthiazol-2-yl)-5-(3-carboxymethoxyphenyl)-2-(4-sulfophenyl)-2H-tetrazolium] assay on healthy lung pericytes transfected with siRNA specific for each gene. To measure the effect of loss of TNIP2 and TRAF2 on NF-kappa-beta (NF-κB) activity, we measured levels of Phospho-p65-NF-κB in siRNA-transfected pericytes using western immunoblotting. Results: We discovered a novel missense variant in the TNIP2 gene in two affected individuals from the same family. The two patients had a complex form of PAH with interatrial communication and scleroderma. In the second family, WES of the proband with PAH and primary biliary cirrhosis revealed a de novo protein-truncating variant in the TRAF2. The knockdown of TNIP2 and TRAF2 increased NF-κB activity in healthy lung pericytes, which correlated with a significant increase in proliferation over 24 h. Conclusions: We have identified two rare novel variants in TNIP2 and TRAF2 using WES. We speculate that loss of function in these genes promotes pulmonary vascular remodeling by allowing overactivation of the NF-κB signaling activity. Our findings support a role for WES in helping identify novel genetic variants associated with dysfunctional immune response in PAH. Frontiers Media S.A. 2021-04-30 /pmc/articles/PMC8119639/ /pubmed/33996849 http://dx.doi.org/10.3389/fmed.2021.625763 Text en Copyright © 2021 Pienkos, Gallego, Condon, Cruz-Utrilla, Ochoa, Nevado, Arias, Agarwal, Patel, Chakraborty, Lapunzina, Escribano, Tenorio-Castaño and de Jesús Pérez. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Medicine
Pienkos, Shaun
Gallego, Natalia
Condon, David F.
Cruz-Utrilla, Alejandro
Ochoa, Nuria
Nevado, Julián
Arias, Pedro
Agarwal, Stuti
Patel, Hiral
Chakraborty, Ananya
Lapunzina, Pablo
Escribano, Pilar
Tenorio-Castaño, Jair
de Jesús Pérez, Vinicio A.
Novel TNIP2 and TRAF2 Variants Are Implicated in the Pathogenesis of Pulmonary Arterial Hypertension
title Novel TNIP2 and TRAF2 Variants Are Implicated in the Pathogenesis of Pulmonary Arterial Hypertension
title_full Novel TNIP2 and TRAF2 Variants Are Implicated in the Pathogenesis of Pulmonary Arterial Hypertension
title_fullStr Novel TNIP2 and TRAF2 Variants Are Implicated in the Pathogenesis of Pulmonary Arterial Hypertension
title_full_unstemmed Novel TNIP2 and TRAF2 Variants Are Implicated in the Pathogenesis of Pulmonary Arterial Hypertension
title_short Novel TNIP2 and TRAF2 Variants Are Implicated in the Pathogenesis of Pulmonary Arterial Hypertension
title_sort novel tnip2 and traf2 variants are implicated in the pathogenesis of pulmonary arterial hypertension
topic Medicine
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8119639/
https://www.ncbi.nlm.nih.gov/pubmed/33996849
http://dx.doi.org/10.3389/fmed.2021.625763
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