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Mechanical Strain Induces Transcriptomic Reprogramming of Saphenous Vein Progenitors

Intimal hyperplasia is the leading cause of graft failure in aortocoronary bypass grafts performed using human saphenous vein (SV). The long-term consequences of the altered pulsatile stress on the cells that populate the vein wall remains elusive, particularly the effects on saphenous vein progenit...

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Autores principales: Maselli, Davide, Garoffolo, Gloria, Cassanmagnago, Giada Andrea, Vono, Rosa, Ruiter, Matthijs S., Thomas, Anita C., Madeddu, Paolo, Pesce, Maurizio, Spinetti, Gaia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9197233/
https://www.ncbi.nlm.nih.gov/pubmed/35711359
http://dx.doi.org/10.3389/fcvm.2022.884031
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author Maselli, Davide
Garoffolo, Gloria
Cassanmagnago, Giada Andrea
Vono, Rosa
Ruiter, Matthijs S.
Thomas, Anita C.
Madeddu, Paolo
Pesce, Maurizio
Spinetti, Gaia
author_facet Maselli, Davide
Garoffolo, Gloria
Cassanmagnago, Giada Andrea
Vono, Rosa
Ruiter, Matthijs S.
Thomas, Anita C.
Madeddu, Paolo
Pesce, Maurizio
Spinetti, Gaia
author_sort Maselli, Davide
collection PubMed
description Intimal hyperplasia is the leading cause of graft failure in aortocoronary bypass grafts performed using human saphenous vein (SV). The long-term consequences of the altered pulsatile stress on the cells that populate the vein wall remains elusive, particularly the effects on saphenous vein progenitors (SVPs), cells resident in the vein adventitia with a relatively wide differentiation capacity. In the present study, we performed global transcriptomic profiling of SVPs undergoing uniaxial cyclic strain in vitro. This type of mechanical stimulation is indeed involved in the pathology of the SV. Results showed a consistent stretch-dependent gene regulation in cyclically strained SVPs vs. controls, especially at 72 h. We also observed a robust mechanically related overexpression of Adhesion Molecule with Ig Like Domain 2 (AMIGO2), a cell surface type I transmembrane protein involved in cell adhesion. The overexpression of AMIGO2 in stretched SVPs was associated with the activation of the transforming growth factor β pathway and modulation of intercellular signaling, cell-cell, and cell-matrix interactions. Moreover, the increased number of cells expressing AMIGO2 detected in porcine SV adventitia using an in vivo arterialization model confirms the upregulation of AMIGO2 protein by the arterial-like environment. These results show that mechanical stress promotes SVPs' molecular phenotypic switching and increases their responsiveness to extracellular environment alterations, thus prompting the targeting of new molecular effectors to improve the outcome of bypass graft procedure.
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spelling pubmed-91972332022-06-15 Mechanical Strain Induces Transcriptomic Reprogramming of Saphenous Vein Progenitors Maselli, Davide Garoffolo, Gloria Cassanmagnago, Giada Andrea Vono, Rosa Ruiter, Matthijs S. Thomas, Anita C. Madeddu, Paolo Pesce, Maurizio Spinetti, Gaia Front Cardiovasc Med Cardiovascular Medicine Intimal hyperplasia is the leading cause of graft failure in aortocoronary bypass grafts performed using human saphenous vein (SV). The long-term consequences of the altered pulsatile stress on the cells that populate the vein wall remains elusive, particularly the effects on saphenous vein progenitors (SVPs), cells resident in the vein adventitia with a relatively wide differentiation capacity. In the present study, we performed global transcriptomic profiling of SVPs undergoing uniaxial cyclic strain in vitro. This type of mechanical stimulation is indeed involved in the pathology of the SV. Results showed a consistent stretch-dependent gene regulation in cyclically strained SVPs vs. controls, especially at 72 h. We also observed a robust mechanically related overexpression of Adhesion Molecule with Ig Like Domain 2 (AMIGO2), a cell surface type I transmembrane protein involved in cell adhesion. The overexpression of AMIGO2 in stretched SVPs was associated with the activation of the transforming growth factor β pathway and modulation of intercellular signaling, cell-cell, and cell-matrix interactions. Moreover, the increased number of cells expressing AMIGO2 detected in porcine SV adventitia using an in vivo arterialization model confirms the upregulation of AMIGO2 protein by the arterial-like environment. These results show that mechanical stress promotes SVPs' molecular phenotypic switching and increases their responsiveness to extracellular environment alterations, thus prompting the targeting of new molecular effectors to improve the outcome of bypass graft procedure. Frontiers Media S.A. 2022-05-27 /pmc/articles/PMC9197233/ /pubmed/35711359 http://dx.doi.org/10.3389/fcvm.2022.884031 Text en Copyright © 2022 Maselli, Garoffolo, Cassanmagnago, Vono, Ruiter, Thomas, Madeddu, Pesce and Spinetti. 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 Cardiovascular Medicine
Maselli, Davide
Garoffolo, Gloria
Cassanmagnago, Giada Andrea
Vono, Rosa
Ruiter, Matthijs S.
Thomas, Anita C.
Madeddu, Paolo
Pesce, Maurizio
Spinetti, Gaia
Mechanical Strain Induces Transcriptomic Reprogramming of Saphenous Vein Progenitors
title Mechanical Strain Induces Transcriptomic Reprogramming of Saphenous Vein Progenitors
title_full Mechanical Strain Induces Transcriptomic Reprogramming of Saphenous Vein Progenitors
title_fullStr Mechanical Strain Induces Transcriptomic Reprogramming of Saphenous Vein Progenitors
title_full_unstemmed Mechanical Strain Induces Transcriptomic Reprogramming of Saphenous Vein Progenitors
title_short Mechanical Strain Induces Transcriptomic Reprogramming of Saphenous Vein Progenitors
title_sort mechanical strain induces transcriptomic reprogramming of saphenous vein progenitors
topic Cardiovascular Medicine
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9197233/
https://www.ncbi.nlm.nih.gov/pubmed/35711359
http://dx.doi.org/10.3389/fcvm.2022.884031
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