Calpain‐2‐Mediated Endothelial Focal Adhesion Disruption in Thoracic Aortic Dissection

Abstract Thoracic aortic dissection (TAD) is a life‐threatening condition with high mortality rates. Recent research suggests a potential link between early‐stage TAD and endothelial barrier dysfunction, although the underlying mechanisms remain unclear. Single‐cell RNA sequencing data from patients...

Full description

Saved in:
Bibliographic Details
Main Authors: Xiaomei Teng, Yansong Wang, Haoyue Huang, Yinglong Ding, Jun Wang, Meili Liu, Kun Song, Lianbo Shao, You Yu, Ziying Yang, Zhenya Shen
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202501112
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849708676834656256
author Xiaomei Teng
Yansong Wang
Haoyue Huang
Yinglong Ding
Jun Wang
Meili Liu
Kun Song
Lianbo Shao
You Yu
Ziying Yang
Zhenya Shen
author_facet Xiaomei Teng
Yansong Wang
Haoyue Huang
Yinglong Ding
Jun Wang
Meili Liu
Kun Song
Lianbo Shao
You Yu
Ziying Yang
Zhenya Shen
author_sort Xiaomei Teng
collection DOAJ
description Abstract Thoracic aortic dissection (TAD) is a life‐threatening condition with high mortality rates. Recent research suggests a potential link between early‐stage TAD and endothelial barrier dysfunction, although the underlying mechanisms remain unclear. Single‐cell RNA sequencing data from patients reveal that dysregulated Calpain‐2 expression modulates endothelial focal adhesion proteins, serving as an early pathological hallmark and driver of TAD. Elevated plasma calpain activity is strongly associated with an increased risk of TAD and organ dysfunction. Both endogenous and exogenous calpain inhibitors effectively prevent TAD onset and progression in murine models induced by β‐aminopropionitrile (BAPN). In early TAD, endothelial junction integrity in the ascending aorta and aortic arch is compromised. Endothelial‐specific deletion of Capns1 mitigates early and sustained endothelial focal adhesion damage by reducing aberrant expression of Integrin alpha‐V(Itgav), vinculin, and talin‐1, thereby decreasing TAD incidence. In contrast, macrophage‐specific Capns1 knockout does not impact TAD development but accelerates aortic dissection rupture in later stages. Mechanistically, angiotensin II upregulates Calpain‐2, leading to endothelial focal adhesion activation through talin1 cleavage and Itgav assembly, thereby compromising endothelial integrity and permeability. These findings identify potential therapeutic targets for TAD prevention and treatment.
format Article
id doaj-art-3641346b582249b9ac258bc5fa3eae65
institution DOAJ
issn 2198-3844
language English
publishDate 2025-07-01
publisher Wiley
record_format Article
series Advanced Science
spelling doaj-art-3641346b582249b9ac258bc5fa3eae652025-08-20T03:15:35ZengWileyAdvanced Science2198-38442025-07-011225n/an/a10.1002/advs.202501112Calpain‐2‐Mediated Endothelial Focal Adhesion Disruption in Thoracic Aortic DissectionXiaomei Teng0Yansong Wang1Haoyue Huang2Yinglong Ding3Jun Wang4Meili Liu5Kun Song6Lianbo Shao7You Yu8Ziying Yang9Zhenya Shen10Department of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaInstitute for Cardiovascular Science Soochow University 178 Ganjiang Road Suzhou 215006 ChinaDepartment of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaDepartment of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaDepartment of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaDepartment of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaDepartment of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaDepartment of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaInstitute for Cardiovascular Science Soochow University 178 Ganjiang Road Suzhou 215006 ChinaDepartment of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaDepartment of Cardiovascular Surgery of the First Affiliated Hospital of Soochow University 899 Pinghai Road Suzhou 215006 ChinaAbstract Thoracic aortic dissection (TAD) is a life‐threatening condition with high mortality rates. Recent research suggests a potential link between early‐stage TAD and endothelial barrier dysfunction, although the underlying mechanisms remain unclear. Single‐cell RNA sequencing data from patients reveal that dysregulated Calpain‐2 expression modulates endothelial focal adhesion proteins, serving as an early pathological hallmark and driver of TAD. Elevated plasma calpain activity is strongly associated with an increased risk of TAD and organ dysfunction. Both endogenous and exogenous calpain inhibitors effectively prevent TAD onset and progression in murine models induced by β‐aminopropionitrile (BAPN). In early TAD, endothelial junction integrity in the ascending aorta and aortic arch is compromised. Endothelial‐specific deletion of Capns1 mitigates early and sustained endothelial focal adhesion damage by reducing aberrant expression of Integrin alpha‐V(Itgav), vinculin, and talin‐1, thereby decreasing TAD incidence. In contrast, macrophage‐specific Capns1 knockout does not impact TAD development but accelerates aortic dissection rupture in later stages. Mechanistically, angiotensin II upregulates Calpain‐2, leading to endothelial focal adhesion activation through talin1 cleavage and Itgav assembly, thereby compromising endothelial integrity and permeability. These findings identify potential therapeutic targets for TAD prevention and treatment.https://doi.org/10.1002/advs.202501112Calpain‐2focal adhesionItgavTalinthoracic aortic dissection
spellingShingle Xiaomei Teng
Yansong Wang
Haoyue Huang
Yinglong Ding
Jun Wang
Meili Liu
Kun Song
Lianbo Shao
You Yu
Ziying Yang
Zhenya Shen
Calpain‐2‐Mediated Endothelial Focal Adhesion Disruption in Thoracic Aortic Dissection
Advanced Science
Calpain‐2
focal adhesion
Itgav
Talin
thoracic aortic dissection
title Calpain‐2‐Mediated Endothelial Focal Adhesion Disruption in Thoracic Aortic Dissection
title_full Calpain‐2‐Mediated Endothelial Focal Adhesion Disruption in Thoracic Aortic Dissection
title_fullStr Calpain‐2‐Mediated Endothelial Focal Adhesion Disruption in Thoracic Aortic Dissection
title_full_unstemmed Calpain‐2‐Mediated Endothelial Focal Adhesion Disruption in Thoracic Aortic Dissection
title_short Calpain‐2‐Mediated Endothelial Focal Adhesion Disruption in Thoracic Aortic Dissection
title_sort calpain 2 mediated endothelial focal adhesion disruption in thoracic aortic dissection
topic Calpain‐2
focal adhesion
Itgav
Talin
thoracic aortic dissection
url https://doi.org/10.1002/advs.202501112
work_keys_str_mv AT xiaomeiteng calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT yansongwang calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT haoyuehuang calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT yinglongding calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT junwang calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT meililiu calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT kunsong calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT lianboshao calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT youyu calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT ziyingyang calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection
AT zhenyashen calpain2mediatedendothelialfocaladhesiondisruptioninthoracicaorticdissection