The T‐Type Calcium Channel CACNA1H is Required for Smooth Muscle Cytoskeletal Organization During Tracheal Tubulogenesis

Abstract Abnormalities of tracheal smooth muscle (SM) formation are associated with several clinical disorders including tracheal stenosis and tracheomalacia. However, the cellular and molecular mechanisms underlying tracheal SM formation remain poorly understood. Here, it is shown that the T‐type c...

Full description

Saved in:
Bibliographic Details
Main Authors: Ziying Liu, Chunyan Lu, Li Ma, Changjiang Li, Haiyun Luo, Yiqi Liu, Xinyuan Liu, Haiqing Li, Yachao Cui, Jiahang Zeng, Natalia Bottasso‐Arias, Debora Sinner, Le Li, Jian Wang, Didier Y. R. Stainier, Wenguang Yin
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202308622
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846151476548730880
author Ziying Liu
Chunyan Lu
Li Ma
Changjiang Li
Haiyun Luo
Yiqi Liu
Xinyuan Liu
Haiqing Li
Yachao Cui
Jiahang Zeng
Natalia Bottasso‐Arias
Debora Sinner
Le Li
Jian Wang
Didier Y. R. Stainier
Wenguang Yin
author_facet Ziying Liu
Chunyan Lu
Li Ma
Changjiang Li
Haiyun Luo
Yiqi Liu
Xinyuan Liu
Haiqing Li
Yachao Cui
Jiahang Zeng
Natalia Bottasso‐Arias
Debora Sinner
Le Li
Jian Wang
Didier Y. R. Stainier
Wenguang Yin
author_sort Ziying Liu
collection DOAJ
description Abstract Abnormalities of tracheal smooth muscle (SM) formation are associated with several clinical disorders including tracheal stenosis and tracheomalacia. However, the cellular and molecular mechanisms underlying tracheal SM formation remain poorly understood. Here, it is shown that the T‐type calcium channel CACNA1H is a novel regulator of tracheal SM formation and contraction. Cacna1h in an ethylnitrosourea forward genetic screen for regulators of respiratory disease using the mouse as a model is identified. Cacna1h mutants exhibit tracheal stenosis, disorganized SM and compromised tracheal contraction. CACNA1H is essential to maintain actin polymerization, which is required for tracheal SM organization and tube formation. This process appears to be partially mediated through activation of the actin regulator RhoA, as pharmacological increase of RhoA activity ameliorates the Cacna1h‐mutant trachea phenotypes. Analysis of human tracheal tissues indicates that a decrease in CACNA1H protein levels is associated with congenital tracheostenosis. These results provide insight into the role for the T‐type calcium channel in cytoskeletal organization and SM formation during tracheal tube formation and suggest novel targets for congenital tracheostenosis intervention.
format Article
id doaj-art-8e921e1b85084c32a1f45689b90f74a4
institution Kabale University
issn 2198-3844
language English
publishDate 2024-11-01
publisher Wiley
record_format Article
series Advanced Science
spelling doaj-art-8e921e1b85084c32a1f45689b90f74a42024-11-27T11:21:53ZengWileyAdvanced Science2198-38442024-11-011144n/an/a10.1002/advs.202308622The T‐Type Calcium Channel CACNA1H is Required for Smooth Muscle Cytoskeletal Organization During Tracheal TubulogenesisZiying Liu0Chunyan Lu1Li Ma2Changjiang Li3Haiyun Luo4Yiqi Liu5Xinyuan Liu6Haiqing Li7Yachao Cui8Jiahang Zeng9Natalia Bottasso‐Arias10Debora Sinner11Le Li12Jian Wang13Didier Y. R. Stainier14Wenguang Yin15State Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaHeart center & Department of Pediatric Surgery Guangdong Provincial Key Laboratory of Research in Structural Birth Defect Disease Guangzhou Women and Children's Medical Center Guangzhou Medical University Guangzhou Guangdong 510623 P. R. ChinaState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaDepartment of Thoracic Surgery Guangzhou Women and Children's Medical Center Guangzhou Medical University Guangzhou 510623 P. R. ChinaDivision of Neonatology and Pulmonary Biology CCHMC College of Medicine University of Cincinnati Cincinnati OH 45221 USADivision of Neonatology and Pulmonary Biology CCHMC College of Medicine University of Cincinnati Cincinnati OH 45221 USADepartment of Thoracic Surgery Guangzhou Women and Children's Medical Center Guangzhou Medical University Guangzhou 510623 P. R. ChinaState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaDepartment of Developmental Genetics Max Planck Institute for Heart and Lung Research Member of the German Center for Lung Research (DZL) 61231 Bad Nauheim GermanyState Key Laboratory of Respiratory Disease National Clinical Research Center for Respiratory Disease Guangzhou Institute of Respiratory Health the First Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510182 P. R. ChinaAbstract Abnormalities of tracheal smooth muscle (SM) formation are associated with several clinical disorders including tracheal stenosis and tracheomalacia. However, the cellular and molecular mechanisms underlying tracheal SM formation remain poorly understood. Here, it is shown that the T‐type calcium channel CACNA1H is a novel regulator of tracheal SM formation and contraction. Cacna1h in an ethylnitrosourea forward genetic screen for regulators of respiratory disease using the mouse as a model is identified. Cacna1h mutants exhibit tracheal stenosis, disorganized SM and compromised tracheal contraction. CACNA1H is essential to maintain actin polymerization, which is required for tracheal SM organization and tube formation. This process appears to be partially mediated through activation of the actin regulator RhoA, as pharmacological increase of RhoA activity ameliorates the Cacna1h‐mutant trachea phenotypes. Analysis of human tracheal tissues indicates that a decrease in CACNA1H protein levels is associated with congenital tracheostenosis. These results provide insight into the role for the T‐type calcium channel in cytoskeletal organization and SM formation during tracheal tube formation and suggest novel targets for congenital tracheostenosis intervention.https://doi.org/10.1002/advs.202308622Cacna1hcytoskeletonRhoAsmooth muscletracheal stenosis
spellingShingle Ziying Liu
Chunyan Lu
Li Ma
Changjiang Li
Haiyun Luo
Yiqi Liu
Xinyuan Liu
Haiqing Li
Yachao Cui
Jiahang Zeng
Natalia Bottasso‐Arias
Debora Sinner
Le Li
Jian Wang
Didier Y. R. Stainier
Wenguang Yin
The T‐Type Calcium Channel CACNA1H is Required for Smooth Muscle Cytoskeletal Organization During Tracheal Tubulogenesis
Advanced Science
Cacna1h
cytoskeleton
RhoA
smooth muscle
tracheal stenosis
title The T‐Type Calcium Channel CACNA1H is Required for Smooth Muscle Cytoskeletal Organization During Tracheal Tubulogenesis
title_full The T‐Type Calcium Channel CACNA1H is Required for Smooth Muscle Cytoskeletal Organization During Tracheal Tubulogenesis
title_fullStr The T‐Type Calcium Channel CACNA1H is Required for Smooth Muscle Cytoskeletal Organization During Tracheal Tubulogenesis
title_full_unstemmed The T‐Type Calcium Channel CACNA1H is Required for Smooth Muscle Cytoskeletal Organization During Tracheal Tubulogenesis
title_short The T‐Type Calcium Channel CACNA1H is Required for Smooth Muscle Cytoskeletal Organization During Tracheal Tubulogenesis
title_sort t type calcium channel cacna1h is required for smooth muscle cytoskeletal organization during tracheal tubulogenesis
topic Cacna1h
cytoskeleton
RhoA
smooth muscle
tracheal stenosis
url https://doi.org/10.1002/advs.202308622
work_keys_str_mv AT ziyingliu thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT chunyanlu thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT lima thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT changjiangli thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT haiyunluo thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT yiqiliu thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT xinyuanliu thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT haiqingli thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT yachaocui thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT jiahangzeng thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT nataliabottassoarias thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT deborasinner thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT leli thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT jianwang thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT didieryrstainier thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT wenguangyin thettypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT ziyingliu ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT chunyanlu ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT lima ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT changjiangli ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT haiyunluo ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT yiqiliu ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT xinyuanliu ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT haiqingli ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT yachaocui ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT jiahangzeng ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT nataliabottassoarias ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT deborasinner ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT leli ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT jianwang ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT didieryrstainier ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis
AT wenguangyin ttypecalciumchannelcacna1hisrequiredforsmoothmusclecytoskeletalorganizationduringtrachealtubulogenesis