Spns1-dependent endocardial lysosomal function drives valve morphogenesis through Notch1-signaling

Summary: Autophagy-lysosomal degradation is a conserved homeostatic process considered to be crucial for cardiac morphogenesis. However, both its cell specificity and functional role during heart development remain unclear. Here, we introduced zebrafish models to visualize autophagic vesicles in viv...

Full description

Saved in:
Bibliographic Details
Main Authors: Myra N. Chávez, Prateek Arora, Marco Meer, Ines J. Marques, Alexander Ernst, Rodrigo A. Morales Castro, Nadia Mercader
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004224026312
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850100686429093888
author Myra N. Chávez
Prateek Arora
Marco Meer
Ines J. Marques
Alexander Ernst
Rodrigo A. Morales Castro
Nadia Mercader
author_facet Myra N. Chávez
Prateek Arora
Marco Meer
Ines J. Marques
Alexander Ernst
Rodrigo A. Morales Castro
Nadia Mercader
author_sort Myra N. Chávez
collection DOAJ
description Summary: Autophagy-lysosomal degradation is a conserved homeostatic process considered to be crucial for cardiac morphogenesis. However, both its cell specificity and functional role during heart development remain unclear. Here, we introduced zebrafish models to visualize autophagic vesicles in vivo and track their temporal and cellular localization in the larval heart. We observed a significant accumulation of autolysosomal and lysosomal vesicles in the atrioventricular and bulboventricular regions and their respective valves. We addressed the role of lysosomal degradation based on the Spinster homolog 1 (spns1) mutant (not really started, nrs). nrs larvae displayed morphological and functional cardiac defects, including abnormal endocardial organization, impaired valve formation and retrograde blood flow. Single-nuclear transcriptome analyses revealed endocardial-specific differences in lysosome-related genes and alterations of notch1-signalling. Endocardial-specific overexpression of spns1 and notch1 rescued features of valve formation and function. Altogether, our results reveal a cell-autonomous role of lysosomal processing during cardiac valve formation affecting notch1-signalling.
format Article
id doaj-art-60869df8fb554298b03dc5dc463b6eba
institution DOAJ
issn 2589-0042
language English
publishDate 2024-12-01
publisher Elsevier
record_format Article
series iScience
spelling doaj-art-60869df8fb554298b03dc5dc463b6eba2025-08-20T02:40:14ZengElsevieriScience2589-00422024-12-01271211140610.1016/j.isci.2024.111406Spns1-dependent endocardial lysosomal function drives valve morphogenesis through Notch1-signalingMyra N. Chávez0Prateek Arora1Marco Meer2Ines J. Marques3Alexander Ernst4Rodrigo A. Morales Castro5Nadia Mercader6Department of Developmental Biology and Regeneration, Institute of Anatomy, University of Bern, 3012 Bern, Switzerland; Corresponding authorDepartment of Developmental Biology and Regeneration, Institute of Anatomy, University of Bern, 3012 Bern, Switzerland; Department for Biomedical Research, University of Bern, 3008 Bern, SwitzerlandDepartment of Developmental Biology and Regeneration, Institute of Anatomy, University of Bern, 3012 Bern, Switzerland; Department for Biomedical Research, University of Bern, 3008 Bern, SwitzerlandDepartment of Developmental Biology and Regeneration, Institute of Anatomy, University of Bern, 3012 Bern, Switzerland; Department for Biomedical Research, University of Bern, 3008 Bern, SwitzerlandDepartment of Developmental Biology and Regeneration, Institute of Anatomy, University of Bern, 3012 Bern, SwitzerlandDivision of Immunology and Allergy, Department of Medicine Solna, Karolinska Institutet and University Hospital, Stockholm, Sweden; Center of Molecular Medicine, Karolinska Institutet, 17176 Stockholm, SwedenDepartment of Developmental Biology and Regeneration, Institute of Anatomy, University of Bern, 3012 Bern, Switzerland; Department for Biomedical Research, University of Bern, 3008 Bern, Switzerland; Centro Nacional de Investigaciones Cardiovasculares Carlos III, 28029 Madrid, Spain; Corresponding authorSummary: Autophagy-lysosomal degradation is a conserved homeostatic process considered to be crucial for cardiac morphogenesis. However, both its cell specificity and functional role during heart development remain unclear. Here, we introduced zebrafish models to visualize autophagic vesicles in vivo and track their temporal and cellular localization in the larval heart. We observed a significant accumulation of autolysosomal and lysosomal vesicles in the atrioventricular and bulboventricular regions and their respective valves. We addressed the role of lysosomal degradation based on the Spinster homolog 1 (spns1) mutant (not really started, nrs). nrs larvae displayed morphological and functional cardiac defects, including abnormal endocardial organization, impaired valve formation and retrograde blood flow. Single-nuclear transcriptome analyses revealed endocardial-specific differences in lysosome-related genes and alterations of notch1-signalling. Endocardial-specific overexpression of spns1 and notch1 rescued features of valve formation and function. Altogether, our results reveal a cell-autonomous role of lysosomal processing during cardiac valve formation affecting notch1-signalling.http://www.sciencedirect.com/science/article/pii/S2589004224026312Molecular biologyCell biologyDevelopmental biologyTranscriptomicsModel organism
spellingShingle Myra N. Chávez
Prateek Arora
Marco Meer
Ines J. Marques
Alexander Ernst
Rodrigo A. Morales Castro
Nadia Mercader
Spns1-dependent endocardial lysosomal function drives valve morphogenesis through Notch1-signaling
iScience
Molecular biology
Cell biology
Developmental biology
Transcriptomics
Model organism
title Spns1-dependent endocardial lysosomal function drives valve morphogenesis through Notch1-signaling
title_full Spns1-dependent endocardial lysosomal function drives valve morphogenesis through Notch1-signaling
title_fullStr Spns1-dependent endocardial lysosomal function drives valve morphogenesis through Notch1-signaling
title_full_unstemmed Spns1-dependent endocardial lysosomal function drives valve morphogenesis through Notch1-signaling
title_short Spns1-dependent endocardial lysosomal function drives valve morphogenesis through Notch1-signaling
title_sort spns1 dependent endocardial lysosomal function drives valve morphogenesis through notch1 signaling
topic Molecular biology
Cell biology
Developmental biology
Transcriptomics
Model organism
url http://www.sciencedirect.com/science/article/pii/S2589004224026312
work_keys_str_mv AT myranchavez spns1dependentendocardiallysosomalfunctiondrivesvalvemorphogenesisthroughnotch1signaling
AT prateekarora spns1dependentendocardiallysosomalfunctiondrivesvalvemorphogenesisthroughnotch1signaling
AT marcomeer spns1dependentendocardiallysosomalfunctiondrivesvalvemorphogenesisthroughnotch1signaling
AT inesjmarques spns1dependentendocardiallysosomalfunctiondrivesvalvemorphogenesisthroughnotch1signaling
AT alexanderernst spns1dependentendocardiallysosomalfunctiondrivesvalvemorphogenesisthroughnotch1signaling
AT rodrigoamoralescastro spns1dependentendocardiallysosomalfunctiondrivesvalvemorphogenesisthroughnotch1signaling
AT nadiamercader spns1dependentendocardiallysosomalfunctiondrivesvalvemorphogenesisthroughnotch1signaling