Initiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of Rasip1

Abstract De novo lumen formation necessitates the precise segregation of junctional proteins from apical surfaces, yet the underlying mechanisms remain unclear. Using a zebrafish model, we develop a series of molecular reporters, photo-convertible and optogenetic tools to study the establishment of...

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Main Authors: Jianmin Yin, Niels Schellinx, Ludovico Maggi, Kathrin Gundel, Cora Wiesner, Maria Paraskevi Kotini, Minkyoung Lee, Li-Kun Phng, Heinz-Georg Belting, Markus Affolter
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54143-y
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author Jianmin Yin
Niels Schellinx
Ludovico Maggi
Kathrin Gundel
Cora Wiesner
Maria Paraskevi Kotini
Minkyoung Lee
Li-Kun Phng
Heinz-Georg Belting
Markus Affolter
author_facet Jianmin Yin
Niels Schellinx
Ludovico Maggi
Kathrin Gundel
Cora Wiesner
Maria Paraskevi Kotini
Minkyoung Lee
Li-Kun Phng
Heinz-Georg Belting
Markus Affolter
author_sort Jianmin Yin
collection DOAJ
description Abstract De novo lumen formation necessitates the precise segregation of junctional proteins from apical surfaces, yet the underlying mechanisms remain unclear. Using a zebrafish model, we develop a series of molecular reporters, photo-convertible and optogenetic tools to study the establishment of apical domains. Our study identifies Rasip1 as one of the earliest apical proteins recruited, which suppresses actomyosin contractility at junctional patches by inhibiting NMII, thereby allowing for the sustained outward flow of junctional complexes. Following the establishment of apical compartments, Rasip1 shuttles between junctions and the apical compartments in response to local high tension. Rasip1 confines Cdh5 to junctions by suppressing apical contractility. Conversely, the recruitment of Rasip1 to junctions is regulated by Heg1 and Krit1 to modulate contractility along junctions. Overall, de novo lumen formation and maintenance depend on the precise control of contractility within apical compartments and junctions, orchestrated by the dynamic recruitment of Rasip1.
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institution Kabale University
issn 2041-1723
language English
publishDate 2024-11-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-cac7d75bd81e4deaae5f1a4918d65a3d2024-11-10T12:32:56ZengNature PortfolioNature Communications2041-17232024-11-0115111810.1038/s41467-024-54143-yInitiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of Rasip1Jianmin Yin0Niels Schellinx1Ludovico Maggi2Kathrin Gundel3Cora Wiesner4Maria Paraskevi Kotini5Minkyoung Lee6Li-Kun Phng7Heinz-Georg Belting8Markus Affolter9Department of Cell Biology, Biozentrum, University of BaselDepartment of Cell Biology, Biozentrum, University of BaselDepartment of Cell Biology, Biozentrum, University of BaselDepartment of Cell Biology, Biozentrum, University of BaselDepartment of Cell Biology, Biozentrum, University of BaselDepartment of Cell Biology, Biozentrum, University of BaselDepartment of Cell Biology, Biozentrum, University of BaselLaboratory for Vascular Morphogenesis, RIKEN Center for Biosystems Dynamics ResearchDepartment of Cell Biology, Biozentrum, University of BaselDepartment of Cell Biology, Biozentrum, University of BaselAbstract De novo lumen formation necessitates the precise segregation of junctional proteins from apical surfaces, yet the underlying mechanisms remain unclear. Using a zebrafish model, we develop a series of molecular reporters, photo-convertible and optogenetic tools to study the establishment of apical domains. Our study identifies Rasip1 as one of the earliest apical proteins recruited, which suppresses actomyosin contractility at junctional patches by inhibiting NMII, thereby allowing for the sustained outward flow of junctional complexes. Following the establishment of apical compartments, Rasip1 shuttles between junctions and the apical compartments in response to local high tension. Rasip1 confines Cdh5 to junctions by suppressing apical contractility. Conversely, the recruitment of Rasip1 to junctions is regulated by Heg1 and Krit1 to modulate contractility along junctions. Overall, de novo lumen formation and maintenance depend on the precise control of contractility within apical compartments and junctions, orchestrated by the dynamic recruitment of Rasip1.https://doi.org/10.1038/s41467-024-54143-y
spellingShingle Jianmin Yin
Niels Schellinx
Ludovico Maggi
Kathrin Gundel
Cora Wiesner
Maria Paraskevi Kotini
Minkyoung Lee
Li-Kun Phng
Heinz-Georg Belting
Markus Affolter
Initiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of Rasip1
Nature Communications
title Initiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of Rasip1
title_full Initiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of Rasip1
title_fullStr Initiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of Rasip1
title_full_unstemmed Initiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of Rasip1
title_short Initiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of Rasip1
title_sort initiation of lumen formation from junctions via differential actomyosin contractility regulated by dynamic recruitment of rasip1
url https://doi.org/10.1038/s41467-024-54143-y
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