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Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins

Angiogenesis is regulated in coordinated fashion by chemical and mechanical cues acting on endothelial cells (ECs). However, the mechanobiological mechanisms of angiogenesis remain unknown. Herein, we demonstrate a crucial role of blood flow-driven intraluminal pressure (IP) in regulating wound angi...

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Autores principales: Yuge, Shinya, Nishiyama, Koichi, Arima, Yuichiro, Hanada, Yasuyuki, Oguri-Nakamura, Eri, Hanada, Sanshiro, Ishii, Tomohiro, Wakayama, Yuki, Hasegawa, Urara, Tsujita, Kazuya, Yokokawa, Ryuji, Miura, Takashi, Itoh, Toshiki, Tsujita, Kenichi, Mochizuki, Naoki, Fukuhara, Shigetomo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9098626/
https://www.ncbi.nlm.nih.gov/pubmed/35551172
http://dx.doi.org/10.1038/s41467-022-30197-8
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author Yuge, Shinya
Nishiyama, Koichi
Arima, Yuichiro
Hanada, Yasuyuki
Oguri-Nakamura, Eri
Hanada, Sanshiro
Ishii, Tomohiro
Wakayama, Yuki
Hasegawa, Urara
Tsujita, Kazuya
Yokokawa, Ryuji
Miura, Takashi
Itoh, Toshiki
Tsujita, Kenichi
Mochizuki, Naoki
Fukuhara, Shigetomo
author_facet Yuge, Shinya
Nishiyama, Koichi
Arima, Yuichiro
Hanada, Yasuyuki
Oguri-Nakamura, Eri
Hanada, Sanshiro
Ishii, Tomohiro
Wakayama, Yuki
Hasegawa, Urara
Tsujita, Kazuya
Yokokawa, Ryuji
Miura, Takashi
Itoh, Toshiki
Tsujita, Kenichi
Mochizuki, Naoki
Fukuhara, Shigetomo
author_sort Yuge, Shinya
collection PubMed
description Angiogenesis is regulated in coordinated fashion by chemical and mechanical cues acting on endothelial cells (ECs). However, the mechanobiological mechanisms of angiogenesis remain unknown. Herein, we demonstrate a crucial role of blood flow-driven intraluminal pressure (IP) in regulating wound angiogenesis. During wound angiogenesis, blood flow-driven IP loading inhibits elongation of injured blood vessels located at sites upstream from blood flow, while downstream injured vessels actively elongate. In downstream injured vessels, F-BAR proteins, TOCA1 and CIP4, localize at leading edge of ECs to promote N-WASP-dependent Arp2/3 complex-mediated actin polymerization and front-rear polarization for vessel elongation. In contrast, IP loading expands upstream injured vessels and stretches ECs, preventing leading edge localization of TOCA1 and CIP4 to inhibit directed EC migration and vessel elongation. These data indicate that the TOCA family of F-BAR proteins are key actin regulatory proteins required for directed EC migration and sense mechanical cell stretching to regulate wound angiogenesis.
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spelling pubmed-90986262022-05-14 Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins Yuge, Shinya Nishiyama, Koichi Arima, Yuichiro Hanada, Yasuyuki Oguri-Nakamura, Eri Hanada, Sanshiro Ishii, Tomohiro Wakayama, Yuki Hasegawa, Urara Tsujita, Kazuya Yokokawa, Ryuji Miura, Takashi Itoh, Toshiki Tsujita, Kenichi Mochizuki, Naoki Fukuhara, Shigetomo Nat Commun Article Angiogenesis is regulated in coordinated fashion by chemical and mechanical cues acting on endothelial cells (ECs). However, the mechanobiological mechanisms of angiogenesis remain unknown. Herein, we demonstrate a crucial role of blood flow-driven intraluminal pressure (IP) in regulating wound angiogenesis. During wound angiogenesis, blood flow-driven IP loading inhibits elongation of injured blood vessels located at sites upstream from blood flow, while downstream injured vessels actively elongate. In downstream injured vessels, F-BAR proteins, TOCA1 and CIP4, localize at leading edge of ECs to promote N-WASP-dependent Arp2/3 complex-mediated actin polymerization and front-rear polarization for vessel elongation. In contrast, IP loading expands upstream injured vessels and stretches ECs, preventing leading edge localization of TOCA1 and CIP4 to inhibit directed EC migration and vessel elongation. These data indicate that the TOCA family of F-BAR proteins are key actin regulatory proteins required for directed EC migration and sense mechanical cell stretching to regulate wound angiogenesis. Nature Publishing Group UK 2022-05-12 /pmc/articles/PMC9098626/ /pubmed/35551172 http://dx.doi.org/10.1038/s41467-022-30197-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Yuge, Shinya
Nishiyama, Koichi
Arima, Yuichiro
Hanada, Yasuyuki
Oguri-Nakamura, Eri
Hanada, Sanshiro
Ishii, Tomohiro
Wakayama, Yuki
Hasegawa, Urara
Tsujita, Kazuya
Yokokawa, Ryuji
Miura, Takashi
Itoh, Toshiki
Tsujita, Kenichi
Mochizuki, Naoki
Fukuhara, Shigetomo
Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins
title Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins
title_full Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins
title_fullStr Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins
title_full_unstemmed Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins
title_short Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins
title_sort mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the toca family of f-bar proteins
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9098626/
https://www.ncbi.nlm.nih.gov/pubmed/35551172
http://dx.doi.org/10.1038/s41467-022-30197-8
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