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

Author

Listed:
  • Shinya Yuge

    (Nippon Medical School)

  • Koichi Nishiyama

    (Kumamoto University
    University of Miyazaki)

  • Yuichiro Arima

    (Kumamoto University
    Kumamoto University)

  • Yasuyuki Hanada

    (Kumamoto University
    Nagoya University)

  • Eri Oguri-Nakamura

    (Nippon Medical School)

  • Sanshiro Hanada

    (Kumamoto University)

  • Tomohiro Ishii

    (Nippon Medical School)

  • Yuki Wakayama

    (National Cerebral and Cardiovascular Center Research Institute)

  • Urara Hasegawa

    (Pennsylvania State University)

  • Kazuya Tsujita

    (Kobe University
    Kobe University Graduate School of Medicine)

  • Ryuji Yokokawa

    (Kyoto University)

  • Takashi Miura

    (Kyushu University)

  • Toshiki Itoh

    (Kobe University
    Kobe University Graduate School of Medicine)

  • Kenichi Tsujita

    (Kumamoto University)

  • Naoki Mochizuki

    (National Cerebral and Cardiovascular Center Research Institute)

  • Shigetomo Fukuhara

    (Nippon Medical School)

Abstract

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.

Suggested Citation

  • Shinya Yuge & Koichi Nishiyama & Yuichiro Arima & Yasuyuki Hanada & Eri Oguri-Nakamura & Sanshiro Hanada & Tomohiro Ishii & Yuki Wakayama & Urara Hasegawa & Kazuya Tsujita & Ryuji Yokokawa & Takashi M, 2022. "Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins," Nature Communications, Nature, vol. 13(1), pages 1-25, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30197-8
    DOI: 10.1038/s41467-022-30197-8
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    References listed on IDEAS

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    1. Daisuke Yamazaki & Shiro Suetsugu & Hiroaki Miki & Yuki Kataoka & Shin-Ichi Nishikawa & Takashi Fujiwara & Nobuaki Yoshida & Tadaomi Takenawa, 2003. "WAVE2 is required for directed cell migration and cardiovascular development," Nature, Nature, vol. 424(6947), pages 452-456, July.
    2. Jiahui Cao & Manuel Ehling & Sigrid März & Jochen Seebach & Katsiaryna Tarbashevich & Tomas Sixta & Mara E. Pitulescu & Ann-Cathrin Werner & Boris Flach & Eloi Montanez & Erez Raz & Ralf H. Adams & Ha, 2017. "Polarized actin and VE-cadherin dynamics regulate junctional remodelling and cell migration during sprouting angiogenesis," Nature Communications, Nature, vol. 8(1), pages 1-20, December.
    3. Cong Xu & Sana S. Hasan & Inga Schmidt & Susana F. Rocha & Mara E. Pitulescu & Jeroen Bussmann & Dana Meyen & Erez Raz & Ralf H. Adams & Arndt F. Siekmann, 2014. "Arteries are formed by vein-derived endothelial tip cells," Nature Communications, Nature, vol. 5(1), pages 1-11, December.
    4. Hyouk-Bum Kwon & Shengpeng Wang & Christian S. M. Helker & S. Javad Rasouli & Hans-Martin Maischein & Stefan Offermanns & Wiebke Herzog & Didier Y. R. Stainier, 2016. "In vivo modulation of endothelial polarization by Apelin receptor signalling," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
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