IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30197-8.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30197-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-30197-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jonas Stewen & Kai Kruse & Anca T. Godoi-Filip & Zenia & Hyun-Woo Jeong & Susanne Adams & Frank Berkenfeld & Martin Stehling & Kristy Red-Horse & Ralf H. Adams & Mara E. Pitulescu, 2024. "Eph-ephrin signaling couples endothelial cell sorting and arterial specification," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    2. Laetitia Préau & Anna Lischke & Melanie Merkel & Neslihan Oegel & Maria Weissenbruch & Andria Michael & Hongryeol Park & Dietmar Gradl & Christian Kupatt & Ferdinand Noble, 2024. "Parenchymal cues define Vegfa-driven venous angiogenesis by activating a sprouting competent venous endothelial subtype," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    3. Nicholas W. Chavkin & Gael Genet & Mathilde Poulet & Erin D. Jeffery & Corina Marziano & Nafiisha Genet & Hema Vasavada & Elizabeth A. Nelson & Bipul R. Acharya & Anupreet Kour & Jordon Aragon & Steph, 2022. "Endothelial cell cycle state determines propensity for arterial-venous fate," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Gianfranco Matrone & Sung Yun Jung & Jong Min Choi & Antrix Jain & Hon-Chiu Eastwood Leung & Kimal Rajapakshe & Cristian Coarfa & Julie Rodor & Martin A. Denvir & Andrew H. Baker & John P. Cooke, 2021. "Nuclear S-nitrosylation impacts tissue regeneration in zebrafish," Nature Communications, Nature, vol. 12(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30197-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.