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Arteries are formed by vein-derived endothelial tip cells

Author

Listed:
  • Cong Xu

    (Max Planck Institute for Molecular Biomedicine)

  • Sana S. Hasan

    (Max Planck Institute for Molecular Biomedicine)

  • Inga Schmidt

    (Max Planck Institute for Molecular Biomedicine)

  • Susana F. Rocha

    (Max Planck Institute for Molecular Biomedicine)

  • Mara E. Pitulescu

    (Max Planck Institute for Molecular Biomedicine)

  • Jeroen Bussmann

    (Max Planck Institute for Molecular Biomedicine)

  • Dana Meyen

    (Institute of Cell Biology, ZMBE)

  • Erez Raz

    (Institute of Cell Biology, ZMBE)

  • Ralf H. Adams

    (Max Planck Institute for Molecular Biomedicine
    University of Münster, Faculty of Medicine)

  • Arndt F. Siekmann

    (Max Planck Institute for Molecular Biomedicine)

Abstract

Tissue vascularization entails the formation of a blood vessel plexus, which remodels into arteries and veins. Here we show, by using time-lapse imaging of zebrafish fin regeneration and genetic lineage tracing of endothelial cells in the mouse retina, that vein-derived endothelial tip cells contribute to emerging arteries. Our movies uncover that arterial-fated tip cells change migration direction and migrate backwards within the expanding vascular plexus. This behaviour critically depends on chemokine receptor cxcr4a function. We show that the relevant Cxcr4a ligand Cxcl12a selectively accumulates in newly forming bone tissue even when ubiquitously overexpressed, pointing towards a tissue-intrinsic mode of chemokine gradient formation. Furthermore, we find that cxcr4a mutant cells can contribute to developing arteries when in association with wild-type cells, suggesting collective migration of endothelial cells. Together, our findings reveal specific cell migratory behaviours in the developing blood vessel plexus and uncover a conserved mode of artery formation.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms6758
    DOI: 10.1038/ncomms6758
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    Cited by:

    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. 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.
    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. 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.

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