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Glycolytic regulation of cell rearrangement in angiogenesis

Author

Listed:
  • Bert Cruys

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Brian W. Wong

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Anna Kuchnio

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Dries Verdegem

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Anna Rita Cantelmo

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Lena-Christin Conradi

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Saar Vandekeere

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Ann Bouché

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Ivo Cornelissen

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Stefan Vinckier

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Roeland M. H. Merks

    (Life Sciences Group, Centrum Wiskunde and Informatica
    Mathematical Institute, Leiden University)

  • Elisabetta Dejana

    (Genetics and Pathology, Rudbeck Laboratory, Uppsala University
    FIRC Institute of Molecular Oncology
    Milan University)

  • Holger Gerhardt

    (Vascular Patterning Laboratory
    Vesalius Research Center, Vascular Patterning Laboratory
    Integrative Vascular Biology Laboratory, Max-Delbrück-Center for Molecular Medicine)

  • Mieke Dewerchin

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

  • Katie Bentley

    (Genetics and Pathology, Rudbeck Laboratory, Uppsala University
    Computational Biology Laboratory, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Peter Carmeliet

    (Laboratory of Angiogenesis and Vascular Metabolism
    Vesalius Research Center, Laboratory of Angiogenesis and Vascular Metabolism)

Abstract

During vessel sprouting, endothelial cells (ECs) dynamically rearrange positions in the sprout to compete for the tip position. We recently identified a key role for the glycolytic activator PFKFB3 in vessel sprouting by regulating cytoskeleton remodelling, migration and tip cell competitiveness. It is, however, unknown how glycolysis regulates EC rearrangement during vessel sprouting. Here we report that computational simulations, validated by experimentation, predict that glycolytic production of ATP drives EC rearrangement by promoting filopodia formation and reducing intercellular adhesion. Notably, the simulations correctly predicted that blocking PFKFB3 normalizes the disturbed EC rearrangement in high VEGF conditions, as occurs during pathological angiogenesis. This interdisciplinary study integrates EC metabolism in vessel sprouting, yielding mechanistic insight in the control of vessel sprouting by glycolysis, and suggesting anti-glycolytic therapy for vessel normalization in cancer and non-malignant diseases.

Suggested Citation

  • Bert Cruys & Brian W. Wong & Anna Kuchnio & Dries Verdegem & Anna Rita Cantelmo & Lena-Christin Conradi & Saar Vandekeere & Ann Bouché & Ivo Cornelissen & Stefan Vinckier & Roeland M. H. Merks & Elisa, 2016. "Glycolytic regulation of cell rearrangement in angiogenesis," Nature Communications, Nature, vol. 7(1), pages 1-15, November.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12240
    DOI: 10.1038/ncomms12240
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    Cited by:

    1. Rocío Vega & Manuel Carretero & Rui D M Travasso & Luis L Bonilla, 2020. "Notch signaling and taxis mechanisms regulate early stage angiogenesis: A mathematical and computational model," PLOS Computational Biology, Public Library of Science, vol. 16(1), pages 1-31, January.
    2. Noemi Gioelli & Lisa J. Neilson & Na Wei & Giulia Villari & Wenqian Chen & Bernhard Kuhle & Manuel Ehling & Federica Maione & Sander Willox & Serena Brundu & Daniele Avanzato & Grigorios Koulouras & M, 2022. "Neuropilin 1 and its inhibitory ligand mini-tryptophanyl-tRNA synthetase inversely regulate VE-cadherin turnover and vascular permeability," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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