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Time to Decide? Dynamical Analysis Predicts Partial Tip/Stalk Patterning States Arise during Angiogenesis.

Lakshmi Venkatraman1, Erzsébet Ravasz Regan1,2, Katie Bentley1,3

  • 1Centre for Vascular Biology Research, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, United States of America.

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Mathematical modeling reveals that internal and external factors influence endothelial cell tip/stalk fate decisions during angiogenesis. This study uncovers novel intermediate cell states and a two-stage mechanism for adaptive behavior in dynamic vascular environments.

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Area of Science:

  • * Molecular and cellular biology
  • * Developmental biology
  • * Mathematical modeling of biological systems

Background:

  • * Angiogenesis is a dynamic process with poorly understood molecular timing.
  • * The VEGF-notch-DLL4 pathway is crucial for tip/stalk cell competition in sprouting angiogenesis.
  • * Individual cell-level dynamics of tip/stalk phenotype switching remain unclear.

Purpose of the Study:

  • * To investigate how local conditions influence endothelial cell (EC) tip/stalk phenotype switching kinetics using mathematical modeling.
  • * To elucidate the dynamic properties of the VEGF-notch-DLL4 signaling pathway at the individual cell level.
  • * To identify factors modulating tip/stalk decision speed and explore novel intermediate cell states.

Main Methods:

  • * Construction of an ordinary differential equation model for VEGF-notch-DLL4 signaling in coupled endothelial cells.
  • * Simulation of cell behavior under varying local conditions to analyze phenotype switching kinetics.
  • * Identification of internal cellular factors (e.g., Sirt1, Lfng1) influencing intermediate state duration.

Main Results:

  • * Significant asynchrony in tip/stalk cell decisions along angiogenic vessels, accelerating competition.
  • * Discovery of stable, intermediate
  • partial
  • cell states between tip and stalk fates.
  • * Identification of Sirt1 and Lfng1 as key regulators of time spent in partial states.
  • * Prediction that partial EC states occur during normal angiogenesis, especially during sprout rearrangement.

Conclusions:

  • * A novel two-stage mechanism for rapid adaptive behavior in dynamic angiogenic environments is proposed.
  • * Internal and external factors can modulate the speed of tip/stalk decisions in ECs.
  • * Findings offer new avenues for therapeutic targeting to manipulate vascular network topology and understand angiogenesis.