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Controlling periodic long-range signalling to drive a morphogenetic transition.

Hugh Z Ford1, Angelika Manhart2,3, Jonathan R Chubb1

  • 1Laboratory for Molecular Cell Biology and Department of Cell and Developmental Biology, University College London, London, United Kingdom.

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|March 1, 2023
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Summary

Cells use cyclic adenosine monophosphate (cAMP) waves for long-range signaling during collective migration. Increased wave frequency, driven by a positive feedback loop, triggers cell movement and regulates developmental patterns.

Keywords:
collective migrationdevelopmental biologydictyosteliumexcitable mediafrequency codingmorphogenesisphysics of living systemssignal relayspiral wave

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Area of Science:

  • Cellular biology
  • Developmental biology
  • Biophysics

Background:

  • Cells communicate using signal relay for tissue-scale information transmission.
  • The mechanisms generating information in signal relay systems are not fully understood.
  • Periodic cyclic adenosine monophosphate (cAMP) waves in Dictyostelium discoideum facilitate collective cell migration.

Purpose of the Study:

  • To investigate how coding features of signal relay are generated.
  • To determine the mechanisms regulating cAMP wave circulation and frequency.
  • To elucidate the positive feedback loop between cell state and signaling patterns.

Main Methods:

  • Live imaging of Dictyostelium cell signaling.
  • Optogenetic perturbation of cell signaling states.
  • Mathematical modeling and general theory of excitable media.
  • Mechanical perturbations to test competing models.

Main Results:

  • Cell migration is initiated by an increased wave frequency from the signaling center.
  • Wave frequency is modulated by cAMP wave circulation, organizing long-range signals.
  • A positive feedback model, where wave circulation enhances signal relay and circulation rate, best explains the observed signaling dynamics.
  • Models based on cell density or spatial patterning do not account for temporal signaling evolution.

Conclusions:

  • A positive feedback mechanism between cell state and signaling patterns regulates long-range signal coding.
  • This feedback loop is crucial for driving collective cell migration and morphogenesis.
  • Understanding cAMP wave dynamics provides insights into cellular communication and pattern formation.