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Mechanical signaling coordinates the embryonic heartbeat.

Kevin K Chiou1, Jason W Rocks1, Christina Yingxian Chen2

  • 1Department of Physics and Astronomy, University of Pennsylvania, Philadelphia, PA 19104;

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|July 27, 2016
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In early embryonic hearts, mechanical signaling, not electrical, coordinates beats. This biophysical model explains heartbeat velocity and strain, suggesting matrix stiffness initiates the first heartbeats.

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Area of Science:

  • Cardiovascular Physiology
  • Biophysics
  • Developmental Biology

Background:

  • Cardiac myocytes (CMs) coordinate contractions via signaling mechanisms.
  • Electrical signaling through gap junctions is the established mechanism in adult hearts.
  • The early embryonic heart's signaling mechanism remains less understood.

Purpose of the Study:

  • To propose and model mechanical signaling as the primary mechanism coordinating beats in the early embryonic heart.
  • To investigate the role of extracellular matrix (ECM) stiffness in mechanical wave propagation.
  • To differentiate between electrical and mechanical signaling in embryonic versus adult hearts.

Main Methods:

  • Developed a biophysical model of mechanically excitable CMs in an elastic-fluid biphasic ECM.
  • Predicted heartbeat velocity and strain based on matrix stiffness.
  • Used gap junction blocker (β-glycyrrhetinic acid, BGA) to disrupt electrical conduction in embryonic and adult hearts.
  • Measured matrix stiffness at the onset of embryonic heart beating.

Main Results:

  • Model predictions for stiffness dependence of heartbeat velocity and strain quantitatively matched experimental data.
  • BGA disrupted adult hearts but not embryonic hearts, supporting mechanical signaling in embryos.
  • A minimum matrix stiffness was predicted and found to correlate with the onset of beating.

Conclusions:

  • Mechanical signaling, mediated by ECM stiffness, is crucial for coordinating beats in the early embryonic heart.
  • This contrasts with the electrical signaling dominant in adult hearts.
  • Mechanical signaling likely initiates the very first heartbeats due to sufficient matrix stiffness.