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Evolutionarily conserved Tbx5-Wnt2/2b pathway orchestrates cardiopulmonary development.

Jeffrey D Steimle1,2,3, Scott A Rankin4,5,6,5, Christopher E Slagle7,8,9,10

  • 1Department of Pediatrics, University of Chicago, Chicago, IL 60637.

Proceedings of the National Academy of Sciences of the United States of America
|October 25, 2018
PubMed
Summary

The transcription factor TBX5 initiates a signaling loop between heart and lung progenitors, crucial for developing pulmonary circulation and atrial septation during the transition to land. This finding clarifies the coevolution of heart and lung structures.

Keywords:
Hedgehog signalingTBX5Wnt signalingheart developmentlung development

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Area of Science:

  • Developmental Biology
  • Evolutionary Biology
  • Cardiovascular Research

Background:

  • The co-development of lungs and heart is vital for terrestrial life.
  • Second heart field (SHF) cardiopulmonary progenitors (CPPs) form cardiac structures supporting pulmonary circulation.
  • Previously, transcription factors like Tbx5 were thought to directly regulate cardiac morphogenesis genes.

Purpose of the Study:

  • To investigate the precise role of TBX5 in cardiac septation and pulmonary development.
  • To elucidate the molecular mechanisms underlying the coevolution of pulmonary and cardiac structures.
  • To determine if TBX5 directly drives cardiac morphogenesis or initiates signaling pathways.

Main Methods:

  • Analysis of Tbx5 function in mouse and amphibian models.
  • TBX5 ChIP-sequencing to identify direct gene targets.
  • In vitro studies using precardiac mesoderm.
  • Investigation of Tbx5 haploinsufficiency in a mouse model of Holt-Oram syndrome.

Main Results:

  • TBX5 directly drives Wnt ligands (Wnt2, Wnt2b), initiating a bidirectional signaling loop between mesoderm and endoderm.
  • This loop is essential for pulmonary endoderm specification and subsequent atrial septation.
  • Tbx5 is required for lung specification in mice and amphibians, but not swim bladder development in zebrafish.
  • Tbx5 cooperates with Shh signaling for lung morphogenesis.
  • Tbx5 haploinsufficiency disrupts this signaling loop, impacting both cardiac and pulmonary development.

Conclusions:

  • TBX5 acts non-cell- autonomously to initiate a mesoderm-endoderm-mesoderm signaling loop essential for lunged vertebrates.
  • This signaling loop provides a molecular basis for the coevolution of pulmonary and cardiac structures necessary for terrestrial life.
  • The findings challenge the direct gene-regulatory network model, highlighting TBX5's role in initiating complex signaling interactions.