Sinus venosus adaptation models prolonged cardiovascular disease and reveals insights into evolutionary transitions of the vertebrate heart

Jacob T. Gafranek, Enrico D’Aniello, Padmapriyadarshini Ravisankar, Kairavee Thakkar, Ronald J. Vagnozzi, Hee-Woong Lim, Nathan Salomonis and Joshua S. Waxman ()
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Jacob T. Gafranek: University of Cincinnati College of Medicine
Enrico D’Aniello: Stazione Zoologica Anton Dohrn
Padmapriyadarshini Ravisankar: Cincinnati Children’s Hospital Medical Center
Kairavee Thakkar: Cincinnati Children’s Hospital Medical Center
Ronald J. Vagnozzi: University of Colorado Anschutz Medical Campus
Hee-Woong Lim: Cincinnati Children’s Hospital Medical Center
Nathan Salomonis: Cincinnati Children’s Hospital Medical Center
Joshua S. Waxman: Cincinnati Children’s Hospital Medical Center

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: Abstract How two-chambered hearts in basal vertebrates have evolved from single-chamber hearts found in ancestral chordates remains unclear. Here, we show that the teleost sinus venosus (SV) is a chamber-like vessel comprised of an outer layer of smooth muscle cells. We find that in adult zebrafish nr2f1a mutants, which lack atria, the SV comes to physically resemble the thicker bulbus arteriosus (BA) at the arterial pole of the heart through an adaptive, hypertensive response involving smooth muscle proliferation due to aberrant hemodynamic flow. Single cell transcriptomics show that smooth muscle and endothelial cell populations within the adapting SV also take on arterial signatures. Bulk transcriptomics of the blood sinuses flanking the tunicate heart reinforce a model of greater equivalency in ancestral chordate BA and SV precursors. Our data simultaneously reveal that secondary complications from congenital heart defects can develop in adult zebrafish similar to those in humans and that the foundation of equivalency between flanking auxiliary vessels may remain latent within basal vertebrate hearts.

Date: 2023
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DOI: 10.1038/s41467-023-41184-y

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