Nr2f1a suppresses bulbous arteriosus identity in the zebrafish atrium

NIH RePORTER · NIH · F31 · $40,686 · view on reporter.nih.gov ↗

Abstract

Project Summary/Abstract Normal vertebrate heart development involves the preservation of proper cardiac chamber proportions. Improper maintenance of cardiomyocyte (CM) identity underlies numerous congenital heart defects (CHDs), which can lead to cardiomyopathy and morbity in newborns as well as throughout adulthood. Nr2f orphan nuclear hormone receptors are conserved regulators of atrial development in vertebrates. NR2F2 mutations are associated with CHDs in humans. Our recent work demonstrates that zebrafish Nr2f1ais the functional equivalent of mammalian Nr2f2 with respect to early chamber development, as it is specifically expressed in the atrium and is vital for proper atrial differentiation. Here, we use a novel ENU-induced mutant named acorn worm (aco), which exhibits a loss of Nr2f1a expression. While engineered nr2f1a mutant embryos are early lethal in our hands, we have found that some aco mutants are viable to adulthood, affording a unique opportunity to investigate the effects of prolonged Nr2f1a loss in the mature heart. Adult aco hearts develop a non-contractile atrial chamber, which is surrounded by opaque connective tissue. Surprisingly, in contrast to the prediction from mouse conditional Nr2f2 KOs that atrial CMs lacking Nr2f2 would take on ventricular CM identity, histological analysis using AFOG staining revealed the adult aco atria lack pectinate or trabecular structures and instead have collagenous matrix similar to the bulbous arteriosus (BA) of the outflow tract. Transcriptome analyses from isolated aco cardiac chambers and in situ hybridization affirmed that aco mutant atria express BA-specific genes while upregulating retinoic acid (RA) signaling components. We find the BA-like identity of the atrium is first observed at the venous pole starting at 3 weeks post fertilization (wpf). In Aim 1, we will use a sophisticated genetic lineage tracing system to permanently label atrial CMs and elucidate the origin of the BA-like atrial chamber in aco mutant adults. In Aim 2, we will use novel transgenic tools to restore nr2f1a specifically in atrial CMs beginning at 2 wpf to determine the developmental window when Nr2f1a is critical to suppress the BA-like atria. In Aim 3, we will use pharmacological methods to modulate retinoic acid signaling (RA) signaling levels from 2 to 3 wpf to elucidate excess RA signaling downstream of Nr2f1a in aco mutants promotes the formation of the BA-like atrial chamber. Therefore, our findings highlight an unexpected role for Nr2f1a in repressing BA-identity within atria, which may yield novel insight into the molecular and cellular etiology of CHDs found in children and adults.

Key facts

NIH application ID
9921208
Project number
5F31HL147399-02
Recipient
CINCINNATI CHILDRENS HOSP MED CTR
Principal Investigator
Jacob Gafranek
Activity code
F31
Funding institute
NIH
Fiscal year
2020
Award amount
$40,686
Award type
5
Project period
2019-04-11 → 2022-04-10