Disruption of planar cell polarity signaling results in congenital heart defects and cardiomyopathy attributable to early cardiomyocyte disorganization
Open accessAbstract
The Drosophila scribble gene regulates apical-basal polarity and is implicated in control of cellular architecture and cell growth control. Mutations in mammalian Scrib ( circletail ; Crc mutant) also result in abnormalities suggestive of roles in planar cell polarity regulation. We show that Crc mutants develop heart malformations and cardiomyopathy attributable to abnormalities in cardiomyocyte organization within the early heart tube. N-Cadherin is lost from the cardiomyocyte cell membrane and cell–cell adhesion is disrupted. This results in abnormalities in heart looping and formation of both the trabeculae and compact myocardium, which ultimately results in cardiac misalignment defects and ventricular noncompaction. Thus, these late abnormalities arise from defects occurring at the earliest stages of heart development. Mislocalization of Vangl2 in Crc/Crc cardiomyocytes suggests Scrib is acting in the planar cell polarity pathway in this tissue. Moreover, double heterozygosity for mutations in both Scrib and Vangl2 can cause cardiac defects similar to those found in homozygous mutants for each gene but without other major defects. We propose that heterozygosity for mutations in different genes in the planar cell polarity pathway may be an important mechanism for congenital heart defects and cardiomyopathy in humans.
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The early defect in heart tube organization corresponds with the displacement of N-cadherin from the cardiomyocyte membrane.
“Interestingly, the early defect in heart tube organization corresponds with the displacement of N-cadherin from the cardiomyocyte membrane.”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Phillips et al., 2007
Characterization of both lung and cardiac defects in circletail mutants highlighted a role for the PCP pathway in these tissues-in both cases, the distribution of planar polarity protein Vangl2 is disrupted.
“Characterization of both lung and cardiac defects in circletail mutants also highlighted a role for the PCP pathway in these tissues—in both cases, the distribution of planar polarity protein Vangl2 is disrupted (Phillips et al., 2007; Yates et al., 2013).”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Phillips et al., 2007
Animals homozygous for the circletail allele also have subtle abnormalities in cardiomyocyte organization within the primary heart tube which manifest as gross abnormalities in heart formation at later stages of development.
“Animals homozygous for the circletail allele also have subtle abnormalities in cardiomyocyte organization within the primary heart tube which manifest as gross abnormalities in heart formation at later stages of development (Phillips et al., 2007).”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Phillips et al., 2007
Scribble and Vangl have collaborative roles in PCP in diverse other mouse tissues, mediating axon guidance in the hindbrain and heart looping and subsequent cardiac development.
“Subsequently, collaborative roles for Scribble and Vangl in PCP were uncovered in diverse other mouse tissues, mediating axon guidance in the hindbrain (Walsh et al., 2011) and heart looping and subsequent cardiac development (Phillips et al., 2007).”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Phillips et al., 2007
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“Animals homozygous for the circletail allele also have subtle abnormalities in cardiomyocyte organization within the primary heart tube which manifest as gross abnormalities in heart formation at later stages of development (Phillips et al., 2007).”
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- Authors
- Phillips, H. M., Rhee, H. J., Murdoch, J. N., Hildreth, V., Peat, J. D., Anderson, R. H., Copp, A. J., Chaudhry, B., & Henderson, D. J.
- Affiliations
- University College London (GB)
- Venue
- Circulation Research
- Published
- 2007-07-20
- Volume
- 101
- Issue
- 2
- Pages
- 137-145
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- OpenAlex
- W2140577425
- Cited by
- 133
- References
- 28
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 10 · 2023: 4 · 2022: 7 · 2021: 4 · 2020: 4 · 2019: 5 · 2018: 13 · 2017: 5 · 2016: 5 · 2015: 9 · 2014: 6 · 2013: 7 · 2012: 10
- FWCI
- 3.84
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- Wellcome Trust (068883)
- British Heart Foundation (PG/11/76/29108)
- Medical Research Council
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Keywords
- planar cell polarity, Scribble, Vangl2, congenital heart disease, cardiomyopathy, heart tube, N-cadherin, cell-cell adhesion, heart looping, ventricular noncompaction, trabeculae, compact myocardium, heterozygosity, Drosophila heart development
- MeSH terms
- Animals, Breeding, Heart Defects, Congenital, Heart Ventricles, Heterozygote, Humans, Mice, Mutant Strains, Mutation, Cardiomyopathies, Myocardium, Nerve Tissue Proteins, Cell Polarity, Protein Transport, Myocytes, Cardiac, Intracellular Signaling Peptides and Proteins, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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