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Research Article
Loss of αT-catenin alters the hybrid adhering junctions in the heart and leads to dilated cardiomyopathy and ventricular arrhythmia following acute ischemia
Jifen Li, Steven Goossens, Jolanda van Hengel, Erhe Gao, Lan Cheng, Koen Tyberghein, Xiying Shang, Riet De Rycke, Frans van Roy, Glenn L. Radice
Journal of Cell Science 2012 125: 1058-1067; doi: 10.1242/jcs.098640
Jifen Li
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  • For correspondence: jifen.li@jefferson.edu frans.vanroy@dmbr.vib-UGent.be
Steven Goossens
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Jolanda van Hengel
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Erhe Gao
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Lan Cheng
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Koen Tyberghein
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Xiying Shang
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Riet De Rycke
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Frans van Roy
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  • For correspondence: jifen.li@jefferson.edu frans.vanroy@dmbr.vib-UGent.be
Glenn L. Radice
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Summary

It is generally accepted that the intercalated disc (ICD) required for mechano-electrical coupling in the heart consists of three distinct junctional complexes: adherens junctions, desmosomes and gap junctions. However, recent morphological and molecular data indicate a mixing of adherens junctional and desmosomal components, resulting in a ‘hybrid adhering junction’ or ‘area composita’. The α-catenin family member αT-catenin, part of the N-cadherin–catenin adhesion complex in the heart, is the only α-catenin that interacts with the desmosomal protein plakophilin-2 (PKP2). Thus, it has been postulated that αT-catenin might serve as a molecular integrator of the two adhesion complexes in the area composita. To investigate the role of αT-catenin in the heart, gene targeting technology was used to delete the Ctnna3 gene, encoding αT-catenin, in the mouse. The αT-catenin-null mice are viable and fertile; however, the animals exhibit progressive cardiomyopathy. Adherens junctional and desmosomal proteins were unaffected by loss of αT-catenin, with the exception of the desmosomal protein PKP2. Immunogold labeling at the ICD demonstrated in the αT-catenin-null heart a preferential reduction of PKP2 at the area composita compared with the desmosome. Furthermore, gap junction protein Cx43 was reduced at the ICD, including its colocalization with N-cadherin. Gap junction remodeling in αT-catenin-knockout hearts was associated with an increased incidence of ventricular arrhythmias after acute ischemia. This novel animal model demonstrates for the first time how perturbation in αT-catenin can affect both PKP2 and Cx43 and thereby highlights the importance of understanding the crosstalk between the junctional proteins of the ICD and its implications for arrhythmogenic cardiomyopathy.

Footnotes

  • ↵‡ These authors contributed equally to this work

  • Funding

    This work was supported by the Jefferson Kimmel Cancer Center [NIH Cancer Center Core grant number 5 P30 CA-56036]; American Heart Association Scientist Development [grant number N2080068 to J.L.]; National Institutes of Health [grant number HL081569 to G.R.]; the Research Foundation – Flanders (FWO) [grant number G.0104.09N to F.v.R.]; and the Concerted Research Actions – Ghent University (GOA) [grant number 01G01908 to F.v.R.]. S.G. is a postdoctoral fellow with the FWO, and K.T. is a predoctoral fellow with the Flemish Agency for Innovation by Science and Technology (IWT). Deposited in PMC for release after 12 months.

  • Supplementary material available online at http://jcs.biologists.org/lookup/suppl/doi:10.1242/jcs.098640/-/DC1

  • Accepted October 4, 2011.
  • © 2012.
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Research Article
Loss of αT-catenin alters the hybrid adhering junctions in the heart and leads to dilated cardiomyopathy and ventricular arrhythmia following acute ischemia
Jifen Li, Steven Goossens, Jolanda van Hengel, Erhe Gao, Lan Cheng, Koen Tyberghein, Xiying Shang, Riet De Rycke, Frans van Roy, Glenn L. Radice
Journal of Cell Science 2012 125: 1058-1067; doi: 10.1242/jcs.098640
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Research Article
Loss of αT-catenin alters the hybrid adhering junctions in the heart and leads to dilated cardiomyopathy and ventricular arrhythmia following acute ischemia
Jifen Li, Steven Goossens, Jolanda van Hengel, Erhe Gao, Lan Cheng, Koen Tyberghein, Xiying Shang, Riet De Rycke, Frans van Roy, Glenn L. Radice
Journal of Cell Science 2012 125: 1058-1067; doi: 10.1242/jcs.098640

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