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Molecular Determinants of Calpain-dependent Cleavage of Junctophilin-2 Protein in Cardiomyocytes
Journal article   Open access   Peer reviewed

Molecular Determinants of Calpain-dependent Cleavage of Junctophilin-2 Protein in Cardiomyocytes

Ang Guo, Duane Hall, Caimei Zhang, Tianqing Peng, Jordan D Miller, William Kutschke, Chad E Grueter, Frances L Johnson, Richard Z Lin and Long-Sheng Song
The Journal of biological chemistry, Vol.290(29), pp.17946-17955
07/17/2015
DOI: 10.1074/jbc.M115.652396
PMCID: PMC4505042
PMID: 26063807
url
https://doi.org/10.1074/jbc.M115.652396View
Published (Version of record) Open Access

Abstract

Background: Down-regulation of junctophilin-2 is associated with a variety of cardiac diseases. Results: Junctophilin-2 is cleaved by calpain at multiple sites, resulting in dysfunctional junctophilin-2 truncations. Conclusion: Calpain-mediated proteolysis contributes to posttranslational down-regulation of junctophilin-2. Significance: These data reveal, for the first time, the detailed molecular determinants responsible for calpain proteolysis of junctophilin-2. Junctophilin-2 (JP2), a membrane-binding protein that provides a structural bridge between the plasmalemma and sarcoplasmic reticulum, is essential for precise Ca 2+ -induced Ca 2+ release during excitation-contraction coupling in cardiomyocytes. In animal and human failing hearts, expression of JP2 is decreased markedly, but the molecular mechanisms underlying JP2 down-regulation remain incompletely defined. In mouse hearts, ischemia/reperfusion injury resulted in acute JP2 down-regulation, which was attenuated by pretreatment with the calpain inhibitor MDL-28170 or by transgenic overexpression of calpastatin, an endogenous calpain inhibitor. Using a combination of computational analysis to predict calpain cleavage sites and in vitro calpain proteolysis reactions, we identified four putative calpain cleavage sites within JP2 with three N-terminal and one C-terminal cleavage sites. Mutagenesis defined the C-terminal region of JP2 as the predominant calpain cleavage site. Exogenous expression of putative JP2 cleavage fragments was not sufficient to rescue Ca 2+ handling in JP2-deficient cardiomyocytes, indicating that cleaved JP2 is non-functional for normal Ca 2+ -induced Ca 2+ release. These data provide new molecular insights into the posttranslational regulatory mechanisms of JP2 in cardiac diseases.
Heart Molecular Bases of Disease calpain calcium excitation-contraction coupling (E-C coupling) junctophilin-2 proteolysis

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