Abstract

Calcium release from the sarcoplasmic reticulum (SR) plays a central role in the regulation of cardiac contraction and rhythm in mammals and humans but its role is controversial in teleosts. Since the zebrafish is an emerging model for studies of cardiovascular function and regeneration we here sought to determine if basic features of SR calcium release are phylogenetically conserved. Confocal calcium imaging was used to detect spontaneous calcium release (calcium sparks and waves) from the SR. Calcium sparks were detected in 16 of 38 trout atrial myocytes and 6 of 15 ventricular cells. The spark amplitude was 1.45±0.03 times the baseline fluorescence and the time to half maximal decay of sparks was 27±3 ms. Spark frequency was 0.88 sparks µm−1 min−1 while calcium waves were 8.5 times less frequent. Inhibition of SR calcium uptake reduced the calcium transient (F/F0) from 1.77±0.17 to 1.12±0.18 (p = 0.002) and abolished calcium sparks and waves. Moreover, elevation of extracellular calcium from 2 to 10 mM promoted early and delayed afterdepolarizations (from 0.6±0.3 min−1 to 8.1±2.0 min−1, p = 0.001), demonstrating the ability of SR calcium release to induce afterdepolarizations in the trout heart. Calcium sparks of similar width and duration were also observed in zebrafish ventricular myocytes. In conclusion, this is the first study to consistently report calcium sparks in teleosts and demonstrate that the basic features of calcium release through the ryanodine receptor are conserved, suggesting that teleost cardiac myocytes is a relevant model to study the functional impact of abnormal SR function.

Highlights

  • Calcium release from the sarcoplasmic reticulum (SR) plays a central role in the regulation of the contraction and rhythm of the mammalian heart [1]

  • Identification and characterization of calcium sparks in teleost cardiomyocytes To determine whether spontaneous calcium release through the RyR2 occurs in the teleost heart, trout cardiomyocytes were used first because it is the best characterized teleost species

  • Myocytes were loaded with fluo-4 and local calcium release from the SR was detected using confocal line scanning

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Summary

Introduction

Calcium release from the sarcoplasmic reticulum (SR) plays a central role in the regulation of the contraction and rhythm of the mammalian heart [1]. Contraction can be elicited by asynchronous calcium release from the SR, which typically occurs under pathological conditions in the mammalian and human heart [4,5,6] Such asynchronous release gives rise to calcium waves, and subsequent membrane depolarizations [7] that can induce arrhythmias [8]. Because of this predominant role of the SR in the regulation of cardiac contraction and rhythm, calcium release from the SR through the ryanodine receptor might be expected to be a conserved mechanism, and investigation of the functional role of the SR in the teleost heart, which phylogenetically is the ancestor of other vertebrate hearts, may bring important information on evolutionary changes in the SR function

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