Terentyev Dmitry, Viatchenko-Karpinski Serge, Vedamoorthyrao Srikanth, Oduru Sridhar, Györke Inna, Williams Simon C, Györke Sandor
Department of Physiology and Cell Biology, 505 Davis Heart and Lung Research Institute, The Ohio State University, 473 W 12th Ave, Columbus, OH 43210, USA.
J Physiol. 2007 Aug 15;583(Pt 1):71-80. doi: 10.1113/jphysiol.2007.136879. Epub 2007 Jun 14.
In cardiac muscle, intracellular Ca2+ release is controlled by a number of proteins including the ryanodine receptor (RyR2), calsequestrin (CASQ2), triadin-1 (Trd) and junctin (Jn) which form a complex in the junctional sarcoplasmic reticulum (SR) membrane. Within this complex, Trd appears to link CASQ2 to RyR2 although the functional significance of this interaction is unclear. In this study, we explored the functional importance of Trd-CASQ2 interactions for intracellular Ca2+ handling in rat ventricular myocytes. A peptide encompassing the homologous CASQ2 binding domain of Trd (residues 206-230 in the rat; TrdPt) was expressed in the lumen of the SR to disrupt Trd-CASQ2 interactions. Myocytes expressing TrdPt exhibited increased responsiveness of SR Ca2+ release to activation by ICa as manifested by flattened and broadened voltage dependency of the amplitude of cytosolic Ca2+ transients. Rhythmically paced, TrdPt-expressing myocytes exhibited spontaneous arrhythmogenic oscillations of intracellular Ca2+ and membrane potential that was not seen in control cells. In addition, the frequency of spontaneous Ca2+ sparks and Ca2+ waves was significantly increased in TrdPt-expressing, permeabilized myocytes. These alterations in SR Ca2+ release were accompanied by a significant decrease in basal free intra-SR[Ca2+] and total SR Ca2+ content in TrdPt-expressing cells. At the same time a synthetic peptide corresponding to the CASQ2 binding domain of Trd produced no direct effects on the activity of single RyR2 channels incorporated into lipid bilayers while interfering with the ability of CASQ2 to inhibit the RyR2 channel. These results suggest that CASQ2 stabilizes SR Ca2+ release by inhibiting the RyR2 channel through interaction with Trd. They also show that intracellular Ca2+ cycling in the heart relies on coordinated interactions between proteins of the RyR2 channel complex and that disruption of these interactions may represent a molecular mechanism for cardiac disease.
在心肌中,细胞内Ca2+释放受多种蛋白质控制,包括兰尼碱受体(RyR2)、肌集钙蛋白(CASQ2)、三联蛋白-1(Trd)和连接蛋白(Jn),它们在连接肌浆网(SR)膜中形成复合物。在这个复合物中,Trd似乎将CASQ2与RyR2连接起来,尽管这种相互作用的功能意义尚不清楚。在本研究中,我们探讨了Trd-CASQ2相互作用对大鼠心室肌细胞内Ca2+处理的功能重要性。在SR腔中表达包含Trd同源CASQ2结合域的肽(大鼠中的206-230位氨基酸;TrdPt),以破坏Trd-CASQ2相互作用。表达TrdPt的心肌细胞表现出SR Ca2+释放对ICa激活的反应性增加,表现为胞质Ca2+瞬变幅度的电压依赖性变平变宽。有节律起搏时,表达TrdPt的心肌细胞表现出细胞内Ca2+和膜电位的自发性致心律失常振荡,而对照细胞中未观察到。此外,在表达TrdPt的透化心肌细胞中,自发性Ca2+火花和Ca2+波的频率显著增加。SR Ca2+释放的这些改变伴随着表达TrdPt的细胞中基础游离SR[Ca2+]和总SR Ca2+含量的显著降低。同时,对应于Trd的CASQ2结合域的合成肽对整合到脂质双层中的单个RyR2通道的活性没有直接影响,同时干扰了CASQ2抑制RyR2通道的能力。这些结果表明,CASQ2通过与Trd相互作用抑制RyR2通道来稳定SR Ca2+释放。它们还表明,心脏中的细胞内Ca2+循环依赖于RyR2通道复合物蛋白质之间的协调相互作用,这些相互作用的破坏可能代表心脏病的分子机制。