Circulation Research. 2002
Published online before print August 8, 2002, doi: 10.1161/01.RES.0000032490.04207.BD
Published online before print August 8, 2002, doi: 10.1161/01.RES.0000032490.04207.BD
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Submitted on April 30, 2002
Revised on July 25, 2002
Accepted on July 26, 2002
Luminal Ca2+ Controls Termination and Refractory Behavior of Ca2+-Induced Ca2+ Release in Cardiac Myocytes
Dmitry Terentyev ;
From Texas Tech University HSC (D.T., S.V.-K., A.L.E., S.G.), Lubbock, Tex; and the University of Wisconsin (H.H.V.), Madison, Wis.
* To whom correspondence should be addressed. E-mail: sandor.gyorke{at}ttuhsc.edu.
Despite extensive research, the mechanisms responsible for the graded nature and early termination of Ca2+-induced Ca2+ release (CICR) in cardiac muscle remain poorly understood. Suggested mechanisms include ryanodine receptor (RyR) inactivation/adaptation and functional depletion of Ca2+ in the sarcoplasmic reticulum (SR) at cytosolic and luminal Ca2+ regulatory sites, respectively. To explore the importance of cytosolic versus luminal Ca2+ regulatory mechanisms, we assessed the impact of intra-SR Ca2+ buffering on global and local Ca2+ release properties of patch-clamped or permeabilized rat ventricular myocytes. Exogenous, low-affinity Ca2+ buffers (5 to 20 mmol/L ADA, citrate or maleate) were introduced into the SR by exposing the cells to "internal" solutions containing the buffers. Enhanced Ca2+ buffering in the SR was confirmed by an increase in the total SR Ca2+ content, as revealed by application of caffeine. At the whole-cell level, intra-SR [Ca2+] buffering dramatically increased the magnitude of Ca2+ transients induced by ICa and deranged the smoothly graded ICa-SR Ca2+ release relationship. The amplitude and time-to-peak of local Ca2+ release events, Ca2+ sparks, as well as the duration of local Ca2+ release fluxes underlying sparks were increased up to 2- to 3-fold. The exogenous Ca2+ buffers in the SR also reduced the frequency of repetitive activity observed at individual release sites in the presence of the RyR activator Imperatoxin A. We conclude that regulation of RyR openings by local intra-SR [Ca2+] is responsible for termination of CICR and for the subsequent restitution behavior of Ca2+ release sites in cardiac muscle.
Key words: sarcoplasmic reticulum • excitation-contraction coupling • calcium-induced calcium release • ryanodine receptor
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|
|
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|
|
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|
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|
|
|
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|
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|
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|
|
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|
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|
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|
|
|
|
|
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|
|
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|
|
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|
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|
|
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|
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|
|
|
|
|
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|
|
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