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Direct measurement of SR release flux by tracking ‘Ca2+ spikes’ in rat cardiac myocytes
Journal article   Open access   Peer reviewed

Direct measurement of SR release flux by tracking ‘Ca2+ spikes’ in rat cardiac myocytes

Long-Sheng Song, James S K Sham, Michael D Stern, Edward G Lakatta and Heping Cheng
The Journal of physiology, Vol.512(Pt 3), pp.677-691
11/01/1998
DOI: 10.1111/j.1469-7793.1998.677bd.x
PMCID: PMC2231234
PMID: 9769413
url
https://doi.org/10.1111/j.1469-7793.1998.677bd.xView
Published (Version of record) Open Access

Abstract

Ca 2+ release flux across the sarcoplasmic reticulum (SR) during cardiac excitation-contraction coupling was investigated using a novel fluorescence method. Under whole-cell voltage-clamp conditions, rat ventricular myocytes were dialysed with a high concentration of EGTA (4.0 m m , 150 n m free Ca 2+ ), to minimize the residence time of released Ca 2+ in the cytoplasm, and a low-affinity, fast Ca 2+ indicator, Oregon Green 488 BAPTA-5N (OG-5N; 1.0 m m , K d ≈ 31 μ m ), to optimize the detection of localized high [Ca 2+ ] in release site microdomains. Confocal microscopy was employed to resolve intracellular [Ca 2+ ] at high spatial and temporal resolution. Analytical and numerical analyses indicated that, under conditions of high EGTA concentration, the free [Ca 2+ ] change is the sum of two terms: one major term proportional to the SR release flux/Ca 2+ influx, and the other reflecting the running integral of the released Ca 2+ . Indeed, the OG-5N transients in EGTA-containing cells consisted of a prominent spike followed by a small pedestal. The OG-5N spike closely resembled the first derivative (d[Ca 2+ ]/d t ) of the conventional Ca 2+ transient (with no EGTA), and mimicked the model-derived SR Ca 2+ release function reported previously. In SR Ca 2+ -depleted cells, the OG-5N transient also closely followed the waveform of L-type Ca 2+ current ( I Ca ). Using I Ca as a known source of Ca 2+ influx, SR flux can be calibrated in vivo by a linear extrapolation of the I Ca -elicited OG-5N signal. The OG-5N image signal was localized to discrete release sites at the Z-line level of sarcomeres, indicating that the local OG-5N spike arises from ‘Ca 2+ spikes’ at transverse (T) tubule-SR junctions (due to the imbalance between calcium ions entering the cytosol and the buffer molecules). Both peak SR release flux and total amount of released Ca 2+ exhibited a bell-shaped voltage dependence. The temporal pattern of SR release also varied with membrane voltage: Ca 2+ release was most synchronized and produced maximal peak release flux (4.2 m m s −1 ) at 0 mV; in contrast, maximal total release occurred at −20 mV (71 versus 61 μ m at 0 mV), but the localized release signals were partially asynchronous. Since the maximal conventional [Ca 2+ ] transient and contraction were elicited at 0 mV, it appears that not only the amount of Ca 2+ released, but also the synchronization among release sites affects the whole-cell Ca 2+ transient and the Ca 2+ -myofilament interaction.
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