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Concerted vs. sequential. Two activation patterns of vast arrays of intracellular Ca2+ channels in muscle.

Zhou J, Brum G, González A, Launikonis BS, Stern MD, Ríos E - J. Gen. Physiol. (2005)

Bottom Line: When sulfate was combined with a reduced cytosolic [Ca(2+)] (50 nM) these sparks coexisted (and interfered) with a sequential progression of channel opening, probably mediated by Ca(2+)-induced Ca(2+) release (CICR).Sequential propagation, observed only in frogs, may require parajunctional channels, of RyR isoform beta, which are absent in the rat.Concerted opening instead appears to be a property of RyR alpha in the amphibian and the homologous isoform 1 in the mammal.

View Article: PubMed Central - PubMed

Affiliation: Section of Cellular Signaling, Rush University, Chicago, IL 60612, USA.

ABSTRACT
To signal cell responses, Ca(2+) is released from storage through intracellular Ca(2+) channels. Unlike most plasmalemmal channels, these are clustered in quasi-crystalline arrays, which should endow them with unique properties. Two distinct patterns of local activation of Ca(2+) release were revealed in images of Ca(2+) sparks in permeabilized cells of amphibian muscle. In the presence of sulfate, an anion that enters the SR and precipitates Ca(2+), sparks became wider than in the conventional, glutamate-based solution. Some of these were "protoplatykurtic" (had a flat top from early on), suggesting an extensive array of channels that activate simultaneously. Under these conditions the rate of production of signal mass was roughly constant during the rise time of the spark and could be as high as 5 microm(3) ms(-1), consistent with a release current >50 pA since the beginning of the event. This pattern, called "concerted activation," was observed also in rat muscle fibers. When sulfate was combined with a reduced cytosolic [Ca(2+)] (50 nM) these sparks coexisted (and interfered) with a sequential progression of channel opening, probably mediated by Ca(2+)-induced Ca(2+) release (CICR). Sequential propagation, observed only in frogs, may require parajunctional channels, of RyR isoform beta, which are absent in the rat. Concerted opening instead appears to be a property of RyR alpha in the amphibian and the homologous isoform 1 in the mammal.

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Sparks at high temporal resolution. Line scans transversal to fiber axis, obtained with the video-rate confocal system. Traces plot ΔF/F0 averaged at three central pixels. (A and B) Frog cells in glutamate. (C and D) Frog cells in sulfate. (F) Rat cells in sulfate. (E and G) Evolution of variables, calculated for sparks in D and F, respectively. Blue, ΔF/F0 (full scale is 2 and 2.4 in E and G); green, signal mass M(t); red,  Ṁ(t); black, Ṁ (t) in simulation with source of 75 pA, open for 3 ms. Identifiers: A, 091302a4; B, 112902a76; C–E, 032802a3, 2; F and G, 032002a24 and 032002d17.
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fig2: Sparks at high temporal resolution. Line scans transversal to fiber axis, obtained with the video-rate confocal system. Traces plot ΔF/F0 averaged at three central pixels. (A and B) Frog cells in glutamate. (C and D) Frog cells in sulfate. (F) Rat cells in sulfate. (E and G) Evolution of variables, calculated for sparks in D and F, respectively. Blue, ΔF/F0 (full scale is 2 and 2.4 in E and G); green, signal mass M(t); red, Ṁ(t); black, Ṁ (t) in simulation with source of 75 pA, open for 3 ms. Identifiers: A, 091302a4; B, 112902a76; C–E, 032802a3, 2; F and G, 032002a24 and 032002d17.

Mentions: Signal mass of events was calculated as a function of time t by the approximation M ≈ 1.206 × ΔF/F0 (t, x = 0) × FWHM(t)3 (Chandler et al., 2003). x = 0 is the spatial location of the spark's peak. FWHM(t) is 2(2 ln2)0.5 σ, where σ is the standard deviation of a Gaussian fitted to the spatial profile ΔF/F0 (t, x) at each t. The assumption needed, Gaussian profiles with spherical symmetry, will not apply in general. Arguments and conclusions that depend on these estimates, however, should remain valid in spite of large errors. Signal mass production rate, Ṁ(t), was calculated numerically from M. For Fig. 2, Ṁ(t) was calculated similarly for a spark simulated as described by Csernoch et al. (2004) with a current of 75 pA, lasting 4 ms, originating at a cylindric source of 1.0 μm length and 0.1 μm radius, with axis on the scanning line. Resting [Ca2+] was 50 nM. Other parameters values are listed in table 1 of the same reference. Images shown are digitally filtered at corner frequencies equal to 0.33 of the Nyquist frequencies.


Concerted vs. sequential. Two activation patterns of vast arrays of intracellular Ca2+ channels in muscle.

Zhou J, Brum G, González A, Launikonis BS, Stern MD, Ríos E - J. Gen. Physiol. (2005)

Sparks at high temporal resolution. Line scans transversal to fiber axis, obtained with the video-rate confocal system. Traces plot ΔF/F0 averaged at three central pixels. (A and B) Frog cells in glutamate. (C and D) Frog cells in sulfate. (F) Rat cells in sulfate. (E and G) Evolution of variables, calculated for sparks in D and F, respectively. Blue, ΔF/F0 (full scale is 2 and 2.4 in E and G); green, signal mass M(t); red,  Ṁ(t); black, Ṁ (t) in simulation with source of 75 pA, open for 3 ms. Identifiers: A, 091302a4; B, 112902a76; C–E, 032802a3, 2; F and G, 032002a24 and 032002d17.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2266625&req=5

fig2: Sparks at high temporal resolution. Line scans transversal to fiber axis, obtained with the video-rate confocal system. Traces plot ΔF/F0 averaged at three central pixels. (A and B) Frog cells in glutamate. (C and D) Frog cells in sulfate. (F) Rat cells in sulfate. (E and G) Evolution of variables, calculated for sparks in D and F, respectively. Blue, ΔF/F0 (full scale is 2 and 2.4 in E and G); green, signal mass M(t); red, Ṁ(t); black, Ṁ (t) in simulation with source of 75 pA, open for 3 ms. Identifiers: A, 091302a4; B, 112902a76; C–E, 032802a3, 2; F and G, 032002a24 and 032002d17.
Mentions: Signal mass of events was calculated as a function of time t by the approximation M ≈ 1.206 × ΔF/F0 (t, x = 0) × FWHM(t)3 (Chandler et al., 2003). x = 0 is the spatial location of the spark's peak. FWHM(t) is 2(2 ln2)0.5 σ, where σ is the standard deviation of a Gaussian fitted to the spatial profile ΔF/F0 (t, x) at each t. The assumption needed, Gaussian profiles with spherical symmetry, will not apply in general. Arguments and conclusions that depend on these estimates, however, should remain valid in spite of large errors. Signal mass production rate, Ṁ(t), was calculated numerically from M. For Fig. 2, Ṁ(t) was calculated similarly for a spark simulated as described by Csernoch et al. (2004) with a current of 75 pA, lasting 4 ms, originating at a cylindric source of 1.0 μm length and 0.1 μm radius, with axis on the scanning line. Resting [Ca2+] was 50 nM. Other parameters values are listed in table 1 of the same reference. Images shown are digitally filtered at corner frequencies equal to 0.33 of the Nyquist frequencies.

Bottom Line: When sulfate was combined with a reduced cytosolic [Ca(2+)] (50 nM) these sparks coexisted (and interfered) with a sequential progression of channel opening, probably mediated by Ca(2+)-induced Ca(2+) release (CICR).Sequential propagation, observed only in frogs, may require parajunctional channels, of RyR isoform beta, which are absent in the rat.Concerted opening instead appears to be a property of RyR alpha in the amphibian and the homologous isoform 1 in the mammal.

View Article: PubMed Central - PubMed

Affiliation: Section of Cellular Signaling, Rush University, Chicago, IL 60612, USA.

ABSTRACT
To signal cell responses, Ca(2+) is released from storage through intracellular Ca(2+) channels. Unlike most plasmalemmal channels, these are clustered in quasi-crystalline arrays, which should endow them with unique properties. Two distinct patterns of local activation of Ca(2+) release were revealed in images of Ca(2+) sparks in permeabilized cells of amphibian muscle. In the presence of sulfate, an anion that enters the SR and precipitates Ca(2+), sparks became wider than in the conventional, glutamate-based solution. Some of these were "protoplatykurtic" (had a flat top from early on), suggesting an extensive array of channels that activate simultaneously. Under these conditions the rate of production of signal mass was roughly constant during the rise time of the spark and could be as high as 5 microm(3) ms(-1), consistent with a release current >50 pA since the beginning of the event. This pattern, called "concerted activation," was observed also in rat muscle fibers. When sulfate was combined with a reduced cytosolic [Ca(2+)] (50 nM) these sparks coexisted (and interfered) with a sequential progression of channel opening, probably mediated by Ca(2+)-induced Ca(2+) release (CICR). Sequential propagation, observed only in frogs, may require parajunctional channels, of RyR isoform beta, which are absent in the rat. Concerted opening instead appears to be a property of RyR alpha in the amphibian and the homologous isoform 1 in the mammal.

Show MeSH
Related in: MedlinePlus