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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: This pattern, called "concerted activation," was observed also in rat muscle fibers.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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Protoplatykurtic sparks in frogs and rats. (A) Normalized fluorescence F/F0, in an image of a permeabilized frog fiber immersed in reference solution. Graph, spatial profiles of event in A at times indicated (ms). Kurtosis κ was 3.25, 3.05, and 3.59 at 2, 4, and 6 ms, respectively. (B) F/F0 in a frog fiber in “sulfate” solution. κ was 1.17 and 1.25 at 2 and 4 ms. (C) Spark in a rat fiber in sulfate. κ was 2.16 at 2 ms. Sparks in B and C are therefore protoplatykurtic. Identifiers of cell and image: A, 102901a306; B, 111301a1_2; C, 082702b411.
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fig1: Protoplatykurtic sparks in frogs and rats. (A) Normalized fluorescence F/F0, in an image of a permeabilized frog fiber immersed in reference solution. Graph, spatial profiles of event in A at times indicated (ms). Kurtosis κ was 3.25, 3.05, and 3.59 at 2, 4, and 6 ms, respectively. (B) F/F0 in a frog fiber in “sulfate” solution. κ was 1.17 and 1.25 at 2 and 4 ms. (C) Spark in a rat fiber in sulfate. κ was 2.16 at 2 ms. Sparks in B and C are therefore protoplatykurtic. Identifiers of cell and image: A, 102901a306; B, 111301a1_2; C, 082702b411.

Mentions: Sparks recorded in the frog in glutamate are illustrated in Fig. 1 A. The vast majority were bell shaped, approximately Gaussian. The kurtosis (a measure of peakedness defined in MATERIALS AND METHODS) of the three spatial profiles in Fig. 1 A is between 3.05 and 3.59, hence they are mesokurtic or slightly leptokurtic. By contrast, with sulfate solutions and transversal scanning, a fraction of sparks had flatter tops (examples in Fig. 1 B). Their kurtosis is correspondingly lower, 1.17 and 1.25 for the curves in Fig. 1 B. They are platykurtic. In simulations with a point source of Ca2+ current, sparks are mesokurtic until Ca2+ builds up sufficiently to saturate the dye; then, upon saturation, they become platykurtic (Izu et al., 2001). Panels B and C exemplify instead sparks of flat top right from the scan of first detection (named “protoplatykurtic” or PPK). These suggest the involvement of an extensive source. Fig. 1 C illustrates PPK sparks in rat muscle (which were observed whether sulfate was present or not).


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)

Protoplatykurtic sparks in frogs and rats. (A) Normalized fluorescence F/F0, in an image of a permeabilized frog fiber immersed in reference solution. Graph, spatial profiles of event in A at times indicated (ms). Kurtosis κ was 3.25, 3.05, and 3.59 at 2, 4, and 6 ms, respectively. (B) F/F0 in a frog fiber in “sulfate” solution. κ was 1.17 and 1.25 at 2 and 4 ms. (C) Spark in a rat fiber in sulfate. κ was 2.16 at 2 ms. Sparks in B and C are therefore protoplatykurtic. Identifiers of cell and image: A, 102901a306; B, 111301a1_2; C, 082702b411.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2266625&req=5

fig1: Protoplatykurtic sparks in frogs and rats. (A) Normalized fluorescence F/F0, in an image of a permeabilized frog fiber immersed in reference solution. Graph, spatial profiles of event in A at times indicated (ms). Kurtosis κ was 3.25, 3.05, and 3.59 at 2, 4, and 6 ms, respectively. (B) F/F0 in a frog fiber in “sulfate” solution. κ was 1.17 and 1.25 at 2 and 4 ms. (C) Spark in a rat fiber in sulfate. κ was 2.16 at 2 ms. Sparks in B and C are therefore protoplatykurtic. Identifiers of cell and image: A, 102901a306; B, 111301a1_2; C, 082702b411.
Mentions: Sparks recorded in the frog in glutamate are illustrated in Fig. 1 A. The vast majority were bell shaped, approximately Gaussian. The kurtosis (a measure of peakedness defined in MATERIALS AND METHODS) of the three spatial profiles in Fig. 1 A is between 3.05 and 3.59, hence they are mesokurtic or slightly leptokurtic. By contrast, with sulfate solutions and transversal scanning, a fraction of sparks had flatter tops (examples in Fig. 1 B). Their kurtosis is correspondingly lower, 1.17 and 1.25 for the curves in Fig. 1 B. They are platykurtic. In simulations with a point source of Ca2+ current, sparks are mesokurtic until Ca2+ builds up sufficiently to saturate the dye; then, upon saturation, they become platykurtic (Izu et al., 2001). Panels B and C exemplify instead sparks of flat top right from the scan of first detection (named “protoplatykurtic” or PPK). These suggest the involvement of an extensive source. Fig. 1 C illustrates PPK sparks in rat muscle (which were observed whether sulfate was present or not).

Bottom Line: This pattern, called "concerted activation," was observed also in rat muscle fibers.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