A Capacitative Calcium Current in Cultured Skeletal Muscle Cells Is Mediated by the Calcium-specific Leak Channel and Inhibited by Dihydropyridine Compounds

Hopf, F. Woodward; Reddy, P. Jagan Mohan; Hong, Joe C.; Steinhardt, Richard A.

doi:10.1074/jbc.271.37.22358

Cited by 105 publications

(106 citation statements)

References 73 publications

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“…For skeletal muscle cells there had been some controversy. The evidence that skeletal muscle CCE was mediated by a "leak channel" was based on observations of Mn 2ϩ entry, used as a surrogate of Ca 2ϩ (12). However, we observed that Mn 2ϩ entry is not capacitative (14).…”

Section: Complications Of the Existing Cce Models-mentioning

confidence: 66%

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A Direct Mass-action Mechanism Explains Capacitative Calcium Entry in Jurkat and Skeletal L6 Muscle Cells

Narayanan

Islam

Bartelt

et al. 2003

Journal of Biological Chemistry

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We examined capacitative calcium entry (CCE) in Jurkat and in L6 skeletal muscle cells. We found that extracellular Ca 2؉ can enter the endoplasmic reticulum (ER) of both cell types even in the presence of thapsigargin, which blocks entry into the ER from the cytosol through the CaATPase. Moreover, extracellular Ca 2؉ entry into the ER was evident even when intracellular flow of Ca 2؉ was in the direction of ER to cytosol due to the presence of caffeine. ER Ca 2؉ content was assessed by two separate means. First, we used the Mag-Fura fluorescent dye, which is sensitive only to the relatively high concentrations of Ca 2؉ found in the ER. Second, we transiently expressed an ER-targeted derivative of aequorin, which reports Ca 2؉ by luminescence. In both cases, the Ca 2؉ concentration in the ER increased in response to extracellular Ca 2؉ after the ER had been previously depleted despite blockade by thapsigargin. We found two differences between the Jurkat and L6 cells. L6, but not Jurkat cells, inhibited Ca 2؉ uptake at very high Ca 2؉ concentrations. Second, ryanodine receptor blockers inhibited the appearance of cytosolic Ca 2؉ during CCE if added before Ca 2؉ in both cases, but the L6 cells were much more sensitive to ryanodine. Both of these can be explained by the known difference in ryanodine receptors between these cell types. These findings imply that the origin of cytosolic Ca 2؉ during CCE is the ER. Furthermore, kinetic data demonstrated that Ca 2؉ filled the ER before the cytosol during CCE. Our results suggest a plasma membrane Ca 2؉ channel and an ER Ca 2؉ channel joined in tandem, allowing Ca 2؉ to flow directly from the extracellular space to the ER. This explains CCE; any decrease in ER [Ca 2؉ ] relative to extracellular [Ca 2؉ ] would provide the gradient for refilling the ER through a mass-action mechanism.Ca 2ϩ is a critical regulator for a large number of cells, and it is known that for many, the key signaling event is the release of this ion from the ER 1 (1, 2). After release most of the Ca 2ϩ is re-sequestered to the ER through the CaATPase, although some is lost through the plasma membrane to the cell exterior. Maintaining the ER pool of Ca 2ϩ requires re-entry from outside the cell. Casteels and Droogmans (3) first reported a correlation between depletion of ER [Ca 2ϩ ] and entry of Ca 2ϩ from extracellular sources into the cell. This phenomenon was then extensively studied by Putney (4) and named "store-operated" or capacitative calcium entry (CCE).The mechanism for CCE remains unknown, although two general models have been proposed. One, borrowed from the known association of the skeletal muscle plasma membrane potential sensor (L channel) and ER protein (ryanodine receptor), posits a direct connection in which Ca 2ϩ depletion within the ER is sensed by an ER protein, transmitted by proteinprotein interaction to the plasma membrane protein, which then allows entry of Ca 2ϩ into the cytosol. A second, based on second messenger signaling systems such as that for cyclic AMP, posits a mess...

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Section: Complications Of the Existing Cce Models-mentioning

confidence: 66%

“…We had previously shown that CCE occurs in L6 skeletal muscle cells (11), and others demonstrated subsequently that CCE occurs in skeletal muscle (12,13). In our prior studies of L6 cells, we determined Ca 2ϩ in both cytosol and ER using fluorescent dyes, finding that Ca 2ϩ enters the ER even in the presence of thapsigargin (14).…”

mentioning

confidence: 92%

A Direct Mass-action Mechanism Explains Capacitative Calcium Entry in Jurkat and Skeletal L6 Muscle Cells

Narayanan

Islam

Bartelt

et al. 2003

Journal of Biological Chemistry

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“…Other myotube studies have established a link between mitochondrial depolarization and reduced SOCE (Vandebrouck et al 2006) or sarcolemmal TRPC1 channels anchored to the dystrophin-associated glycoprotein complex via α1-syntrophin with compromised SOCE in dystrophic myotubes where this molecular lattice would be disrupted (Vandebrouck et al 2007). Another early study found a store-dependent capacitive Ca 2+ current in cultured myotubes that was mediated by Ca 2+ -specific leak channels and, interestingly, inhibited by dihydropyridines (Hopf et al 1996).…”

Section: Store-operated Ca 2+ Entry (Soce) In Skeletal Musclementioning

confidence: 99%

“…Another concern in most electrophysiological cellattached patch clamp studies connecting SOCE to plasma membrane Ca 2+ influx is the use of >100 mM Ca 2+ concentrations in the pipettes that vastly increase driving force both in myotubes (Hopf et al 1996) and adult fibers. In this regard, Allard et al (2006) challenged the physiological role of store-operated membrane conductance in adult skeletal muscle by showing no increase in whole cell conductance or single channel activity in single fibers severely depleted by prolonged depolarizing pulses under voltage-clamp conditions, either in the presence or in the absence of CPA or in the presence of 25 mM caffeine (Allard et al 2006).…”

Section: Store-operated Ca 2+ Entry (Soce) In Skeletal Musclementioning

confidence: 99%

“…This has to be kept in mind, as most studies on SOCE detected by Mn 2+ quench did not keep divalent ion concentrations constant (Hopf et al 1996;Boittin et al 2006;Zhao et al 2006). A further artificial condition in the quest for the physiological relevance of SOCE is introduced by severe SR depletion using high-dose caffeine or SERCA pump blockers to chronically deplete the store in Ca 2+ -free external solution with subsequent recordings of force, intracellular Ca 2+ , or Ca 2+ entry (Zhao et al 2006;Boittin et al 2006;Kurebayashi and Ogawa 2001;Cherednichenko et al 2004).…”

Section: Store-operated Ca 2+ Entry (Soce) In Skeletal Musclementioning

confidence: 99%

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New factors contributing to dynamic calcium regulation in the skeletal muscle triad—a crowded place

2009

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Skeletal muscle is a highly organized tissue that has to be optimized for fast signalling events conveying electrical excitation to contractile response. The site of electro-chemico-mechanical coupling is the skeletal muscle triad where two membrane systems, the extracellular ttubules and the intracellular sarcoplasmic reticulum, come into very close contact. Structure fits function here and the signalling proteins DHPR and RyR1 were the first to be discovered to bridge this gap in a conformational coupling arrangement. Since then, however, new proteins and more signalling cascades have been identified just in the last decade, adding more diversity and fine tuning to the regulation of excitation-contraction coupling (ECC) and control over Ca 2+ store content. The concept of Ca 2+ entry into working skeletal muscle has become attractive again with the experimental evidence summarized in this review. Store-operated Ca 2+ entry (SOCE), excitation-coupled Ca 2+ entry (ECCE), action-potential-activated Ca 2+ current (APACC), and retrograde EC-coupling (ECC) are new concepts additional to the conventional orthograde ECC; they have provided fascinating new insights into muscle physiology. In this review, we discuss the discovery of these pathways, their potential roles, and the signalling proteins involved that show that the triad may become a crowded place in time.

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Subcellular concentration of ?-dystroglycan in photoreceptors and glial cells of the chick retina

1997

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Mutations in the dystrophin-glycoprotein complex cause muscle degeneration and dysfunctions in the central nervous system, including an impaired synaptic transmission in the outer plexiform layer (OPL) of the retina. To investigate the basis for this ocular phenotype, we analyzed the distribution of beta-dystroglycan, a central member of the dystrophin-glycoprotein complex, in the chick retina by using the 43DAG/8D5 monoclonal antibody. This antibody reacted specifically with chick beta-dystroglycan, as indicated by its staining of the neuromuscular junction, and its reactivity with a single 43-kilodalton band in Western blots. In the retina, beta-dystroglycan was highly concentrated in the OPL and at the vitreal border of the retina, around the inner limiting membrane. Mechanically isolated and flat-mounted inner limiting membranes were stained by the anti-beta-dystroglycan antibody, and this immunoreactivity could be extracted by detergent, indicating that beta-dystroglycan is associated with membranous structures bound to the basal lamina. Consistently, electron microscopy showed a concentration of beta-dystroglycan in the endfeet of Müller glial cells exclusively in the region of direct contact to the inner limiting membrane. In the OPL, beta-dystroglycan immunoreactivity was concentrated in the distal extensions of rod and cone terminals protruding into the outer plexiform layer. There, beta-dystroglycan codistributed with the alpha1beta subunit of the N-type voltage-gated calcium channel. By contrast to previous reports, we did not detect beta-dystroglycan directly associated with the synaptic regions of conventional or ribbon synapses of the retina. These results show that in the retina beta-dystroglycan is exclusively expressed by photoreceptors and glial cells and that beta-dystroglycan is highly concentrated in subcellular regions of glial cell endfeet and photoreceptor terminals. Moreover, the colocalization of beta-dystroglycan with N-type calcium channels in the outer plexiform layer indicates that both proteins might be part of a macromolecular complex.

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A Capacitative Calcium Current in Cultured Skeletal Muscle Cells Is Mediated by the Calcium-specific Leak Channel and Inhibited by Dihydropyridine Compounds

Cited by 105 publications

References 73 publications

A Direct Mass-action Mechanism Explains Capacitative Calcium Entry in Jurkat and Skeletal L6 Muscle Cells

A Direct Mass-action Mechanism Explains Capacitative Calcium Entry in Jurkat and Skeletal L6 Muscle Cells

New factors contributing to dynamic calcium regulation in the skeletal muscle triad—a crowded place

Subcellular concentration of ?-dystroglycan in photoreceptors and glial cells of the chick retina

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