Calcium influx and its control by calcium release

doi:10.1016/0959-4388(93)90130-Q

Current Opinion in Neurobiology

Volume 3, Issue 3, June 1993, Pages 368-374

https://doi.org/10.1016/0959-4388(93)90130-Q Get rights and content

Abstract

Changes in the concentration of intracellular Ca²⁺ are crucial for signal transduction in virtually every cell. In the past year, more of the diversity of receptor-mediated Ca²⁺ influx mechanisms has been shown, and it has been disclosed that one of the most effective Ca²⁺ influx pathways, known as ‘capacitative Ca²⁺ entry’, occurs via Ca²⁺-selective ion channels in the plasma membrane that are activated following depletion of intracellular Ca²⁺ stores. Although the exact activation mechanism of capacitative Ca²⁺ entry still remains a mystery, the identification of plasma membrane currents following store depletion and the characterization of their biophysical properties opens the possibility of unraveling the features and molecular components of the phenomenon of capacitative Ca²⁺ entry.

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For this purpose, Ca2+ ATPase helps cells to remove excess Ca2+ into the extracellular matrix. On the other hand, the inward flux of calcium is controlled by the second messenger-operated channels (SMOC), receptor-operated channels (ROC) and voltage operated channels (VOC) (Penner et al., 1993). Magnesium is another divalent cation of importance.
Skin constitutes a barrier protecting the organism against physical and chemical factors. Therefore, it is constantly exposed to the xenobiotics, including inorganic ions that are ubiquitous in the environment. Some of them play important roles in homeostasis and regulatory functions of the body, also in the skin, while others can be considered dangerous. Many authors have shown that inorganic ions could penetrate inside the skin and possibly induce local effects. In this review, we give an account of the current knowledge on the effects of skin exposure to inorganic ions. Beneficial effects on skin conditions related to the use of thermal spring waters are discussed together with the application of aluminium in underarm hygiene products and silver salts in treatment of difficult wounds. Finally, the potential consequences of dermal exposure to topical sensitizers and harmful heavy ions including radionuclides are discussed.
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ICRAC has several key electrophysiological characteristics that preclude confusion with other types of ionic currents. Its current-voltage (I/V) curve displays a strong inward rectification, with a reversal potential (Erev) > +60 mV reflecting the high Ca2+ selectivity [5,6]. The current is efficiently blocked by trivalent cations like Gd3+ or La3+.
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Familial Alzheimer's disease-linked presenilin mutants and intracellular Ca <sup>2+</sup> handling: A single-organelle, FRET-based analysis
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The maximal rate of [Ca2+]c increase was also calculated and was clearly decreased in PSs-expressing cells (Fig. 7C and Table S6). Alterations in PM potential can affect the rate and extent of SOCE, by altering the driving force for Ca2+ entry [39]. To exclude the possibility that PSs expression could affect PM potential, a set of experiments has been performed using a protocol similar to that described above, except that cells were perfused with a medium in which NaCl was iso-osmotically substituted by KCl (K+-based medium; see Materials and Methods).
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To fulfil the need of a direct investigation of intracellular stores Ca²⁺ dynamics, we here present a detailed and quantitative single-cell analysis of FAD-PSs effects on organelle Ca²⁺ handling using specifically targeted, FRET (Fluorescence/Förster Resonance Energy Transfer)-based Ca²⁺ indicators. In SH-SY5Y human neuroblastoma cells and in patient-derived fibroblasts expressing different FAD-PSs mutations, we directly measured Ca²⁺ concentration within the main intracellular Ca²⁺ stores, e.g., Endoplasmic Reticulum (ER) and Golgi Apparatus (GA) medial- and trans-compartment. We unambiguously demonstrate that the expression of FAD-PS2 mutants, but not FAD-PS1, in either SH-SY5Y cells or FAD patient-derived fibroblasts, is able to alter Ca²⁺ handling of ER and medial-GA, but not trans-GA, reducing, compared to control cells, the Ca²⁺ content within these organelles by partially blocking SERCA (Sarco/Endoplasmic Reticulum Ca²⁺-ATPase) activity. Moreover, by using a cytosolic Ca²⁺ probe, we show that the expression of both FAD-PS1 and -PS2 reduces the Ca²⁺ influx activated by stores depletion (Store-Operated Ca²⁺ Entry; SOCE), by decreasing the expression levels of one of the key molecules, STIM1 (STromal Interaction Molecule 1), controlling this pathway.
Our data indicate that FAD-linked PSs mutants differentially modulate the Ca²⁺ content of intracellular stores yet leading to a complex dysregulation of Ca²⁺ homeostasis, which represents a common disease phenotype of AD.
Molecular regulation of MCU: Implications in physiology and disease
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Ca²⁺ flux across the inner mitochondrial membrane (IMM) regulates cellular bioenergetics, intra-cellular cytoplasmic Ca²⁺ signals, and various cell death pathways. Ca²⁺ entry into the mitochondria occurs due to the highly negative membrane potential (ΔΨ_m) through a selective inward rectifying MCU channel. In addition to being regulated by various mitochondrial matrix resident proteins such as MICUs, MCUb, MCUR1 and EMRE, the channel is transcriptionally regulated by upstream Ca²⁺ cascade, post transnational modification and by divalent cations. The mode of regulation either inhibits or enhances MCU channel activity and thus regulates mitochondrial metabolism and cell fate.
Neuroprotective effect of weak static magnetic fields in primary neuronal cultures
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Citation Excerpt :
Rosen (1993b, 2003) has previously suggested that SMFs may directly affect PM proteins, such as calcium channels, thereby increasing their ion permeability. In addition to a voltage-gated Ca2+ entry through transmembrane Ca2+ channels in response to depolarization, or to Ca2+ entry via receptor-operated channels (e.g., NMDA), Ca2+ may also enter excitable cells via SOCs (Penner et al., 1993; Putney, 2001; Uehara et al., 2002). These channels are activated as a result of intracellular Ca2+ mobilization, such as ER Ca2+ depletion by ThG, that induces a subsequent Ca2+ entry termed capacitative Ca2+ influx (Putney, 2003), aimed at replenishing ER Ca2+ stores (Emptage et al., 2001; Parekh and Putney, 2005).
Low intensity static magnetic fields (SMFs) interact with various biological tissues including the CNS, thereby affecting key biological processes such as gene expression, cell proliferation and differentiation, as well as apoptosis. Previous studies describing the effect of SMFs on apoptotic cell death in several non-neuronal cell lines, emphasize the importance of such a potential modulation in the case of neurodegenerative disorders, where apoptosis constitutes a major route via which neurons degenerate and die.
In this study, we examine the effect of SMFs on neuronal survival in primary cortical and hippocampal neurons that constitute a suitable experimental system for modeling the neurodegenerative state in vitro. We show that weak SMF exposure interferes with the apoptotic programing in rat primary cortical and hippocampal neurons, thereby providing protection against etoposide-induced apoptosis in a dose- and time-dependent manner. Primary cortical neurons exposed to SMF (50 G) for 7 days exhibited a 57.1 ± 6.3% decrease in the percentage of cells undergoing apoptosis induced by etoposide (12 μM), accompanied by a marked decrease in the expression of the pro-apoptotic markers: cleaved poly ADP ribose polymerase-1, cleaved caspase-3, active caspase-9 and the phospho-histone H2A variant (Ser139) by 41.0 ± 5.0%, 81.2 ± 5.0%, 72.9 ± 6.4%, 42.75 ± 2.9%, respectively, and by a 57.2 ± 1.0% decrease in the extent of mitochondrial membrane potential collapse. Using the L-type voltage-gated Ca²⁺ channel inhibitor nifedipine, which is selective to Ca²⁺ influx through Ca_v1.2, we found that the anti-apoptotic effect of SMFs was mediated by Ca²⁺ influx through these channels. Our findings demonstrating altered Ca²⁺-influx in response to thapsigargin stimulation in SMF-exposed cortical neurons, along with enhanced inhibition of KCl-induced Ca²⁺-influx through Ca_v1.2 channels and enhanced expression of Ca_v1.2 and Ca_v1.3 channels, allude to the involvement of voltage- and store-operated Ca²⁺ channels in various aspects of the protective effect exerted by SMFs. These findings show the potential susceptibility of the CNS to weak SMF exposure and have implications for the design of novel strategies for the treatment and/or prevention of neurodegenerative diseases.
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Movements of Cl− and K+ therefore maintain a hyperpolarised mast cell membrane, modulate Ca2+ influx, and further enhance mast cell degranulation [33]. There are two phases of [Ca2+]i elevation during mast cell activation following cross-linking of FcεRI: an initial phase, which is due to inositol 1,4,5-triphosphate-dependent release of [Ca2+]i from the internal Ca2+ store; and a sustained phase, which is due to the influx of Ca2+ via the activated CRAC [5,30,34,35]. Based on the [Ca2+]i measurements obtained, a reduction in the sustained [Ca2+]i levels, which represent the influx of Ca2+, in Cl−-depleted buffers during antigen-stimulated peritoneal mast cell activation (Fig. 4) suggests that extracellular Cl− ions play a crucial role in modulating the extent of Ca2+ influx.
The microelectrode array (MEA) was used to investigate the pharmacological relevance of chloride (Cl⁻) ions in antigen-dependent mast cell activation and the inhibitory effect of disodium cromoglycate (DSCG) on mast cell activation.
The movements of ions across the cellular membrane and the potential relationship between Cl⁻ channels and DSCG during immunological activation were investigated using the MEA. The results were then subsequently compared with the amount of histamine released from anti-IgE activated peritoneal mast cells.
The inclusion of charybdotoxin (ChTX) in Cl⁻-free buffer showed that the measured field potentials during antigen-stimulated peritoneal mast cell were a combination of Cl⁻ influx and K⁺ efflux. The delayed onset time of Cl⁻ influx indicated the presence of a delayed outwardly-rectifying Cl⁻ current in the antigen-stimulated peritoneal mast cells. The use of 5-nitro-2-(3-phenylpropylamino) benzoic acid demonstrated that the activated mast cell membrane potential can be stabilised, thereby reducing the amount of histamine released from the anti-IgE activated mast cells. The correlation between the results of the histamine release assay and the electrophysiological measurements demonstrated the importance of Cl⁻ to anti-IgE dependent mast cell activation. The inhibitory effect of DSCG on anti-IgE activated cells, however, did not correlate with the presumed influx of Cl⁻.
The MEA data suggest that Cl⁻ influx is crucial to IgE-dependent mast cell degranulation.
While the MEA cannot yield information about single channel properties, it is convenient to use and can provide information on the global changes in electrophysiological responses of non-excitable cells.

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Calcium influx and its control by calcium release

Abstract

Cell Calcium

Eur J Biochem

Physiol Rev

Nature

Nature

Cell Calcium

FASEB J

Neuron

Neuron

Neuron

Biocbem J

Biochem J

Endocrinology

Nature

Inositol Trisphosphate and Calcium Signalling

Nature

Calcium Channels, Stores, and Oscillations

Annu Rev Cell Biol

Exchange Characteristics of the Noradrenaline-Sensitive Calcium Store in Vascular Smooth Muscle Cells of Rabbit Ear Artery

J Physiol (Loud)

A Model for Receptor-Regulated Calcium Entry

Cell Calcium

‘Quantal’ Ca2+ Release and the Control of Cat + Entry by Inositol Phosphates — a Possible Mechanism

FEBS Lett

Functional Expression of the Calcium Release Channel from Skeletal Muscle Ryanodine Receptor cDNA

FEBS Lett

Calcium and Inositol 1,4,5Trisphosphate Receptors: a Complex Relationship

Trends Biocbem Sci

InsP3 and Ins(1,3,4,5)P4 Act in Synergy to Stimulate Influx of Extracellular Ca2+ in Xenopus Oocytes

Am J Physiol

Ins(1,3,4,5)P4 Promotes Sustained Activation of the Ca2+-Dependent Cl- Current in Isolated Mouse Lacrimal Cells

Biocbem J

Inositol Phosphates and Ca2+ Entry: Toward a Proliferation or Simplification?

FASEB J

Activation of Cat+ Entry into Acinar Cells by a Non-Phosphorylatable Inositol Trisphosphate

Nature

How do Inositol Phosphates Regulate Calcium Signaling?

FASEB J

‘Quantal’ Ca²⁺ Release and the Control of Cat + Entry by Inositol Phosphates — a Possible Mechanism

InsP3 and Ins(1,3,4,5)P4 Act in Synergy to Stimulate Influx of Extracellular Ca²⁺ in Xenopus Oocytes

Ins(1,3,4,5)P4 Promotes Sustained Activation of the Ca^2+-Dependent Cl- Current in Isolated Mouse Lacrimal Cells

Inositol Phosphates and Ca²⁺ Entry: Toward a Proliferation or Simplification?