Separation and characterization of currents through store-operated CRAC channels and Mg2+-inhibited cation (MIC) channels

doi:10.1085/jgp.20028551

. 2002 May;119(5):487-507.

doi: 10.1085/jgp.20028551.

Separation and characterization of currents through store-operated CRAC channels and Mg2+-inhibited cation (MIC) channels

Murali Prakriya¹, Richard S Lewis

Affiliations

PMID: 11981025
PMCID: PMC2233817
DOI: 10.1085/jgp.20028551

Separation and characterization of currents through store-operated CRAC channels and Mg2+-inhibited cation (MIC) channels

Murali Prakriya et al. J Gen Physiol. 2002 May.

. 2002 May;119(5):487-507.

doi: 10.1085/jgp.20028551.

Authors

Murali Prakriya¹, Richard S Lewis

Affiliation

¹ Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA 94305, USA.

PMID: 11981025
PMCID: PMC2233817
DOI: 10.1085/jgp.20028551

Erratum in

J Gen Physiol 2002 Jun;119(6):613

Abstract

Although store-operated calcium release-activated Ca(2+) (CRAC) channels are highly Ca(2+)-selective under physiological ionic conditions, removal of extracellular divalent cations makes them freely permeable to monovalent cations. Several past studies have concluded that under these conditions CRAC channels conduct Na(+) and Cs(+) with a unitary conductance of approximately 40 pS, and that intracellular Mg(2+) modulates their activity and selectivity. These results have important implications for understanding ion permeation through CRAC channels and for screening potential CRAC channel genes. We find that the observed 40-pS channels are not CRAC channels, but are instead Mg(2+)-inhibited cation (MIC) channels that open as Mg(2+) is washed out of the cytosol. MIC channels differ from CRAC channels in several critical respects. Store depletion does not activate MIC channels, nor does store refilling deactivate them. Unlike CRAC channels, MIC channels are not blocked by SKF 96365, are not potentiated by low doses of 2-APB, and are less sensitive to block by high doses of the drug. By applying 8-10 mM intracellular Mg(2+) to inhibit MIC channels, we examined monovalent permeation through CRAC channels in isolation. A rapid switch from 20 mM Ca(2+) to divalent-free extracellular solution evokes Na(+) current through open CRAC channels (Na(+)-I(CRAC)) that is initially eightfold larger than the preceding Ca(2+) current and declines by approximately 80% over 20 s. Unlike MIC channels, CRAC channels are largely impermeable to Cs(+) (P(Cs)/P(Na) = 0.13 vs. 1.2 for MIC). Neither the decline in Na(+)-I(CRAC) nor its low Cs(+) permeability are affected by intracellular Mg(2+) (90 microM to 10 mM). Single openings of monovalent CRAC channels were not detectable in whole-cell recordings, but a unitary conductance of 0.2 pS was estimated from noise analysis. This new information about the selectivity, conductance, and regulation of CRAC channels forces a revision of the biophysical fingerprint of CRAC channels, and reveals intriguing similarities and differences in permeation mechanisms of voltage-gated and store-operated Ca(2+) channels.

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F<sc>igure</sc> 7. — **Figure 7.**
Effects of extracellular divalent cations on MIC current. The cell was treated with 100 μM 2-APB for 15 min before seal formation to irreversibly inhibit I_CRAC. Data are not corrected for leak current. Internal solution: MGF. Extracellular solution was alternated between 20 mM Ca²⁺ and DVF Ringer's as currents were measured in response to voltage ramps from −110 to 90 mV. (A) Parallel activation of inward Na⁺ current at −110 mV (measured in DVF Ringer's) and outward Cs⁺ current at 90 mV (measured in 20 mM Ca²⁺ _o). (B) Ramp currents collected at the times shown by the open symbols in A. The similar activation time courses of the currents in 20 mM Ca²⁺ and DVF conditions (shown in A) suggest that the outwardly rectifying currents in 20 mM Ca²⁺ are due to MIC channels. (C) Removal of extracellular Ca²⁺ (2 mM Mg²⁺ _o) does not alter the inward MIC current.

F<sc>igure</sc> 1. — **Figure 1.**
Activation of monovalent current in a Jurkat cell in the absence of extracellular divalent ions and intracellular Mg²⁺. (A) Time course and selectivity of the current developing in the presence of DVF extracellular solution. The bar indicates sequential changes in the bath solution from 20 mM Ca²⁺ Ringer's to Na⁺-DVF to NMDG-DVF (see materials and methods). Each point represents the mean current during 100-ms steps to −110 mV, after subtraction of the leak current recorded in 20 mM Ca²⁺ immediately after break-in (time = 0). Internal solution: Cs methanesulfonate/10 HEDTA/0 Mg²⁺ (MGF). (B) Current-voltage relationship from the cell in A recorded with Na⁺- or NMDG-based DVF extracellular solution. A 100-ms voltage ramp from −110 to 90 mV was applied. (C) Currents at −110 mV recorded at early times after break-in show progressive activation of single Na⁺-conducting channels. Channels appear to activate sequentially, opening to very high probabilities in an all-or-none fashion. Numbers on the left indicate time after whole-cell break-in; numbers on the right indicate multiples of −3.9 pA. Same experimental protocol as in A, from another cell. (D) Current-voltage relationship of single channels conducting monovalent ions in an inside-out patch. Same voltage protocol as in B. Bath solution: MGF. Pipette solution: Na⁺-DVF. (E) Single-channel currents at different potentials in an excised patch. Same conditions as in D. The closed level is indicated by the dashed lines.

F<sc>igure</sc> 2. — **Figure 2.**
Depletion of Ca²⁺ stores does not activate the large monovalent current. (A) Activation of Ca²⁺ and Na⁺ currents in a Jurkat cell treated with 1 μM TG for 5 min before seal formation. Current at −110 mV (corrected for leak current collected in 0 Ca²⁺ Ringer's) is plotted against time after break-in. As indicated by the bar, the extracellular solution was periodically switched between a 20 mM Ca²⁺ Ringer's and standard DVF solution to measure the Ca²⁺ and Na⁺ currents, respectively. (left graph) The Ca²⁺ current I_CRAC is present at the time of break-in, and at these early times only a small transient Na⁺ current is seen under DVF conditions (arrow). Large currents outside the graph boundaries are omitted for clarity. (Right graph) The same experiment at lower gain shows the slow development of a large Na⁺ current in DVF solution following break-in. Internal solution: MGF. (B) Plot of the peak Ca²⁺ (•) and Na⁺ (○) currents measured during applications of 20 mM Ca²⁺ or DVF solutions, respectively. (C) Monovalent current-voltage relationships recorded under DVF conditions early (41 s; small transient current in A) and late (595 s; large sustained current in A) in the experiment. Note the changes in size, rectification, and reversal potential of the current with time. (D) Current-voltage relations recorded in the presence of 20 mM Ca²⁺ at early (37 s) and late (565 s) times. A large outwardly rectifying current develops with time. In C and D, the currents from the upper graphs are reproduced as dashed lines in the lower graphs for comparison.

F<sc>igure</sc> 3. — **Figure 3.**
I_CRAC and the large monovalent current do not deactivate in parallel. (A) Following store depletion by passive dialysis with 1.2 mM EGTA, exposure to 20 mM Ca²⁺ evokes I_CRAC, which progressively declines due to elevation of intracellular [Ca²⁺]_i and refilling of Ca²⁺ stores. Current at −110 mV (corrected for leak current collected in 0 Ca²⁺ Ringer's) is plotted against time after break-in. Periodic exposure to DVF solution shows the development of the large monovalent current, shown at lower gain in the right graph. Note that I_CRAC depotentiates during the second exposure to DVF (left), even though the Na⁺ current during that same period is fairly constant (right). Internal solution: Cs methanesulfonate/1.2 EGTA/0 Mg²⁺. (B) The Ca²⁺ (•) and Na⁺ currents (○) measured immediately before and during applications of the DVF solution in A. The monovalent current continues to increase as I_CRAC deactivates.

F<sc>igure</sc> 4. — **Figure 4.**
I_CRAC and the large monovalent current exhibit different sensitivities to SKF 96365. All cells were pretreated with 1 μM TG. In B and C, the recordings began after the monovalent current had activated to a steady-state level, as described in Fig. 2. Both currents were measured during steps to −110 mV. (A) Inhibition of I_CRAC by SKF 96365 (20 μM). Inhibition and recovery followed exponential time courses with time constants of 17.5 and 19 s, respectively. Internal solution: Cs methanesulfonate/10 BAPTA/8 Mg²⁺. External: 20 mM Ca²⁺. (B) The large monovalent current is relatively insensitive to 20 μM SKF 96365. Internal solution: MGF. (C) Even after nearly complete inhibition of I_CRAC by SKF 96365 (20 μM), removal of external divalent ions causes the monovalent current to rise rapidly to control levels. Thus, the insensitivity of the monovalent current to SKF 96365 is not explained by a failure to block CRAC channels under DVF conditions. Internal solution: MGF.

F<sc>igure</sc> 5. — **Figure 5.**
I_CRAC and the large monovalent current have differing sensitivities to 2-APB. (A) A low concentration of 2-APB (5 μM) enhances I_CRAC after full store depletion by TG. I_CRAC is shown at −110 mV. Internal solution: Cs methanesulfonate/10 BAPTA/8 Mg²⁺. Holding potential: −40 mV (B) A high concentration of 2-APB (50 μM) initially enhances, then produces nearly complete and irreversible inhibition of I_CRAC. Experimental conditions as described in A. (C) Effects of 2-APB on the large monovalent current. A high concentration (50 μM) inhibits the current partially and reversibly. In contrast, the irreversible inhibition of I_CRAC in the same cell is shown by comparing currents during the first and second applications of Ca²⁺. 5 μM 2-APB fails to enhance the large monovalent current, although it enhances I_CRAC as shown in A. Internal solution: MGF.

F<sc>igure</sc> 6. — **Figure 6.**
The large monovalent current is inhibited by intracellular Mg²⁺ and MgATP. (A) High intracellular [Mg²⁺] prevents activation of the large monovalent current. Mean currents at −110 mV in the presence of DVF Ringer's are shown as a function of time following break-in. Internal solution: Cs methanesulfonate containing either 10 HEDTA/0 Mg²⁺ (○; six cells) or 10 BAPTA/8 mM Mg²⁺ (•; four cells). (B) Dose-response curves for Mg²⁺-dependent inhibition of the inward Na⁺ current (•) recorded at −110 mV in DVF solution and the outward Cs⁺ current (○) at 90 mV in 20 mM Ca²⁺ _o solution. The two extracellular solutions were periodically alternated as described in Fig. 2. Each point represents the mean ± SEM of 5–7 cells. The solid and dotted lines are fits of the equation I = 1/(1 + ([Mg²⁺]/K_1/2)ⁿ) with the following parameter values: K_1/2 = 0.6 mM and n = 2.4 for the inward current in DVF; K_1/2 = 0.66 mM and n = 2.6 for the outward current in 20 mM Ca²⁺ _o. Internal solution: Cs methanesulfonate/10 mM BAPTA containing indicated levels of calculated free Mg²⁺. (C) The large monovalent current is inhibited by intracellular MgATP. Shown are the mean whole-cell current amplitudes 400 s after break-in with internal solutions containing 4–8 mM MgATP (five cells) or 0 Mg²⁺/10 HEDTA (six cells), in experiments like the one shown in A. (D) Reversible inhibition of MIC channels by 100 μM Mg²⁺ _i in excised patches. Channel activity persisted in this inside-out patch after excision into MGF solution. Application of 100 μM Mg²⁺ (free concentration, buffered with 10 mM HEDTA) to the cytoplasmic face resulted in reversible closure of two channels. The average current amplitudes during 250-ms steps to −115 mV are shown, with selected sweeps shown at higher time resolution to the right (dashed line indicates 0 current level). Pipette solution: Na-DVF. (E) 2 mM Mg²⁺ inhibits single-channel monovalent currents irreversibly. Same conditions as in D, except 2 mM Mg²⁺ was applied with 10 mM BAPTA.

F<sc>igure</sc> 8. — **Figure 8.**
Activation and deactivation of Ca²⁺ and Na⁺ currents through CRAC channels. Currents were measured during steps to −110 mV. (A) Activation of I_CRAC and the transient Na⁺ current during passive store depletion with a pipette solution containing 10 mM BAPTA + 8 mM Mg²⁺. Periodic removal of external divalent ions reveals a transient monovalent current that increases in parallel with I_CRAC. (B) The Ca²⁺ current (•) and the peak Na⁺ current (○) measured immediately before and during each application of DVF solution activate with similar kinetics. (C) Deactivation of I_CRAC and the transient monovalent current during intracellular dialysis with 1 mM BAPTA + 8 mM Mg²⁺. As described in Fig. 3 A, I_CRAC deactivates in the presence of low intracellular Ca²⁺ buffering, presumably due to store refilling. (D) The Ca²⁺ current (•) and the peak Na⁺ current (○) decline in parallel in the experiment in C. The similar activation and deactivation kinetics for the Na⁺ and Ca²⁺ currents support the idea that the transient monovalent current represents Na⁺ flux through CRAC channels.

F<sc>igure</sc> 9. — **Figure 9.**
Pharmacological evidence for monovalent currents through CRAC channels. I_CRAC was activated by treatment with 1 μM TG for 5 min before seal formation (in A and B) or by passive depletion with 10 mM intracellular BAPTA (in C), with 10 mM intracellular Mg²⁺ to inhibit I_MIC. (A) SKF 96365 (20 μM) inhibits both I_CRAC and the transient monovalent current (under DVF conditions). Both currents recover following washout of the drug. (B) A low concentration of 2-APB (5 μM) enhances both I_CRAC and the transient monovalent current by severalfold. (C) A high concentration of 2-APB (40 μM) significantly reduces both I_CRAC and the transient monovalent current. The inhibition of both currents persists after washout of the drug.

F<sc>igure</sc> 10. — **Figure 10.**
CRAC channels have a low permeability to Cs⁺. I_CRAC was activated by treatment with 1 μM TG, and measured in response to steps to −110 mV and ramps from −110 to 50 mV. (A) Positive reversal potential of monovalent CRAC current with Cs⁺ and Na⁺ as the primary intracellular and extracellular current carriers, respectively. Three ramp currents collected during the depotentiation of Na⁺-I_CRAC (left graph) converge at ∼50 mV (right). (A and B) Internal solution: Cs methanesulfonate/10 BAPTA/8 Mg²⁺. (B) Extracellular Cs⁺ does not conduct significant inward current through CRAC channels under DVF conditions. When the bath solution is changed to a Cs⁺-based DVF solution, the current at −110 mV drops to ∼15% of its previous value in 20 mM Ca²⁺; in contrast, Na⁺-DVF causes an approximately eightfold increase in the current. Thus, Na⁺ is ∼50-fold more conductive than Cs⁺. (C) Measurement of the CRAC-channel current-voltage relation under DVF conditions in the absence of intracellular Mg²⁺. A low concentration of 2-APB (5 μM) induces an inward current that sums with I_MIC. Ramp currents were averaged before and after 2-APB treatment (bars). Because 2-APB selectively enhances CRAC channel activity (Fig. 5), the difference between the two averaged currents isolates monovalent I_CRAC (right). The net current reverses at ∼40 mV, indicating that the low Cs⁺ permeability of the CRAC channel is independent of intracellular Mg²⁺. Internal solution: MGF.

F<sc>igure</sc> 11. — **Figure 11.**
Intracellular Mg²⁺ is not involved in the depotentiation of CRAC channels following removal of extracellular Ca²⁺. I_CRAC was activated by treatment with 1 μM TG, and currents were measured at a step potential of −110 mV. (A) Depotentiation of Na⁺-I_CRAC occurs even in the presence of low cytoplasmic [Mg²⁺]. The pipette solution contained 8 mM MgATP to inhibit I_MIC and 6 mM Na₂ATP to reduce free [Mg²⁺] to 131 μM (calculated). Ramp currents collected at several times during the decline of Na⁺-I_CRAC are shown at the right. (B) The kinetics of Na⁺-I_CRAC decline are not voltage dependent. Transient Na⁺-I_CRAC was evoked by exposure to DVF solution at a holding potential of 40 or −110 mV, with the same intracellular solutions as in A. The peak amplitude of Na⁺-I_CRAC (measured during steps to −110 mV) is larger at the more negative holding potential, presumably due to the voltage dependence of CDP (see Zweifach and Lewis, 1996). However, the extent and rate of depotentiation are unaffected. (C) The rate of depotentiation is unaffected by the level of [Mg²⁺]_i or membrane potential. Exponential curves were fitted to the depotentiation time course with 8 mM Mg²⁺ _i at 20 mV (seven cells), 90–131 μM Mg²⁺ _i at 20 mV (7 cells), or 131 μM Mg²⁺ at −110 mV holding potential (three cells). (D) Removal of intracellular Mg²⁺ does not affect CDP. After exposure to Ca²⁺-free conditions, readdition of extracellular Ca²⁺ causes I_CRAC to reappear gradually over 10–20 s due to CDP. The extent and time course of CDP were similar in experiments with 8 mM Mg²⁺ _i (left) or 0 Mg²⁺ _i (right). Holding potential, 20 mV.

F<sc>igure</sc> 12. — **Figure 12.**
Fluctuation analysis of the Na⁺ current through CRAC channels. I_CRAC was induced by treatment with 1 μM TG and was recorded at a constant holding potential of −110 mV. All data are from the same experiment. Internal solution: Cs methanesulfonate/10 BAPTA/8 Mg²⁺. (A) Mean value and variance of CRAC current in response to 2-APB (5 μM) and removal of divalent cations. Each point represents the values calculated from a 200-ms segment of current data. (B) Sample 200-ms segments of Na⁺-I_CRAC as it depotentiates in the presence of DVF Ringer's. The zero-current level is indicated by the dashed line. (C) Mean-variance analysis of Na⁺-I_CRAC. The plot shows the mean value and variance of 200-ms current sweeps collected as Na⁺-I_CRAC depotentiated in the presence of DVF Ringer's. The data points are well fit by a line with a slope of −31.2 fA. (D) Mean-variance analysis of Ca⁺-I_CRAC. The plot shows the mean value and variance of 200-ms current sweeps collected as Ca⁺-I_CRAC was enhanced by 2-APB in 20 mM Ca²⁺ Ringer's. The data points are well fit by a line with a slope of −3.9 fA. (E) Spectral analysis of Na⁺-I_CRAC. Spectra were collected and averaged in 0 Ca²⁺ + 2 μM Ni²⁺ (dotted trace, “bkgd”), and near the peak of the transient Na⁺ CRAC current (“peak”) and after Na⁺-I_CRAC reached steady-state (“s-s”). Each trace is the average of 3–20 spectra. There is little power above background levels associated with Na⁺-I_CRAC at frequencies >1 kHz.

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References

1. Almers, W., and E.W. McCleskey. 1984. Non-selective conductance in calcium channels of frog muscle: calcium selectivity in a single-file pore. J. Physiol. 353:585–608. - PMC - PubMed
1. Bakowski, D., and A.B. Parekh. 2002. Monovalent cation permeability and Ca2+ block of the store-operated Ca2+ current ICRAC in rat basophilic leukemia cells. Pflügers Arch. 443:892–902. - PubMed
1. Braun, F.J., L.M. Broad, D.L. Armstrong, and J.W. Putney, Jr. 2001. Stable activation of single Ca2+ release-activated Ca2+ channels in divalent cation-free solutions. J. Biol. Chem. 276:1063–1070. - PubMed
1. Broad, L.M., F.J. Braun, J.P. Lievremont, G.S. Bird, T. Kurosaki, and J.W. Putney, Jr. 2001. Role of the phospholipase C-inositol 1,4,5-trisphosphate pathway in calcium release-activated calcium current and capacitative calcium entry. J. Biol. Chem. 276:15945–15952. - PubMed
1. Christian, E.P., K.T. Spence, J.A. Togo, P.G. Dargis, and E. Warawa. 1996. a. Extracellular site for econazole-mediated block of Ca2+ release-activated Ca2+ current (I crac) in T lymphocytes. Br. J. Pharmacol. 119:647–654. - PMC - PubMed

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[1] Almers, W., and E.W. McCleskey. 1984. Non-selective conductance in calcium channels of frog muscle: calcium selectivity in a single-file pore. J. Physiol. 353:585–608. - PMC - PubMed

[2] Almers, W., and E.W. McCleskey. 1984. Non-selective conductance in calcium channels of frog muscle: calcium selectivity in a single-file pore. J. Physiol. 353:585–608. - PMC - PubMed

[3] Bakowski, D., and A.B. Parekh. 2002. Monovalent cation permeability and Ca2+ block of the store-operated Ca2+ current ICRAC in rat basophilic leukemia cells. Pflügers Arch. 443:892–902. - PubMed

[4] Bakowski, D., and A.B. Parekh. 2002. Monovalent cation permeability and Ca2+ block of the store-operated Ca2+ current ICRAC in rat basophilic leukemia cells. Pflügers Arch. 443:892–902. - PubMed

[5] Braun, F.J., L.M. Broad, D.L. Armstrong, and J.W. Putney, Jr. 2001. Stable activation of single Ca2+ release-activated Ca2+ channels in divalent cation-free solutions. J. Biol. Chem. 276:1063–1070. - PubMed

[6] Braun, F.J., L.M. Broad, D.L. Armstrong, and J.W. Putney, Jr. 2001. Stable activation of single Ca2+ release-activated Ca2+ channels in divalent cation-free solutions. J. Biol. Chem. 276:1063–1070. - PubMed

[7] Broad, L.M., F.J. Braun, J.P. Lievremont, G.S. Bird, T. Kurosaki, and J.W. Putney, Jr. 2001. Role of the phospholipase C-inositol 1,4,5-trisphosphate pathway in calcium release-activated calcium current and capacitative calcium entry. J. Biol. Chem. 276:15945–15952. - PubMed

[8] Broad, L.M., F.J. Braun, J.P. Lievremont, G.S. Bird, T. Kurosaki, and J.W. Putney, Jr. 2001. Role of the phospholipase C-inositol 1,4,5-trisphosphate pathway in calcium release-activated calcium current and capacitative calcium entry. J. Biol. Chem. 276:15945–15952. - PubMed

[9] Christian, E.P., K.T. Spence, J.A. Togo, P.G. Dargis, and E. Warawa. 1996. a. Extracellular site for econazole-mediated block of Ca2+ release-activated Ca2+ current (I crac) in T lymphocytes. Br. J. Pharmacol. 119:647–654. - PMC - PubMed

[10] Christian, E.P., K.T. Spence, J.A. Togo, P.G. Dargis, and E. Warawa. 1996. a. Extracellular site for econazole-mediated block of Ca2+ release-activated Ca2+ current (I crac) in T lymphocytes. Br. J. Pharmacol. 119:647–654. - PMC - PubMed

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Separation and characterization of currents through store-operated CRAC channels and Mg2+-inhibited cation (MIC) channels

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Separation and characterization of currents through store-operated CRAC channels and Mg2+-inhibited cation (MIC) channels

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