Closure of membrane channels gated by glutamate receptors may be a two-step process

Gration, K.A.F.; Lambert, Jeremy J.; Ramsey, R. L.; Rand, R. P.; Usherwood, P.N.R.

doi:10.1038/295599a0

Cited by 51 publications

(27 citation statements)

References 10 publications

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“…In the present study, we evaluated the distribution of openings in one to five opening bursts, openings at any position of two to five opening bursts, the first to the fourth opening (Gration, Lambert, Ramsey, Rand & Usherwood, 1982). In general, however, the properties of the open states presented in this study are consistent with those predicted by kinetic scheme (3).…”

Section: Discussionsupporting

confidence: 70%

Intraburst kinetic properties of the GABAA receptor main conductance state of mouse spinal cord neurones in culture.

Twyman

Rogers

Macdonald

1990

The Journal of Physiology

110

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5. The open time distribution for all intraburst openings was best fitted by three exponential functions with time constants of 06, 2-9 and 8-9 ms.6. Intraburst open time and total open time distributions for bursts with one to five openings were fitted with two or three exponential functions or gamma distributions, respectively. The number of components, time constants and relative areas were similar for both distributions. R. E. TWYMAN, C. J. ROGERS AND R. L. MACDONALD 9. The total closed time distributions for bursts containing two to four closings, however, were all best fitted with only a single gamma distribution with a time constant of 1-3 ms.10

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Section: Discussionsupporting

confidence: 70%

Intraburst kinetic properties of the GABAA receptor main conductance state of mouse spinal cord neurones in culture.

Twyman

Rogers

Macdonald

1990

The Journal of Physiology

110

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“…First is the stereotyped rise time of sparks. In theory a channel could have a modal distribution of open times under special conditions (9,36,37), but there are exceedingly few experimental examples of such distributions (28).…”

Section: Discussionmentioning

confidence: 99%

Involvement of multiple intracellular release channels in calcium sparks of skeletal muscle

Gonzalez

Kirsch

Shirokova

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

110

100

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In many types of muscle, intracellular Ca 2؉ release for contraction consists of brief Ca 2؉ sparks. Whether these result from the opening of one or many channels in the sarcoplasmic reticulum is not known. Examining massive numbers of sparks from frog skeletal muscle and evaluating their Ca 2؉ release current, we provide evidence that they are generated by multiple channels. A mode is demonstrated in the distribution of spark rise times in the presence of the channel activator caffeine. This finding contradicts expectations for single channels evolving reversibly, but not for channels in a group, which collectively could give rise to a stereotyped spark. The release channel agonists imperatoxin A, ryanodine, and bastadin 10 elicit fluorescence events that start with a spark, then decay to steady levels roughly proportional to the unitary conductances of 35%, 50%, and 100% that the agonists, respectively, promote in bilayer experiments. This correspondence indicates that the steady phase is produced by one open channel. Calculated Ca 2؉ release current decays 10-to 20-fold from spark to steady phase, which requires that six or more channels be open during the spark. (4, 5), and smooth muscle (6). Sparks are fundamental in health and disease (7), but their mechanism, especially whether one or many channels are involved in the spark generator or ''release unit,'' remains unclear (8-10). Answering this question, which pervades the field since its inception (2), will help understand how the channels are coaxed by their agonists (Ca, membrane voltage; reviewed in refs. 11 and 12) and restrained by their antagonists (Ca, Mg) to shape these events.Here we improve a technique for detection of massive numbers of sparks (13) Materials and MethodsExperiments were carried out at 17°C in cut skeletal muscle fibers from Rana pipiens semitendinosus muscle, stretched at 3-3.5 m͞sarcomere, either voltage-clamped in a two-Vaseline gap chamber or permeabilized and immersed in internal solution, on an inverted microscope. Adult frogs anaesthetized in 15% ethanol were killed by pithing. The external solution contained 10 mM Ca(CH 3 SO 3 ) 2 , 130 mM tetraethylammonium-CH 3 SO 3 , 5 mM Tris maleate, 1 mM 3,4 diaminopyridine, and 1 M tetrodotoxin. The internal solution contained 110 mM Cs-glutamate, 1 mM EGTA, 5 mM glucose, 5 mM Mg-ATP, 5 mM phosphocreatine, 10 mM Hepes, 0.2 mM fluo-3, with 100 nM free [Ca 2ϩ ] and 1.8 mM [Mg 2ϩ ]. For permeabilized cells the internal solution contained 0.05 mM fluo-3 and 0.34 mM [Mg 2ϩ ] and included 4% 10-kDa dextran. Solutions were adjusted to pH 7 and 270 mosmol͞kg. The scanning microscope (MRC 1000, Bio-Rad) was in fluo-3 configuration (14) using a 40ϫ, 1.2 numerical aperture water immersion objective (Zeiss). Images shown are of fluorescence determined at 2-ms intervals (4.3 ms in toxin experiments) along a parallel to the fiber axis. Fluorescence F(x,t) is presented normalized to its average F 0 (x) before the voltage pulse. Sparks are located on a spatially filtered version of...

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“…Channel amplitudes were measured for at least 30 individual openings. Kinetic measurements were performed using a modification of the dual threshold crossing algorithm previously described (Gration et al, 1982;Kerry et at., 1986). The modification provided an interactive element whereby the user was able to verify each channel event and to intervene where necessary.…”

Section: Data Reduction and Analysismentioning

confidence: 99%

Characterization of a delayed rectifier K+ channel in NG108-15 neuroblastomaX glioma cells: Gating kinetics and the effects of enrichment of membrane phospholipids with arachidonic acid

1988

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A voltage-sensitive K+ channel with characteristics of the delayed rectifier was studied in NG108-15 cells using the cell-attached patch-clamp technique. The primary conductance of the channel was 18 pS, but occasional openings to a subconductance state were observed. The average latency to first opening of the channel was about 4 msec. Based on about 20,000 channel openings, the open time probability density function (pdf) required at least three exponentials (time constants of about 0.2, 3 and 9 msec) to achieve an adequate fit to the data. The closed time pdf required at least six exponentials to describe the data (time constants ranging from 0.093 to 440 msec). Thus, the channel exists in at least three open and six closed states. The ensemble average describing the inactivation of the channel was well fit by two exponentials with time constants of 170 msec and 4.2 sec. To examine the effect of changes in membrane lipid composition on the properties of the channel, the phospholipids of the cells were enriched with polyunsaturated fatty acids. In patches from 20:4-enriched cells the conductance, mean first latency, and open-time pdf were similar to control cells. However, the open state probability was increased from 0.25 to 0.44 and the mean closed time was decreased from 20 to 9 msec. The closed time pdf exhibited a higher proportion of closing events associated with short time constants, i.e., the probability of the channel closing into a long-lived closed state was decreased. The decay phase of the ensemble average also was changed; the proportion of the curve described by the slower time constant was almost doubled. Thus, the delayed rectifier from NG108-15 cells can exist in at least three open and six closed states, and changes in membrane lipid composition may have subtle effects on the gating kinetics of the channel.

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Closure of membrane channels gated by glutamate receptors may be a two-step process

Cited by 51 publications

References 10 publications

Intraburst kinetic properties of the GABAA receptor main conductance state of mouse spinal cord neurones in culture.

Intraburst kinetic properties of the GABAA receptor main conductance state of mouse spinal cord neurones in culture.

Involvement of multiple intracellular release channels in calcium sparks of skeletal muscle

Characterization of a delayed rectifier K+ channel in NG108-15 neuroblastomaX glioma cells: Gating kinetics and the effects of enrichment of membrane phospholipids with arachidonic acid

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