Rapid filtration studies of the effect of cytosolic Ca2+ on inositol 1,4,5-trisphosphate-induced 45Ca2+ release from cerebellar microsomes

Combettes, Laurent; Hannaert-Merah, Zalika; Coquil, Jean-François; Rousseau, Caroline; Claret, M; Swillens, Stéphane; Champeil, Philippe

doi:10.1016/s0021-9258(17)32478-x

Cited by 45 publications

(7 citation statements)

References 88 publications

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“…The delayed inactivation of IP 3 receptors by the increase in cytosolic [Ca 2+ ] that inevitably follows opening of the intrinsic Ca 2+ channel (Figure 7b) has been observed in many experimental settings [5][6][7]11,23,36,37]. Such feedback inhibition undoubtedly influences the kinetics of Ca 2+ release in intact cells [11,37] and has been proposed to contribute both to quantal Ca 2+ release [31,36] and to 516 Current Biology, Vol 7 No 7 The proposed sequence of events leading to IP 3 receptor activation is shown for only a single subunit of the tetrameric IP 3 receptor. Binding of IP 3 rapidly changes the conformation of the receptor exposing a Ca 2+ -binding site.…”

Section: Coincidence Detection Provides a Further Defence From Noisementioning

confidence: 86%

“…Previous analyses of IP 3 -evoked Ca 2+ release from broken cells [5,23,31] and reconstituted receptors [3] have either lacked the temporal resolution to detect an absolute latency or the latencies observed (20-65 msec) have been impossible to resolve from delays attributable to diffusion barriers or to the properties of fluorescent indicators [8,16,32]. Our methods circumvent both of these limitations and demonstrate that, with Ca 2+ buffered at a level comparable to that found in the cytosol of unstimulated hepatocytes (200 nM), there is a delay of ~30 msec between IP 3 binding to its receptor and the opening of the intrinsic Ca 2+ channel of the receptor.…”

Section: Slow Opening Of Ip 3 Receptors Contrasts With Rapid Gating Of Plasma Membrane Ion Channelsmentioning

confidence: 99%

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Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca2+ safeguards against spontaneous activity

1997

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We propose that the closed conformation of the IP3 receptor is very stable and therefore minimally susceptible to spontaneous activation; at least three (probably four) IP3 molecules may be required to provide enough binding energy to drive the receptor into a stable open conformation. We suggest that a further defence from noise is provided by an extreme form of coincidence detection. Binding of IP3 to each of its four receptor subunits unmasks a site to which Ca2+ must bind before the channel can open. As IP3 binding may also initiate receptor inactivation, there may be only a narrow temporal window during which each receptor subunit must bind both of its agonists if the channel is to open rather than inactivate.

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Section: Coincidence Detection Provides a Further Defence From Noisementioning

confidence: 86%

Section: Slow Opening Of Ip 3 Receptors Contrasts With Rapid Gating Of Plasma Membrane Ion Channelsmentioning

confidence: 99%

Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca2+ safeguards against spontaneous activity

1997

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“…The simplest explanation would be repeated activation of receptors recovering from Ca 2ϩ inactivation, an effect that would be prolonged by the higher concentrations. Alternatively, a weaker inhibitory effect of elevated free Ca 2ϩ at higher InsP 3 concentrations (Combettes et al, 1994) or a reduced rate of Ca 2ϩ pumping into stores or out of the cell may account for the prolonged responses in double flash experiments.…”

Section: Prolongation Of [Ca 2ϩ ] I Increase By High Insp 3 Concentrationmentioning

confidence: 99%

Regulation of Ca2+ Release by InsP3 in Single Guinea Pig Hepatocytes and Rat Purkinje Neurons

Ogden¹,

Capiod²

1997

The Journal of General Physiology

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The repetitive spiking of free cytosolic [Ca2+] ([Ca2+]i) during hormonal activation of hepatocytes depends on the activation and subsequent inactivation of InsP3-evoked Ca2+ release. The kinetics of both processes were studied with flash photolytic release of InsP3 and time resolved measurements of [Ca2+]i in single cells. InsP3 evoked Ca2+ flux into the cytosol was measured as d[Ca2+]i/dt, and the kinetics of Ca2+ release compared between hepatocytes and cerebellar Purkinje neurons. In hepatocytes release occurs at InsP3 concentrations greater than 0.1–0.2 μM. A comparison with photolytic release of metabolically stable 5-thio-InsP3 suggests that metabolism of InsP3 is important in determining the minimal concentration needed to produce Ca2+ release. A distinct latency or delay of several hundred milliseconds after release of low InsP3 concentrations decreased to a minimum of 20–30 ms at high concentrations and is reduced to zero by prior increase of [Ca2+]i, suggesting a cooperative action of Ca2+ in InsP3 receptor activation. InsP3-evoked flux and peak [Ca2+]i increased with InsP3 concentration up to 5–10 μM, with large variation from cell to cell at each InsP3 concentration. The duration of InsP3-evoked flux, measured as 10–90% risetime, showed a good reciprocal correlation with d[Ca2+]i/dt and much less cell to cell variation than the dependence of flux on InsP3 concentration, suggesting that the rate of termination of the Ca2+ flux depends on the free Ca2+ flux itself. Comparing this data between hepatocytes and Purkinje neurons shows a similar reciprocal correlation for both, in hepatocytes in the range of low Ca2+ flux, up to 50 μM · s−1 and in Purkinje neurons at high flux up to 1,400 μM · s−1. Experiments in which [Ca2+]i was controlled at resting or elevated levels support a mechanism in which InsP3-evoked Ca2+ flux is inhibited by Ca2+ inactivation of closed receptor/channels due to Ca2+ accumulation local to the release sites. Hepatocytes have a much smaller, more prolonged InsP3-evoked Ca2+ flux than Purkinje neurons. Evidence suggests that these differences in kinetics can be explained by the much lower InsP3 receptor density in hepatocytes than Purkinje neurons, rather than differences in receptor isoform, and, more generally, that high InsP3 receptor density promotes fast rising, rapidly inactivating InsP3-evoked [Ca2+]i transients.

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“…Since platelets express primarily the type 1 isoform of the IP 3 -R (O' Rourke et al, 1995;Quinton and Dean, 1996) and megakaryocytes are the precursors of platelets, our findings may directly reflect properties of the type 1 IP 3 -R. Remember that, as mentioned in the introduction, cerebellar microsomes (Joseph et al, 1989;Combettes et al, 1994;Hannaert-Merah et al, 1995) and permeabilized A7r5 smooth muscle cells (Bootman et al, 1995), which contain primarily the type 1 isoform of the IP 3 -R, exhibit decreased Ca 2ϩ -dependent inhibition at elevated IP 3 concentrations. Moreover, single channel recordings from the cerebellar type 1 IP 3 -R (Kaftan et al, 1997) and a similar receptor found in Xenopus oocytes (Mak et al, 1998) indicate that the open probability remains high in the presence of a saturating level of IP 3 , even if [Ca 2ϩ ] i is raised to high concentrations.…”

Section: Discussionmentioning

confidence: 60%

“…A possible answer might come from in vitro studies, which have shown that the extent of Ca 2 ϩ -dependent inhibition may be regulated by the concentration IP 3 . For example, the inhibition by Ca 2 ϩ of IP 3 -induced Ca 2 ϩ release from cerebellar microsomes (Joseph et al, 1989;Combettes et al, 1994;Hannaert-Merah et al, 1995) and permeabilized A7r5 smooth muscle cells (Bootman et al, 1995) decreases as the IP 3 concentration is elevated. Likewise, a similar effect is seen at the level of the single IP 3 -gated Ca 2 ϩ channel (Kaftan et al, 1997;Mak et al, 1998).…”

mentioning

confidence: 99%

Dual Regulation of Calcium Mobilization by Inositol 1,4,5-Trisphosphate in a Living Cell

Tertyshnikova

Fein

2000

The Journal of General Physiology

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Changes in cytosolic free calcium ([Ca2+]i) often take the form of a sustained response or repetitive oscillations. The frequency and amplitude of [Ca2+]i oscillations are essential for the selective stimulation of gene expression and for enzyme activation. However, the mechanism that determines whether [Ca2+]i oscillates at a particular frequency or becomes a sustained response is poorly understood. We find that [Ca2+]i oscillations in rat megakaryocytes, as in other cells, results from a Ca2+-dependent inhibition of inositol 1,4,5-trisphosphate (IP3)–induced Ca2+ release. Moreover, we find that this inhibition becomes progressively less effective with higher IP3 concentrations. We suggest that disinhibition, by increasing IP3 concentration, of Ca2+-dependent inhibition is a common mechanism for the regulation of [Ca2+]i oscillations in cells containing IP3-sensitive Ca2+ stores.

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Rapid filtration studies of the effect of cytosolic Ca2+ on inositol 1,4,5-trisphosphate-induced 45Ca2+ release from cerebellar microsomes

Cited by 45 publications

References 88 publications

Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca2+ safeguards against spontaneous activity

Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca2+ safeguards against spontaneous activity

Regulation of Ca2+ Release by InsP3 in Single Guinea Pig Hepatocytes and Rat Purkinje Neurons

Dual Regulation of Calcium Mobilization by Inositol 1,4,5-Trisphosphate in a Living Cell

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