Origin and Mechanisms of Ca2+ Waves in Smooth Muscle as Revealed by Localized Photolysis of Caged Inositol 1,4,5-Trisphosphate

McCarron, John G.; MacMillan, Debbi; Bradley, Karen N.; Chalmers, Susan; Muir, T. C.

doi:10.1074/jbc.m311797200

Cited by 58 publications

(71 citation statements)

References 56 publications

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“…A localized feedback deactivation of IP 3 R produced by an increased [Ca 2+ ] c caused the functional compartmentalization [16]. The deactivation of the IP 3 R was delayed in onset, compared with the time of the rise in [Ca 2+ ] c and persisted (>30 s) even when [Ca 2+ ] c had been restored to resting levels [13,16]. This feedback deactivation ensures the wave's progressive movement in a single direction [16].…”

Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

“…Ca2+waves: Ca 2+ waves are the progressive movement of Ca 2+ through the cell following Ca 2+ release from the internal store. Using localized activation of IP 3 R, the forward movement of the Ca 2+ wave was shown to arise from CICR at the IP 3 R [13,16]. The decline in [Ca 2+ ] c -the back of the wave-occurred not because of depletion of separate stores but from a functional compartmentalization of the store which rendered the site of IP 3 -mediated Ca 2+ release-and only this site-refractory to IP 3 after Ca 2+ release .…”

Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

“…The decline in [Ca 2+ ] c -the back of the wave-occurred not because of depletion of separate stores but from a functional compartmentalization of the store which rendered the site of IP 3 -mediated Ca 2+ release-and only this site-refractory to IP 3 after Ca 2+ release . A localized feedback deactivation of IP 3 R produced by an increased [Ca 2+ ] c caused the functional compartmentalization [16]. The deactivation of the IP 3 R was delayed in onset, compared with the time of the rise in [Ca 2+ ] c and persisted (>30 s) even when [Ca 2+ ] c had been restored to resting levels [13,16].…”

Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

“…However, if Ca 2+ -dependent inactivation terminated release [16,79] [45]. Localized Ca2+responses IP 3 is a rapidly diffusing messenger and IP 3 R are subject to positive feedback CICR on a single luminally-continuous entity, so how do highly-localized Ca 2+ changes occur?…”

Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

“…11.3). For Ca 2+ waves to progress through the cell, sequential activation of IP 3 R [13], by Ca 2+ itself, occur in a repeating positive feedback CICR-like process [15,16], i.e. Ca 2+ release from one IP 3 R activates neighbouring receptors to progress the wave.…”

Section: Fig 111mentioning

confidence: 99%

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Calcium Mobilization via Intracellular Ion Channels, Store Organization and Mitochondria in Smooth Muscle

McCarron

Chalmers

Wilson

et al. 2016

Vascular Ion Channels in Physiology and Disease

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This version is available at https://strathprints.strath.ac.uk/55095/ Strathprints is designed to allow users to access the research output of the University of Strathclyde. Unless otherwise explicitly stated on the manuscript, Copyright © and Moral Rights for the papers on this site are retained by the individual authors and/or other copyright owners. Please check the manuscript for details of any other licences that may have been applied. You may not engage in further distribution of the material for any profitmaking activities or any commercial gain. You may freely distribute both the url (https://strathprints.strath.ac.uk/) and the content of this paper for research or private study, educational, or not-for-profit purposes without prior permission or charge.Any correspondence concerning this service should be sent to the Strathprints administrator: strathprints@strath.ac.ukThe Strathprints institutional repository (https://strathprints.strath.ac.uk) is a digital archive of University of Strathclyde research outputs. It has been developed to disseminate open access research outputs, expose data about those outputs, and enable the management and persistent access to Strathclyde's intellectual output. Abstract In smooth muscle, Ca 2+ release from the internal store into the cytoplasm occurs via inositol trisphosphate (IP 3 R) and ryanodine receptors (RyR). The internal Ca 2+ stores containing IP 3 R and RyR may be arranged as multiple separate compartments with various IP 3 R and RyR arrangements, or there may be a single structure containing both receptors. The existence of multiple stores is proposed to explain several physiological responses which include the progression of Ca 2+ waves, graded Ca 2+ release from the store and various local responses and sensitivities. We suggest that, rather than multiple stores, a single luminally-continuous store exists in which Ca 2+ is in free diffusional equilibrium throughout. Regulation of Ca 2+ release via IP 3 R and RyR by the local Ca 2+ concentration within the stores explains the apparent existence of multiple stores and physiological processes such as graded Ca 2+ release and Ca 2+ waves. Close positioning of IP 3 R on the store with mitochondria or with receptors on the plasma membrane creates 'IP 3 junctions' to generate local responses on the luminally-continuous store.

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Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

Section: Fig 111mentioning

confidence: 99%

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Calcium Mobilization via Intracellular Ion Channels, Store Organization and Mitochondria in Smooth Muscle

McCarron

Chalmers

Wilson

et al. 2016

Vascular Ion Channels in Physiology and Disease

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Subplasma membrane Ca²⁺ signals

et al. 2012

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Ca2+ may selectively activate various processes in part by the cell's ability to localize changes in the concentration of the ion to specific subcellular sites. Interestingly, these Ca2+ signals begin most often at the plasma membrane space so that understanding subplasma membrane signals is central to an appreciation of local signaling. Several experimental procedures have been developed to study Ca2+ signals near the plasma membrane, but probably the most prevalent involve the use of fluorescent Ca2+ indicators and fall into two general approaches. In the first, the Ca2+ indicators themselves are specifically targeted to the subplasma membrane space to measure Ca2+ only there. Alternatively, the indicators are allowed to be dispersed throughout the cytoplasm, but the fluorescence emanating from the Ca2+ signals at the subplasma membrane space is selectively measured using high resolution imaging procedures. Although the targeted indicators offer an immediate appeal because of selectivity and ease of use, their limited dynamic range and slow response to changes in Ca2+ are a shortcoming. Use of targeted indicators is also largely restricted to cultured cells. High resolution imaging applied with rapidly responding small molecule Ca2+ indicators can be used in all cells and offers significant improvements in dynamic range and speed of response of the indicator. The approach is technically difficult, however, and realistic calibration of signals is not possible. In this review, a brief overview of local subplasma membrane Ca2+ signals and methods for their measurement is provided. © 2012 IUBMB IUBMB Life, 64(7): 573–585, 2012

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Agonist‐evoked Ca²⁺ wave progression requires Ca²⁺ and IP₃

McCarron

Chalmers

MacMillan

et al. 2010

Journal Cellular Physiology

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Smooth muscle responds to IP 3 -generating agonists by producing Ca 2+ waves. Here, the mechanism of wave progression has been investigated in voltage-clamped single smooth muscle cells using localized photolysis of caged IP 3 and the caged Ca 2+ buffer diazo-2. Waves, evoked by the IP 3 -generating agonist carbachol (CCh), initiated as a uniform rise in cytoplasmic Ca 2+ concentration ([Ca 2+ ] c ) over a single though substantial length (~30 μm) of the cell. During regenerative propagation, the wave-front was about 1/3 the length (~9 μm) of the initiation site. The wave-front progressed at a relatively constant velocity although amplitude varied through the cell; differences in sensitivity to IP 3 may explain the amplitude changes. Ca 2+ was required for IP 3 -mediated wave progression to occur. Increasing the Ca 2+ buffer capacity in a small (2 μm) region immediately in front of a CCh-evoked Ca 2+ wave halted progression at the site. However, the wave front does not progress by Ca 2+ -dependent positive feedback alone. In support, colliding [Ca 2+ ] c increases from locally-released IP 3 did not annihilate but approximately doubled in amplitude. This result suggests that local IP 3 -evoked [Ca 2+ ] c increases diffused passively. Failure of local increases in IP 3 to evoke waves appears to arise from the restricted nature of the IP 3 increase. When IP 3 was elevated throughout the cell, a localized increase in Ca 2+ now propagated as a wave. Together, these results suggest that waves initiate over a surprisingly large length of the cell and that both IP 3 and Ca 2+ are required for active propagation of the wave front to occur.

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Origin and Mechanisms of Ca2+ Waves in Smooth Muscle as Revealed by Localized Photolysis of Caged Inositol 1,4,5-Trisphosphate

Cited by 58 publications

References 56 publications

Calcium Mobilization via Intracellular Ion Channels, Store Organization and Mitochondria in Smooth Muscle

Calcium Mobilization via Intracellular Ion Channels, Store Organization and Mitochondria in Smooth Muscle

Subplasma membrane Ca²⁺ signals

Agonist‐evoked Ca²⁺ wave progression requires Ca²⁺ and IP₃

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Origin and Mechanisms of Ca2+ Waves in Smooth Muscle as Revealed by Localized Photolysis of Caged Inositol 1,4,5-Trisphosphate

Cited by 58 publications

References 56 publications

Calcium Mobilization via Intracellular Ion Channels, Store Organization and Mitochondria in Smooth Muscle

Calcium Mobilization via Intracellular Ion Channels, Store Organization and Mitochondria in Smooth Muscle

Subplasma membrane Ca2+ signals

Agonist‐evoked Ca2+ wave progression requires Ca2+ and IP3

Contact Info

Product

Resources

About

Subplasma membrane Ca²⁺ signals

Agonist‐evoked Ca²⁺ wave progression requires Ca²⁺ and IP₃