Functionally Separate Intracellular Ca2+ Stores in Smooth Muscle

Flynn, Elaine R. M.; Bradley, Karen N.; Muir, T. C.; McCarron, John G.

doi:10.1074/jbc.m104308200

Cited by 76 publications

(77 citation statements)

References 68 publications

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“…portal vein, pulmonary artery and taenia caeci), one store may express RyR and IP 3 R and other stores, in the same cell, only IP 3 R [11,35,42]. This conclusion came from the finding that depletion of the IP 3 R-containing store abolished Ca 2+ release via RyR, while depletion of the RyR-containing store did not abolish Ca 2+ release via IP 3 R. In further studies in other cell types (mesenteric artery) and in our own investigations in colonic smooth muscle [43], some stores may express both RyR and IP 3 R while others only RyR [30,43]. In this case, depletion of the RyR-containing store abolished Ca 2+ release via IP 3 R, while depletion of the IP 3 R-containing store did not abolish Ca 2+ release via RyR-a result apparently consistent with there being a store which contained RyR alone.…”

Section: Methods Used To Investigate Stores May Create the Appearancesupporting

confidence: 50%

“…On the other hand, after the store had been apparently depleted of Ca 2+ by IP 3 (at a concentration which produced a maximal response) a substantial response to caffeine persisted (Fig. 11.9c), suggesting there was a store which only contains RyR [30,43]. In yet other experiments, in the same cell type, when the concentration of IP 3 used to deplete the store of Ca 2+ was increased, no Ca 2+ response to caffeine occurred i.e.…”

Section: Methods Used To Investigate Stores May Create the Appearancementioning

confidence: 99%

“…Together, these experiments suggest the store is a luminally-continuous entity in which Ca 2+ can diffuse freely throughout. How then does the appearance of multiple stores [43] occur on a single luminally-continuous store structure?…”

Section: Methods Used To Investigate Stores May Create the Appearancementioning

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 Appearancesupporting

confidence: 50%

Section: Methods Used To Investigate Stores May Create the Appearancementioning

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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“…One store may express RyR and IP 3 R and other stores, in the same cell, only IP 3 R (24 -26). This conclusion followed the finding that depletion of the IP 3 -sensitive store abolished caffeine-evoked Ca 2ϩ release, whereas depletion of the caffeine-sensitive store did not abolish Ca 2ϩ release via IP 3 R. In yet other cell types (mesenteric artery, colonic smooth muscle) one store may express both RyR and IP 3 R, whereas a second, in the same cell, only RyR (27,28).…”

mentioning

confidence: 51%

A Single Luminally Continuous Sarcoplasmic Reticulum with Apparently Separate Ca2+ Stores in Smooth Muscle

McCarron

Olson

2008

Journal of Biological Chemistry

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In smooth muscle, the endoplasmic reticulum (ER) 2 exists as an extensive membrane network of tubules, flattened cisternae, and vesicles (1, 2) to comprise rough (RER, which carries ribosomes) and smooth (SER) reticula. RER predominates around the nucleus and is scattered throughout the cytoplasm and appears to be in luminal continuity with the SER (1, 3, 4). SER is found mainly near the cell surface to run in close apposition to the plasma membrane. In various tissues, changes in ER structure may occur at different developmental stages and when the cells experience prolonged activation (reviewed in Ref. 5). These changes may give the impression of a labile (pleiomorphic) ER network capable of modifications in structure and, consequently, function.The Ca 2ϩ storage element of the ER, the sarcoplasmic reticulum (SR), may be a specialized region of the SER that is endowed with those proteins responsible for the uptake (Ca 2ϩ pumps), storage (calsequestrin), and release ryanodine receptor ((RyR) and inositol 1,4,5-trisphosphate receptor (IP 3 R)) of Ca 2ϩ (4, 6). The SR, by regulating the cytoplasmic Ca 2ϩ concentration ([Ca 2ϩ ] c ), plays a central role in Ca 2ϩ signaling to contribute to activities such as gene expression, growth, contraction, and cell death (reviewed in Refs. 7-10). In determining the qualitative nature of the biological response, the structural arrangement of the SR through the cell may be instrumental in enabling different functions to occur and proceed from various regions of the cell. For example, the SR, as a series of multiple, separate Ca 2ϩ -storage elements, each with their own limited measure of Ca 2ϩ , may explain localized all-or-none responses in restricted regions of the cell, the graded release of Ca 2ϩ from the SR in the "quantal" release process and the various sensitivities to IP 3 measured throughout the cell (11-15). Yet, whether or not the SR exists as multiple separate Ca 2ϩ storage units or as a single luminally continuous entity in which Ca 2ϩ diffuses freely throughout, is unclear.Evidence for the existence of multiple Ca 2ϩ storage units comes from the heterogeneity of the SR in its Ca 2ϩ handling capacity in smooth muscle (1, 4, 16). The SR near the center of the cells may be depleted less readily of its Ca 2ϩ than that of peripherally located SR (1) and x-ray microprobe analysis revealed Ca 2ϩ -rich spots in the central and peripheral SR in portal vein and taenia coli (17, 18). Calsequestrin was not uniformly distributed through the SR network but clustered preferentially at sites most often within the peripheral SR (4). These calsequestrin-rich elements of the SR were also enriched with IP 3 R (4). This evidence provides a morphological basis for the existence of various arrangements of Ca 2ϩ release channels. The SR Ca 2ϩ stores have been classified on the basis of the arrangement of IP 3 R and RyR and conflicting evidence exists regarding their number and receptor arrangement. To determine the organization of the SR Ca 2ϩ stores, in native cells, the predominant...

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“…Phosphorylation of Ser-19 of MLC then allows myosin ATPase to be activated by actin and muscle contraction takes place. When cytoplasmic (Ca 2+ )i is reduced, MLC phosphatase dephosphorylates MLC 20 , thereby deactivating actomyosin ATPase and causing relaxation (29,30). Ca 2+ is provided by both extracellular and intracellular sources (31)(32)(33).…”

Section: Discussionmentioning

confidence: 99%

Roles of calcium and IP3 in impaired colon contractility of rats following multiple organ dysfunction syndrome

Zheyu

Yan

2007

Braz J Med Biol Res

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The purpose of the present study was to explore changes in rat colon motility, and determine the roles of calcium and inositol (1,4,5)-triphosphate (IP 3 ) in colon dysmotility induced by multiple organ dysfunction syndrome (MODS) caused by bacteria peritonitis. The number of stools, the contractility of the muscle strips and the length of smooth muscle cells (SMC) in the colon, the concentration of calcium and IP 3 in SMC, and serum nitric oxide were measured. Number of stools, fecal weight, IP 3 concentration in SMC and serum nitric oxide concentration were 0.77 ± 0.52 pellets, 2.51 ± 0.39 g, 4.14 ± 2.07 pmol/tube, and 113.95 ± 37.89 µmol/L, respectively, for the MODS group (N = 11) vs 1.54 ± 0.64 pellets, 4.32 ± 0.57 g, 8.19 ± 3.11 pmol/tube, and 37.42 ± 19.56 µmol/L for the control group (N = 20; P < 0.05). After treatment with 0.1 mM acetylcholine and 0.1 M potassium chloride, the maximum contraction stress of smooth muscle strips, the length of SMC and the changes of calcium concentration were 593 ± 81 and 458 ± 69 g/cm 3 , 48.1 ± 11.8 and 69.2 ± 15.7 µM, 250 ± 70 and 167 ± 48%, respectively, for the control group vs 321 ± 53 and 284 ± 56 g/cm 3 , 65.1 ± 18.5 and 87.2 ± 23.7 µM, 127 ± 35 and 112 ± 35% for the MODS group (P < 0.05). Thus, colon contractility was decreased in MODS, a result possibly related to reduced calcium concentration and IP 3 in SMC.

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Functionally Separate Intracellular Ca2+ Stores in Smooth Muscle

Cited by 76 publications

References 68 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

A Single Luminally Continuous Sarcoplasmic Reticulum with Apparently Separate Ca2+ Stores in Smooth Muscle

Roles of calcium and IP3 in impaired colon contractility of rats following multiple organ dysfunction syndrome

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