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Topical Review |
1 Ion Channel and Cell Signalling, Division of Basic Medical Sciences, St George's, University of London, Cranmer Terrace, London SW17 ORE, UK
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Abstract |
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 Top Abstract IntroductionNote added in proofReferences |
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(Received 1 June 2007;
accepted after revision 2 July 2007;
first published online 5 July 2007)
Corresponding author A. P. Albert: Ion Channel and Cell Signalling, Division of Basic Medical Sciences, St George's, University of London, Cranmer Terrace, London SW17 ORE, UK. Email: aalbert{at}sgul.ac.uk
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Introduction |
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TopAbstractIntroductionNote added in proofReferences |
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Similar to many other cell types there is significant evidence for the expression of Ca2+-permeable cation channels in smooth muscle which are classified as receptor-operated (ROCs) and store-operated channels (SOCs; see reviews by Large, 2002; McFadzean & Gibson, 2002; Albert & Large, 2003; Beech et al. 2004). Moreover there is accumulating evidence that members of the canonical subgroup of transient receptor potential (TRPC) channels constitute both ROCs and SOCs in smooth muscle. ROCs are activated in response to cell surface receptor (usually GPCR) stimulation which is independent of depletion of internal Ca2+ stores. For example, the native TRPC6-like channel in rabbit portal vein is activated by noradrenaline acting on 
-adrenoceptors but this channel is not stimulated by agents that directly release Ca2+ from the SR (Wang & Large, 1991; Inoue et al. 2001). Generally ROCs are activated by GPCRs coupled to phospholipase C (PLC) although in rabbit ear artery myocytes ROCs may be constitutively driven by phospholipase D (Albert et al. 2005). In contrast SOCs are plasmalemmal ion channels which are proposed to be stimulated by depletion of internal Ca2+ stores. The strict definition of a SOC is a channel which is activated by a decrease in the Ca2+ concentration within the SR ([Ca2+]SR, or endoplasmic reticulum, ER) and not by the subsequent rise (or reduction) in [Ca2+]c (Parekh & Putney, 2005). Further it is sometimes stated that SOCs are not activated by second messengers generated by PLC (Lewis, 2007). An important question is whether a single cellular mechanism activates SOCs and several hypotheses have been tested over the years (see Parekh & Putney, 2005 for a detailed review). In the present review we will briefly summarize the properties of SOCs in smooth muscle where they have been studied at the single channel level. It is intended to highlight the fact that SOCs in smooth muscle have diverse biophysical properties and multiple activation mechanisms and to indicate possible molecular explanations for these different characteristics.
Single channel properties of SOCs in smooth muscle
In physiological conditions SOCs are evoked by stimulation of plasmalemmal GPCRs (e.g. -adrenoceptors in vascular smooth muscle) coupled to PLC with subsequent formation of inositol-1,4,5-trisphosphate (IP3) which causes release of Ca2+ ions from the SR and subsequent opening of SOCs. However, receptor agonists are rarely used to study SOCs because they are expected to simultaneously activate ROCs which would complicate interpretation of data from such experiments. Consequently the usual method to record SOC activity in isolation is to study responses evoked by the selective SR Ca2+-ATPase (SERCA) inhibitors thapsigargin and cyclopiazonic acid (CPA). In smooth muscle the first recording of a store-operated conductance was measured with whole-cell recording from a single mouse anococcygeus myocyte treated with CPA (Wayman et al. 1996). This type of experiment has been carried out in several laboratories (see Albert & Large, 2003) but often the [Ca2+]c is not buffered to a fixed concentration and it is possible that the observed current is therefore evoked by changes in [Ca2+]c.
The gold standard method of recording SOC activity is to measure whole-cell currents evoked by depleting intracellular Ca2+ stores, e.g. with SERCA inhibitors, while clamping the [Ca2+]c to approximately resting levels with high (10 mM) concentrations of a calcium chelator such as BAPTA or EGTA. It is important to point out that these conditions are unlikely to be achieved physiologically and cell stimulation will normally be accompanied by an increase in [Ca2+]c. Nevertheless such experiments have demonstrated that CPA induces a whole-cell current in freshly dispersed rabbit portal vein myocytes (Albert & Large, 2002a; Liu et al. 2005b) and human airway smooth muscle (Peel et al. 2006). In these conditions it is assumed that the channel underlying the whole-cell current is a SOC according to the strict definition of SOC activation.
However, there is a great advantage in recording SOC activity at the single channel level because it is possible to be more confident of studying a single molecular mechanism which may not be the case with whole-cell recording or measurement of [Ca2+]c with dyes. There have been several studies which demonstrate that single Ca2+-permeable cation channels with unitary conductances of 2–5 pS can be recorded in the cell-attached configuration in isolated smooth muscle cells in response to application of CPA or thapsigargin (Table 1, mesangial cells are included because they possess a similar phenotype to smooth muscle). In contrast the widely studied Ca2+-release-activated current (ICRAC) has not been studied at the single channel level but a unitary conductance has been estimated to be approximately 0.02 pS from stationary noise analysis (Table 1). The disparity in unitary conductances highlights important differences between SOCs in smooth muscle and ICRAC in non-excitable cells and indicates that these channels are likely to possess different molecular structures (see later).
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Diverse biophysical properties and activation mechanisms of SOCs in vascular smooth muscle
Parekh & Putney (2005) have discussed the variety of store-operated calcium entry mechanisms in different cell types but it also seems that there are at least two classes of SOCs in smooth muscle. This issue is described in detail by Albert & Large (2003) but Table 1 illustrates the two main different biophysical characteristics of SOCs in rabbit aortic myocytes compared to portal vein/mesenteric artery myocytes. The unitary conductances are similar in all three preparations in 1.5 mM extracellular Ca2+ concentration ([Ca2+]o) but they have significantly different Ca2+ permeabilities. SOCs in portal vein/mesenteric artery myocytes are approximately 50 times more permeable to Ca2+ ions than the SOC in aortic myocytes when estimated from reversal potentials in different [Ca2+]o (Table 1).
It is apparent that the relative Ca2+ permeability of SOCs in smooth muscle is considerably smaller than ICRAC (see Table 1) and thus SOCs in smooth muscle are non-selective cation channels with a degree of Ca2+ permeability. It seems that ICRAC is well suited for refilling intracellular Ca2+ stores whereas in smooth muscle SOCs may also represent a depolarizing mechanism as well as a Ca2+ influx pathway. These differences in Ca2+ permeability between SOCs in smooth muscle and ICRAC in non-excitable cells provide further evidence that these channels are likely to possess different molecular structures (see later).
In addition there appears to be at least two activation mechanisms of SOCs in smooth muscle. In aortic myocytes it has been proposed that depletion of [Ca2+]SR releases a calcium influx factor (CIF) from the stores which displaces calmodulin (CaM) bound to membrane-delimited Ca2+-independent phospholipase A2 (iPLA2) which produces lysophospholipids to open SOCs (Smani et al. 2004). This represents a classical store-dependent activation mechanism. In contrast, in rabbit portal vein and mesenteric artery myocytes, SOCs evoked by both CPA and BAPTA-AM are almost completely blocked by inhibitors of protein kinase C (PKC) indicating a pivotal role for this kinase in SOC activation (Albert & Large, 2002b; Saleh et al. 2006). Moreover the diacylglycerol (DAG) analogue 1-oleoyl-sn-glycerol (OAG), and phorbol esters which stimulate PKC, also induced SOC activity in portal vein and mesenteric artery myocytes (Albert & Large, 2002b; Saleh et al. 2006). However, it is not clear how a reduction of [Ca2+]SR leads to activation of PKC and subsequent SOC opening. Therefore the SOCs in aorta versus portal vein/mesenteric artery differ in both biophysical properties and gating mechanisms.
Store-independent activation of SOCs in rabbit portal vein myocytes
A significant observation was that the sympathetic neurotransmitter noradrenaline activated SOCs in outside-out patches of portal vein myocytes in which CPA had no effect (Fig. 1A). These channels had identical characteristics to SOCs evoked by CPA and BAPTA-AM in cell-attached patches which were blocked by PKC inhibitors and therefore this noradrenaline-induced activity can be termed store-independent activation of SOCs (Albert & Large, 2002b). Presumably noradrenaline activates membrane-delimited PKC which is mediated by the production of DAG. In addition the phosphatase inhibitor calyculin A also evoked SOCs (Fig. 1B) in outside-out patches. This result not only supports the notion that a kinase may be involved in SOC activation but also suggests that there is a constitutively active phosphorylating pathway working independently of intracellular stores which can open SOCs. This store-independent pathway is in contrast to the established definition of SOC activation.
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-adrenoceptor stimulation inhibits SOC activity via PKA in portal vein myocytes and therefore this mechanism may contribute to the vasodilatation mediated by -adrenoceptors (Liu et al. 2005b). An interesting finding was that although IP3 applied on its own to the cytoplasmic surface did not induce SOC activity it did markedly potentiate the probability of channel opening of SOCs evoked by PKC catalytic subunit (Fig. 2D) and by PDBu, CPA and BAPTA-AM (Liu et al. 2005a). Therefore the intracellular mediator which releases Ca2+ from the SR also potentiates the influx mechanism for refilling the store. Previously one hypothesis for SOC activation is the conformational coupling mechanism whereby IP3 receptors in the SR couple to the plasmalemmal SOC on depletion of [Ca2+]SR to cause channel opening (Parekh & Putney, 2005). However, in our experiments there is no evidence for the presence of SR in inside-out patches (due to lack of effect of CPA) and therefore this effect may be due to IP3 itself acting on or close to the SOC. Application of the PKA inhibitor H-89 also induced channel activity (Fig. 2C), which supports the hypothesis that there is a tonically active stimulation mechanism which is independent of [Ca2+]SR and also that there is a constitutive inhibitory pathway involving PKA.
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Calmodulin stimulates SOCs in rabbit portal vein myocytes
The hypothesis that there is a constitutive driver causing SOC opening, which is counteracted by constitutive inhibitory PKA stimulation, provoked us to investigate whether calmodulin (CaM) stimulates SOCs as this Ca2+-binding protein is known to modulate many types of ion channel, including Ca2+-permeable channels. Application of 100 nM CaM to the intracellular surface of an inside-out patch stimulates a 2 pS channel in portal vein myocytes (Fig. 3Aa and b) which has identical properties to SOCs (Albert et al. 2006a). This stimulation of SOCs by CaM is Ca2+ dependent and SOCs are stimulated in 1 nM [Ca2+]c with a maximal effect around 100 nM [Ca2+]c. In higher [Ca2+]c the excitatory effects of CaM decrease (Fig. 3Ac). It should be noted that direct application of Ca2+ ions (up to 2 µM) alone to the cytoplasmic surface of inside-out patches never evokes these channels (Albert & Large, 2002b).
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In summary, different gating mechanisms exist for SOCs in different smooth muscle types (aorta versus portal vein/mesenteric artery in rabbit) and, in addition, studies in the portal vein indicate that SOCs can be activated by diverse pathways which do not require depletion of intracellular Ca2+ stores with one pathway involving activation by PKC and the other utilizing CaM. Two noteworthy points are that, first, CaM evokes SOC activity in physiological concentrations ([CaM]c in many cell types is about 1–10 µM; Saimi & Kung, 2002) and in [Ca2+]c between 1 and 100 nM providing a possible basis for a constitutive driver mechanism. Secondly, it is possible that SOCs may be activated by increasing [Ca2+]c via CaM (or perhaps a Ca2+-dependent PKC). Additionally SOCs may also be stimulated by a decrease in [Ca2+]c due to the removal of the inhibitory influence of CaM kinase II. With respect to these points it should be remembered that in an intact cell, as when recording from a cell-attached patch, it is likely that CPA will increase [Ca2+]c whereas BAPTA-AM will reduce [Ca2+]c. Hence the effect of these agents on [Ca2+]c should always be taken into account when appraising experimental approaches used to investigate SOC activity.
Molecular composition of SOCs
The discovery of mammalian homologues of the Drosophila transient receptor potential (TRP) gene which encode 28 non-selective cation channel proteins with varying permeabilities to Ca2+ ions, has lead to a plethora of studies on the possible role of TRP channels underlying SOCs. Many of these studies have focused on the canonical transient receptor potential (TRPC) subfamily which comprises seven channel proteins (TRPC1–C7, C2 is a pseudogene in humans). Over-expression studies in cultured cell lines have shown that almost all TRPC channel proteins can be activated by SERCA inhibitors and by dialysing the intracellular medium with high concentrations of Ca2+ chelators, which suggests that TRPCs may represent SOCs (Parekh & Putney, 2005).
An important point when considering the molecular composition of TRPCs underlying SOCs is the general opinion that the majority of functional TRPCs in vivo consist of different TRPC subunits associated together in complex heterotetrameric structures. A variety of techniques including co-immunoprecipitation, fluorescence resonance energy transfer (FRET) and expression of dominant-negative TRPC subunits have shown that TRPC1 can form interactions with TRPC4/C5 and that TRPC3/C6/C7 channel proteins can also interact with one another (Goel et al. 2002; Hofmann et al. 2002). Moreover in embryonic rat brain microsomes associations between TRPC1 and TRPC4/C5 and between TRPC3/C6 have also been described (Strübing et al. 2003). Functional studies have shown that TRPC1 and TRPC3 associate to form distinct channels in human parotid gland ductal cells (HSY) cells which were activated by store depletion using thapsigargin and also by the DAG analogue 2-acetyl-sn-glycerol indicating a possible store-independent activation pathway (Liu X. et al. 2005). In rat H19-7 hippocampal cell lines TRPC1/TRPC3 have also been proposed to mediate store-operated Ca2+ entry (Wu et al. 2004). Moreover TRPC1 and TRPC4 proteins are thought to form a heterotetrameric SOC in endothelial cells (Brough et al. 2001; Freichel et al. 2001; Ahmmed et al. 2004) and TRPC1/C3/C7 are thought to form endogenous SOCs in HEK-293 cells (Zagranichnaya et al. 2005). In summary, it is apparent that numerous TRPC subunits can interact in a highly complex manner to form SOCs in several cell types.
A recent advance in the understanding of the potential molecular composition of SOCs has been the discovery of two families of transmembrane proteins, STIM and Orai, which have been proposed to mediate ICRAC in non-excitable cells with STIM1 acting as an ER Ca2+ sensor/activator of Orai1 and Orai1 constituting the CRAC channel/ion transport mechanism (see Lewis, 2007 for review and references). As there are vast differences between the biophysical properties of ICRAC and many SOCs (see above and Table 1) it seems unlikely that Orai proteins alone mediate the pore-forming subunits of all SOCs. However, recent studies have suggested that STIM1 and Orai1 may interact with TRPC proteins to modify their function. Huang and colleagues showed that over-expression of the cytosolic terminus of STIM1 increased TRPC1 activity and also demonstrated that STIM1 and TRPC1 proteins can associate with one another (Huang et al. 2006). In addition over-expression of Orai proteins was shown to enable thapsigargin to activate TRPC3 and TRPC6 activity through a STIM1-mediated mechanism which was not present in the absence of Orai proteins (Liao et al. 2007). These results indicate that STIM proteins may act as store-operated regulators of SOCs and also that Orai proteins may combine with TRPCs to produce functional store-operated channels either through acting as a pore-forming subunit or as a regulatory -subunit (Huang et al. 2006). STIM1 has also been shown to regulate agonist-evoked activity of all TRPC subunits, except TRPC7, through either directly binding to TRPC1, TRPC4 and TRPC5 proteins or mediating heteromultimerization of TRPC3 and TRPC6 proteins with these STIM1-binding TRPC subunits (Yuan et al. 2007). Importantly this study proposed a new definition of SOCs, as channels that are regulated by STIM1 and require store-depletion-mediated clustering of STIM1 for activation, and concluded that all TRPCs, except TRPC7, can function as SOCs (Yuan et al. 2007). Furthermore TRPC1 has been suggested to produce a ternary complex with STIM and Orai1 which is important for activating SOCs in human salivary glands (Ong et al. 2007).
To date there is little information on the role of STIM and Orai in smooth muscle although human airway myocytes have been shown to express STIM1/2 mRNA and siRNA targeted at STIM1 markedly reduced Ca2+ influx and whole-cell currents evoked by CPA (Peel et al. 2006) indicating a potentially important role for STIM in mediating SOCs in these myocytes. In light of the proposed roles of STIM1 in regulating TRPC activity (see above) and the increasing evidence indicating that TRPCs mediate SOCs in smooth muscle (see below) an important area of future research will be to investigate the roles/mechanisms of STIM proteins in regulating SOC activity in smooth muscle.
The diverse molecular compositions of ICRAC (by Orai proteins) and SOCs (possibly a heterotetrameric TRPC structures) provides a possible explanation as to why there are many types of SOCs with different biophysical properties, permeabilites to Ca2+ and activation mechanisms. Furthermore this potential diversity in the make-up of SOCs poses the question against the strict definition of SOCs: is it probable that activation of these channels is governed only by a single store-operated mechanism?
Molecular identity of SOCs in vascular smooth muscle
Recently several groups using different experimental approaches have presented evidence for TRPC1 being an essential component of SOCs in smooth muscle. In rabbit cerebral artery myocytes anti-TRPC1 antibodies raised against a putative extracellular epitope of TRPC1 reduced thapsigargin-induced Ca2+ influx (Xu & Beech, 2001) and in pulmonary artery myocytes inhibition of endogenous TRPC1 expression by specific antisense oligonucleotides reduced CPA-evoked whole-cell currents (Sweeney et al. 2002). In addition, in the aorta A7r5 cell line knockdown of endogenous TRPC1 expression with siRNA and antisense methods reduced endogenous whole-cell currents induced by thapsigargin (Brueggemann et al. 2006). Moreover Fig. 4Aa and Ba illustrates work from our laboratory with single channel studies which show that bath application of anti-TRPC1 antibodies, raised against a putative intracellular epitope, to the cytoplasmic surface of inside-out patches produced marked inhibition of SOC activity evoked by CaM in portal vein myocytes (AP Albert, SN Saleh, CM Peppiatt-Wildman & WA Large unpublished data) and of SOCs stimulated by angiotensin II in mesenteric artery (see Saleh et al. 2006).
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These data provide strong evidence that TRPC1, possibly as a heterotetramer with TRPC5, is an essential component of SOCs in vascular smooth muscle. However, it is likely that other TRPC proteins are involved and the difference in biophysical properties between SOCs in aorta myocytes versus portal vein/mesenteric myocytes results from different heterotetrameric structures.
Multiple activation mechanisms of TRPCs proposed to mediate SOCs in vascular smooth muscle
We have shown that PKC and CaM can activate SOCs in vascular myocytes and there is support for TRPC1 and TRPC5 being components of these channels. Therefore it is interesting to consider the evidence for activation of expressed TRPC1 and TRPC5 by PKC and CaM.
Stimulation of PKC activates TRPC1.
A unique property of TRPC1 is that stimulation of PKC has been shown to be required for its activation by store depletion (Ahmmed et al. 2004) whereas the activity of all other TRPCs have been shown to be inhibited by stimulation of this kinase (Soboloff et al. 2007). In cultured human umbilical vein endothelial cells pharmacological inhibitors of PKC, expression of a PKC-defective mutant and an anti-TRPC1 antibody, reduced Ca2+ influx and whole-cell currents induced by thrombin, thapsigargin and intracellular application of IP3. Moreover this study showed that thrombin and thapsigargin produced PKC-dependent phosphorylation of TRPC1 proteins (Ahmmed et al. 2004). These data provide compelling evidence for PKC-mediated phosphorylation of TRPC1 proteins having a critical role in activating SOC activity. The DAG analogue and PKC activator, OAG, has also been shown to activate expressed TRPC1 (Lintschinger et al. 2000). In addition, stimulation of PKC has also been shown to be essential in the activation of SOCs in mesangial cells (Ma et al. 2002) although these channels are proposed to consist of TRPC4 proteins (Wang et al. 2004).
It is tempting to speculate that TRPC1 subunits confer PKC sensitivity to SOC activation previously described in portal vein/mesenteric artery myocytes (Fig. 5Ba, Albert & Large, 2002b; Saleh et al. 2006).
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Therefore these facilitatory actions of CaM on TRPC5 activity may indicate that the excitatory effect of CaM on SOCs in rabbit portal vein is conferred by TRPC5 subunits (see above, Albert et al. 2006a) and involves a direct interaction with TRPC5 proteins since inhibitors of CaM-dependent enzymes, e.g. MLCK, CaM kinase II and calcineurin, do not inhibit CaM-evoked SOC activity (Albert et al. 2006a).
In addition, expressed TRPC5 activity has also been shown to be activated by lysophospholipids, including lysophosphatidylinositol (LPI), via a relatively direct interaction with the channel proteins (Flemming et al. 2005). This may relate to the proposed role of iPLA2-mediated production of LPIs in activating native SOCs in aorta myocytes (Smani et al. 2004) and suggest that TRPC5 subunits are also components of these SOCs.
Conclusion
Experimental evidence indicates that it is unlikely that a single mechanism is involved in activating SOCs in smooth muscle and Fig. 5 summarizes our proposal for the activation of SOCs in rabbit portal vein myocytes. We suggest that TRPC1 and TRPC5 proteins are components of SOCs but it is probable that other TRPC subunits and possibly Orai and STIM proteins are involved. Figure 5A and B shows that CPA and BAPTA-AM may activate SOC activity in portal vein according to the strict definition of SOCs whereby these agents produce a reduction of [Ca2+]SR to activate SOCs. Evidence shows that both CaM and PKC are involved in this process (see earlier) but it is not clear how a reduction in [Ca2+]SR stimulates PKC and CaM. Alternatively it is possible that activation of SOCs by CPA results from an increase of [Ca2+]c which stimulates Ca2+-sensitive PKC and/or CaM which evoke SOCs (Fig. 5A). Also, BAPTA-AM may activate SOCs by reducing [Ca2+]c to remove the inhibitory effect of CaM kinase II with subsequent opening of channels through constitutive driver activity involving PKC and/or CaM. Finally Fig. 5C shows that physiological agonists such as noradrenaline acting on a GPCR linked to the classical phosphoinositol biochemical cascade activates SOCs via two separate pathways: (i) a store-dependent pathway involving production of IP3 which releases Ca2+ from internal stores leading to a rise in [Ca2+]c and stimulation of PKC/CaM to cause channel opening, and (ii) a store-independent/membrane-delimited pathway involving generation of DAG which stimulates PKC to induce SOC activity. Our evidence suggests that the primary mechanisms of activation of SOCs in smooth muscle in physiological conditions involve PKC and CaM mechanisms, perhaps mediated by changes in [Ca2+]c. In addition it is possible that several cellular mechanisms contribute to the whole-cell current or intracellular Ca2+ signal produced by agents that deplete intracellular Ca2+ stores.
In summary there is strong evidence that vascular smooth muscle expresses diverse SOCs that differ in biophysical properties and activation mechanisms. This heterogeneity in channel properties is likely to be mediated by TRPC proteins assembled together into different heterotetrameric channel structures.
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Note added in proof |
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TopAbstractIntroductionNote added in proofReferences |
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TopAbstractIntroductionNote added in proofReferences |
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