Inositol 1,3,4,5-tetrakisphosphate as a second messenger—a special role in neurones?

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Chemistry and Physics of Lipids 98 (1999) 49 – 57

Inositol 1,3,4,5-tetrakisphosphate as a second messenger—a special role in neurones? Robin F. Irvine *, Tracy J. McNulty, Michael J. Schell Department of Pharmacology, Uni6ersity of Cambridge, Tennis Court Road, Cambridge CB2 1QJ, UK

Abstract There has been much controversy over the possibility that inositol 1,3,4,5-tetrakisphosphate (InsP4) may have a second messenger function. A possible resolution to this controversy may stem from the recent cloning of two putative receptors for InsP4, GAP1IP4BP and GAP1m. Both these proteins are expressed at high levels in neurones, as is inositol 1,4,5-trisphosphate 3-kinase, the enzyme that makes InsP4. In this review we discuss the possible relevance of these high expression levels to the complex way in which neurones control Ca2 + and use it as a second messenger. © 1999 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Inositol; Calcium; Neurone; Inositol 1,3,4,5-tetrakisphosphate

1. Introduction Inositol 1,3,4,5-tetrakisphosphate (InsP4) is not a lipid, so its suitability as a subject for review in this journal could be questioned. However, this ‘special issue’ focuses on inositol lipid signalling, and because InsP4 is synthesised directly from inositol 1,4,5-trisphosphate (InsP3), it forms an important part of the phosphoinositidase C signalling pathway. In addition, the purpose of this special issue is to highlight ‘new developments’ which have occurred within the field of phospho-

inositide signalling, and it is particularly appropriate that InsP4 should be discussed in this context because over the past 3 years we have gained important new information about the cellular components which mediate the effects of InsP4. Moreover, we are just beginning to appreciate that, like other components of the phosphoinositide cascade, InsP4 and its effectors have a particularly specialised signalling role to play in neurones.

2. The function of InsP3 3-kinase * Corresponding author. Tel.: +44-1223-339683/2; fax: + 44-1223-334040. E-mail address: [email protected] (R.F. Irvine)

It is now well established that for many different cell types, agonist exposure often causes the

0009-3084/99/$ - see front matter © 1999 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 0 0 9 - 3 0 8 4 ( 9 9 ) 0 0 0 1 7 - 1

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hydrolysis of phosphatidylinositol 4,5-bisphosphate and the production of the second messengers, diacylglycerol and InsP3 (Berridge and Irvine, 1989). While diacylglycerol remains in the plasma membrane where it helps to activate protein kinase C enzymes (Nishizuka, 1995), InsP3 is released into the cytosol where it serves to activate InsP3 receptors and allow Ca2 + to be released from intracellular stores which reside in the endoplasmic reticulum (Berridge, 1993). By empying intracellular Ca2 + stores, InsP3 also causes activation of the capacitative Ca2 + entry pathway and allows further Ca2 + to enter the cytosol from the extracellular space (Berridge, 1993). Clearly, since many important cellular processes are regulated by Ca2 + , it is vital that the cytosolic concentration of InsP3 is carefully controlled and in most animal cells, this can be achieved through phosphorylation and dephosphorylation. InsP3 3-kinase can reduce the cytosolic concentration of InsP3 by catalysing its phosphorylation and conversion into InsP4 (Irvine et al., 1986a). Although it is more than a decade since InsP3 3-kinase was discovered (Irvine et al., 1986a), the reason for its existence is not yet fully understood. InsP4 does not activate InsP3 receptors (Irvine et al., 1986b) except at very high concentrations (e.g. Wilcox et al., 1994), so under physiological circumstances, one function of InsP3 3-kinase will be to ‘turn off’ the InsP3 signal. InsP3 can, however, be dephosphorylated and the signal that it carries is thus attenuated. This reaction is catalysed by InsP3/InsP4 5-phosphatase, and recent data from Erneux’s laboratory has suggested that this enzyme may be the major regulator of InsP3 levels (De Smedt et al., 1997). The fact that InsP3 3-kinase consumes ATP in order to metabolise InsP3, whereas InsP3/InsP4 5-phosphatase does not, could be taken as suggesting that there is another reason for the existence of the former enzyme: that InsP3 3-kinase functions to produce InsP4 which also acts as a second messenger (see Irvine, 1992 and discussion below for review). However, InsP3 3-kinase is tightly regulated by Ca2 + , both directly (via calmodulin Takazawa et al., 1990) and indirectly as a result of phosphorylation by Cam kinase II (Communi et al., 1997),

whereas so far, no regulation of InsP3/InsP4 5phosphatase by Ca2 + has been documented, so the kinase reaction may have evolved to generate a Ca2 + -regulated pathway for the removal of InsP3. These two raisons d’eˆtre are not of course mutually exclusive; whenever InsP3 is eliminated by InsP3 3-kinase, InsP4 is the result. However, as we discuss below, depending on the relative abundance of InsP3 and InsP4 effectors, the two functions of InsP3 3-kinase can be exploited to different extents both by different cell types and at different subcellular locations within the same cell.

3. Second messenger function of InsP4 It has always seemed likely, given the unequivocal function of InsP3 and the intimate link between InsP3 and InsP4 production, that if InsP4 were to act as a second messenger, its function would be in some way connected with Ca2 + . The role of InsP4 in Ca2 + homoeostasis has, however, proved to be a very complex and contentious issue (Irvine, 1992). Indeed, much of the research which was conducted to investigate the function of InsP4 has produced results which are difficult to interpret, not least because many of the InsP4 preparations which are commercially available contain significant amounts of InsP3 (J. Loomis Husselbee, unpublished observations) and, as well as protecting InsP3 from InsP3/InsP4 5-phosphatase, InsP4 can be converted into InsP3 by a 3-phosphatase enzyme (Cullen et al., 1989). Furthermore, even when these factors are taken into consideration, it seems that the effects of InsP4 can be difficult to study for other reasons, as we discuss below. As one illustrative example, InsP4 was found to have an extraordinarily clear effect in mouse lacrimal acinar cells (Morris et al., 1987). Using this cell type, Changya et al. (1989a) found that Ca2 + was released from intracellular stores when InsP4 was perfused into cells which had previously been perfused with either InsP3 or its more slowly metabolised analogue, inositol 2,4,5-trisphosphate (Ins(2,4,5)P3). As Ca2 + mobilisation did not occur when InsP4 was perfused into control cells,

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this observation suggested that InsP3 and Ins(2,4,5)P3 could both release additional Ca2 + from intracellular stores when InsP4 was present. In addition, Changya et al. also showed that in the presence of extracellular Ca2 + , prolonged Ca2 + entry only occurred in cells which contained both InsP3 and InsP4 and that this effect of InsP4 occurred through a mechanism that was distinct from that of InsP3 (Changya et al., 1989b). Bird et al. (1991) subsequently studied mouse lacrimal acinar cells and reported that InsP3 alone was required to evoke sustained Ca2 + entry and suggested that the effects of InsP4 which had been previously reported were the result of InsP4’s ability to generate InsP3 or protect it from degradation (Putney et al., 1993). However, we have since learned that the lacrimal cells used by Bird et al. (1991) were maintained in culture overnight before use whereas those used by Petersen’s laboratory (Morris et al., 1987; Changya et al., 1989a) were freshly isolated. Recently, we have re-examined the role of InsP4 in mouse lacrimal cells in collaboration with Peter Smith and found that the apparently conflicting results of Bird et al. and Petersen et al. arise entirely because of this difference in cell preparation: in cultured cells, the effect of InsP4 is much less pronounced (although it is detectable), whereas in freshly isolated cells, the mobilisation and entry of Ca2 + induced by even high (1 mM) concentrations of Ins(2,4,5)P3 is almost completely dependent on the presence of a low (1–10 mM) concentration of InsP4 (Smith and Irvine, 1998). Thus it is clear that InsP4 can influence InsP3-mediated Ca2 + mobilisation and entry, but the ‘visibility’ of this influence is strongly dependent on experimental conditions. The explanation for this probably lies in the complexity of what currently appears to be the molecular mechanism of action of InsP4. We have purified a protein that binds the 1,3,4,5 isomer of inositol tetrakisphosphate with both high affinity and specificity (Cullen et al., 1995a), and cloned it (Cullen et al., 1995b) to reveal that it is a member of the GAP1 family; as such, it must interact with a monomeric G-protein of the ras sub-family whose identity is not yet firmly established. Recently we have shown that this protein GAP1IP4BP (which is also known as GAPIII (Baba et al.,

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1995) and R-ras GAP (Yamamoto et al., 1995)), or its close relative, GAP1m (Maekawa et al., 1994), probably mediates the effect of InsP4 observed on Ins(2,4,5)P3-stimulated Ca2 + mobilisation in permeabilised L-1210 cells (Loomis-Husselbee et al., 1998; McNulty, T.J., Irvine, R.F., unpublished data). This effect (Loomis-Husselbee et al., 1996) is an increased release of Ca2 + by Ins(2,4,5)P3 with altered kinetics, and the data suggest that the GAP1 concerned is acting together with an activated monomeric G-protein to control either the amount of Ca2 + to which the InsP3 receptors have access, or the kinetics of their action such that more Ca2 + is mobilised by Ins(2,4,5)P3 when InsP4 is present (Loomis-Husselbee et al., 1998). It seems highly likely that this is the same phenomenon that we have documented in mouse lacrimal acinar cells (see above), and the variation in the magnitude of the InsP4 response which is apparent between freshly isolated and cultured lacrimal cells presumably lies in the fact that the effects of InsP4 are brought about by the interaction of several proteins (including a ras sub-family member) in a complex signalling mechanism. GAP1IP4BP and GAP1m are co-expressed in most mammalian tissues (McNulty and Irvine, unpublished data), and at present we suspect that these proteins universally allow InsP4 to potentiate InsP3-mediated Ca2 + mobilisation and Ca2 + entry. It has taken us nearly a decade to appreciate this, not just because of the difficulties of studying the effects of InsP4 in vitro (discussed above) but because we have underestimated the complexity of the signalling processes that lie downstream from InsP4. One important question that remains unanswered with regard to the studies of mouse lacrimal acinar cells conducted by Petersen et al. is whether InsP4 is required for sustained Ca2 + entry simply because it allows InsP3 to release Ca2 + from the stores which control capacitative Ca2 + entry (Changya et al., 1989a) or whether InsP4 has a more direct effect on the activity of a plasma membrane Ca2 + channel. In this context, it is worth noting that Lockyer et al. have recently shown that in unstimulated COS-7 cells, GAP1IP4BP is associated with the plasma mem-

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brane whereas GAP1m is located in the cytosol, close to intracellular Ca2 + stores (Lockyer et al., 1997). This observation could be taken to suggest that in vivo, the potentiating effect of InsP4 on InsP3-stimulated Ca2 + release is likely to be mediated by GAP1m whereas any store-independent effect of InsP4 on Ca2 + entry is probably the result of its interaction with GAP1IP4BP. This is, however, likely to be an oversimplification because it appears that at least in vitro, GAP1IP4BP can mediate the effect of InsP4 on InsP3-dependent Ca2 + mobilisation (Loomis-Husselbee et al., 1998) and we do not yet know whether the subcellular distribution of the GAP1 proteins changes when cells are exposed to agonists which stimulate phosphoinositidase C. Nevertheless, it is relevant to add here that by examining blood taken from several different animal species, we have found that platelets are particularly enriched in GAP1IP4BP whereas they contain very little, if any GAP1m (McNulty and Irvine, unpublished data). Moreover, we (Cullen et al., 1994) and O’Rourke et al. (1996) have shown that in unstimulated human platelets, GAP1IP4BP is predominately associated with the plasma membrane (indeed, it is the only detectable protein in this location which specifically binds InsP4). Recently, O’Rourke et al. (1996) and El-Daher et al. (unpublished data) showed that InsP4 can specifically stimulate the efflux of Ca2 + from inside-out plasma membrane vesicles, implying that at least in platelets, GAP1IP4BP does directly control Ca2 + entry. It remains to be seen, however, whether this storeindependent, InsP4-controlled Ca2 + entry pathway is employed by other cell types because with the possible exception of neurones, platelets appear to contain more GAP1IP4BP than any other cell type and this suggests that they may use InsP4 in a very specialised manner. Finally, we should add in this context that Hashii et al. (1994) have reported an InsP4-regulated Ca2 + influx in rastransformed NIH3T3 cells, which could be interptreted as implying an involvement of GAP1IP4BP in Ca2 + influx in these cells also. Amino acid sequence analysis has revealed that the GAP1 proteins each contain three domains which they may use to bind phospholipids and associate with intracellular membranes; the C2A

domain, the C2B domain and the PH domain (Cullen et al., 1995b). In addition, the studies of Fukuda and Mikoshiba (1996), Lockyer et al. (1997) have suggested that both GAP1IP4BP and GAP1m bind InsP4 using the site in their PH domains which can bind phospholipids. In this context, it is important to consider, as we have previously (see Cullen et al., 1997), whether the GAP1 proteins can bind phosphatidylinositol 3,4,5-trisphosphate (PtdInsP3) as strongly and specifically as they bind InsP4, and whether in vivo they could function as receptors for PtdInsP3 rather that InsP4. It is now evident that many of the proteins which function as PtdInsP3 receptors can also bind InsP4 with a high degree of specificity. This is to be expected since InsP4 essentally forms the head-group of PtdInsP3. However, whereas ARNO (Venkateswarlu et al., 1998), Bruton’s tyrosine kinase, Grp-1 and cytohesin-1 (Cullen, personal communication) all bind diacetyl–PtdInsP3 or GroPInsP3 with an affinity similar to or greater than InsP4, GAP1IP4BP ‘prefers’ InsP4 over diacetyl–PtdInsP3 and GroPInsP3 by at least an order of magnitude (see Cullen et al., 1997) suggesting that in vivo, it acts as a receptor for InsP4 rather than PtdInsP3. Unfortunately, we have not yet been able to assess whether GAP1m exhibits a similar preference for InsP4 in vitro. Of course, comparing the relative ability of proteins to bind InsP4 and PtdInsP3 derivatives is not the ideal way to determine whether they are regulated by InsP4 or PtdInsP3 in vivo, but it is the only meaningful way we have of addressing this question because as a lipid, PtdInsP3 cannot be uniformly dispersed in aqueous solution. Nevertheless, the observation that GAP1IP4BP can potentiate the effect of InsP4 on InsP3-mediated Ca2 + release (Loomis-Husselbee et al., 1998) adds further weight to the idea that GAP1IP4BP is controlled by InsP4, rather than PtdInsP3, in vivo. In contrast to GAP1IP4BP, many of the proteins which are believed to act as PtdInsP3 receptors are located in the cytosol of unstimulated cells and translocate to the plasma membrane when cells are exposed to agonists which stimulate the production of PtdInsP3 (see Irvine, 1998 for review). Its seems, therefore, that in order to further

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evaluate whether the GAP1 proteins are regulated by InsP4 or PtdInsP3 in vivo, it would be useful to know whether their subcellular distribution is changed by agonists which activate PI 3-kinase. Such studies would of course be particularly useful in evaluating the function of GAP1m which appears to be cytosolic in unstimulated cells (Lockyer et al., 1997).

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they have very high levels of InsP3 3-kinase (the A isoform, unique to brain and testis e.g. Mailleux et al., 1991a), and this is especially concentrated in dendrites, and in their spines in particular (Go et al., 1993). As with the basic mechanism of action of InsP3, it is easy to produce a simple answer to the question, what is InsP3 3-kinase doing there?— it is phosphorylating InsP3 to produce InsP4 —but how that contributes to the physiological action of neurones is a much more complicated question.

4. The role of InsP3 in the brain The action of InsP3 as a second messenger, mobilising Ca2 + from intracellular stores, is now firmly established (Streb et al., 1983; Berridge, 1993). But what is still a subject of active research in many laboratories is how this mechanism fits into the physiological and pathological actions of tissues in vivo. This is particularly true of the brain, where there is still much debate and investigation concerning the various roles that intracellular Ca2 + stores, and the two families of receptors that control the release of Ca2 + from them (ryanodine and InsP3 receptors), play in the physiology and pathology of neuronal function. Neurones have many ways of stimulating Ca2 + entry, and thus simplistically one might suppose that they do not need intracellular Ca2 + stores. But there is increasing evidence that these stores fulfil crucial functions (e.g. in long-term potentiation (LTP) or long-term depression (LTD), and Berridge (1998) has recently reviewed this area, and described the complexity of the architecture of the endoplasmic reticulum system in neurones, and the multiple ways in which its ability to release Ca2 + can contribute to many aspects of neuronal action. Neurones have extraordinarily high levels of InsP3 receptors — Purkinje cells, for example, have more than an order of magnitude more receptors than any peripheral cell type (Ross et al., 1989). Thus although we now know a lot about how InsP3 regulates Ca2 + in non-excitable cells, we still have a lot to learn about how its actions contribute to neuronal function.

5. InsP3 3-kinase in the brain Another remarkable property of neurones is that

6. InsP4 and its putative receptors in the brain Although part of the reason for our considering neurones here lies in the fact that they may use InsP3 3-kinase and InsP4 in a different manner to non-excitable cells (see below), it is also true that the basic action of InsP3 3-kinase and InsP4 in neurones will be essentially the same as in other cell types, but on a more pronounced scale. It is therefore very exciting to us that, following on from the data showing the high levels of InsP3 3-kinase in brain (above) we have detected, using antibodies specific to GAP1IP4BP and GAP1m (Cullen et al., 1995b; Lockyer et al., 1997), very high levels of GAP1IP4BP and GAP1m in brain, especially in neurones (Schell et al., unpublished data). These observations indeed confirm published suggestions made using in situ hybridisations by Maekawa et al. (1994), Baba et al. (1995), who independently cloned GAP1IP4BP and GAP1m respectively (though neither group knew that these proteins bind InsP4). There are already several indicators that InsP4 may play a role in neuronal Ca2 + homoeostasis. Firstly, Jun et al. (1998) have produced a knockout mouse deficient in InsP3 3-kinase isoform A. These animals show increased LTP in their hippocampal CA1 pyramidal cells. This phenomenon may be as much a consequence of the InsP3-removing action of InsP3 3-kinase as any action of InsP4 itself (see above), and some recent data on a mutant C. elegans lacking InsP3 3-kinase suggests a similar story (Clandinin et al., 1998), though in both cases a negative influence of InsP4 on Ca2 + signalling is an alternative explanation for the data. Secondly, Szinyei et al. (1998)

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have recently shown that in hippocampal neurones, intracellular application of InsP4 enhances LTP (whereas a non-metabolisable inositol trisphosphate does not, thus reducing the likelihood that InsP4 acts simply to protect InsP3 from the actions of InsP3/InsP4 5-phosphatase). This is superficially contradictory to the InsP3 3-kinase knock-out study (Jun et al., 1998), but a frequent problem with genetic knockouts is that compensatory mechanisms are up-regulated, and perhaps more acute knock-out experiments, employing neurones in primary or organotypic culture would allow us to reconcile these differences. Another connection between InsP4 and Ca2 + in neurones comes from Kawai’s laboratory (Tsubokawa et al., 1994, 1996); they have observed InsP4-stimulated Ca2 + entry in hippocampal CA1 neurones and suggested it contributes to ischaemia-induced neuronal death. They found initially that InsP4 infused into CA1 cells killed neurones taken from gerbils which had previously suffered an ischaemic episode (Tsubokawa et al., 1994). This action of InsP4 was apparently due to stimulation of Ca2 + entry (an effect that was specific to the 1,3,4,5 isomer of inositol tetrakisphosphate, and was prevented by an inhibitory InsP3 3-kinase antibody). Subsequently they showed that prior ischaemia in vivo caused the appearance of an v-conotoxin-blockable Ca2 + channel that was directly and specifically controlled by InsP4 (Tsubokawa et al., 1996). It is an open question whether this channel is related to the one whose existence is implied by Szinyei et al. (1998), or to a Ca2 + channel stimulated by InsP3 and InsP4 that was studied in cerebellar cells by De Waard et al. (1992) — there appear to be a number of differences between them that suggest they may not be the same. Overall, however, there is already substantial evidence to implicate InsP4 in neuronal Ca2 + homeostasis.

7. Other aspects of InsP3 3-kinase As mentioned previously, the A isoform of InsP3 3-kinase is found in high concentrations in the dendrites (and spines thereof) of hippocampal CA1 cells (Mailleux et al., 1991b). This has led to

the logical deduction that it is there to control the amount of InsP3 in the spine, and/or to form InsP4 there. The InsP3 will mobilise Ca2 + from the endoplasmic reticulum within the spine with all the consequences for integration, after-hyperpolarisations etc. that have been proposed (Berridge, 1998). However, we think that there may be another important aspect to the presence of InsP3 3-kinase at such high levels, together with such a high concentration of calmodulin and Cam kinase II in spines (Kelly et al., 1984). The latter enzyme is a potent activator of InsP3 3-kinase, and has also been suggested (Meyer et al., 1992; Hanson et al., 1994) and recently very elegantly shown (De Koninck and Schulman, 1998) to be an integrator of pulsatile Ca2 + signals. Any InsP3 formed post-synaptically in spines will be subject to intense metabolism by InsP3 3-kinase, and this metabolism will be greater if a ‘recent’ Ca2 + signal has been received in that particular spine (because the Cam kinase II will have already phosphorylated InsP3 3-kinase and activated it). Although spines are usually represented as having endoplasmic reticulum (and therefore InsP3 receptors) in them (e.g. Berridge, 1998), this may only apply to those of the cerebellar Purkinje cells. A very careful and quantitative study of hippocampal CA1 cells (Spacek and Harris, 1997) has shown that in fact 60% of spines have no endoplasmic reticulum at all. Thus for any InsP3 produced within such spines to mobilise Ca2 + , it must exit from the spine and enter the dendrite body, where the InsP3 receptors will be. This throws a whole new light on the extraordinary concentration of InsP3 3-kinase and its Ca2 + -dependent regulators in spines, because, depending on the intensity and possibly the frequency (see above) of stimulation, the InsP3 may not ‘escape’ into the dendrite at all, and thus will have no effect. Thus InsP3 3-kinase may function partly as a co-incidence detector and it may be a key effector of the ‘frequency-reading’ Cam kinase II (Meyer et al., 1992; Hanson et al., 1994; De Koninck and Schulman, 1998). If InsP3 does indeed cause little Ca2 + mobilisation in some spines, then in those circumstances activation of protein kinase C by diacylglycerol may therefore be the major local signal (note the abundance of

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protein kinase C-g in spines, and its implied role in LTP Saito et al., 1994). Finally, it remains possible that InsP4 has a physiological action in spines, but we do not yet know whether either GAP1IP4BP or GAP1m, or any other as yet undiscovered target of InsP4, exist within these specialised dendritic structures.

8. Conclusions We still face some major areas of uncertainty as we try to understand a very simple question: why do cells use IP3 3-kinase to phosphorylate InsP3 and produce InsP4? This question may engender a different set of answers in the brain as compared with other tissues, because it seems that InsP3 has itself been subverted by neurones to fulfil a particularly specialised role. As discussed above, at present we have no clear answers, but we believe that as we begin to dissect out in more detail why some systems appear more responsive to InsP4 than others, and also as we probe further into whether GAP1IP4BP and GAP1m are InsP4 receptors, and the nature of their signal transduction mechanisms, we hope that we are progressing along the right lines. We also hope that some clarification may be within our grasp in the near future.

Acknowledgements We are grateful to other members of our lab, and to Mike Berridge, for helpful discussions. M.J.S. is a recipient of a Burroughs Wellcome Fund Hitchings–Elion Fellowship. T.J.M. is supported by a grant from the BBSRC, and R.F.I. is supported by the Royal Society and the Wellcome Trust.

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