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Ca2 + microdomains, NAADP and type 1 ryanodine receptor in cell activation
BBAMCR-17784; No. of pages: 6; 4C: 2, 4 Biochimica et Biophysica Acta xxx (2016) xxx–xxx
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Biochimica et Biophysica Acta journal homepage: www.elsevier.com/locate/bbamcr
Review
Ca2 + microdomains, NAADP and type 1 ryanodine receptor in cell activation☆ Andreas H. Guse ⁎, Insa M.A. Wolf The Calcium Signalling Group, Department of Biochemistry and Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246 Hamburg, Germany
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Article history: Received 28 October 2015 Received in revised form 5 January 2016 Accepted 18 January 2016 Available online xxxx Keywords: NAADP Ryanodine receptor T cell Signal transduction
a b s t r a c t Nicotinic acid adenine dinucleotide phosphate (NAADP) is a Ca2+ mobilizing second messenger that belongs to the superfamily of regulatory adenine nucleotides. Though NAADP has been known since 20 years, several aspects of its metabolism and molecular mode of action are still under discussion. Though the importance of the type 1 ryanodine receptor was discovered and published already in 2002 Hohenegger et al. (2002 Oct 15) , recent data re-emphasize these original findings in pancreatic acinar cells and in T-lymphocytes. Here we review recent developments in NAADP formation and metabolism, putative target Ca2+ channels for NAADP with special emphasis on the type 1 ryanodine receptor, and NAADP binding proteins. The latter are basis for a unifying hypothesis for NAADP action. Finally, the role of NAADP in T cell Ca2+ signaling and activation is discussed. This article is part of a Special Issue entitled: Calcium and Cell Fate edited by Jacques Haiech, Claus Heizmann and Joachim Krebs. © 2016 Published by Elsevier B.V.
1. Regulatory adenine nucleotides and NAADP NAADP belongs to a superfamily of signaling molecules, the regulatory adenine nucleotides. These comprise the long known intracellular co-substrates adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide (NAD) and their metabolites (Fig. 1). Although the intracellular functions of ATP and NAD in energy metabolism have been known for decades, it only became evident in the past couple of years that ATP and NAD can be released from cells. ATP and its metabolites adenosine diphosphate, adenosine monophosphate and adenosine, generated by ectoenzymes CD39 and CD73, fulfill important paracrine signaling functions, especially regulating local inflammatory responses (Fig. 1; reviewed in [2]). In a similar manner, NAD, when released from cells, may serve on the one hand as substrate for ADPribosylation of target proteins (Fig. 1), e.g. the P2X7 purinergic receptor (reviewed in [2]). On the other hand NAD can be converted by CD38 in type II conformation to generate extracellular cyclic adenosine
Abbreviations: ATP, adenosine triphosphate; ADPR, adenosine diphosphoribose; cADPR, cyclic adenosine diphosphoribose; ER, endoplasmic reticulum; IP3, D-myoinositol 1,4,5-trisphosphate; IP3R, D-myo-inositol 1,4,5-trisphosphate receptor; NAADP, nicotinic acid adenine dinucleotide phosphate; NAADP-BP, NAADP binding protein; NAD(P), nicotinamide adenine dinucleotide (phosphate); NFAT, nuclear factor of T cells; RyR, ryanodine receptors; RyR1 (or 2, or 3), type 1 (or 2, or 3) ryanodine receptor; TRPML1, transient receptor potential cation channel, subtype mucolipin 1; TRPM2, transient receptor potential cation channel, subtype melastatin 2. ☆ This article is part of a Special Issue entitled: Calcium and Cell Fate edited by Jacques Haiech, Claus Heizmann and Joachim Krebs. ⁎ Corresponding author. E-mail address: [email protected] (A.H. Guse).
diphosphoribose (cADPR) and adenosine diphosphoribose (ADPR) (Fig. 1). The former acts as paracrine signaling molecule in several cell systems (reviewed in [3]). In addition, ATP and NAD can also be converted inside cells to second messenger molecules involved in the transmission of extracellular signals into the intracellular machinery to generate appropriate cellular responses. ATP can be converted to the second messenger 3′,5′-cyclic adenosine monophosphate (Fig. 1), while NAD serves as precursor of cADPR and ADPR. The intracellular conversion of NAD to ADPR and cADPR likely proceeds via CD38 in type III conformation, meaning that the N-terminus of CD38 is located within the cytosol (Fig. 1). ADPR may also be produced by degradation of poly-ADP-ribosylated proteins (reviewed in [4]). The synthetic pathway to NAADP is less clear and will be discussed below. In addition to these well studied messenger molecules, additional signaling metabolites of NAD have been described, e.g. 2′-phospho-cyclic adenosine diphosphoribose [5,6] and diadenosine homodinucleotide compounds P18 and P24 [7,8]. While 3′,5′-cyclic adenosine monophosphate activates protein kinase A, the NAD metabolites cADPR, ADPR and NAADP are all regulators of the free cytosolic Ca2+ concentration. ADPR, the main product of CD38, binds to the NudT9 homology domain to open the non-specific cation channel transient receptor potential, subtype melastatin 2 (TRPM2; [9]). cADPR evokes release of Ca2+ from the endoplasmic reticulum (ER) by opening of ryanodine receptors (RyR), likely via a specific binding protein [10,11]. In this review we will concentrate on NAADP (Figs. 1, 2), the most potent endogenous Ca2+ releasing molecule known to date. It is confirmed that NAADP is rapidly produced upon cell stimulation [12–15] and releases Ca2+ from endogenous Ca2+ stores. As will be specified
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Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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Fig. 1. Overview of extra- and intracellular regulatory adenine nucleotides. While ATP and NAD fulfill their classical roles in energy metabolism inside cells, they may be released from cells, e.g. at sites of inflammation. ATP may act on purinergic receptors and/or is converted by ecto-enzymes CD39 and CD73 via ADP and AMP to adenosine. Purinoceptors and adenosine receptors activate specific intracellular signaling that is not discussed in detail here. Extracellular NAD either serves as substrate for ADP-ribosylation (reviewed in [2]) or may be converted by ecto-enzyme CD38 (in type II conformation) to cADPR and ADPR. Work mainly carried out by De Flora and co-workers (reviewed in [3]) showed extracellular (paracrine) effects of cADPR and ADPR. Here, cADPR is taken up by certain cell types via nucleoside transporters and acts intracellularly on RyR, while ADPR appears to act via purinergic receptors. cAMP signaling, the canonical 2nd messenger pathway, is briefly displayed, too. The adenine nucleotide 2nd messengers cADPR and NAADP both release Ca2+ from intracellular stores; while ER/SR is accepted as target store for cADPR, different types of intracellular membrane compartments have been postulated as target store for NAADP, e.g. ER, nuclear membrane, acidic stores, or exocrine granules. Thus, the target store for Ca2+ releasing 2nd messengers is termed ‘Ca2+ stores’ here. The part dealing with NAADP is intended to highlight facts generally accepted: NAADP is rapidly formed inside the cell, but the precursor is still under debate. Further, it is accepted that NAADP likely does not bind to any channel directly, but rather acts via binding proteins. These NAADP-BP then may activate different ion channels located on ‘Ca2+ stores’.
Fig. 2. Definitive vs speculative aspects of NAADP signaling. The figure displays aspects of NAADP signaling that are generally accepted (‘definitive’; left side) vs aspects that are controversially discussed (‘in discussion’; right side). In summary, rapid formation of NAADP, its metabolism to 2′-phospho-ADPR or to NAAD, and its strong Ca2+ releasing activity are well acknowledged. In contrast, enzymes, organelles and channels involved in this process are less clear; the main controversial points are summarized in the box below ‘in discussion’.
Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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in the subsequent chapters, NAADP's metabolism and mechanism of action, e.g. nature of its target organelle and channel, have been controversially discussed in recent years. We will review recent developments and present hypotheses that may help to develop the field. 2. NAADP formation and metabolism All second messengers are formed enzymatically from inactive precursors. Since NAADP was discovered as impurity of NADP [16,17] and since its structure is almost identical to NAADP, conversion of NADP to NAADP was studied from the 1990s onward. Since NADP does not show any Ca2+ releasing activity, the general idea of NADP as the inactive precursor fits well. In fact, studies using NADP as substrate for NADglycohydrolase/ADP-ribosyl cyclase CD38 resulted in the discovery of the ‘base-exchange’ reaction [18]. This reaction in which nicotinamide in NADP is exchange by nicotinic acid added as second substrate is the only proven reaction to yield NAADP. However, the reaction conditions are somewhat critical since an acidic pH and a high concentration of nicotinic acid are required, conditions that are difficult to find in the cytosol of living cells (Fig. 2). Further, at least in some tissues and cells knockout of cd38 had no effect on endogenous NAADP, or resulted in even increased NAADP concentrations [19,20] indicating that CD38 might be involved in NAADP catabolism rather than in its formation (Fig. 2). Other possible reactions to NAADP, e.g. deamidation of NADP or phosphorylation of nicotinic acid adenine dinucleotide, have been postulated, but corresponding enzyme activities have not yet been detected (Fig. 2). In contrast to NAADP formation, degradation of NAADP proceeds to 2′-phospho-ADPR via CD38 [20], or by dephosphorylation to nicotinic acid adenine dinucleotide [21,22]. Candidates for the dephosphorylation reaction are a specific and Ca2+-dependent NAADP phosphatase [21] and alkaline phosphatase [22]. 3. Putative target Ca2+ channels for NAADP Since its discovery in 1995 there has been intense research with regard to the receptor for NAADP. Interestingly, a number of candidates have been introduced by different laboratories (Fig. 2), starting with type 2 and type 1 ryanodine receptor (RyR2, RyR1; [23], [1]). However, the discovery of the lysosome-related reserve granule of sea urchin egg as a NAADP-sensitive Ca2+ store [24] shifted the search more to channels potentially expressed in acidic stores. Such candidates comprise the two-pore channels type 1 and 2 (TPC1, TPC2; [25–27]), transient receptor potential channel type mucolipin 1 (TRP-ML1; [28], or TRPM2; [29]). In a very recent review we compared literature data for intracellular NAADP concentrations with published EC50 data for NAADP at these respective channels (reviewed in [30,31]). Collectively, these data suggest that TRPM2 and RyR2 are activated by NAADP at non-physiological concentrations. Moreover, in case of TRPM2 it was published recently that careful purification of the NAADP used in patch-clamp experiments abolished TRPM2 activation even at high NAADP concentrations [32]. Thus, contaminating ADPR in NAADP preparations may have been the reason for TRPM2 activation by NAADP observed previously [33]. TRPML1, TPC2 and RyR1 are activated in the physiological concentration range of NAADP (reviewed in [30,31]). It should be noted here that the ‘physiological concentration range’ of NAADP was determined by enzymatic cycling assays carried out in extracts produced from very high numbers of non-stimulated or stimulated cells [12–15]. Though results from these studies are similar in terms of absolute amplitude and kinetics, the following limitations exist: homogenizing and extracting large cells numbers is difficult to perform precisely at short stimulation periods, e.g. after single seconds. Thus, available kinetics in the range from 1 to 10 s must be regarded with caution. Moreover, sub-second kinetics for NAADP are not available at present. Further, since extracts are
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pooled from many cells, potential intracellular NAADP concentration gradients cannot be resolved by this method. In the same review we compared confirmatory and negatory papers regarding activation by NAADP ([30], Tab. 1). The data in those papers were obtained in different cell systems by different techniques or different animal models were employed. Unfortunately, these differences complicate direct comparison of primary data making clear judgments difficult. Thus, at least RyR1 and TPC1/2 remain as candidates for the NAADP sensitive channel(s) (Fig. 2). Since the potential role of TPCs in NAADP signaling has been reviewed recently in an excellent manner [34,35], in this review we will concentrate on RyR1. 4. Type 1 ryanodine receptor NAADP activation of native RyR1 from skeletal muscle fused into lipid planar bilayers significantly increased RyR1's open probability while the amplitude of channel opening was almost unchanged. The dynamic range of NAADP was between approx. 20 and 100 nM [1], concentrations compatible with endogenous NAADP concentrations in different cell types [12–15]. In contrast to most other studies on NAADP evoked Ca2+ signals, a bell-shaped concentration–response curve was not found in these partially purified RyR1 preparations [1] indicating loss of factors necessary for desensitization of the response. Further, to partially purified RyR1 from rabbit muscle, in other cell systems an involvement of RyR in NAADP evoked Ca2+ release was confirmed. In pancreatic acinar cells extracellular acetylcholine or intracellular infusion of D-myo-inositol 1,4,5-trisphosphate (IP3), cADPR or NAADP all induced repetitive Ca2+ spikes, all of which were sensitive to ryanodine [35]. Although the interpretation of these data contained a separate, unknown receptor for NAADP (not RyR), in a subsequent publication using isolated nuclei from pancreatic acinar cells, it was shown that the RyR blockers ryanodine or ruthenium red efficiently antagonized Ca2+ release by NAADP, while compounds interfering with acidic compartments, e.g. bafilomycin A1, brefeldin A, or nigericin, did not inhibit NAADP evoked Ca2 + release from the nuclear envelope [37]. These data resulted in a refinement of the previous model suggesting RyR to respond to both cADPR and NAADP; however, specific binding proteins were proposed for both second messengers that would mediate activation of RyR [37]. It is important to note that the NAADPsensitive nuclear Ca2+ store characterized by Gerasimenko and coworkers, ‘… is ATP dependent and thapsigargin sensitive, and is distinct from any acidic, endocytic or Golgi-type Ca2+ store’ [38]. Using permeabilized pancreatic acinar cells it was further shown that also acidic stores in the secretory granular region respond to NAADP and that this response was sensitive to ryanodine [39]. Very recent work in pancreatic acinar cells confirmed NAADP evoked Ca2+ release via RyR1 (and to a lower extent also via RyR3) located in zymogen granules and in the ER, and via TPC2 located in acidic stores [40]. The other cell system in which effects of NAADP on RyR were studied in detail is T-lymphocytes. In Jurkat T cells, a human T-lymphoma cell line often used in investigations of T cell activation, global Ca2+ signals evoked by NAADP microinjection were effectively blocked by RyR antagonist ruthenium red, but not by IP3 antagonist heparin [41]. Further, gene silencing of RyR in Jurkat T cells [42] efficiently diminished NAADP, but not IP3 mediated global Ca2+ signaling [41]. These data demonstrate that, at least for NAADP-evoked global Ca2+ signaling, RyR are required in the T cell. For pancreatic acinar cells a ‘two-pool’ model was hypothesized. According to this model NAADP triggers a small, short-lived Ca2+ signal, termed trigger Ca2+, which is then further amplified by IP3 receptors and/or RyR [36,43]. However, Langhorst et al. [41] did not specifically check for small, short-lived Ca2+ signals in Jurkat T cells lacking expression of RyR. Therefore, Dammermann & Guse [44] and Wolf et al. [45] showed in fast and very fast Ca2+ imaging studies that small, short-lived Ca2+ signals markedly decrease in Jurkat T cells lacking expression of RyR. Further, primary RyR1−/− mouse T cells showed largely diminished initial, short lived Ca2+ signals upon
Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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directed cell stimulation, e.g. upon contact to a bead coated with antiCD3 and anti-CD28 antibodies [45]. Important to note here that the temporal resolution in these experiments was approx. 25 ms [45]. Thus, evidence for trigger Ca2+ formed independently of RyR1, as hypothesized by Cancela and colleagues [36,43], was not yet obtained in T cells. If such RyR1-independent trigger Ca2+ exists, it must be an extremely short-lived, transient signal, at least in T cells. Collectively these data suggest that RyR, most likely RyR1, is essentially necessary for NAADP action, including formation of initial, short lived Ca2+ signals. In addition, further studies support a major role for RyR1 in NAADP signaling in T cells. Inhibition of lysosome function by the H+-ATPase inhibitor bafilomycin A1 did not affect NAADP effects in T cells, whereas the SERCA inhibitor thapsigargin at least partially blocked global Ca2 + signaling upon NAADP administration [46]. Further, channel opening of RyR1 by NAADP, as measured by binding of [3H]ryanodine to partially purified RyR1, was efficiently blocked by a novel synthetic NAADP antagonist, termed BZ194 [47]. Taken together, evidence from different cell systems suggests that NAADP activates RyR1. Whether this includes direct or indirect interaction remains to be determined.
In 2012 a radioactively labeled photoaffinity analogue of NAADP, [32P]5-N3-NAADP, was used to directly label NAADP-BP from different cell types [48–50]. Though labeling of one (or more) of the candidate channels was expected, in all cell systems analyzed, the NAADP-BP were small proteins found preferentially in the cytosol, but not in membrane fractions. Photoaffinity labeling of sea urchin egg homogenates showed a somewhat different pattern as compared to homogenates prepared from mammalian cell lines or tissues [48–50]. In the latter it was also shown that neither overexpression of TPC1 or TPC2 nor knockout of these channels significantly changed the labeling pattern [49]. This result suggests that the proteins specifically labeled by [32P]5-N3NAADP may represent NAADP-BP. However, up to now the molecular identity of these proteins was not published. Nevertheless, these findings prompted us to re-vitalize the original idea by Gerasimenko and colleagues as [37] as unifying hypothesis for NAADP action [51]. This hypothesis simply expands the number of channels that may be activated by the NAADP-BP from RyR, as suggested by Gerasimenko and colleagues [37], to TPCs and TRP-ML1. However, identification of the NAADP-BP is necessary to confirm or disprove this idea. 6. NAADP in T cell Ca2+ signaling
5. NAADP binding proteins — a unifying hypothesis for NAADP action Reviewing the data published regarding the NAADP sensitive cellular compartment and also the NAADP sensitive channel illustrates the controversial views and models. However, already in 2003 Gerasimenko and colleagues [37] hypothesized that NAADP may not directly bind to RyR, but may in the first step interact with a specific NAADP binding protein (NAADP-BP) which upon binding of NAADP is activated and subsequently activates RyR [37]. In the same publication, a similar model was proposed for cADPR [37].
For T cells there is evidence that NAADP is raised rapidly and transiently upon T cell receptor/CD3 complex stimulation with a peak at approx. 10 s (Fig. 3; [13]). If such formation is mimicked by microinjection of physiological concentrations of NAADP, local, RyR-dependent Ca2+ signals are observed within 20 ms [45]. Similarly, directed activation of primary T cells via localized T cell receptor/CD3 complexes very rapidly, e.g. in the millisecond range, evokes Ca2+ microdomains that depend on RyR1, but not TRPM2 expression [45]. Further, experiments in the absence of extracellular Ca2+ indicate involvement of a Ca2+ entry component in this early signaling process [45].
Fig. 3. Connection between short-lived local and long lasting global Ca2+ signaling in T-lymphocytes. T cell activation requires ligation of the T cell receptor/CD3 complex by the respective peptide ligand in MCH context. Recent data suggest involvement of NAADP and RyR1 in the first seconds of T cell activation [13,41,44]. Both act in concert to generate Ca2+ microdomains [45], possibly via NAADP-BP. This very rapid phase is followed by global Ca2+ signaling (tens of second to minutes). In this phase, further Ca2+ mobilizing 2nd messengers are formed, e.g. IP3 and cADPR, acting on their respective target channels, IP3R and RyR. Local Ca2+ signals generated by NAADP are believed to act as co-agonists at IP3R and RyR to amplify Ca2+ release. This in turn leads to store-operated Ca2+ entry via the Stim/Orai system resulting in further amplification of the Ca2+ signal of T cells.
Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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These findings raise the question whether the initial network of local Ca2+ microdomains influences later stages of T cell Ca2+ signaling and T cell activation. Experiments in rat myelin basic protein-specific T cells suggest that indeed NAADP-evoked initial Ca2+ microdomains determine the amplitude of subsequent global Ca2+ signaling. This was shown using the NAADP antagonist BZ194 that partially blocked global Ca2+ signaling and nuclear NFAT translocation as a major element of downstream signal transduction during activation of primary T cells [47]. Fig. 3 shows how the early, ‘millisecond to second’ period of local Ca2+ microdomains is coupled to the ‘second to minutes/hours’ period: the local Ca2+ microdomains act as co-agonists at both RyR and IP3R once these second messengers are produced. It might well be that local Ca2+ microdomains play a more important role in case of weak or medium activation of cADPR and/or IP3 formation. The medical implication of this co-activation of RyR and IP3R by Ca2+ ions stemming from NAADP-dependent initial local Ca2+ microdomains was shown in experimental autoimmune encephalomyelitis, an animal model for multiple sclerosis. Here NAADP antagonist BZ194 diminished accumulation of autoreactive T cells in the CNS and reduced reactivation of MBP-specific effector T cells at inflammatory sites. As a result, clinical symptoms of EAE were partially diminished [52]. In summary, the Ca2+ mobilizing second messenger NAADP and RyR1 are major players in initial, rapid Ca2+ microdomains, observed in the first milliseconds and lasting for approx. 10 to 20 s upon directed stimulation of the T cell receptor/CD3 complex. These Ca2+ microdomains are important as co-agonists to shape the global Ca2+ signal. The latter is composed of IP3- as well as cADPR-induced Ca2+ release followed by capacitative Ca2+ entry. Funding Work on adenine nucleotides in T cells was supported by the Deutsche Forschungsgemeinschaft (grant numbers GU 360/15-1 and 360/16-1, to A.H.G.), by the Forschungszentrum Medizintechnik Hamburg (to I.M.A.W.), by Förderfonds Medizin (FFM) of the University Medical Center Hamburg-Eppendorf (grant no. NWF 15/13 to I.M.A.W.), by the Hertie Foundation (grant number P1140086 to A.H.G.), and by the Landesforschungs-Förderung of the City of Hamburg (Research Group ReAd Me, project 1; to A.H.G. and I.M.A.W.). Competing interests The authors declare that they have no competing interests. Transparency document The Transparency document associated with this article can be found, in online version. Acknowledgments We are grateful to our present and past co-workers for their creative power and our collaborators for inspiring discussions and great mutual projects. Interest of the European Calcium Society in NAADP signaling is also gratefully acknowledged. References [1] M. Hohenegger, J. Suko, R. Gscheidlinger, H. Drobny, A. Zidar, Nicotinic acid–adenine dinucleotide phosphate activates the skeletal muscle ryanodine receptor, Biochem. J. 367 (Pt 2) (2002 Oct 15) 423-423. [2] B. Rissiek, F. Haag, O. Boyer, F. Koch-Nolte, S. Adriouch, P2X7 on mouse T cells: one channel, many functions, Front Immunol. 6 (2015 May 19) 204, http://dx.doi.org/ 10.3389/fimmu.2015.00204. [3] A. De Flora, E. Zocchi, L. Guida, L. Franco, S. Bruzzone, Autocrine and paracrine calcium signaling by the CD38/NAD+/cyclic ADP-ribose system, Ann. N. Y. Acad. Sci. 1028 (2004 Dec) 176–191.
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Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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Review
Ca2 + microdomains, NAADP and type 1 ryanodine receptor in cell activation☆ Andreas H. Guse ⁎, Insa M.A. Wolf The Calcium Signalling Group, Department of Biochemistry and Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246 Hamburg, Germany
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Article history: Received 28 October 2015 Received in revised form 5 January 2016 Accepted 18 January 2016 Available online xxxx Keywords: NAADP Ryanodine receptor T cell Signal transduction
a b s t r a c t Nicotinic acid adenine dinucleotide phosphate (NAADP) is a Ca2+ mobilizing second messenger that belongs to the superfamily of regulatory adenine nucleotides. Though NAADP has been known since 20 years, several aspects of its metabolism and molecular mode of action are still under discussion. Though the importance of the type 1 ryanodine receptor was discovered and published already in 2002 Hohenegger et al. (2002 Oct 15) , recent data re-emphasize these original findings in pancreatic acinar cells and in T-lymphocytes. Here we review recent developments in NAADP formation and metabolism, putative target Ca2+ channels for NAADP with special emphasis on the type 1 ryanodine receptor, and NAADP binding proteins. The latter are basis for a unifying hypothesis for NAADP action. Finally, the role of NAADP in T cell Ca2+ signaling and activation is discussed. This article is part of a Special Issue entitled: Calcium and Cell Fate edited by Jacques Haiech, Claus Heizmann and Joachim Krebs. © 2016 Published by Elsevier B.V.
1. Regulatory adenine nucleotides and NAADP NAADP belongs to a superfamily of signaling molecules, the regulatory adenine nucleotides. These comprise the long known intracellular co-substrates adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide (NAD) and their metabolites (Fig. 1). Although the intracellular functions of ATP and NAD in energy metabolism have been known for decades, it only became evident in the past couple of years that ATP and NAD can be released from cells. ATP and its metabolites adenosine diphosphate, adenosine monophosphate and adenosine, generated by ectoenzymes CD39 and CD73, fulfill important paracrine signaling functions, especially regulating local inflammatory responses (Fig. 1; reviewed in [2]). In a similar manner, NAD, when released from cells, may serve on the one hand as substrate for ADPribosylation of target proteins (Fig. 1), e.g. the P2X7 purinergic receptor (reviewed in [2]). On the other hand NAD can be converted by CD38 in type II conformation to generate extracellular cyclic adenosine
Abbreviations: ATP, adenosine triphosphate; ADPR, adenosine diphosphoribose; cADPR, cyclic adenosine diphosphoribose; ER, endoplasmic reticulum; IP3, D-myoinositol 1,4,5-trisphosphate; IP3R, D-myo-inositol 1,4,5-trisphosphate receptor; NAADP, nicotinic acid adenine dinucleotide phosphate; NAADP-BP, NAADP binding protein; NAD(P), nicotinamide adenine dinucleotide (phosphate); NFAT, nuclear factor of T cells; RyR, ryanodine receptors; RyR1 (or 2, or 3), type 1 (or 2, or 3) ryanodine receptor; TRPML1, transient receptor potential cation channel, subtype mucolipin 1; TRPM2, transient receptor potential cation channel, subtype melastatin 2. ☆ This article is part of a Special Issue entitled: Calcium and Cell Fate edited by Jacques Haiech, Claus Heizmann and Joachim Krebs. ⁎ Corresponding author. E-mail address: [email protected] (A.H. Guse).
diphosphoribose (cADPR) and adenosine diphosphoribose (ADPR) (Fig. 1). The former acts as paracrine signaling molecule in several cell systems (reviewed in [3]). In addition, ATP and NAD can also be converted inside cells to second messenger molecules involved in the transmission of extracellular signals into the intracellular machinery to generate appropriate cellular responses. ATP can be converted to the second messenger 3′,5′-cyclic adenosine monophosphate (Fig. 1), while NAD serves as precursor of cADPR and ADPR. The intracellular conversion of NAD to ADPR and cADPR likely proceeds via CD38 in type III conformation, meaning that the N-terminus of CD38 is located within the cytosol (Fig. 1). ADPR may also be produced by degradation of poly-ADP-ribosylated proteins (reviewed in [4]). The synthetic pathway to NAADP is less clear and will be discussed below. In addition to these well studied messenger molecules, additional signaling metabolites of NAD have been described, e.g. 2′-phospho-cyclic adenosine diphosphoribose [5,6] and diadenosine homodinucleotide compounds P18 and P24 [7,8]. While 3′,5′-cyclic adenosine monophosphate activates protein kinase A, the NAD metabolites cADPR, ADPR and NAADP are all regulators of the free cytosolic Ca2+ concentration. ADPR, the main product of CD38, binds to the NudT9 homology domain to open the non-specific cation channel transient receptor potential, subtype melastatin 2 (TRPM2; [9]). cADPR evokes release of Ca2+ from the endoplasmic reticulum (ER) by opening of ryanodine receptors (RyR), likely via a specific binding protein [10,11]. In this review we will concentrate on NAADP (Figs. 1, 2), the most potent endogenous Ca2+ releasing molecule known to date. It is confirmed that NAADP is rapidly produced upon cell stimulation [12–15] and releases Ca2+ from endogenous Ca2+ stores. As will be specified
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Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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Fig. 1. Overview of extra- and intracellular regulatory adenine nucleotides. While ATP and NAD fulfill their classical roles in energy metabolism inside cells, they may be released from cells, e.g. at sites of inflammation. ATP may act on purinergic receptors and/or is converted by ecto-enzymes CD39 and CD73 via ADP and AMP to adenosine. Purinoceptors and adenosine receptors activate specific intracellular signaling that is not discussed in detail here. Extracellular NAD either serves as substrate for ADP-ribosylation (reviewed in [2]) or may be converted by ecto-enzyme CD38 (in type II conformation) to cADPR and ADPR. Work mainly carried out by De Flora and co-workers (reviewed in [3]) showed extracellular (paracrine) effects of cADPR and ADPR. Here, cADPR is taken up by certain cell types via nucleoside transporters and acts intracellularly on RyR, while ADPR appears to act via purinergic receptors. cAMP signaling, the canonical 2nd messenger pathway, is briefly displayed, too. The adenine nucleotide 2nd messengers cADPR and NAADP both release Ca2+ from intracellular stores; while ER/SR is accepted as target store for cADPR, different types of intracellular membrane compartments have been postulated as target store for NAADP, e.g. ER, nuclear membrane, acidic stores, or exocrine granules. Thus, the target store for Ca2+ releasing 2nd messengers is termed ‘Ca2+ stores’ here. The part dealing with NAADP is intended to highlight facts generally accepted: NAADP is rapidly formed inside the cell, but the precursor is still under debate. Further, it is accepted that NAADP likely does not bind to any channel directly, but rather acts via binding proteins. These NAADP-BP then may activate different ion channels located on ‘Ca2+ stores’.
Fig. 2. Definitive vs speculative aspects of NAADP signaling. The figure displays aspects of NAADP signaling that are generally accepted (‘definitive’; left side) vs aspects that are controversially discussed (‘in discussion’; right side). In summary, rapid formation of NAADP, its metabolism to 2′-phospho-ADPR or to NAAD, and its strong Ca2+ releasing activity are well acknowledged. In contrast, enzymes, organelles and channels involved in this process are less clear; the main controversial points are summarized in the box below ‘in discussion’.
Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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in the subsequent chapters, NAADP's metabolism and mechanism of action, e.g. nature of its target organelle and channel, have been controversially discussed in recent years. We will review recent developments and present hypotheses that may help to develop the field. 2. NAADP formation and metabolism All second messengers are formed enzymatically from inactive precursors. Since NAADP was discovered as impurity of NADP [16,17] and since its structure is almost identical to NAADP, conversion of NADP to NAADP was studied from the 1990s onward. Since NADP does not show any Ca2+ releasing activity, the general idea of NADP as the inactive precursor fits well. In fact, studies using NADP as substrate for NADglycohydrolase/ADP-ribosyl cyclase CD38 resulted in the discovery of the ‘base-exchange’ reaction [18]. This reaction in which nicotinamide in NADP is exchange by nicotinic acid added as second substrate is the only proven reaction to yield NAADP. However, the reaction conditions are somewhat critical since an acidic pH and a high concentration of nicotinic acid are required, conditions that are difficult to find in the cytosol of living cells (Fig. 2). Further, at least in some tissues and cells knockout of cd38 had no effect on endogenous NAADP, or resulted in even increased NAADP concentrations [19,20] indicating that CD38 might be involved in NAADP catabolism rather than in its formation (Fig. 2). Other possible reactions to NAADP, e.g. deamidation of NADP or phosphorylation of nicotinic acid adenine dinucleotide, have been postulated, but corresponding enzyme activities have not yet been detected (Fig. 2). In contrast to NAADP formation, degradation of NAADP proceeds to 2′-phospho-ADPR via CD38 [20], or by dephosphorylation to nicotinic acid adenine dinucleotide [21,22]. Candidates for the dephosphorylation reaction are a specific and Ca2+-dependent NAADP phosphatase [21] and alkaline phosphatase [22]. 3. Putative target Ca2+ channels for NAADP Since its discovery in 1995 there has been intense research with regard to the receptor for NAADP. Interestingly, a number of candidates have been introduced by different laboratories (Fig. 2), starting with type 2 and type 1 ryanodine receptor (RyR2, RyR1; [23], [1]). However, the discovery of the lysosome-related reserve granule of sea urchin egg as a NAADP-sensitive Ca2+ store [24] shifted the search more to channels potentially expressed in acidic stores. Such candidates comprise the two-pore channels type 1 and 2 (TPC1, TPC2; [25–27]), transient receptor potential channel type mucolipin 1 (TRP-ML1; [28], or TRPM2; [29]). In a very recent review we compared literature data for intracellular NAADP concentrations with published EC50 data for NAADP at these respective channels (reviewed in [30,31]). Collectively, these data suggest that TRPM2 and RyR2 are activated by NAADP at non-physiological concentrations. Moreover, in case of TRPM2 it was published recently that careful purification of the NAADP used in patch-clamp experiments abolished TRPM2 activation even at high NAADP concentrations [32]. Thus, contaminating ADPR in NAADP preparations may have been the reason for TRPM2 activation by NAADP observed previously [33]. TRPML1, TPC2 and RyR1 are activated in the physiological concentration range of NAADP (reviewed in [30,31]). It should be noted here that the ‘physiological concentration range’ of NAADP was determined by enzymatic cycling assays carried out in extracts produced from very high numbers of non-stimulated or stimulated cells [12–15]. Though results from these studies are similar in terms of absolute amplitude and kinetics, the following limitations exist: homogenizing and extracting large cells numbers is difficult to perform precisely at short stimulation periods, e.g. after single seconds. Thus, available kinetics in the range from 1 to 10 s must be regarded with caution. Moreover, sub-second kinetics for NAADP are not available at present. Further, since extracts are
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pooled from many cells, potential intracellular NAADP concentration gradients cannot be resolved by this method. In the same review we compared confirmatory and negatory papers regarding activation by NAADP ([30], Tab. 1). The data in those papers were obtained in different cell systems by different techniques or different animal models were employed. Unfortunately, these differences complicate direct comparison of primary data making clear judgments difficult. Thus, at least RyR1 and TPC1/2 remain as candidates for the NAADP sensitive channel(s) (Fig. 2). Since the potential role of TPCs in NAADP signaling has been reviewed recently in an excellent manner [34,35], in this review we will concentrate on RyR1. 4. Type 1 ryanodine receptor NAADP activation of native RyR1 from skeletal muscle fused into lipid planar bilayers significantly increased RyR1's open probability while the amplitude of channel opening was almost unchanged. The dynamic range of NAADP was between approx. 20 and 100 nM [1], concentrations compatible with endogenous NAADP concentrations in different cell types [12–15]. In contrast to most other studies on NAADP evoked Ca2+ signals, a bell-shaped concentration–response curve was not found in these partially purified RyR1 preparations [1] indicating loss of factors necessary for desensitization of the response. Further, to partially purified RyR1 from rabbit muscle, in other cell systems an involvement of RyR in NAADP evoked Ca2+ release was confirmed. In pancreatic acinar cells extracellular acetylcholine or intracellular infusion of D-myo-inositol 1,4,5-trisphosphate (IP3), cADPR or NAADP all induced repetitive Ca2+ spikes, all of which were sensitive to ryanodine [35]. Although the interpretation of these data contained a separate, unknown receptor for NAADP (not RyR), in a subsequent publication using isolated nuclei from pancreatic acinar cells, it was shown that the RyR blockers ryanodine or ruthenium red efficiently antagonized Ca2+ release by NAADP, while compounds interfering with acidic compartments, e.g. bafilomycin A1, brefeldin A, or nigericin, did not inhibit NAADP evoked Ca2 + release from the nuclear envelope [37]. These data resulted in a refinement of the previous model suggesting RyR to respond to both cADPR and NAADP; however, specific binding proteins were proposed for both second messengers that would mediate activation of RyR [37]. It is important to note that the NAADPsensitive nuclear Ca2+ store characterized by Gerasimenko and coworkers, ‘… is ATP dependent and thapsigargin sensitive, and is distinct from any acidic, endocytic or Golgi-type Ca2+ store’ [38]. Using permeabilized pancreatic acinar cells it was further shown that also acidic stores in the secretory granular region respond to NAADP and that this response was sensitive to ryanodine [39]. Very recent work in pancreatic acinar cells confirmed NAADP evoked Ca2+ release via RyR1 (and to a lower extent also via RyR3) located in zymogen granules and in the ER, and via TPC2 located in acidic stores [40]. The other cell system in which effects of NAADP on RyR were studied in detail is T-lymphocytes. In Jurkat T cells, a human T-lymphoma cell line often used in investigations of T cell activation, global Ca2+ signals evoked by NAADP microinjection were effectively blocked by RyR antagonist ruthenium red, but not by IP3 antagonist heparin [41]. Further, gene silencing of RyR in Jurkat T cells [42] efficiently diminished NAADP, but not IP3 mediated global Ca2+ signaling [41]. These data demonstrate that, at least for NAADP-evoked global Ca2+ signaling, RyR are required in the T cell. For pancreatic acinar cells a ‘two-pool’ model was hypothesized. According to this model NAADP triggers a small, short-lived Ca2+ signal, termed trigger Ca2+, which is then further amplified by IP3 receptors and/or RyR [36,43]. However, Langhorst et al. [41] did not specifically check for small, short-lived Ca2+ signals in Jurkat T cells lacking expression of RyR. Therefore, Dammermann & Guse [44] and Wolf et al. [45] showed in fast and very fast Ca2+ imaging studies that small, short-lived Ca2+ signals markedly decrease in Jurkat T cells lacking expression of RyR. Further, primary RyR1−/− mouse T cells showed largely diminished initial, short lived Ca2+ signals upon
Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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directed cell stimulation, e.g. upon contact to a bead coated with antiCD3 and anti-CD28 antibodies [45]. Important to note here that the temporal resolution in these experiments was approx. 25 ms [45]. Thus, evidence for trigger Ca2+ formed independently of RyR1, as hypothesized by Cancela and colleagues [36,43], was not yet obtained in T cells. If such RyR1-independent trigger Ca2+ exists, it must be an extremely short-lived, transient signal, at least in T cells. Collectively these data suggest that RyR, most likely RyR1, is essentially necessary for NAADP action, including formation of initial, short lived Ca2+ signals. In addition, further studies support a major role for RyR1 in NAADP signaling in T cells. Inhibition of lysosome function by the H+-ATPase inhibitor bafilomycin A1 did not affect NAADP effects in T cells, whereas the SERCA inhibitor thapsigargin at least partially blocked global Ca2 + signaling upon NAADP administration [46]. Further, channel opening of RyR1 by NAADP, as measured by binding of [3H]ryanodine to partially purified RyR1, was efficiently blocked by a novel synthetic NAADP antagonist, termed BZ194 [47]. Taken together, evidence from different cell systems suggests that NAADP activates RyR1. Whether this includes direct or indirect interaction remains to be determined.
In 2012 a radioactively labeled photoaffinity analogue of NAADP, [32P]5-N3-NAADP, was used to directly label NAADP-BP from different cell types [48–50]. Though labeling of one (or more) of the candidate channels was expected, in all cell systems analyzed, the NAADP-BP were small proteins found preferentially in the cytosol, but not in membrane fractions. Photoaffinity labeling of sea urchin egg homogenates showed a somewhat different pattern as compared to homogenates prepared from mammalian cell lines or tissues [48–50]. In the latter it was also shown that neither overexpression of TPC1 or TPC2 nor knockout of these channels significantly changed the labeling pattern [49]. This result suggests that the proteins specifically labeled by [32P]5-N3NAADP may represent NAADP-BP. However, up to now the molecular identity of these proteins was not published. Nevertheless, these findings prompted us to re-vitalize the original idea by Gerasimenko and colleagues as [37] as unifying hypothesis for NAADP action [51]. This hypothesis simply expands the number of channels that may be activated by the NAADP-BP from RyR, as suggested by Gerasimenko and colleagues [37], to TPCs and TRP-ML1. However, identification of the NAADP-BP is necessary to confirm or disprove this idea. 6. NAADP in T cell Ca2+ signaling
5. NAADP binding proteins — a unifying hypothesis for NAADP action Reviewing the data published regarding the NAADP sensitive cellular compartment and also the NAADP sensitive channel illustrates the controversial views and models. However, already in 2003 Gerasimenko and colleagues [37] hypothesized that NAADP may not directly bind to RyR, but may in the first step interact with a specific NAADP binding protein (NAADP-BP) which upon binding of NAADP is activated and subsequently activates RyR [37]. In the same publication, a similar model was proposed for cADPR [37].
For T cells there is evidence that NAADP is raised rapidly and transiently upon T cell receptor/CD3 complex stimulation with a peak at approx. 10 s (Fig. 3; [13]). If such formation is mimicked by microinjection of physiological concentrations of NAADP, local, RyR-dependent Ca2+ signals are observed within 20 ms [45]. Similarly, directed activation of primary T cells via localized T cell receptor/CD3 complexes very rapidly, e.g. in the millisecond range, evokes Ca2+ microdomains that depend on RyR1, but not TRPM2 expression [45]. Further, experiments in the absence of extracellular Ca2+ indicate involvement of a Ca2+ entry component in this early signaling process [45].
Fig. 3. Connection between short-lived local and long lasting global Ca2+ signaling in T-lymphocytes. T cell activation requires ligation of the T cell receptor/CD3 complex by the respective peptide ligand in MCH context. Recent data suggest involvement of NAADP and RyR1 in the first seconds of T cell activation [13,41,44]. Both act in concert to generate Ca2+ microdomains [45], possibly via NAADP-BP. This very rapid phase is followed by global Ca2+ signaling (tens of second to minutes). In this phase, further Ca2+ mobilizing 2nd messengers are formed, e.g. IP3 and cADPR, acting on their respective target channels, IP3R and RyR. Local Ca2+ signals generated by NAADP are believed to act as co-agonists at IP3R and RyR to amplify Ca2+ release. This in turn leads to store-operated Ca2+ entry via the Stim/Orai system resulting in further amplification of the Ca2+ signal of T cells.
Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014
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These findings raise the question whether the initial network of local Ca2+ microdomains influences later stages of T cell Ca2+ signaling and T cell activation. Experiments in rat myelin basic protein-specific T cells suggest that indeed NAADP-evoked initial Ca2+ microdomains determine the amplitude of subsequent global Ca2+ signaling. This was shown using the NAADP antagonist BZ194 that partially blocked global Ca2+ signaling and nuclear NFAT translocation as a major element of downstream signal transduction during activation of primary T cells [47]. Fig. 3 shows how the early, ‘millisecond to second’ period of local Ca2+ microdomains is coupled to the ‘second to minutes/hours’ period: the local Ca2+ microdomains act as co-agonists at both RyR and IP3R once these second messengers are produced. It might well be that local Ca2+ microdomains play a more important role in case of weak or medium activation of cADPR and/or IP3 formation. The medical implication of this co-activation of RyR and IP3R by Ca2+ ions stemming from NAADP-dependent initial local Ca2+ microdomains was shown in experimental autoimmune encephalomyelitis, an animal model for multiple sclerosis. Here NAADP antagonist BZ194 diminished accumulation of autoreactive T cells in the CNS and reduced reactivation of MBP-specific effector T cells at inflammatory sites. As a result, clinical symptoms of EAE were partially diminished [52]. In summary, the Ca2+ mobilizing second messenger NAADP and RyR1 are major players in initial, rapid Ca2+ microdomains, observed in the first milliseconds and lasting for approx. 10 to 20 s upon directed stimulation of the T cell receptor/CD3 complex. These Ca2+ microdomains are important as co-agonists to shape the global Ca2+ signal. The latter is composed of IP3- as well as cADPR-induced Ca2+ release followed by capacitative Ca2+ entry. Funding Work on adenine nucleotides in T cells was supported by the Deutsche Forschungsgemeinschaft (grant numbers GU 360/15-1 and 360/16-1, to A.H.G.), by the Forschungszentrum Medizintechnik Hamburg (to I.M.A.W.), by Förderfonds Medizin (FFM) of the University Medical Center Hamburg-Eppendorf (grant no. NWF 15/13 to I.M.A.W.), by the Hertie Foundation (grant number P1140086 to A.H.G.), and by the Landesforschungs-Förderung of the City of Hamburg (Research Group ReAd Me, project 1; to A.H.G. and I.M.A.W.). Competing interests The authors declare that they have no competing interests. Transparency document The Transparency document associated with this article can be found, in online version. Acknowledgments We are grateful to our present and past co-workers for their creative power and our collaborators for inspiring discussions and great mutual projects. Interest of the European Calcium Society in NAADP signaling is also gratefully acknowledged. References [1] M. Hohenegger, J. Suko, R. Gscheidlinger, H. Drobny, A. Zidar, Nicotinic acid–adenine dinucleotide phosphate activates the skeletal muscle ryanodine receptor, Biochem. J. 367 (Pt 2) (2002 Oct 15) 423-423. [2] B. Rissiek, F. Haag, O. Boyer, F. Koch-Nolte, S. Adriouch, P2X7 on mouse T cells: one channel, many functions, Front Immunol. 6 (2015 May 19) 204, http://dx.doi.org/ 10.3389/fimmu.2015.00204. [3] A. De Flora, E. Zocchi, L. Guida, L. Franco, S. Bruzzone, Autocrine and paracrine calcium signaling by the CD38/NAD+/cyclic ADP-ribose system, Ann. N. Y. Acad. Sci. 1028 (2004 Dec) 176–191.
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Please cite this article as: A.H. Guse, I.M.A. Wolf, Ca2+ microdomains, NAADP and type 1 ryanodine receptor in cell activation, Biochim. Biophys. Acta (2016), http://dx.doi.org/10.1016/j.bbamcr.2016.01.014