Tài liệu Báo cáo khoa học: Synchronization of Ca2+ oscillations: a capacitative (AC) electrical coupling model in neuroepithelium pptx

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Tài liệu Báo cáo khoa học: Synchronization of Ca2+ oscillations: a capacitative (AC) electrical coupling model in neuroepithelium pptx

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MINIREVIEW Synchronization of Ca 2+ oscillations: a capacitative (AC) electrical coupling model in neuroepithelium Masayuki Yamashita Department of Physiology I, Nara Medical University, Kashihara, Japan Structural organization of intracellular Ca 2+ stores and coupling modes of Ca 2+ increase Chemical coupling and DC electrical coupling The lumen of the endoplasmic reticulum (ER) is continuous with a space between the outer nuclear membrane (ONM) and inner nuclear membrane (INM) [1–3]. Intracellular Ca 2+ stores are formed within the ER lumen and the space between the ONM and the INM [1,2]. In cells with a centralized nucleus surrounded by the ER (Fig. 1A), intercellular commu- nication may be mediated by the release of a transmit- Keywords Ca 2+ oscillation; Ca 2+ store; neuronal development; synchronization; voltage fluctuation Correspondence M. Yamashita, Department of Physiology I, Nara Medical University, Shijo-cho 840, Kashihara 634-8521, Japan Fax: +81 744 29 0306 Tel: +81 744 29 8827 E-mail: yama@naramed-u.ac.jp (Received 23 March 2009, revised 2 October 2009, accepted 9 October 2009) doi:10.1111/j.1742-4658.2009.07439.x Increases in intracellular [Ca 2+ ] occur synchronously between cells in the neuroepithelium. If neuroepithelial cells were capable of generating action potentials synchronized by gap junctions (direct current electrical coupling), the influx of Ca 2+ through voltage-activated Ca 2+ channels would lead to a synchronous increase in intracellular [Ca 2+ ]. However, no action poten- tial is generated in neuroepithelial cells, and the [Ca 2+ ] increase is instead produced by the release of Ca 2+ from intracellular Ca 2+ stores. Recently, synchronous fluctuations in the membrane potential of Ca 2+ stores were recorded using an organelle-specific voltage-sensitive dye. On the basis of these recordings, a capacitative [alternating current (AC)] electrical cou- pling model for the synchronization of voltage fluctuations of Ca 2+ store potential was proposed [Yamashita M (2006) FEBS Lett 580, 4979–4983; Yamashita M (2008) FEBS J 275, 4022–4032]. Ca 2+ efflux from the Ca 2+ store and K + counterinflux into the store cause alternating voltage changes across the store membrane, and the voltage fluctuation induces ACs. In cases where the store membrane is closely apposed to the plasma mem- brane and the cells are tightly packed, which is true of neuroepithelial cells, the voltage fluctuation of the store membrane is synchronized between the cells by the AC currents through the series capacitance of these mem- branes. This article provides a short review of the model and its relation- ship to the structural organization of the Ca 2+ store. This is followed by a discussion of how the mode of synchronization of [Ca 2+ ] increase may change during central nervous system development and new molecular insights into the synchronicity of [Ca 2+ ] increase. Abbreviations AC, alternating current; BK channel, big K + channel; CNS, central nervous system; DC, direct current; DiOC 5 (3), 3,3¢-dipentyloxacarbocyanine iodide; ER, endoplasmic reticulum; I C , capacitative current; INM, inner nuclear membrane; Ins(1,4,5)P 3 , inositol 1,4,5-trisphosphate; mAChR, muscarinic acetylcholine receptor; ONM, outer nuclear membrane; Pyk2, proline-rich tyrosine kinase 2; RGC, retinal ganglion cell. FEBS Journal 277 (2010) 293–299 ª 2009 The Author Journal compilation ª 2009 FEBS 293 ter (e.g. ATP) and its receptors, which stimulate the release of Ca 2+ from intracellular Ca 2+ stores (Fig. 1B and Koizumi in this minireview series). This mode of coupling is referred to as chemical coupling. When gap junctions are present between adjacent cells, electrical coupling through gap junction channels may synchro- nize plasma membrane potentials, and Ca 2+ influx through voltage-activated Ca 2+ channels should lead to a synchronous increase in intracellular [Ca 2+ ] (Fig. 1B and Imtiaz et al. in this minireview series). This coupling mode is mediated by direct currents (DCs) through gap junction channels, and may be called DC electrical coupling. Alternatively, a second messenger molecule such as inositol 1,4,5-trisphosphate [Ins(1,4,5)P 3 ] and ⁄ or Ca 2+ ions may pass gap junction channels, and such pas- sive diffusion might lead to a synchronous increase in intracellular [Ca 2+ ]. However, the results of our stud- ies on the retinal neuroepithelium contradict this dif- fusion model and provide evidence for an alternative model. We have found that Ins(1,4,5)P 3 -mediated robust Ca 2+ increases induced by a supramaximal amount of an agonist do not synchronize, despite strong gap junctional coupling in the retinal neuroepi- thelium [4,5]. It has also been shown that synchro- nous Ca 2+ oscillations occur in newborn retinal ganglion cells (RGCs), which lose gap junctions [5]. On the basis of these findings, an alternative model to the passive diffusion of Ins(1,4,5)P 3 or Ca 2+ through gap junction channels is provided to explain the synchronization of Ca 2+ oscillation between these cells. AB CD Fig. 1. Structure of intracellular Ca 2+ stores and coupling modes of intracellular [Ca 2+ ] increase. (A) Cells in which the nucleus is located in the center of the cell and is surrounded by ER. Modified from Fig. 1 in [1] with permission. (B) Chemical coupling and DC electrical coupling. Stored Ca 2+ ions are released by the activation of receptors by a transmitter, such as ATP (chemical coupling). Depolarization (DV) synchro- nized by gap junctional coupling activates voltage-dependent Ca 2+ channels to cause synchronous Ca 2+ influx (DC electrical coupling). The Ca 2+ influx may cause Ca 2+ -induced Ca 2+ release to amplify the [Ca 2+ ] increase. (C) Neuroepithelial cells in which the ONM is closely apposed to the plasma membrane (PM) and the cells are tightly packed in the basal layer. Modified from Fig. 2 in [6]. (D) Capacitative (AC) electrical coupling. Efflux of Ca 2+ from Ca 2+ stores and counterinflux of K + cause fluctuations in the membrane potential of the Ca 2+ store, inducing ACs, which can pass the membranes as capacitative currents (I C ). The current loop is closed via cytoplasm and the PM or gap junc- tion (GJ), and also via the extracellular space, even in the absence of GJs. NPC, nuclear pore complex; Nu, nucleoplasm. Capacitative electrical coupling of Ca 2+ release M. Yamashita 294 FEBS Journal 277 (2010) 293–299 ª 2009 The Author Journal compilation ª 2009 FEBS Capacitative [alternating current (AC)] electrical coupling A novel mechanism of coupling between cells that does not depend on gap junctions or transmitters has been proposed, on the basis of the observation that the membrane potential of Ca 2+ stores oscillates synchro- nously between cells in the retinal neuroepithelium [4,6]. The voltage change exhibited a bistable alteration of fast rising and fast falling, which oscillated at the same frequency as the Ca 2+ oscillations [4]. The volt- age change was recorded using an organelle-specific, voltage-sensitive fluorescent dye, 3,3¢-dipentyloxacarbo- cyanine iodide [DiOC 5 (3)], and a highly sensitive video camera, which was connected to a high-speed confocal scanner (Nipkow disk type) [4]. When the voltage change was recorded using a photomultiplier, it was found, surprisingly, that the bistable voltage alteration consisted of periodic repeats of a burst of high fre- quency (> 200 Hz) voltage fluctuations [5]. The low time resolution of the video camera (15 images per sec- ond) did cover the high-frequency voltage fluctuation. To explain the synchronization of the store poten- tial, a capacitative (AC) electrical coupling model has been proposed, because the fast voltage change across the store membrane produces ACs, which can pass the plasma membrane capacitatively when the store mem- brane is in close proximity to the plasma membrane. The neuroepithelium consists of bipolar cells, in which the nuclei are positioned at different levels (pseudostr- atified columnar epithelium). In the retinal neuroepi- thelium, the ONM is closely apposed to the plasma membrane, and the cells are tightly packed in the basal layer (Fig. 1C). The voltage fluctuations of the Ca 2+ store will induce ACs, which can pass the series capaci- tance of the ONM and the plasma membrane as capa- citative currents (I C in Fig. 1D). The AC could synchronize the voltage fluctuations of the Ca 2+ store between the cells by capacitative (AC) electrical coupling [5]. The cytoplasm and the plasma membrane will make a closed-current loop of I C (Fig. 1D). Gap junctions may also contribute to the formation of the current loop. Another path for I C is the extracellular space, because I C can pass the plasma membrane capacita- tively. Thus, the current loop can be closed via the extracellular space and the plasma membrane. This may allow capacitative electrical coupling between neuroepithelial cells and newborn RGCs, which lack gap junctions (Fig. 1D). The electrical circuits of the current loop are presented in Doc. S2 of [5]. The fluctuation in the membrane potential of the Ca 2+ store may be due to the movement of Ca 2+ ions and the concomitant movement of other ions across the store membrane. The Ca 2+ efflux causes a negative change in the store potential towards the equilibrium potential of Ca 2+ (lumen-negative), which in turn induces a counterinflux of K + ions to depolarize the store potential, unless a [K + ] gradient is formed across the store membrane. Efflux of Cl ) or influx of Mg 2+ may also contribute to the depolarization of the store potential. The depolarization provides the driving force for Ca 2+ efflux, and the Ca 2+ release may also be enhanced by Ca 2+ -induced Ca 2+ release. Such fluctua- tions in the membrane potential of the Ca 2+ store would continue as a burst of high-frequency voltage fluctuations. In fact, an increase in intracellular [Ca 2+ ] coincides with an increase in DiOC 5 (3) fluorescence, which is caused by the burst of high-frequency voltage fluctuations [5]. It has been shown that voltage- and Ca 2+ -activated K + channels [big K + channels (BK channels)] are present in the membrane of the Ca 2+ store or the ONM [4,7]. The store BK channels are activated by a positive voltage change on the luminal side and by an increase in the luminal [Ca 2+ ] [4,7]. Because the clos- ing of the store BK channels attenuates Ca 2+ release [4], the Ca 2+ efflux will decrease when the luminal Ca 2+ levels decrease to the point at which the store BK channels close. The decrease in the luminal [Ca 2+ ] should also decrease the driving force for Ca 2+ efflux. The closing of the store BK channels increases the time constant for the store membrane to dampen the high- frequency voltage fluctuation of the Ca 2+ store, which will inhibit the synchronous burst of the voltage fluctu- ations of the Ca 2+ store [5]. When the Ca 2+ store is replenished with Ca 2+ ions by Ca 2+ pumps in the store membrane, and the store BK channels are reacti- vated, the voltage fluctuations of the Ca 2+ store will resume. Synchronous intracellular Ca 2+ increase in central nervous system (CNS) development Figure 2 illustrates the development of neural activities relative to the cellular events that occur during the course of CNS development. Neurons are born from neuroepithelial cells after they have exited the cell cycle. It has been shown that the Ca 2+ mobilization (Ca 2+ release from Ca 2+ stores) and the synchronous Ca 2+ oscillations are essential for neuroepithelial cell proliferation, for ventricular cell proliferation, and for cell cycle progression [8–17]. Thus, the synchronous Ca 2+ oscillations continue during neurogenesis. Cell death occurs naturally, leading to a reduction in the M. Yamashita Capacitative electrical coupling of Ca 2+ release FEBS Journal 277 (2010) 293–299 ª 2009 The Author Journal compilation ª 2009 FEBS 295 number of neurons by approximately one-half. The surviving neurons begin to generate action potentials. At this stage, the surviving neurons exhibit a charac- teristic synchronous burst spiking, which leads to tran- sient, synchronous increases in intracellular [Ca 2+ ] between the cells [18,19]. Although transmitters may play a role in modulating the bursting activity, chemi- cal transmission is unlikely to mediate the synchroniza- tion of spikes between the cells [18] (discussed later). It has been proposed that the synchronous increase in intracellular [Ca 2+ ] is essential for the fine-tuning of synaptic connections [18–20]. Glial cells are born following neurogenesis [21]. The glial cells provide elec- trical insulation to neurons, thereby making it possible for individual neurons to generate action potentials asynchronously, depending on the synaptic inputs that they receive. Thus, neural circuits are precisely formed, and each neuron can respond to appropriate natural stimuli. Biological significance of Ca 2+ synchronicity The above overview of the steps of CNS development raises questions regarding the molecular events that accompany the synchronous increase in intracellular [Ca 2+ ]. The following sections describe a new model and provide possible explanations regarding the bio- logical significance of the synchronous increases in intracellular [Ca 2+ ] between cells. Cell cycle-dependent Ca 2+ mobilization and cell–cell adhesion in the neuroepithelium Neuroepithelial cells undergo interkinetic nuclear migration along the apicobasal axis during cell cycle progression [21,22]. Stimulation of G-protein-coupled receptors causes the robust release of Ca 2+ from intra- cellular Ca 2+ stores in S-phase cells in the basal layer, whereas the ER and the nuclear envelope are broken down and the Ca 2+ mobilization declines in M-phase cells in the apical layer [12]. Spontaneous, synchronous Ca 2+ oscillations occur between S-phase neuroepit- helial cells and newborn RGCs [4,5]. The interkinetic cell shows a polarized bipolar struc- ture, whereas the M-phase cell is round. Fujita and Yasuda [23] have suggested that this morphological difference is due to a change in cell–cell adhesion that is mediated by cadherin–catenin complexes within each cell and by cadherin–cadherin interactions between the two cells. The interkinetic cells adhere to each other via cadherin–catenin complexes, and these complexes are anchored to F-actin (Fig. 3A). During M-phase, the cadherin–catenin complex dissociates, thereby dis- rupting cell–cell adhesion [23]. As a result, M-phase cells are round (Fig. 3B). These morphological and molecular changes point to a relationship between cell–cell adhesion and the synchronous Ca 2+ oscilla- tions, and suggest that cadherin–catenin complexes connect interkinetic cells with each other. Synchronous Ca 2+ oscillations occur in S-phase cells and newborn RGCs. In contrast, in M-phase cells, the Ca 2+ mobili- zation system, including the ER and the nuclear enve- lope, disappears and cadherin–catenin complexes are disassembled. It is proposed that cell–cell adhesion may be regulated by the synchronous increases in intracellular [Ca 2+ ], as described below. Synchronous increases in intracellular [Ca 2+ ] and disassembly of cadherin–catenin complexes The cytoplasmic domain of cadherin interacts with F-actin via b-catenin and a-catenin; b-catenin binds to cadherin and a-catenin, which in turn interacts with F-actin (Fig. 3A) [24]. Thus b-catenin plays a pivotal role in the regulation of cell–cell adhesion. The interac- tion of b-catenin with cadherin is regulated by tyrosine phosphorylation of b-catenin [25,26], which leads to disassembly of the cadherin–catenin complex. b-Cate- nin is directly tyrosine-phosphorylated by the nonre- ceptor protein tyrosine kinase proline-rich tyrosine kinase 2 (Pyk2) [26,27], or is indirectly tyrosine- phosphorylated by Src family kinase, which can be activated by Pyk2 [28]. It is likely that tyrosine phos- phorylation of b-catenin is triggered by Ca 2+ ions, because Pyk2 is activated by an increase in intracellu- lar [Ca 2+ ] [29,30]. If Pyk2 is transiently activated by an increase in intracellular [Ca 2+ ] to phosphorylate b-catenin in two Development of neural activities Responses to natural stimuli Spiking in individual neurons Synchronous Ca oscillation Proliferation Cell death Gliogenesis Synapse formation Neurogenesis Synchronous spikes with Ca 2+ transients Fig. 2. Changes in cellular activities during CNS development. Capacitative electrical coupling of Ca 2+ release M. Yamashita 296 FEBS Journal 277 (2010) 293–299 ª 2009 The Author Journal compilation ª 2009 FEBS adherent cells, the synchronous increase in [Ca 2+ ] between the cells could lead to a significant change in the homophilic binding of cadherins. The coactivation of Pyk2 ⁄ Src kinase between the cells would result in the dissociation of cadherins (Fig. 3A). However, if intracellular [Ca 2+ ] were increased in only one of the two adherent cells, the transient activation of Pyk2 would only occur in that cell. In this case, the b-cate- nin would be rapidly dephosphorylated by a phospha- tase in that cell without disrupting the homophilic binding of cadherins (Fig. 3C). If the synchronous increase in intracellular [Ca 2+ ] were responsible for the disruption of cell–cell adhe- sion, it would seem paradoxical that the synchronous Ca 2+ oscillations would occur in S-phase cells, but not in M-phase cells. S-phase cells, however, may gradu- ally disconnect themselves from the surrounding cells before M-phase, at which point almost all cadherin– catenin complexes are disassembled. After mitosis, the cells are reattached by cadherins, and the ER and the nuclear envelope are reorganized before S-phase. Newborn RGCs are also free from surface adhesion as they extend dendrites (Fig. 3B). In summary, a new model is put forward in which synchronous, transient increases in intracellular [Ca 2+ ] between cells can facilitate the disruption of cell–cell adhesion to destabilize cell surface contact. A reduction in the stability of cell–cell adhesion may be an output of a coincidence detector of cellular activi- ties. This decrease in cell-cell contact, in other words, the increase in freedom of cell surface, may play an essential role in the regulation of mitosis, dendrite extension, and synaptic plasticity. Capacitative (AC) electrical coupling in cortical development Synchronous Ca 2+ oscillations occur in the developing cortex even before synapse formation [8,31,32]. Ca 2+ oscillations in the retinal ventricular zone are driven by a muscarinic acetylcholine receptors (mAChRs), which cause the release of Ca 2+ from intracellular Ca 2+ stores [13,14,33]. The activation of mAChRs also induces strongly synchronized electrical activities in the subplate of the cortex of newborn mice [32]. The mAChR-driven electrical activity is blocked by tetro- dotoxin, suggesting that the activation of mAChRs results in the generation of action potentials [32]. How- ever, it remains unknown how the activation of mAChRs induces the synchronous firing activity. The capacitative (AC) coupling model may account for the generation of synchronous bursts of spikes. The AC currents caused by the voltage fluctuations of the Ca 2+ store may pass the plasma membrane capaci- tatively (Fig. 4A). This current may function as a noisy stimulus current to evoke action potentials (Fig. 4B). A C B Fig. 3. Hypothetical role for synchronous [Ca 2+ ] increases in cell–cell adhesion. (A) Simultaneous increases in intracellular [Ca 2+ ] in two adherent cells lead to disrup- tion of cell–cell adhesion through disassem- bly of cadherin–catenin complexes. (B) Changes in cell shape and the plasma mem- brane during mitosis and dendrite extension. (C) An increase in intracellular [Ca 2+ ] in only one of two adherent cells does not disrupt cell–cell adhesion. M. Yamashita Capacitative electrical coupling of Ca 2+ release FEBS Journal 277 (2010) 293–299 ª 2009 The Author Journal compilation ª 2009 FEBS 297 If the voltage fluctuations of the Ca 2+ store are syn- chronous between the cells, synchronous bursts of spikes could be generated. Such capacitative coupling may be the underlying mechanism that mediates the synchronization of spikes during the early stages of neurodevelopment. 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