大鼠海马可塑性改变对谷氨酸受体通道及其相关突触蛋白表达调控的研究
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摘要
长时程增强(long-term potentiation,LTP)是一种由简单的高频刺激兴奋性输入端引起的突触强度的持续性增强,在大鼠海马,来自CA3区锥体细胞的Schaffer侧枝与CAl区锥体细胞树突形成突触,刺激schaffer侧枝使CAl区锥体细胞任何树突层受刺激均可诱出LTP。常用兴奋性突触后场电位(fEPSP)来判定突触传递是否强化以及是否出现。LTP作为神经科学研究当中衡量突触可塑性的一个主要的电生理指标,是研究得最为广泛的活性依赖的突触可塑性的细胞水平的模型,也是研究学习记忆的细胞水平的模型,它反映了突触可塑性变化中的神经电生理活动方面的改变。现在认为,药物依赖和学习记忆之间存在着某种共同的分子机制,即参与正常学习记忆的机制也可能参与了成瘾形成和发展。海马作为脑内主要的学习器官,其CAl区的神经元作为海马信息输出的最主要和最直接的贡献者,可以通过下托投射到其它包括奖励中枢和前额叶等许多脑区。在成瘾和戒断过程中,也可能发生了海马可塑性的改变。
谷氨酸受体是海马内主要的兴奋性神经递质受体,兴奋性突触释放的谷氨酸主要与两种突触后离子型谷氨酸受体结合,它们是NMDA受体和AMPA受体。重组受体药理学和mRNA原位杂交研究提示NMDA受体可能有多种亚型,亚单位的不同组合方式和多样性是决定NMDA受体亚型多样性的重要基础。AMPA受体具有四个亚单位,为GluR1-4,在海马组织,AMPA受体的亚型主要为GluR1/2和GluR2/3,但在各核团,亚单位的分布也有差异。一般认为,NMDA受体在大多数通路中对诱导LTP是必需的,而AMPA受体则主要决定了LTP的表达和维持。神经元通过调节兴奋性突触后膜AMPA受体的数量和亚单位组成,可以改变兴奋性突触的活性和传递效能,因此,AMPA受体的膜转运也被认为是突触可塑性调节的重要环节。在突触上,NMDA受体以多蛋白复合物形式存在并起作用的,其中包括神经递质受体、细胞黏附蛋白、细胞骨架蛋白、支架蛋白、信号分子等,这种NMDA受体与多种信号通路在同一复合物中的共存是NMDA受体在突触可塑性、学习记忆中起重要作用的结构基础。受体在突触上
Physiological activity-dependent long-term changes in synaptic transmission, as long-term potentiation (LTP) are thought to be the substrate of learning and memory. As a form of neuronal plasticity, LTP may form the biological basis for some kinds of memory, reflecting change in the neural electrophysiological activation. LTP, as a measure of experience- or activity-dependent synaptic plasticity, is also the leading experimental model for the synaptic changes underlying brain function alterations, and the currently known cellular and molecular mechanisms underlying the compulsive seeking and taking of drugs resemble those of learning and memory.LTP in hippocampal CA1 area, evoked by high-frequency stimulation (HFS), is mediated by two major postsynaptic ionotropic glutamate receptor types, α-amino-3-hydroxyl-5-methyl-4-isoxazole propionate receptors (AMPARs) and N-methyl-D-aspartate receptors (NMDARs). NR1 and NR2A-D subunits assemble functional NMDARs, in which NR1 is essential and each of the NR2 subunits imparts different characteristics on functional NMDARs. AMPA receptors are composed of GluR1-4 subunits. In hippocampus, there are mainly two AMPA receptor subtypes, GluR1/2 and GluR2/3. A specific set of molecules including glutamate receptors is targeted at excitatory synapses in the brain, where NMDA receptors are physically associated with both scaffolding proteins and signal transduction elements such as the alpha subunit of Ca~(2+)/calmodulin-dependent protein kinase II (CaMKIIα), and each subunit of AMPA receptors, through their C-terminal tails, interacts with specific cytoplasmic proteins, suggested to play important roles in controlling the trafficking of AMPARs and/or their stabilization at synapses, which involved in enhanced excitatory transmission during LTP. Receptor subunit composition and their interaction with cytoplasmic proteins constitute different pathways regulating synaptic plasticity. Thus, the synaptic expression of the glutamate receptors regulated by the protein-protein interaction with other synaptic proteins has been proposed as a cellular mechanism involved in synaptic plasticity as well as learning and memory. The alterations in receptors' number, class, interaction with associated proteins and
downstream signaling pathway can also represent changes of the neural chemical substance activation regulated by synaptic plasticity.Therefore, in order to further understand hippocampal synaptic plasticity from the neural electrophysiological and chemical aspects, we performed the following study on expression alternation of glutamate receptor channels and associated synaptic proteins regulated by hippocampal plasticity. Firstly, we examined the LTP induction and the concomitant expression alterations of synaptic proteins induced by high-frequency stimulation. Secondly, we studied whether and how hippocampal synaptic plasticity changed during morphine addiction and withdrawal, a complicated, activity-dependent animal model.Results1. We recorded field EPSPs from the CA1 stratum radiatum of the hippocampus in response to stimulation of the schaffer collateral-commissural pathway. Synaptic potentiation was measured after a 40 min baseline period and persisted for at least 3 h. We examined the differences in LTP induction in CA1 area between experimental rats with or without pre-application of non-competitive NR2B antagonist Ro25-6981, competitive NMDA receptor antagonist AP-5 and noncompetitive NMDA receptor channel blocker MK-801. We found synaptic potentiation 170-180 min after LTP induction were completely abolished by pretreatment with either AP-5 or MK-801, but not Ro25-6981. Therefore, we provide the first evidence from in vivo that NMDA receptor-mediated LTP evoked at hippocampal CA1 region induced by high-frequency stimulation of the Schaffer collateral-commissural pathway in vivo is not dependent on NMDAR subunit NR2B.2. Protein enrichments in synaptosomes indicates its synaptic localization. Synaptosomes isolated by sucrose density gradient ultracentrirage. Homogenates and synaptosomes was prepared individually from control, sham (40 min after baseline recording at 0.033 Hz) and tetanized hippocampa 30 min and 180 min after LTP induction in the presence or absence of pre-treatment with non-competitive NR2B antagonist Ro25-6981, and 180 min post-HFS after pre-treatment with selective
NMDA receptor antagonist AP-5 or noncompetitive NMDA receptor channel blocker MK-801. Applying semi-quantitative immunoblotting, we found that in the whole tetanized hippocampus, synaptic expression of the NMDA and AMPA receptor subunits (NR1, NR2A, GluRl) and their associated partners, e.g. synaptic associated protein 97, postsynaptic density protein 95, a subunit of Ca2+/calmodulin-dependent protein kinase II (CaMKIIa), neuronal nitricoxide synthase, increased 180 min post-HFS but not after short-term potentiation (30 min post-HFS). After LTP blockade with AP-5 and MK-801, selective upregulations were prevented, indicating that increase in synaptic expression of these proteins was LTP-dependent. Substantial evidence indicates that CaMKII has a pivotal role in LTP. CaMKII interacts with and modulates the functionality of several plasticity-relevant targets, including the AMPA receptors. Here we found that phosphorylation of CaMKIIa at thr286 and GluRl at ser831 were increased 30 min post-HFS and blocked by NMDA receptor antagonists (AP-5 and MK-801).3. hi sham group and controls, these activity-dependent alterations were not observed. The expression of several other synaptic proteins (NR2B, GluR2/3, N-ethylmaleimide sensitive factor) was not affected by LTP induction. Interestingly, after blocking NR2B with Ro25-6981, the expression pattern was identical with normal LTP, except that synaptic expression of CaMKIIa remained almost unchanged 30 min and 180 min post-HFS with the pretreatment of Ro25-6981, suggesting that NR2B blockade miaght prevent synaptic CaMKIIa recruitment. In hippocampal homogenates, the level of these proteins remained unchanged.4. We recorded long-term potentiation in hippocampal schaffer collateral-commissural pathway in vivo in rats after withdrawn 2h, 18h, 4d, 7d and 20d, respectively. We found that through the withdrawal period, hippocampal synaptic plasticity displayed dynamic changes and interestingly, the greatest LTP in the CA1 area of the hippocampus and lower frequencies of LTP induction occurred on day four after withdrawal. Since it has been demonstrated that NR2A-/ NR2B-containing NMDA receptors govern the direction of synaptic plasticity, we then detected
immunoreactivity of NMDA receptor subunits NR2A and NR2B in two subcellular fractions, membrane and synaptosomes, prepared from rats after withdrawn 2h, 18h, 4d, 7d and 20d, respectively. We observed that NR2B subunit expression changes dynamicly and displayed a lowest level on day four after withdrawal, while the NR2A subunit remained at low levels of expression during withdrawal.5. Here, we have examined the expression of GluRl and GluR2/3 at hippocampal membrane and synaptosome fractions following repeated morphine exposure and subsequent morphine withdrawal. Repeated morphine exposure for 13 d increased GluRl and GluR2/3 at synaptosome but not at membrane fraction. Interestingly, CaMKIIa, known able to regulate the functions of AMPA receptors, was decreased at synaptosome but not at membrane fraction;pCaMKIIa, the phosphorylated form of CaMKIIa, was increased at both fractions. Following opiate withdrawal, however, GluRl was generally reduced while GluR2/3 was prominently increased at both fractions;pCaMKIIa was largely decreased immediately but remarkably increased in later phase of morphine withdrawal at both fractions.6. Importantly, the opiate withdrawal-increased GluR2/3 was depended on the glucocorticoid receptors and hippocampal NMDA receptors, because it was prevented by the glucocorticoid receptor antagonist RU38486, or intrahippocampal injection of the NMDA receptor antagonist AP-5 or the antagonist to NR2B-containing NMDA receptors, Ro25-6981. These findings indicate that opiate withdrawal induces dynamic expressions of GluRl and GluR2/3 subunit of AMPA receptors in hippocampus, possibly revealing an adaptive process of the hippocampal functions following opiate withdrawal.Conclusions1. NMDAR-mediated but not NR2B-dependent LTP in CA1 region in vivo mainly affects the synaptic expression of glutamate receptor subunits and associated proteins in the whole hippocampus. The alteration of molecular aspects can play a role in regulating the long-lasting synaptic modification in hippocampal LTP in vivo.
The long term potentiation phenomenon occurs in hippocampus and use multiple mechanisms, such as changes in neurotransmitter release, modulation of transmitter receptors, alterations in synaptic structure, and regulation of gene expression and protein synthesis, as well as protein modification after translation.2. The experience- or activity-dependent changes in opiate addiction affect the degree or direction of synaptic plasticity. Dynamic changes of synaptic structure and function occurring during withdrawal, reflected by neural electrophysiological activation and neural chemical activation, may contribute to the dynamic alterations of hippocampal synaptic plasticity. Adaptive changes in brain areas following drug withdrawal are believed to contribute to drug seeking and relapse.
谷氨酸受体是海马内主要的兴奋性神经递质受体,兴奋性突触释放的谷氨酸主要与两种突触后离子型谷氨酸受体结合,它们是NMDA受体和AMPA受体。重组受体药理学和mRNA原位杂交研究提示NMDA受体可能有多种亚型,亚单位的不同组合方式和多样性是决定NMDA受体亚型多样性的重要基础。AMPA受体具有四个亚单位,为GluR1-4,在海马组织,AMPA受体的亚型主要为GluR1/2和GluR2/3,但在各核团,亚单位的分布也有差异。一般认为,NMDA受体在大多数通路中对诱导LTP是必需的,而AMPA受体则主要决定了LTP的表达和维持。神经元通过调节兴奋性突触后膜AMPA受体的数量和亚单位组成,可以改变兴奋性突触的活性和传递效能,因此,AMPA受体的膜转运也被认为是突触可塑性调节的重要环节。在突触上,NMDA受体以多蛋白复合物形式存在并起作用的,其中包括神经递质受体、细胞黏附蛋白、细胞骨架蛋白、支架蛋白、信号分子等,这种NMDA受体与多种信号通路在同一复合物中的共存是NMDA受体在突触可塑性、学习记忆中起重要作用的结构基础。受体在突触上
Physiological activity-dependent long-term changes in synaptic transmission, as long-term potentiation (LTP) are thought to be the substrate of learning and memory. As a form of neuronal plasticity, LTP may form the biological basis for some kinds of memory, reflecting change in the neural electrophysiological activation. LTP, as a measure of experience- or activity-dependent synaptic plasticity, is also the leading experimental model for the synaptic changes underlying brain function alterations, and the currently known cellular and molecular mechanisms underlying the compulsive seeking and taking of drugs resemble those of learning and memory.LTP in hippocampal CA1 area, evoked by high-frequency stimulation (HFS), is mediated by two major postsynaptic ionotropic glutamate receptor types, α-amino-3-hydroxyl-5-methyl-4-isoxazole propionate receptors (AMPARs) and N-methyl-D-aspartate receptors (NMDARs). NR1 and NR2A-D subunits assemble functional NMDARs, in which NR1 is essential and each of the NR2 subunits imparts different characteristics on functional NMDARs. AMPA receptors are composed of GluR1-4 subunits. In hippocampus, there are mainly two AMPA receptor subtypes, GluR1/2 and GluR2/3. A specific set of molecules including glutamate receptors is targeted at excitatory synapses in the brain, where NMDA receptors are physically associated with both scaffolding proteins and signal transduction elements such as the alpha subunit of Ca~(2+)/calmodulin-dependent protein kinase II (CaMKIIα), and each subunit of AMPA receptors, through their C-terminal tails, interacts with specific cytoplasmic proteins, suggested to play important roles in controlling the trafficking of AMPARs and/or their stabilization at synapses, which involved in enhanced excitatory transmission during LTP. Receptor subunit composition and their interaction with cytoplasmic proteins constitute different pathways regulating synaptic plasticity. Thus, the synaptic expression of the glutamate receptors regulated by the protein-protein interaction with other synaptic proteins has been proposed as a cellular mechanism involved in synaptic plasticity as well as learning and memory. The alterations in receptors' number, class, interaction with associated proteins and
downstream signaling pathway can also represent changes of the neural chemical substance activation regulated by synaptic plasticity.Therefore, in order to further understand hippocampal synaptic plasticity from the neural electrophysiological and chemical aspects, we performed the following study on expression alternation of glutamate receptor channels and associated synaptic proteins regulated by hippocampal plasticity. Firstly, we examined the LTP induction and the concomitant expression alterations of synaptic proteins induced by high-frequency stimulation. Secondly, we studied whether and how hippocampal synaptic plasticity changed during morphine addiction and withdrawal, a complicated, activity-dependent animal model.Results1. We recorded field EPSPs from the CA1 stratum radiatum of the hippocampus in response to stimulation of the schaffer collateral-commissural pathway. Synaptic potentiation was measured after a 40 min baseline period and persisted for at least 3 h. We examined the differences in LTP induction in CA1 area between experimental rats with or without pre-application of non-competitive NR2B antagonist Ro25-6981, competitive NMDA receptor antagonist AP-5 and noncompetitive NMDA receptor channel blocker MK-801. We found synaptic potentiation 170-180 min after LTP induction were completely abolished by pretreatment with either AP-5 or MK-801, but not Ro25-6981. Therefore, we provide the first evidence from in vivo that NMDA receptor-mediated LTP evoked at hippocampal CA1 region induced by high-frequency stimulation of the Schaffer collateral-commissural pathway in vivo is not dependent on NMDAR subunit NR2B.2. Protein enrichments in synaptosomes indicates its synaptic localization. Synaptosomes isolated by sucrose density gradient ultracentrirage. Homogenates and synaptosomes was prepared individually from control, sham (40 min after baseline recording at 0.033 Hz) and tetanized hippocampa 30 min and 180 min after LTP induction in the presence or absence of pre-treatment with non-competitive NR2B antagonist Ro25-6981, and 180 min post-HFS after pre-treatment with selective
NMDA receptor antagonist AP-5 or noncompetitive NMDA receptor channel blocker MK-801. Applying semi-quantitative immunoblotting, we found that in the whole tetanized hippocampus, synaptic expression of the NMDA and AMPA receptor subunits (NR1, NR2A, GluRl) and their associated partners, e.g. synaptic associated protein 97, postsynaptic density protein 95, a subunit of Ca2+/calmodulin-dependent protein kinase II (CaMKIIa), neuronal nitricoxide synthase, increased 180 min post-HFS but not after short-term potentiation (30 min post-HFS). After LTP blockade with AP-5 and MK-801, selective upregulations were prevented, indicating that increase in synaptic expression of these proteins was LTP-dependent. Substantial evidence indicates that CaMKII has a pivotal role in LTP. CaMKII interacts with and modulates the functionality of several plasticity-relevant targets, including the AMPA receptors. Here we found that phosphorylation of CaMKIIa at thr286 and GluRl at ser831 were increased 30 min post-HFS and blocked by NMDA receptor antagonists (AP-5 and MK-801).3. hi sham group and controls, these activity-dependent alterations were not observed. The expression of several other synaptic proteins (NR2B, GluR2/3, N-ethylmaleimide sensitive factor) was not affected by LTP induction. Interestingly, after blocking NR2B with Ro25-6981, the expression pattern was identical with normal LTP, except that synaptic expression of CaMKIIa remained almost unchanged 30 min and 180 min post-HFS with the pretreatment of Ro25-6981, suggesting that NR2B blockade miaght prevent synaptic CaMKIIa recruitment. In hippocampal homogenates, the level of these proteins remained unchanged.4. We recorded long-term potentiation in hippocampal schaffer collateral-commissural pathway in vivo in rats after withdrawn 2h, 18h, 4d, 7d and 20d, respectively. We found that through the withdrawal period, hippocampal synaptic plasticity displayed dynamic changes and interestingly, the greatest LTP in the CA1 area of the hippocampus and lower frequencies of LTP induction occurred on day four after withdrawal. Since it has been demonstrated that NR2A-/ NR2B-containing NMDA receptors govern the direction of synaptic plasticity, we then detected
immunoreactivity of NMDA receptor subunits NR2A and NR2B in two subcellular fractions, membrane and synaptosomes, prepared from rats after withdrawn 2h, 18h, 4d, 7d and 20d, respectively. We observed that NR2B subunit expression changes dynamicly and displayed a lowest level on day four after withdrawal, while the NR2A subunit remained at low levels of expression during withdrawal.5. Here, we have examined the expression of GluRl and GluR2/3 at hippocampal membrane and synaptosome fractions following repeated morphine exposure and subsequent morphine withdrawal. Repeated morphine exposure for 13 d increased GluRl and GluR2/3 at synaptosome but not at membrane fraction. Interestingly, CaMKIIa, known able to regulate the functions of AMPA receptors, was decreased at synaptosome but not at membrane fraction;pCaMKIIa, the phosphorylated form of CaMKIIa, was increased at both fractions. Following opiate withdrawal, however, GluRl was generally reduced while GluR2/3 was prominently increased at both fractions;pCaMKIIa was largely decreased immediately but remarkably increased in later phase of morphine withdrawal at both fractions.6. Importantly, the opiate withdrawal-increased GluR2/3 was depended on the glucocorticoid receptors and hippocampal NMDA receptors, because it was prevented by the glucocorticoid receptor antagonist RU38486, or intrahippocampal injection of the NMDA receptor antagonist AP-5 or the antagonist to NR2B-containing NMDA receptors, Ro25-6981. These findings indicate that opiate withdrawal induces dynamic expressions of GluRl and GluR2/3 subunit of AMPA receptors in hippocampus, possibly revealing an adaptive process of the hippocampal functions following opiate withdrawal.Conclusions1. NMDAR-mediated but not NR2B-dependent LTP in CA1 region in vivo mainly affects the synaptic expression of glutamate receptor subunits and associated proteins in the whole hippocampus. The alteration of molecular aspects can play a role in regulating the long-lasting synaptic modification in hippocampal LTP in vivo.
The long term potentiation phenomenon occurs in hippocampus and use multiple mechanisms, such as changes in neurotransmitter release, modulation of transmitter receptors, alterations in synaptic structure, and regulation of gene expression and protein synthesis, as well as protein modification after translation.2. The experience- or activity-dependent changes in opiate addiction affect the degree or direction of synaptic plasticity. Dynamic changes of synaptic structure and function occurring during withdrawal, reflected by neural electrophysiological activation and neural chemical activation, may contribute to the dynamic alterations of hippocampal synaptic plasticity. Adaptive changes in brain areas following drug withdrawal are believed to contribute to drug seeking and relapse.
引文
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