慢性束缚应激对大鼠行为和中枢AMPA受体的影响及逍遥散的调节作用
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摘要
应激是机体在受到各种应激原剌激时,体内出现的以交感神经兴奋和垂体-肾上腺皮质分泌增多为主的一系列神经内分泌反应,它对个体的存活具有十分重要的意义。对于适度的应激,哺乳动物可以通过行为及内分泌方面的改变以维持内环境稳态,其中,下丘脑-垂体-肾上腺(HPA)轴起着至关重要的作用。但过度的尤其是慢性应激会导致不同程度的生理、心理障碍,甚至引起躯体疾病,可视为是一种由机体对倾向于干扰内环境稳态的外部力量和异常条件的反应引起的病理过程。由于慢性应激涉及人体多个系统,在不同应激原、不同个体、不同环境下,可能导致的结果也不同,给预防和治疗慢性应激性疾病造成了困难,而中医药的整体观念、辨证论治、个体化诊疗等理念在这方面显示出更大的优越性。本课题为国家自然科学基金(NO.30672578)资助课题,从慢性应激反应的中枢机制与逍遥散对其的作用机制两个方面进行了实验研究。
实验研究:
哺乳动物脑中大部分兴奋性信号都发生在以谷氨酸为神经递质的突触。谷氨酸是中枢神经系统(CNS)中的主要兴奋性神经递质,有两种受体,代谢型谷氨酸受体和离子型谷氨酸受体。离子型谷氨酸受体根据药理学、分子和电生理学特性又被分成三种:α-氨基羟甲基恶唑丙酸(AMPA)受体、红藻氨酸(KA)受体和N-甲基-D-天(门)冬氨酸(NMDA)受体。AMPA受体是参与中枢神经系统中快速兴奋性突触传递的主要分子单位。谷氨酸与突触后的AMPA型谷氨酸受体结合后诱发去极化,导致神经元兴奋。这一AMPA受体介导的神经传递促成大脑的瞬时到瞬时活性,包括认知反应和动作。而且,突触上AMPA受体功能的改变也促成了作为学习和记忆的基础的可塑性。GRIP与非磷酸化的PDZ基序结合可能将含有GluR2的受体锚定在突触上,Stargazin在AMPA受体膜表面靶向性调控中起作用,其PDZ结合基序磷酸化是突触AMPA受体浓度和突触强度的调控器,c-fos等即刻早期基因(IEG)成员被认为是神经细胞功能状态的示踪标志。因此本课题选择了AMPA受体的两个亚基GluR1、GluR2,两个相关蛋白GRIP1、Stargazin,IEG成员c-fos作为研究对象,通过对慢性束缚应激大鼠行为改变的观察,运用ELISA、免疫组织化学及RT-PCR等方法,从内分泌、蛋白和基因水平,观察了逍遥散对慢性束缚应激状态下大鼠行为、应激相关激素、AMPA受体的调节作用,探讨慢性应激反应和慢性应激损害的中枢机制及逍遥散对其的调节功能。主要结果如下:
1.动物行为的变化:束缚21天后,动物出现类似肝郁脾虚的不良表现,逍遥散对其有改善作用。慢性束缚应激状态下模型组大鼠在三周实验过程中体重增长量明显减少。在旷场实验第1天模型组大鼠的正中格停留时间、总穿格数明显增多;第21天模型组大鼠的正中格停留时间明显增多、总穿格数、站立次数和修饰次数明显减少。在高架十字迷宫实验第14天模型组大鼠进入开放臂的次数和比例、进入开放臂的时间和比例、进入开放和封闭臂总次数以及向下探究次数均明显降低。在第21天Y迷宫实验模型组大鼠的错误反应次数、全天总反应时间减少,正确反应率增加。逍遥散对体重、旷场和高架十字迷宫各项指标的改善作用明显,而对Y迷宫实验未表现出明显的调节作用。
2.ELISA检测结果:21天束缚应激状态下,大鼠血浆ACTH和血清CORT均升高,但CORT升高有统计学意义,而逍遥散对其有明显的向正常水平的调节作用。
3.免疫组织化学结果:21天束缚应激使模型组CA1、DG、BLA区的c-fos阳性细胞数增多;而模型组的GluR1在CA1和DG区表达增多;GluR2在CA1、CA3和DG区表达下降;GluR1和GluR2在BLA区均无明显变化。逍遥散可下调c-fos阳性细胞数,下调GluR1阳性细胞及免疫阳性物表达,上调GluR2阳性细胞数及免疫阳性物表达。
4.RT-PCR结果:21天束缚应激状态下,模型组GRIP1和Stargazin mRNA在CA1区表达下降;但在CA3、DG区和杏仁核的变化无统计学意义。逍遥散可上调GRIP1和Stargazin mRNA的表达。
以上结果提示: (1)在相同慢性应激刺激下,大鼠不同的行为学检测方法可能结果不同;(2)慢性束缚应激状态下,AMPA受体亚基GluR1和GluR2在海马的表达趋势不同;(3)海马和杏仁核在慢性束缚应激反应中的作用不一致;(4)海马CA1区可能是慢性束缚应激影响突触可塑性的最敏感部位;(5)逍遥散的调节呈现出区域选择性、时相性和双向调节作用。
Stress is a series of neuroendocrine responses which is marked with sympathetic nerves excitement and increase of pituitary -adrenal gland cortex secretion when organisms is expose to stressor stimulation, it’s very important for individual survival. Mammals respond to appropriate stress with characteristic changes in their behaviour as well as in autonomic and neuroendocrine parameters aimed at reinstating their disturbed homeostasis. Among such so-called coping strategies, alterations of the hypothalamic–pituitary–adrenal (HPA) axis play a crucial role. However, excessive, especially chronic stress, causes physical, psychological disorders in vary degrees, and even causes body diseases, can be regarded as a pathological process resulting from the reaction of the body to external forces and abnormal conditions that tend to disturb the organism's homeostasis. Since multiple systems relate to chronic stress, and different stressor, different individuals and different circumstances might lead to different results, it’s so difficult for prevention and treatment to chronic stress diseases, whereas Chinese medicine, which with a concept of whole adjustment, treatment based on syndrome differentiation and individualized diagnosis, has shown greater superiority. The present project was supported by National Natural Science Foundation of China (NO.30672578), and we focus on the experimental study on the central neural system mechanisms of chronic stress response and the role of regulative function of Xiao yao san in chronic stress response.
Experimental study
Most excitatory signalling in mammalian brain occurs at synapses that use glutamate as a neurotransmitter. Glutamate is the major excitatory neurotransmitter in the central nervous system (CNS), and is the agonist of two distinct categories of glutamate receptors, metabotropic glutamate receptors and ionotropic glutamate receptors. Ionotropic glutamate receptors have been divided in three classes, according to their pharmacological, molecular, and electrophysiological properties: alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA), kainite (KA), and N-methyl-D-aspartate (NMDA) receptors. The AMPA receptors are the principal molecular units for fast excitatory synaptic transmission in the central nervous system. Glutamate binding to postsynaptic AMPA-type glutamate receptors induces depolarizations that cause neuronal firing. This AMPA receptor-mediated neurotransmission contributes to the brain’s moment-to-moment activities, including cognitive responses and motor actions. Furthermore, changes in AMPA receptor function at synapses contribute to the plasticity that underlies learning and memory. GRIP binding to the unphosphorylated PDZ motif is proposed to anchor GluR2-containing receptors at synapses, The last four amino acids of stargazin bind to the PDZ domains of a number of synaptic scaffolding proteins, this PDZ interaction mediates synaptic targeting of surface receptors, phosphorylation of the PDZ-binding motif of stargazin is a regulator of synaptic levels of AMPA receptors and synaptic strength. C-fos is a member of immediate early genes (IEG), which belong to a class of genes that be regarded as tracing marker of neurocyte function.
Therefore we chose GluR1, GluR2, two subunit of AMPA receptor, two proteins interacting with AMPA receptor subunits, GRIP1 ((glutamate receptor-interacting protein 1) and Stargazin (voltage-dependent calciumchannel gamma-2 subunit,Cacng2) and c-fos as the research targets, chronic restraint as chronic stress model, using ELISA, immunohistochemistry and RT-PCR methods, to observe Xiaoyaosan’s influence on rats’behaviors, stress related hormones as well as AMPA receptors and its’interacting proteins mRNA expression, and to investigate the central nervous mechanisms and the role of regulative function of Xiao yao san to chronic stress responses and chronic stress impairments. The results were as the following.
Behavioral changes: After 21 days immobilization stress, the rats displayed unhealthy changes, Xiaoyaosan could improve the unhealthy statement. The body weight increase of the rats in model group decreased significantly. At the first day of open-field test, the central grille time, total cross number of the rats in model group increased significantly, at the 21st day, the central grille time increased significantly, but the total cross number, stand number and modify number decreased significantly. At the 14th day of elevated plus-maze test, the open arm entry (OE) and OE%, open arm time (OT) and OT%, open and close arm entry and head dipping of the rats in model group decreased significantly. At the 21st day in Y-maze test, the error number, total reaction time of the rats in model group decreased, with significant increased correct reaction rate. Xiao yao san showed significant improvement to body weight, open-field test and elevated plus-maze test, whereas without significant effect to Y-maze test.
ELISA results: In immobilization stress 21 days rats, the concentration of serum CORT increased, with statistical significance, Xiao yao san could regulate it towards normal level. Immunohistochemistry findings: In immobilization stress 21 days rats, the number of c-fos positive cells increased in CA1, CA3 region of hippocampus and basolateral amygdale (BLA); the number of GluR1 positive cells and immunoreaction products increased in CA1 and DG region of hippocampus; the number of GluR2-positive cells decreased in CA3 and DG region of hippocampus, so did the immunoreaction products in CA1, CA3 and DG region of hippocampus. In BLA, neither GluR1 nor GluR2 expression changes with statistical significance. Xiao yao san could decrease the number of c-fos positive cells in hippocampus and BLA as well as GluR1 positive cells and immunoreaction products in hippocampus, and could increase the number of GluR2 positive cells and immunoreaction products in hippocampus.
RT-PCR results: In immobilization stress 21 days rats, both of the mRNA expression of GRIP1 and Stargazin decreased in CA1 region of hippocampus, whereas without statistical significant changes in CA3, DG region of hippocampus and BLA. Xiao yao san could increase the mRNA expression of GRIP1 and Stargazin.
Results presented above suggest: (1) Under the same chronic stress, different behavioral tests may induce different results; (2) In the state of chronic immobilization stress, the expressional tendency of AMPA receptors subunits GluR1 and GluR2 was different in hippocampus; (3) Hippocampus and amygdala played different role in chronic restraint stress response; (4) The most sensitive target region of the chronic immobilization stress works on synaptic plastisity might be CA1 region of hippocampus; (5) The regulative effect of Xiao yao san shows regional-selective, time-dependent and double-way (up and down) regulative characterization.
实验研究:
哺乳动物脑中大部分兴奋性信号都发生在以谷氨酸为神经递质的突触。谷氨酸是中枢神经系统(CNS)中的主要兴奋性神经递质,有两种受体,代谢型谷氨酸受体和离子型谷氨酸受体。离子型谷氨酸受体根据药理学、分子和电生理学特性又被分成三种:α-氨基羟甲基恶唑丙酸(AMPA)受体、红藻氨酸(KA)受体和N-甲基-D-天(门)冬氨酸(NMDA)受体。AMPA受体是参与中枢神经系统中快速兴奋性突触传递的主要分子单位。谷氨酸与突触后的AMPA型谷氨酸受体结合后诱发去极化,导致神经元兴奋。这一AMPA受体介导的神经传递促成大脑的瞬时到瞬时活性,包括认知反应和动作。而且,突触上AMPA受体功能的改变也促成了作为学习和记忆的基础的可塑性。GRIP与非磷酸化的PDZ基序结合可能将含有GluR2的受体锚定在突触上,Stargazin在AMPA受体膜表面靶向性调控中起作用,其PDZ结合基序磷酸化是突触AMPA受体浓度和突触强度的调控器,c-fos等即刻早期基因(IEG)成员被认为是神经细胞功能状态的示踪标志。因此本课题选择了AMPA受体的两个亚基GluR1、GluR2,两个相关蛋白GRIP1、Stargazin,IEG成员c-fos作为研究对象,通过对慢性束缚应激大鼠行为改变的观察,运用ELISA、免疫组织化学及RT-PCR等方法,从内分泌、蛋白和基因水平,观察了逍遥散对慢性束缚应激状态下大鼠行为、应激相关激素、AMPA受体的调节作用,探讨慢性应激反应和慢性应激损害的中枢机制及逍遥散对其的调节功能。主要结果如下:
1.动物行为的变化:束缚21天后,动物出现类似肝郁脾虚的不良表现,逍遥散对其有改善作用。慢性束缚应激状态下模型组大鼠在三周实验过程中体重增长量明显减少。在旷场实验第1天模型组大鼠的正中格停留时间、总穿格数明显增多;第21天模型组大鼠的正中格停留时间明显增多、总穿格数、站立次数和修饰次数明显减少。在高架十字迷宫实验第14天模型组大鼠进入开放臂的次数和比例、进入开放臂的时间和比例、进入开放和封闭臂总次数以及向下探究次数均明显降低。在第21天Y迷宫实验模型组大鼠的错误反应次数、全天总反应时间减少,正确反应率增加。逍遥散对体重、旷场和高架十字迷宫各项指标的改善作用明显,而对Y迷宫实验未表现出明显的调节作用。
2.ELISA检测结果:21天束缚应激状态下,大鼠血浆ACTH和血清CORT均升高,但CORT升高有统计学意义,而逍遥散对其有明显的向正常水平的调节作用。
3.免疫组织化学结果:21天束缚应激使模型组CA1、DG、BLA区的c-fos阳性细胞数增多;而模型组的GluR1在CA1和DG区表达增多;GluR2在CA1、CA3和DG区表达下降;GluR1和GluR2在BLA区均无明显变化。逍遥散可下调c-fos阳性细胞数,下调GluR1阳性细胞及免疫阳性物表达,上调GluR2阳性细胞数及免疫阳性物表达。
4.RT-PCR结果:21天束缚应激状态下,模型组GRIP1和Stargazin mRNA在CA1区表达下降;但在CA3、DG区和杏仁核的变化无统计学意义。逍遥散可上调GRIP1和Stargazin mRNA的表达。
以上结果提示: (1)在相同慢性应激刺激下,大鼠不同的行为学检测方法可能结果不同;(2)慢性束缚应激状态下,AMPA受体亚基GluR1和GluR2在海马的表达趋势不同;(3)海马和杏仁核在慢性束缚应激反应中的作用不一致;(4)海马CA1区可能是慢性束缚应激影响突触可塑性的最敏感部位;(5)逍遥散的调节呈现出区域选择性、时相性和双向调节作用。
Stress is a series of neuroendocrine responses which is marked with sympathetic nerves excitement and increase of pituitary -adrenal gland cortex secretion when organisms is expose to stressor stimulation, it’s very important for individual survival. Mammals respond to appropriate stress with characteristic changes in their behaviour as well as in autonomic and neuroendocrine parameters aimed at reinstating their disturbed homeostasis. Among such so-called coping strategies, alterations of the hypothalamic–pituitary–adrenal (HPA) axis play a crucial role. However, excessive, especially chronic stress, causes physical, psychological disorders in vary degrees, and even causes body diseases, can be regarded as a pathological process resulting from the reaction of the body to external forces and abnormal conditions that tend to disturb the organism's homeostasis. Since multiple systems relate to chronic stress, and different stressor, different individuals and different circumstances might lead to different results, it’s so difficult for prevention and treatment to chronic stress diseases, whereas Chinese medicine, which with a concept of whole adjustment, treatment based on syndrome differentiation and individualized diagnosis, has shown greater superiority. The present project was supported by National Natural Science Foundation of China (NO.30672578), and we focus on the experimental study on the central neural system mechanisms of chronic stress response and the role of regulative function of Xiao yao san in chronic stress response.
Experimental study
Most excitatory signalling in mammalian brain occurs at synapses that use glutamate as a neurotransmitter. Glutamate is the major excitatory neurotransmitter in the central nervous system (CNS), and is the agonist of two distinct categories of glutamate receptors, metabotropic glutamate receptors and ionotropic glutamate receptors. Ionotropic glutamate receptors have been divided in three classes, according to their pharmacological, molecular, and electrophysiological properties: alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA), kainite (KA), and N-methyl-D-aspartate (NMDA) receptors. The AMPA receptors are the principal molecular units for fast excitatory synaptic transmission in the central nervous system. Glutamate binding to postsynaptic AMPA-type glutamate receptors induces depolarizations that cause neuronal firing. This AMPA receptor-mediated neurotransmission contributes to the brain’s moment-to-moment activities, including cognitive responses and motor actions. Furthermore, changes in AMPA receptor function at synapses contribute to the plasticity that underlies learning and memory. GRIP binding to the unphosphorylated PDZ motif is proposed to anchor GluR2-containing receptors at synapses, The last four amino acids of stargazin bind to the PDZ domains of a number of synaptic scaffolding proteins, this PDZ interaction mediates synaptic targeting of surface receptors, phosphorylation of the PDZ-binding motif of stargazin is a regulator of synaptic levels of AMPA receptors and synaptic strength. C-fos is a member of immediate early genes (IEG), which belong to a class of genes that be regarded as tracing marker of neurocyte function.
Therefore we chose GluR1, GluR2, two subunit of AMPA receptor, two proteins interacting with AMPA receptor subunits, GRIP1 ((glutamate receptor-interacting protein 1) and Stargazin (voltage-dependent calciumchannel gamma-2 subunit,Cacng2) and c-fos as the research targets, chronic restraint as chronic stress model, using ELISA, immunohistochemistry and RT-PCR methods, to observe Xiaoyaosan’s influence on rats’behaviors, stress related hormones as well as AMPA receptors and its’interacting proteins mRNA expression, and to investigate the central nervous mechanisms and the role of regulative function of Xiao yao san to chronic stress responses and chronic stress impairments. The results were as the following.
Behavioral changes: After 21 days immobilization stress, the rats displayed unhealthy changes, Xiaoyaosan could improve the unhealthy statement. The body weight increase of the rats in model group decreased significantly. At the first day of open-field test, the central grille time, total cross number of the rats in model group increased significantly, at the 21st day, the central grille time increased significantly, but the total cross number, stand number and modify number decreased significantly. At the 14th day of elevated plus-maze test, the open arm entry (OE) and OE%, open arm time (OT) and OT%, open and close arm entry and head dipping of the rats in model group decreased significantly. At the 21st day in Y-maze test, the error number, total reaction time of the rats in model group decreased, with significant increased correct reaction rate. Xiao yao san showed significant improvement to body weight, open-field test and elevated plus-maze test, whereas without significant effect to Y-maze test.
ELISA results: In immobilization stress 21 days rats, the concentration of serum CORT increased, with statistical significance, Xiao yao san could regulate it towards normal level. Immunohistochemistry findings: In immobilization stress 21 days rats, the number of c-fos positive cells increased in CA1, CA3 region of hippocampus and basolateral amygdale (BLA); the number of GluR1 positive cells and immunoreaction products increased in CA1 and DG region of hippocampus; the number of GluR2-positive cells decreased in CA3 and DG region of hippocampus, so did the immunoreaction products in CA1, CA3 and DG region of hippocampus. In BLA, neither GluR1 nor GluR2 expression changes with statistical significance. Xiao yao san could decrease the number of c-fos positive cells in hippocampus and BLA as well as GluR1 positive cells and immunoreaction products in hippocampus, and could increase the number of GluR2 positive cells and immunoreaction products in hippocampus.
RT-PCR results: In immobilization stress 21 days rats, both of the mRNA expression of GRIP1 and Stargazin decreased in CA1 region of hippocampus, whereas without statistical significant changes in CA3, DG region of hippocampus and BLA. Xiao yao san could increase the mRNA expression of GRIP1 and Stargazin.
Results presented above suggest: (1) Under the same chronic stress, different behavioral tests may induce different results; (2) In the state of chronic immobilization stress, the expressional tendency of AMPA receptors subunits GluR1 and GluR2 was different in hippocampus; (3) Hippocampus and amygdala played different role in chronic restraint stress response; (4) The most sensitive target region of the chronic immobilization stress works on synaptic plastisity might be CA1 region of hippocampus; (5) The regulative effect of Xiao yao san shows regional-selective, time-dependent and double-way (up and down) regulative characterization.
引文
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