Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, USA; Howard Hughes Medical Institute, Chevy Chase, MD, USA.
Neuroscience. 2013;255:33-44. doi: 10.1016/j.neuroscience.2013.09.051. Epub 2013 Oct 3.
Brain-derived neurotrophic factor (BDNF) is critically involved in synaptic plasticity and neurotransmission. Our lab has previously found that BDNF activation of neurotrophic tyrosine kinase, receptor, type 2 (TrkB) is required for fear memory formation and that GABAA receptor (GABAAR) subunits and the GABAA clustering protein gephyrin are dynamically regulated during fear memory consolidation. We hypothesize that TrkB-dependent internalization of GABAARs may partially underlie a transient period of amygdala hyperactivation during fear memory consolidation. We have previously reported that BDNF modulates GABAAR α1 subunit sequestration in cultured hippocampal and amygdala neurons by differential phosphorylation pathways. At present, no studies have investigated the regulation of gephyrin and GABAAR α1 subunits following BDNF activation in the amygdala. In this study, we confirm the association of GABAAR α1 and γ2 subunits with gephyrin on mouse amygdala neurons by coimmunoprecipitation and immunocytochemistry. We then demonstrate that rapid BDNF treatment, as well as suppression of gephyrin protein levels on amygdala neurons, induced sequestration of surface α1 subunits. Further, we find that rapid exposure of BDNF to primary amygdala cultures produced decreases in gephyrin levels, whereas longer exposure resulted in an eventual increase. While total α1 subunit levels remained unchanged, gephyrin was downregulated in whole cell homogenates, but enhanced in complexes with GABAARs. Our data with anisomycin suggest that BDNF may rapidly induce gephyrin protein degradation, with subsequent gephyrin synthesis occurring. Together, these findings suggest that gephyrin may be a key factor in BDNF-dependent GABAAR regulation in the amygdala. This work may inform future studies aimed at elucidating the pathways connecting BDNF, GABAA systems, gephyrin, and their role in underlying amygdala-dependent learning.
脑源性神经营养因子 (BDNF) 对突触可塑性和神经递质传递至关重要。我们的实验室之前发现,BDNF 激活神经营养酪氨酸激酶受体 2 (TrkB) 是恐惧记忆形成所必需的,而 GABA 受体 (GABAAR) 亚基和 GABAAR 聚类蛋白神经胶质蛋白在恐惧记忆巩固过程中动态调节。我们假设 TrkB 依赖性 GABAAR 内化可能部分解释了恐惧记忆巩固过程中杏仁核短暂过度激活的现象。我们之前的报告表明,BDNF 通过不同的磷酸化途径调节培养的海马和杏仁核神经元中的 GABAARα1 亚基隔离。目前,尚无研究探讨 BDNF 激活后杏仁核中神经胶质蛋白和 GABAARα1 亚基的调节。在这项研究中,我们通过共免疫沉淀和免疫细胞化学证实了 GABAARα1 和γ2 亚基与杏仁核上的神经胶质蛋白的结合。然后,我们证明快速 BDNF 处理以及降低杏仁核神经元上神经胶质蛋白的水平会诱导表面α1 亚基的隔离。此外,我们发现,BDNF 对原代杏仁核培养物的快速暴露会导致神经胶质蛋白水平降低,而较长时间的暴露则会导致最终升高。虽然总α1 亚基水平保持不变,但全细胞匀浆中的神经胶质蛋白下调,而与 GABAAR 结合的则增强。我们用放线菌酮的数据表明,BDNF 可能会迅速诱导神经胶质蛋白蛋白降解,随后发生神经胶质蛋白的合成。总的来说,这些发现表明神经胶质蛋白可能是 BDNF 依赖性 GABAAR 在杏仁核中调节的关键因素。这项工作可能为阐明 BDNF、GABA 系统、神经胶质蛋白及其在杏仁核依赖学习中的作用之间的联系提供信息。