Kambali Maltesh, Li Yan, Unichenko Petr, Feria Pliego Jessica A, Yadav Rachita, Liu Jing, McGuinness Patrick, Cobb Johanna G, Wang Muxiao, Nagarajan Rajasekar, Lyu Jinrui, Vongsouthi Vanessa, Jackson Colin J, Engin Elif, Coyle Joseph T, Shin Jaeweon, Hodgson Nathaniel W, Hensch Takao K, Talkowski Michael E, Homanics Gregg E, Bolshakov Vadim Y, Henneberger Christian, Rudolph Uwe
Department of Comparative Biosciences, College of Veterinary Medicine, University of Illinois Urbana-Champaign, Urbana, IL, USA.
Cellular Neurobiology Laboratory, McLean Hospital Belmont, Belmont, MA, USA.
Mol Psychiatry. 2025 Mar;30(3):927-942. doi: 10.1038/s41380-024-02711-5. Epub 2024 Aug 30.
Glycine is an obligatory co-agonist at excitatory NMDA receptors in the brain, especially in the dentate gyrus, which has been postulated to be crucial for the development of psychotic associations and memories with psychotic content. Drugs modulating glycine levels are in clinical development for improving cognition in schizophrenia. However, the functional relevance of the regulation of glycine metabolism by endogenous enzymes is unclear. Using a chromosome-engineered allelic series in mice, we report that a triplication of the gene encoding the glycine-catabolizing enzyme glycine decarboxylase (GLDC) - as found on a small supernumerary marker chromosome in patients with psychosis - reduces extracellular glycine levels as determined by optical fluorescence resonance energy transfer (FRET) in dentate gyrus (DG) and suppresses long-term potentiation (LTP) in mPP-DG synapses but not in CA3-CA1 synapses, reduces the activity of biochemical pathways implicated in schizophrenia and mitochondrial bioenergetics, and displays deficits in schizophrenia-like behaviors which are in part known to be dependent on the activity of the dentate gyrus, e.g., prepulse inhibition, startle habituation, latent inhibition, working memory, sociability and social preference. Our results demonstrate that Gldc negatively regulates long-term synaptic plasticity in the dentate gyrus in mice, suggesting that an increase in GLDC copy number possibly contributes to the development of psychosis in humans.
甘氨酸是大脑中兴奋性N-甲基-D-天冬氨酸(NMDA)受体的必需协同激动剂,尤其是在齿状回中,据推测这对具有精神病性内容的联想及记忆的发展至关重要。调节甘氨酸水平的药物正处于改善精神分裂症认知功能的临床研发阶段。然而,内源性酶对甘氨酸代谢调节的功能相关性尚不清楚。我们利用经染色体工程改造的小鼠等位基因系列,报告称编码甘氨酸分解代谢酶甘氨酸脱羧酶(GLDC)的基因发生三倍体复制(正如在精神病患者的一条小的额外标记染色体上所发现的那样),会降低齿状回(DG)中通过光学荧光共振能量转移(FRET)测定的细胞外甘氨酸水平,并抑制内侧穿孔通路-齿状回(mPP-DG)突触中的长时程增强(LTP),但不影响CA3-CA1突触中的LTP,降低与精神分裂症及线粒体生物能量学相关的生化途径的活性,并表现出类似精神分裂症的行为缺陷,其中部分缺陷已知依赖于齿状回的活性,例如前脉冲抑制、惊吓习惯化、潜伏抑制、工作记忆、社交能力及社交偏好。我们的结果表明,Gldc对小鼠齿状回中的长时程突触可塑性具有负向调节作用,这表明GLDC拷贝数增加可能在人类精神病的发生中起作用。