Banerjee A, Wang H-Y, Borgmann-Winter K E, MacDonald M L, Kaprielian H, Stucky A, Kvasic J, Egbujo C, Ray R, Talbot K, Hemby S E, Siegel S J, Arnold S E, Sleiman P, Chang X, Hakonarson H, Gur R E, Hahn C-G
Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA.
Department of Physiology, Pharmacology and Neuroscience, City University of New York Medical School, New York, NY, USA.
Mol Psychiatry. 2015 Sep;20(9):1091-100. doi: 10.1038/mp.2014.115. Epub 2014 Oct 21.
Numerous investigations support decreased glutamatergic signaling as a pathogenic mechanism of schizophrenia, yet the molecular underpinnings for such dysregulation are largely unknown. In the post-mortem dorsolateral prefrontal cortex (DLPFC), we found striking decreases in tyrosine phosphorylation of N-methyl-D aspartate (NMDA) receptor subunit 2 (GluN2) that is critical for neuroplasticity. The decreased GluN2 activity in schizophrenia may not be because of downregulation of NMDA receptors as MK-801 binding and NMDA receptor complexes in postsynaptic density (PSD) were in fact increased in schizophrenia cases. At the postreceptor level, however, we found striking reductions in the protein kinase C, Pyk 2 and Src kinase activity that in tandem can decrease GluN2 activation. Given that Src serves as a hub of various signaling mechanisms affecting GluN2 phosphorylation, we postulated that Src hypoactivity may result from convergent alterations of various schizophrenia susceptibility pathways and thus mediate their effects on NMDA receptor signaling. Indeed, the DLPFC of schizophrenia cases exhibit increased PSD-95 and erbB4 and decreased receptor-type tyrosine-protein phosphatase-α (RPTPα) and dysbindin-1, each of which reduces Src activity via protein interaction with Src. To test genomic underpinnings for Src hypoactivity, we examined genome-wide association study results, incorporating 13 394 cases and 34 676 controls. We found no significant association of individual variants of Src and its direct regulators with schizophrenia. However, a protein-protein interaction-based network centered on Src showed significant enrichment of gene-level associations with schizophrenia compared with other psychiatric illnesses. Our results together demonstrate striking decreases in NMDA receptor signaling at the postreceptor level and propose Src as a nodal point of convergent dysregulations affecting NMDA receptor pathway via protein-protein associations.
众多研究支持谷氨酸能信号传递减少是精神分裂症的致病机制,但这种失调的分子基础在很大程度上尚不清楚。在死后的背外侧前额叶皮质(DLPFC)中,我们发现对神经可塑性至关重要的N-甲基-D-天冬氨酸(NMDA)受体亚基2(GluN2)的酪氨酸磷酸化显著降低。精神分裂症中GluN2活性降低可能并非由于NMDA受体下调,因为在精神分裂症病例中,MK-801结合及突触后致密部(PSD)中的NMDA受体复合物实际上增加了。然而,在受体后水平,我们发现蛋白激酶C、Pyk 2和Src激酶活性显著降低,这些活性共同作用可降低GluN2的激活。鉴于Src是影响GluN2磷酸化的各种信号机制的枢纽,我们推测Src活性低下可能是由各种精神分裂症易感途径的汇聚改变导致的,从而介导它们对NMDA受体信号的影响。事实上,精神分裂症病例的DLPFC显示PSD-95和erbB4增加,而受体型酪氨酸蛋白磷酸酶-α(RPTPα)和失调结合蛋白-1减少,它们各自通过与Src的蛋白质相互作用降低Src活性。为了测试Src活性低下的基因组基础,我们检查了包含13394例病例和34676例对照的全基因组关联研究结果。我们发现Src及其直接调节因子的个体变体与精神分裂症无显著关联。然而,与其他精神疾病相比,以Src为中心的基于蛋白质-蛋白质相互作用的网络显示出与精神分裂症的基因水平关联显著富集。我们的结果共同表明在受体后水平NMDA受体信号显著降低,并提出Src是通过蛋白质-蛋白质关联影响NMDA受体途径的汇聚失调的节点。