Department of Pathophysiology, Key Laboratory of Ministry of Education of China for Neurological Disorders, School of Basic Medicine of Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
Key Laboratory of Modern Toxicology of Shenzhen, Shenzhen Center for Disease Control and Prevention, No.8, Longyuan Road, Nanshan District, Shenzhen 518055, China.
Biochim Biophys Acta Mol Basis Dis. 2019 Jun 1;1865(6):1477-1489. doi: 10.1016/j.bbadis.2019.02.020. Epub 2019 Feb 28.
Maternal immune activation (MIA) is an independent risk factor for psychiatric disorders including depression spectrum in the offsprings, but the molecular mechanism is unclear. Recent studies show that interferon-stimulated gene-15 (ISG15) is involved in inflammation and neuronal dendrite development; here we studied the role of ISG15 in MIA-induced depression and the underlying mechanisms.
By vena caudalis injecting polyinosinic: polycytidylic acid (poly I:C) into the pregnant rats to mimic MIA, we used AAV or lentivirus to introduce or silence ISG15 expression. Synaptic plasticity was detected by confocal microscope and Golgi staining. Cognitive performances of the offspring were measured by Open field, Forced swimming and Sucrose preference test.
We found that MIA induced depression-like behaviors with dendrite impairments in the offspring with ISG15 level increased in the offsprings' brain. Overexpressing ISG15 in the prefrontal cortex of neonatal cubs (P0) could mimic dendritic pathology and depressive like behaviors, while downregulating ISG15 rescued these abnormalities in the offsprings. Further studies demonstrated that MIA-induced upregulation of inflammatory cytokines promoted ISG15 expression in the offspring' brain which suppressed Rap2A ubiquitination via NEDD4 and thus induced Rap2A accumulation, while upregulating NEDD4 abolished ISG15-induced dendrite impairments.
These data reveal that MIA impedes offsprings' dendrite development and causes depressive like behaviors by upregulating ISG15 and suppressing NEDD4/Rap2A signaling. The current findings suggest that inhibiting ISG15 may be a promising intervention of MIA-induced psychiatric disorders in the offsprings.
母体免疫激活(MIA)是后代出现精神障碍(包括抑郁谱系障碍)的独立危险因素,但具体的分子机制尚不清楚。最近的研究表明干扰素刺激基因 15(ISG15)参与炎症和神经元树突发育;在此,我们研究了 ISG15 在 MIA 诱导的抑郁中的作用及其潜在机制。
通过尾静脉注射聚肌苷酸:聚胞苷酸(poly I:C)模拟 MIA,我们使用 AAV 或慢病毒来引入或沉默 ISG15 的表达。通过共聚焦显微镜和高尔基染色检测突触可塑性。通过旷场、强迫游泳和蔗糖偏好测试来测量后代的认知表现。
我们发现 MIA 导致后代出现抑郁样行为,并伴有树突损伤,同时后代大脑中的 ISG15 水平升高。在新生幼崽(P0)的前额叶皮层中过表达 ISG15 可模拟树突病理和抑郁样行为,而下调 ISG15 可挽救后代的这些异常。进一步的研究表明,MIA 诱导的炎症细胞因子上调促进了后代大脑中 ISG15 的表达,通过 NEDD4 抑制 Rap2A 泛素化,从而导致 Rap2A 积累,而上调 NEDD4 则消除了 ISG15 诱导的树突损伤。
这些数据表明,MIA 通过上调 ISG15 和抑制 NEDD4/Rap2A 信号通路来阻碍后代的树突发育,并导致抑郁样行为。这些发现提示抑制 ISG15 可能是治疗 MIA 诱导的后代精神障碍的一种有前途的方法。