Department of Biomedical Sciences, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, United States.
PK Biosciences, Ames, IA 50011, United States.
Neurobiol Dis. 2020 Jan;133:104443. doi: 10.1016/j.nbd.2019.03.031. Epub 2019 Mar 30.
Chemical nerve agents (CNA) are increasingly becoming a threat to both civilians and military personnel. CNA-induced acute effects on the nervous system have been known for some time and the long-term consequences are beginning to emerge. In this study, we used diisopropylfluorophosphate (DFP), a seizurogenic CNA to investigate the long-term impact of its acute exposure on the brain and its mitigation by an inducible nitric oxide synthase (iNOS) inhibitor, 1400W as a neuroprotectant in the rat model. Several experimental studies have demonstrated that DFP-induced seizures and/or status epilepticus (SE) causes permanent brain injury, even after the countermeasure medication (atropine, oxime, and diazepam). In the present study, DFP-induced SE caused a significant increase in iNOS and 3-nitrotyrosine (3-NT) at 24 h, 48 h, 7d, and persisted for a long-term (12 weeks post-exposure), which led to the hypothesis that iNOS is a potential therapeutic target in DFP-induced brain injury. To test the hypothesis, we administered 1400W (20 mg/kg, i.m.) or the vehicle twice daily for the first three days of post-exposure. 1400W significantly reduced DFP-induced iNOS and 3-NT upregulation in the hippocampus and piriform cortex, and the serum nitrite levels at 24 h post-exposure. 1400W also prevented DFP-induced mortality in <24 h. The brain immunohistochemistry (IHC) at 7d post-exposure revealed a significant reduction in gliosis and neurodegeneration (NeuN+ FJB positive cells) in the 1400W-treated group. 1400W, in contrast to the vehicle, caused a significant reduction in the epileptiform spiking and spontaneous recurrent seizures (SRS) during 12 weeks of continuous video-EEG study. IHC of brain sections from the same animals revealed a significant reduction in reactive gliosis (both microgliosis and astrogliosis) and neurodegeneration across various brain regions in the 1400W-treated group when compared to the vehicle-treated group. A multiplex assay from hippocampal lysates at 6 weeks post-exposure showed a significant increase in several key pro-inflammatory cytokines/chemokines such as IL-1α, TNFα, IL-1β, IL-2, IL-6, IL-12, IL-17a, MCP-1, LIX, and Eotaxin, and a growth factor, VEGF in the vehicle-treated animals. 1400W significantly suppressed IL-1α, TNFα, IL-2, IL-12, and MCP-1 levels. It also suppressed DFP-induced serum nitrite levels at 6 weeks post-exposure. In the Morris water maze, the vehicle-treated animals spent significantly less time in the target quadrant in a probe trial at 9d post-exposure compared to their time spent in the same quadrant 11 days previously (i.e., 2 days prior to DFP exposure). Such a difference was not observed in the 1400W and control groups. However, learning and short-term memory were unaffected when tested at 10-16d and 28-34d post-exposure. Accelerated rotarod, horizontal bar test, and the forced swim test revealed no significant changes between groups. Overall, the findings from this study suggest that 1400W may be considered as a potential therapeutic agent as a follow-on therapy for CNA exposure, after controlling the acute symptoms, to prevent mortality and some of the long-term neurotoxicity parameters such as epileptiform spiking, SRS, neurodegeneration, reactive gliosis in some brain regions, and certain key proinflammatory cytokines and chemokine.
化学神经毒剂(CNA)对平民和军人的威胁日益增加。一段时间以来,人们已经了解到 CNA 对神经系统的急性影响,其长期后果开始显现。在这项研究中,我们使用了二异丙基氟磷酸酯(DFP),一种致痉挛性 CNA,以研究其急性暴露对大脑的长期影响,并使用诱导型一氧化氮合酶(iNOS)抑制剂 1400W 作为神经保护剂,在大鼠模型中减轻其影响。几项实验研究表明,DFP 诱导的癫痫发作和/或癫痫持续状态(SE)会导致永久性脑损伤,即使在采取对抗措施(阿托品、肟和地西泮)后也是如此。在本研究中,DFP 诱导的 SE 在 24 小时、48 小时、7 天和 12 周(暴露后)引起 iNOS 和 3-硝基酪氨酸(3-NT)的显著增加,这导致了 iNOS 是 DFP 诱导的脑损伤的潜在治疗靶点的假说。为了验证这一假说,我们在暴露后的前三天每天两次给予 1400W(20mg/kg,肌内注射)或载体。1400W 显著降低了海马和梨状皮层中 DFP 诱导的 iNOS 和 3-NT 上调,以及暴露后 24 小时的血清亚硝酸盐水平。1400W 还可防止 DFP 在 24 小时内引起的死亡率。暴露后 7 天的脑免疫组织化学(IHC)显示,1400W 治疗组海马和梨状皮层中的神经胶质增生和神经退行性变(NeuN+FJB 阳性细胞)显著减少。与载体相比,1400W 在 12 周的连续视频-EEG 研究期间导致癫痫样尖峰和自发性反复性癫痫发作(SRS)的发生率显著降低。来自同一动物的大脑切片的 IHC 显示,与载体治疗组相比,1400W 治疗组大脑各个区域的反应性神经胶质增生(小胶质细胞和星形胶质细胞)和神经退行性变显著减少。暴露后 6 周的海马裂解物的多重分析显示,载体治疗的动物中几种关键的促炎细胞因子/趋化因子(如 IL-1α、TNFα、IL-1β、IL-2、IL-6、IL-12、IL-17a、MCP-1、LIX 和 Eotaxin)和生长因子 VEGF 的水平显著增加。1400W 显著抑制了 IL-1α、TNFα、IL-2、IL-12 和 MCP-1 的水平。它还抑制了暴露后 6 周时血清中亚硝酸盐的水平。在 Morris 水迷宫中,载体治疗的动物在暴露后 9 天的探测试验中,在目标象限中花费的时间明显少于它们在 11 天前(即 DFP 暴露前 2 天)花费的时间。在 1400W 和对照组中没有观察到这种差异。然而,在暴露后 10-16 天和 28-34 天进行测试时,学习和短期记忆不受影响。加速转棒、横杆测试和强迫游泳测试显示各组之间无显著差异。总的来说,这项研究的结果表明,1400W 可能被认为是一种潜在的治疗药物,作为 CNA 暴露后的后续治疗方法,以控制急性症状,预防死亡率和一些长期神经毒性参数,如癫痫样尖峰、SRS、神经退行性变、某些大脑区域的反应性神经胶质增生和某些关键的促炎细胞因子和趋化因子。