Petro Marianne, Jaffer Hayder, Yang Jun, Kabu Shushi, Morris Viola B, Labhasetwar Vinod
Department of Biomedical Engineering, Lerner Research Institute, Cleveland Clinic, Cleveland, OH 44195, USA.
Department of Biomedical Engineering, Lerner Research Institute, Cleveland Clinic, Cleveland, OH 44195, USA.
Biomaterials. 2016 Mar;81:169-180. doi: 10.1016/j.biomaterials.2015.12.009. Epub 2015 Dec 18.
Inherent neuronal and circulating progenitor cells play important roles in facilitating neuronal and functional recovery post stroke. However, this endogenous repair process is rather limited, primarily due to unfavorable conditions in the infarcted brain involving reactive oxygen species (ROS)-mediated oxidative stress and inflammation following ischemia/reperfusion injury. We hypothesized that during reperfusion, effective delivery of antioxidants to ischemic brain would create an environment without such oxidative stress and inflammation, thus promoting activation and mobilization of progenitor cells in the infarcted brain. We administered recombinant human tissue-type plasminogen activator (tPA) via carotid artery at 3 h post stroke in a thromboembolic rat model, followed by sequential administration of the antioxidants catalase (CAT) and superoxide dismutase (SOD), encapsulated in biodegradable nanoparticles (nano-CAT/SOD). Brains were harvested at 48 h post stroke for immunohistochemical analysis. Ipsilateral brain slices from animals that had received tPA + nano-CAT/SOD showed a widespread distribution of glial fibrillary acidic protein-positive cells (with morphology resembling radial glia-like neural precursor cells) and nestin-positive cells (indicating the presence of immature neurons); such cells were considerably fewer in untreated animals or those treated with tPA alone. Brain sections from animals receiving tPA + nano-CAT/SOD also showed much greater numbers of SOX2- and nestin-positive progenitor cells migrating from subventricular zone of the lateral ventricle and entering the rostral migratory stream than in t-PA alone treated group or untreated control. Further, animals treated with tPA + nano-CAT/SOD showed far fewer caspase-positive cells and fewer neutrophils than did other groups, as well as an inhibition of hippocampal swelling. These results suggest that the antioxidants mitigated the inflammatory response, protected neuronal cells from undergoing apoptosis, and inhibited edema formation by protecting the blood-brain barrier from ROS-mediated reperfusion injury. A longer-term study would enable us to determine if our approach would assist progenitor cells to undergo neurogenesis and to facilitate neurological and functional recovery following stroke and reperfusion injury.
内在的神经元和循环祖细胞在促进中风后的神经元和功能恢复中发挥重要作用。然而,这种内源性修复过程相当有限,主要是由于梗死脑内存在不利条件,包括缺血/再灌注损伤后活性氧(ROS)介导的氧化应激和炎症。我们假设在再灌注期间,将抗氧化剂有效递送至缺血脑会创造一个没有这种氧化应激和炎症的环境,从而促进梗死脑内祖细胞的激活和动员。在血栓栓塞大鼠模型中,我们在中风后3小时通过颈动脉给予重组人组织型纤溶酶原激活剂(tPA),随后依次给予包裹在可生物降解纳米颗粒(纳米CAT/SOD)中的抗氧化剂过氧化氢酶(CAT)和超氧化物歧化酶(SOD)。在中风后48小时收获大脑进行免疫组织化学分析。接受tPA +纳米CAT/SOD的动物的同侧脑切片显示胶质纤维酸性蛋白阳性细胞(形态类似于放射状胶质样神经前体细胞)和巢蛋白阳性细胞广泛分布(表明存在未成熟神经元);在未治疗的动物或仅接受tPA治疗的动物中,此类细胞要少得多。接受tPA +纳米CAT/SOD的动物的脑切片还显示,与仅接受t-PA治疗的组或未治疗的对照组相比,从侧脑室室下区迁移并进入吻侧迁移流的SOX2和巢蛋白阳性祖细胞数量要多得多。此外,接受tPA +纳米CAT/SOD治疗的动物的半胱天冬酶阳性细胞和中性粒细胞比其他组少得多,并且海马肿胀受到抑制。这些结果表明,抗氧化剂减轻了炎症反应,保护神经元细胞免于凋亡,并通过保护血脑屏障免受ROS介导的再灌注损伤来抑制水肿形成。一项长期研究将使我们能够确定我们的方法是否有助于祖细胞进行神经发生,并促进中风和再灌注损伤后的神经和功能恢复。