Franklin Melissa E, Grant Jordan L, Lee Grant M, Alvarez-Ciara Anabel, Bennett Cassie, Mattis Serene, Gallardo Nicolas, Corrales Natalie, Cui Xinyan Tracy, Capadona Jeffrey R, Streit Wolfgang J, Olivier Jean-Hubert, Keane Robert W, Dietrich W Dalton, de Rivero Vaccari Juan Pablo, Prasad Abhishek
Department of Biomedical Engineering, University of Miami, Miami, FL, USA.
Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA.
Acta Biomater. 2025 Jun 15;200:703-723. doi: 10.1016/j.actbio.2025.05.026. Epub 2025 May 10.
Long-term reliability of microelectrodes implanted in the cortex is hindered due to the foreign body response that occurs at the electrode-tissue interface. Following implantation, there is disruption of the blood-brain-barrier and vasculature, resulting in activation of immune cells and release of erythrocytes. As a result of hemolysis, erythrocytes degrade to heme and then to free iron. Excess free iron can participate in the Fenton Reaction, producing reactive oxygen species (ROS). Iron-mediated ROS production can contribute to oxidation of lipids, proteins, and DNA, facilitating a hostile environment of oxidative stress leading to oxidative cellular damage, cytotoxicity, and cell death. The objective of this study was to show the iron accumulation and the downstream effects of oxidative stress at the injury site. A 16-channel microelectrode array (MEA) was implanted in the rat somatosensory cortex. Our results indicated significant elevation of NOX complex subunits across timepoints, suggesting sustained oxidative stress. In a separate group of animals, we administered an iron chelator, deferoxamine mesylate (DFX), to evaluate the effects of chelation on iron accumulation, oxidative stress and damage, and neuronal survival. Results indicate that animals with iron chelation showed reduced ferric iron and markers of oxidative stress and damage corresponding with increased expression of neuronal cell bodies and electrophysiological functional performance. In summary, the study reveals the role of iron in mediating oxidative stress and the effects of modulating iron levels using iron chelation at the electrode-tissue interface. STATEMENT OF SIGNIFICANCE: Iron accumulation has been observed in central nervous system injuries and in neurodegenerative diseases such as Alzheimer's and Parkinson's disease. While the role of iron is studied in various neurodegenerative diseases and traumatic brain injury, iron accumulation and its effect on oxidative stress is not known for intracortical implants where there is a persistent injury due to the presence of a foreign device in the brain tissue. The study seeks to understand the effects of iron accumulation on oxidative stress and damage at the electrode-tissue interface in intracortical implants by using iron chelation as a method of modulating iron levels at the interface.
植入皮质的微电极的长期可靠性受到电极-组织界面处发生的异物反应的阻碍。植入后,血脑屏障和脉管系统遭到破坏,导致免疫细胞激活和红细胞释放。由于溶血,红细胞降解为血红素,然后再降解为游离铁。过量的游离铁可参与芬顿反应,产生活性氧(ROS)。铁介导的ROS生成可导致脂质、蛋白质和DNA氧化,促成氧化应激的不利环境,导致氧化细胞损伤、细胞毒性和细胞死亡。本研究的目的是展示损伤部位的铁积累以及氧化应激的下游效应。将一个16通道微电极阵列(MEA)植入大鼠体感皮层。我们的结果表明,跨时间点NOX复合体亚基显著升高,提示持续的氧化应激。在另一组动物中,我们给予铁螯合剂甲磺酸去铁胺(DFX),以评估螯合对铁积累、氧化应激和损伤以及神经元存活的影响。结果表明,接受铁螯合的动物的三价铁以及氧化应激和损伤标志物减少,同时神经元细胞体的表达增加,电生理功能表现增强。总之,该研究揭示了铁在介导氧化应激中的作用以及在电极-组织界面使用铁螯合调节铁水平的效果。重要性声明:在中枢神经系统损伤以及阿尔茨海默病和帕金森病等神经退行性疾病中已观察到铁积累。虽然在各种神经退行性疾病和创伤性脑损伤中对铁的作用进行了研究,但对于皮层内植入物,由于脑组织中存在外来装置而导致持续损伤,铁积累及其对氧化应激的影响尚不清楚。该研究旨在通过使用铁螯合作为调节界面铁水平的方法,了解铁积累对皮层内植入物电极-组织界面氧化应激和损伤的影响。