Aschner Michael, Skalny Anatoly V, Lu Rongzhu, Martins Airton C, Tizabi Yousef, Nekhoroshev Sergey V, Santamaria Abel, Sinitskiy Anton I, Tinkov Alexey A
Department of Molecular Pharmacology, Albert Einstein College of Medicine, Bronx, NY, United States.
Institute of Bioelementology, Orenburg State University, Orenburg, Russia.
Front Mol Neurosci. 2024 Dec 5;17:1504802. doi: 10.3389/fnmol.2024.1504802. eCollection 2024.
Copper (Cu) is essential for brain development and function, yet its overload induces neuronal damage and contributes to neurodegeneration and other neurological disorders. Multiple studies demonstrated that Cu neurotoxicity is associated with mitochondrial dysfunction, routinely assessed by reduction of mitochondrial membrane potential. Nonetheless, the role of alterations of mitochondrial dynamics in brain mitochondrial dysfunction induced by Cu exposure is still debatable. Therefore, the objective of the present narrative review was to discuss the role of mitochondrial dysfunction in Cu-induced neurotoxicity with special emphasis on its influence on brain mitochondrial fusion and fission, as well as mitochondrial clearance by mitophagy. Existing data demonstrate that, in addition to mitochondrial electron transport chain inhibition, membrane damage, and mitochondrial reactive oxygen species (ROS) overproduction, Cu overexposure inhibits mitochondrial fusion by down-regulation of Opa1, Mfn1, and Mfn2 expression, while promoting mitochondrial fission through up-regulation of Drp1. It has been also demonstrated that Cu exposure induces PINK1/Parkin-dependent mitophagy in brain cells, that is considered a compensatory response to Cu-induced mitochondrial dysfunction. However, long-term high-dose Cu exposure impairs mitophagy, resulting in accumulation of dysfunctional mitochondria. Cu-induced inhibition of mitochondrial biogenesis due to down-regulation of PGC-1α further aggravates mitochondrial dysfunction in brain. Studies from non-brain cells corroborate these findings, also offering additional evidence that dysregulation of mitochondrial dynamics and mitophagy may be involved in Cu-induced damage in brain. Finally, Cu exposure induces cuproptosis in brain cells due mitochondrial proteotoxic stress, that may also contribute to neuronal damage and pathogenesis of certain brain diseases. Based on these findings, it is assumed that development of mitoprotective agents, specifically targeting mechanisms of mitochondrial quality control, would be useful for prevention of neurotoxic effects of Cu overload.
铜(Cu)对大脑发育和功能至关重要,但其过载会导致神经元损伤,并促成神经退行性变和其他神经系统疾病。多项研究表明,铜的神经毒性与线粒体功能障碍有关,线粒体功能障碍通常通过线粒体膜电位降低来评估。尽管如此,铜暴露诱导的脑线粒体功能障碍中线粒体动力学改变的作用仍存在争议。因此,本叙述性综述的目的是讨论线粒体功能障碍在铜诱导的神经毒性中的作用,特别强调其对脑线粒体融合与裂变以及线粒体自噬介导的线粒体清除的影响。现有数据表明,除了抑制线粒体电子传递链、损伤膜以及线粒体活性氧(ROS)过度产生外,铜过量暴露还通过下调Opa1、Mfn1和Mfn2的表达来抑制线粒体融合,同时通过上调Drp1来促进线粒体裂变。还已证明,铜暴露会在脑细胞中诱导PINK1/Parkin依赖性线粒体自噬,这被认为是对铜诱导的线粒体功能障碍的一种代偿反应。然而,长期高剂量铜暴露会损害线粒体自噬,导致功能失调的线粒体积累。由于PGC-1α下调导致铜诱导的线粒体生物合成抑制进一步加重了脑线粒体功能障碍。来自非脑细胞的研究证实了这些发现,并提供了额外证据表明线粒体动力学和线粒体自噬失调可能参与了铜诱导的脑损伤。最后,由于线粒体蛋白毒性应激,铜暴露会在脑细胞中诱导铜死亡,这也可能导致神经元损伤和某些脑部疾病的发病机制。基于这些发现,推测开发专门针对线粒体质量控制机制的线粒体保护剂将有助于预防铜过载的神经毒性作用。