Park Ji Hyun, Back Dong Bin, Guo Shuzhen, Tanaka Masayoshi, Takase Hajime, Whalen Michael J, Arai Ken, Hayakawa Kazuhide, Lo Eng H
Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, USA.
Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, USA.
Brain Res. 2025 Jul 15;1859:149647. doi: 10.1016/j.brainres.2025.149647. Epub 2025 Apr 16.
Damage to vascular cells comprise an important part of traumatic brain injury (TBI) but the underlying pathophysiology remains to be fully elucidated. Here, we investigate the loss of O-Linked β-N-acetylglucosamine(O-GlcNAc) modification (O-GlcNAcylation) and mitochondrial disruption in vascular pericytes as a candidate mechanism. In mouse models in vivo, TBI rapidly induces vascular oxidative stress and down-regulates mitochondrial O-GlcNAcylation. In pericytes but not brain endothelial cultures in vitro, mechanical stretch injury down-regulates mitochondrial O-GlcNAcylation. This is accompanied by disruptions in mitochondrial dynamics, comprising a decrease in mitochondrial fusion and an increase in mitochondrial fission proteins. Pharmacologic rescue of endogenous mitochondrial O-GlcNAcylation with an O-GlcNAcase inhibitor Thiamet-G or addition of exogenous O-GlcNAc-enhanced extracellular mitochondria ameliorates the mitochondrial disruption in pericytes damaged by mechanical injury. Finally, in a pericyte-endothelial co-culture model, mechanical injury increased trans-cellular permeability; adding Thiamet-G or O-GlcNAc-enhanced extracellular mitochondria rescued trans-cellular permeability following mechanical injury. These proof-of-concept findings suggest that mitochondrial O-GlcNAcylation in pericytes may represent a novel therapeutic target for ameliorating oxidative stress and vascular damage after mechanical injury following TBI.
血管细胞损伤是创伤性脑损伤(TBI)的重要组成部分,但其潜在的病理生理学仍有待充分阐明。在此,我们研究了血管周细胞中O-连接的β-N-乙酰葡糖胺(O-GlcNAc)修饰(O-GlcNAcylation)的丧失和线粒体破坏作为一种潜在机制。在体内小鼠模型中,TBI迅速诱导血管氧化应激并下调线粒体O-GlcNAcylation。在体外周细胞而非脑内皮细胞培养物中,机械拉伸损伤下调线粒体O-GlcNAcylation。这伴随着线粒体动力学的破坏,包括线粒体融合减少和线粒体裂变蛋白增加。用O-GlcNAcase抑制剂Thiamet-G对内源性线粒体O-GlcNAcylation进行药理学挽救或添加外源性O-GlcNAc增强的细胞外线粒体可改善机械损伤所致周细胞的线粒体破坏。最后,在周细胞-内皮细胞共培养模型中,机械损伤增加了跨细胞通透性;添加Thiamet-G或O-GlcNAc增强的细胞外线粒体可挽救机械损伤后的跨细胞通透性。这些概念验证结果表明,周细胞中的线粒体O-GlcNAcylation可能是改善TBI后机械损伤后氧化应激和血管损伤的新治疗靶点。