Eleuteri Simona, Wang Bao, Cutillo Gianni, Zhang Fang Tracy Shi, Tao Kai, Qu Yan, Yang Qian, Wei Wenyi, Simon David K
Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA.
Department of Neurosurgery, Tangdu Hospital: Fourth Military Medical University, Xi'an, China.
FEBS J. 2025 Jan;292(2):332-354. doi: 10.1111/febs.17276. Epub 2024 Oct 21.
Peroxisome proliferator-activated receptor gamma coactivator 1-alpha (PGC-1α) is a key regulator of mitochondrial biogenesis and antioxidative defenses, and it may play a critical role in Parkinson's disease (PD). F-box/WD repeat domain-containing protein (FBXW7), an E3 protein ligase, promotes the degradation of substrate proteins through the ubiquitin-proteasome system (UPS) and leads to the clearance of PGC-1α. Here, we elucidate a novel post-translational mechanism for regulating PGC-1α levels in neurons. We show that enhancing chaperone-mediated autophagy (CMA) activity promotes the CMA-mediated degradation of FBXW7 and consequently increases PGC-1α. We confirm the relevance of this pathway in vivo by showing decreased FBXW7 and increased PGC-1α as a result of boosting CMA selectively in dopaminergic (DA) neurons by overexpressing lysosomal-associated membrane protein 2A (LAMP2A) in TH-Cre-LAMP2-loxp conditional mice. We further demonstrate that these mice are protected against MPTP-induced oxidative stress and neurodegeneration. These results highlight a novel regulatory pathway for PGC-1α in DA neurons and suggest targeted increasing of CMA or decreasing FBXW7 in DA neurons as potential neuroprotective strategies in PD.
过氧化物酶体增殖物激活受体γ共激活因子1α(PGC-1α)是线粒体生物合成和抗氧化防御的关键调节因子,可能在帕金森病(PD)中起关键作用。含F盒/ WD重复结构域蛋白(FBXW7)是一种E3蛋白连接酶,通过泛素-蛋白酶体系统(UPS)促进底物蛋白的降解,导致PGC-1α的清除。在此,我们阐明了一种调节神经元中PGC-1α水平的新的翻译后机制。我们发现增强伴侣介导的自噬(CMA)活性可促进CMA介导的FBXW7降解,从而增加PGC-1α。我们通过在TH-Cre-LAMP2-loxp条件小鼠中过表达溶酶体相关膜蛋白2A(LAMP2A),选择性地增强多巴胺能(DA)神经元中的CMA,结果显示FBXW7减少而PGC-1α增加,从而在体内证实了该途径的相关性。我们进一步证明这些小鼠对MPTP诱导的氧化应激和神经退行性变具有保护作用。这些结果突出了DA神经元中PGC-1α的一种新的调节途径,并表明在DA神经元中有针对性地增加CMA或降低FBXW7作为PD潜在的神经保护策略。