Gambarotto Lisa, Russo Loris, Bresolin Silvia, Persano Luca, D'Amore Rachele, Ronchi Giulia, Zen Federica, Muratori Luisa, Cani Alice, Negro Samuele, Megighian Aram, Calabrò Sonia, Braghetta Paola, Bizzotto Dario, Cescon Matilde
Department of Molecular Medicine, University of Padova, Via U. Bassi 58/B, Padova, 35131, Italy.
Department of Biology, University of Padova, Via U. Bassi 58/B, Padova, 35131, Italy.
Adv Sci (Weinh). 2025 Feb;12(5):e2308965. doi: 10.1002/advs.202308965. Epub 2024 Dec 16.
The core component of the class III phosphatidylinositol 3-kinase complex, Beclin 1, takes part in different protein networks, thus switching its role from inducing autophagy to regulating autophagosomal maturation and endosomal trafficking. While assessed in neurons, astrocytes, and microglia, its role is far less investigated in myelinating glia, including Schwann cells (SCs), responsible for peripheral nerve myelination. Remarkably, the dysregulation in endosomal trafficking is emerging as a pathophysiological mechanism underlying peripheral neuropathies, such as demyelinating Charcot-Marie-Tooth (CMT) diseases. By knocking out Beclin 1 in SCs here a novel mouse model (Becn1 cKO) is generated, developing a severe and progressive neuropathy, accompanied by involuntary tremors, body weight loss, and premature death. Ultrastructural analysis revealed abated myelination and SCs displaying enlarged cytoplasm with progressive accumulation of intracellular vesicles. Transcriptomic and histological analysis from sciatic nerves of 10-day and 2-month-old mice revealed pro-mitotic gene deregulation and increased SCs proliferation at both stages with axonal loss and increased immune infiltration in adults, well reflecting the progressive motor and sensory functional impairment that characterizes Becn1 cKO mice, compared to controls. The study establishes a further step in understanding key mechanisms in SC development and points to Beclin 1 and its regulated pathways as targets for demyelinating CMT forms.
III类磷脂酰肌醇3激酶复合物的核心成分Beclin 1参与不同的蛋白质网络,从而将其作用从诱导自噬转变为调节自噬体成熟和内体运输。虽然在神经元、星形胶质细胞和小胶质细胞中对其作用进行了评估,但在包括负责周围神经髓鞘形成的施万细胞(SCs)在内的髓鞘形成胶质细胞中,对其作用的研究要少得多。值得注意的是,内体运输失调正在成为周围神经病变(如脱髓鞘型夏科-马里-图斯病,CMT)的病理生理机制。通过在此处敲除SCs中的Beclin 1,生成了一种新型小鼠模型(Becn1 cKO),该模型出现严重且进行性的神经病变,伴有不自主震颤、体重减轻和过早死亡。超微结构分析显示髓鞘形成减少,SCs细胞质增大,细胞内囊泡逐渐积累。对10日龄和2月龄小鼠坐骨神经的转录组学和组织学分析显示,在两个阶段均存在促有丝分裂基因失调,SCs增殖增加,同时成年小鼠出现轴突损失和免疫浸润增加,这很好地反映了与对照组相比,Becn1 cKO小鼠具有特征性的进行性运动和感觉功能障碍。该研究在理解SCs发育的关键机制方面又迈出了一步,并指出Beclin 1及其调控途径是脱髓鞘型CMT的治疗靶点。