HDAC inhibitor SAHA resolved intermediate filament bundling and defective autophagy caused by the lack of sacsin in ARSACS.

Author:

Paré Alexandre M1,Larochelle Nancy2,Dvorak Ryan A.1,Minotti Sandra2,Atkinson Caitlin S.1,Cheng-Boivin Zacharie1,Gentil Benoit J.1

Affiliation:

1. Department of Kinesiology and Physical Education, McGill University

2. Department of Neurology and Neurosurgery, McGill University

Abstract

Abstract

Autosomal recessive spastic ataxia of the Charlevoix-Saguenay (ARSACS) is a progressive childhood-onset neurological disease caused by loss-of-function mutations in the SACS gene. This condition is characterized by cerebellar ataxia, peripheral neuropathy, and spastic plasticity. ARSACS patient-derived fibroblasts and mouse models lacking sacsin exhibit altered mitochondrial networks, intermediate filament bundling, dysregulated autophagic flux, and aberrant protein/organelle localization. Sacsin, a large multidomain protein, plays a critical role in chaperoning and protein homeostasis, particularly in neurons. Dysregulation of autophagy in ARSACS is evidenced by increased LC3 levels and defective lysosome-autophagosome fusion in the absence of sacsin. Recent omics approaches suggest sacsin’s involvement in cytoskeleton regulation, intracellular transport, calcium homeostasis, synaptic organization, and mitochondrial maintenance. This study aimed to explore the effects of histone deacetylase (HDAC) inhibitors on neurofilament (NF) protein acetylation and autophagic flux in ARSACS. NF proteins from Sacs-/- mice showed no significant acetylation differences compared to controls, though HDAC inhibitor SAHA resolved NF bundling. Purification and analysis of NF proteins confirmed high purity and minor acetylation differences at specific lysines (K214). Treatment with SAHA reduced NF bundling in Sacs-/- motor neurons and promoted lysosomal recruitment to autophagosomes in ARSACS patient-derived fibroblasts, indicating restored autophagic flux. These findings highlight the potential of HDAC inhibitors in resolving cytoskeletal abnormalities and improving autophagic processes in ARSACS, offering promising therapeutic avenues for this debilitating disorder. Further research is needed to elucidate the precise mechanisms underlying these effects and their implications for NF homeostasis and autophagy regulation in ARSACS.

Publisher

Springer Science and Business Media LLC

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