Background: Charcot–Marie–Tooth (CMT) neuropathies encompass a group of diverse clinical and genetic inherited diseases united by length-dependent axonal degeneration. We previously mapped a rare X-linked form, CMTX3, to a 5.7-Mb interval on Xq26.3–q27.1.1 Whole-genome sequencing revealed a striking structural variation (SV) where a 78-kb segment from 8q24.3 was duplicated and inserted into the CMTX3 locus at a recombination hotspot between HAPSTR2 and SOX3.2 The SV (containing ARHGAP39 exons 1-7) fully segregated with disease suggesting a gene regulatory disturbance rather than a classic coding mutation.
Methods: Patient fibroblasts were re-programmed into induced pluripotent stem cells (iPSC) and differentiated into neuroepithelial cells (NEP), motor neuron progenitors (MNP) and spinal motor neurons (sMN). Bulk RNA sequencing of patient sMN assessed global gene dosage changes and potential fusion transcripts arising from the partial ARHGAP39 duplication. Nanostring profiling of CMTX3 candidate genes at multiple stages of differentiation assessed differential gene expression with quantitative proteomics validating expression changes at the protein level.
Results: Bulk RNA-seq showed no dosage increase attributable to the 8q24.3 duplication/insertion and pathogenic fusion transcripts were excluded for ARHGAP39. Nanostring profiling revealed spatiotemporal SOX3 dysregulation, with significantly reduced expression in iPSCs and a similar trend in CMTX3 NEPs. Quantitative proteomics confirmed lower SOX3 abundance in NEPs. Together, these findings prioritise SOX3 as the leading gene perturbed by the structural variation.
Discussion: CMTX3 presents with early onset and faster disability progression than many CMTs.3 SOX3 is among the earliest transcription factors activated in spinal cord development and is pivotal for neuronal fate decisions. A regulatory-disrupting insertion near SOX3, together with stage-specific RNA and protein downregulation of SOX3, provides a coherent mechanism that may underlie CMTX3. Our CMTX3 sMN model can now be paired with a new SOX3 inducible-degron zebrafish model we have made to enable functional validation and pre-clinical studies.