TDP-43 protein inclusion pathology is observed in the primary sites of neurodegeneration (motor cortex and spinal cord) in 97% of motor neuron disease (MND) patients. For non-motor brain regions, some (e.g. prefrontal cortex, hippocampus) demonstrate variable incidence of TDP-43 inclusions across MND patients while others (e.g. occipital cortex, cerebellum) are consistently spared of this pathology and neurodegeneration. Dysregulation of RNA splicing is a key pathological mechanism in MND, with loss of TDP-43 function leading to widespread “cryptic” splicing. We previously conducted a multi-region brain transcriptomic analysis of MND to better understand the alterations occurring across brain regions variably affected by TDP-43 inclusions. Short-read RNA-seq was performed on five regions (motor cortex, prefrontal cortex, hippocampus, occipital cortex, cerebellum) each derived from 22 MND cases and 11 controls. Intriguingly, despite the absence of TDP-43 inclusions, the cerebellum demonstrated the most MND-specific alternative splicing events. This included a switch in POLDIP3 transcript usage, an established marker of TDP-43 loss of function.
To further explore this finding, we have generated parallel PacBio long-read and Illumina short-read RNA-seq for cerebellum tissue derived from 15 controls, 24 sporadic MND cases and nine C9orf72-MND cases. A pathological feature of C9orf72-MND is abundant RNA foci and TDP-43-negative dipeptide-repeat protein inclusions in the cerebellum. Bioinformatic analysis of the short-read RNA-seq using a combination of MAJIQ and LeafCutter identified high levels of intron retention (sporadic MND: 1,027 events [49% de novo], C9orf72-MND: 1,375 events [61% de novo]) and 16 cryptic splicing events associated with TDP-43 loss of function in MND cases. SQANTI3 classification of the FLAIR-generated long-read transcriptome identified 175,945 unique transcripts across our cerebellum samples, 43.8% of which were classified as novel emphasising the utility of long-read sequencing for comprehensive transcriptome characterisation. We hypothesise that identified cerebellar transcriptome alterations may represent early pathological events and/or neuroprotective mechanisms in MND.