TDP-43 represses cryptic exon inclusion in the FTD-ALS gene UNC13A

Nature. 2022 Mar;603(7899):124-130. doi: 10.1038/s41586-022-04424-7. Epub 2022 Feb 23.

Abstract

A hallmark pathological feature of the neurodegenerative diseases amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD) is the depletion of RNA-binding protein TDP-43 from the nucleus of neurons in the brain and spinal cord1. A major function of TDP-43 is as a repressor of cryptic exon inclusion during RNA splicing2-4. Single nucleotide polymorphisms in UNC13A are among the strongest hits associated with FTD and ALS in human genome-wide association studies5,6, but how those variants increase risk for disease is unknown. Here we show that TDP-43 represses a cryptic exon-splicing event in UNC13A. Loss of TDP-43 from the nucleus in human brain, neuronal cell lines and motor neurons derived from induced pluripotent stem cells resulted in the inclusion of a cryptic exon in UNC13A mRNA and reduced UNC13A protein expression. The top variants associated with FTD or ALS risk in humans are located in the intron harbouring the cryptic exon, and we show that they increase UNC13A cryptic exon splicing in the face of TDP-43 dysfunction. Together, our data provide a direct functional link between one of the strongest genetic risk factors for FTD and ALS (UNC13A genetic variants), and loss of TDP-43 function.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Exons / genetics
  • Frontotemporal Dementia* / metabolism
  • Genome-Wide Association Study
  • Humans
  • Motor Neurons / pathology
  • Nerve Tissue Proteins

Substances

  • DNA-Binding Proteins
  • Nerve Tissue Proteins
  • TARDBP protein, human
  • UNC13B protein, human

Supplementary concepts

  • Frontotemporal Dementia With Motor Neuron Disease