Muscle-derived miR-126 regulates TDP-43 axonal local synthesis and NMJ integrity in ALS models

Nat Neurosci. 2025 Nov;28(11):2201-2216. doi: 10.1038/s41593-025-02062-6. Epub 2025 Oct 3.

Abstract

Amyotrophic lateral sclerosis (ALS) is characterized by neuromuscular junction (NMJ) disruption and neurodegeneration. Recent findings highlight a pivotal role for TAR DNA-binding protein 43 (TDP-43) in forming axonal pathological condensates and facilitating NMJ disruption through inhibition of local protein synthesis. However, the mechanisms that drive local TDP-43 accumulation remain unknown. Here we identify that the TDP-43 axonal accumulation in peripheral nerves of SOD1 patients and mice stems from its aberrant local synthesis. This is a non-cell-autonomous process driven by muscle-derived miR-126a-5p extracellular vesicles (EVs). Inhibiting muscle secretion of miR-126a-5p prompts presynaptic TDP-43 synthesis and accumulation, which disrupts axonal translation and causes NMJ degeneration. Introducing miR-126 to SOD1G93A mice, primary co-cultures and human induced pluripotent stem cell (iPSC)-derived co-cultures with ALS mutations exhibits neuroprotective effects and delays motor decline. These findings identify a transcellular communication axis between muscles and motor neurons that regulates axonal local synthesis and NMJ maintenance, offering insights into ALS onset and progression.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / genetics
  • Amyotrophic Lateral Sclerosis* / metabolism
  • Amyotrophic Lateral Sclerosis* / pathology
  • Animals
  • Axons* / metabolism
  • Axons* / pathology
  • DNA-Binding Proteins* / biosynthesis
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Disease Models, Animal
  • Extracellular Vesicles / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Male
  • Mice
  • Mice, Transgenic
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Motor Neurons / metabolism
  • Muscle, Skeletal* / metabolism
  • Neuromuscular Junction* / metabolism
  • Neuromuscular Junction* / pathology
  • Superoxide Dismutase-1 / genetics

Substances

  • MicroRNAs
  • DNA-Binding Proteins
  • TARDBP protein, human
  • MIRN126 microRNA, mouse
  • Tardbp protein, mouse
  • Superoxide Dismutase-1