MuSK frizzled-like domain is critical for mammalian neuromuscular junction formation and maintenance

J Neurosci. 2015 Mar 25;35(12):4926-41. doi: 10.1523/JNEUROSCI.3381-14.2015.

Abstract

The muscle-specific kinase MuSK is one of the key molecules orchestrating neuromuscular junction (NMJ) formation. MuSK interacts with the Wnt morphogens, through its Frizzled-like domain (cysteine-rich domain [CRD]). Dysfunction of MuSK CRD in patients has been recently associated with the onset of myasthenia, common neuromuscular disorders mainly characterized by fatigable muscle weakness. However, the physiological role of Wnt-MuSK interaction in NMJ formation and function remains to be elucidated. Here, we demonstrate that the CRD deletion of MuSK in mice caused profound defects of both muscle prepatterning, the first step of NMJ formation, and synapse differentiation associated with a drastic deficit in AChR clusters and excessive growth of motor axons that bypass AChR clusters. Moreover, adult MuSKΔCRD mice developed signs of congenital myasthenia, including severe NMJs dismantlement, muscle weakness, and fatigability. We also report, for the first time, the beneficial effects of lithium chloride, a reversible inhibitor of the glycogen synthase kinase-3, that rescued NMJ defects in MuSKΔCRD mice and therefore constitutes a novel therapeutic reagent for the treatment of neuromuscular disorders linked to Wnt-MuSK signaling pathway deficiency. Together, our data reveal that MuSK CRD is critical for NMJ formation and plays an unsuspected role in NMJ maintenance in adulthood.

Keywords: MuSK; Wnt; congenital myasthenic syndrome; lithium chloride; neuromuscular junction; synaptogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholinesterase / metabolism
  • Animals
  • Animals, Newborn
  • Fatigue / genetics
  • Fatigue / physiopathology
  • Female
  • Glycoproteins / chemistry*
  • Hand Strength / physiology
  • Intracellular Signaling Peptides and Proteins
  • Lithium Chloride / pharmacology
  • Lithium Chloride / therapeutic use
  • Male
  • Mice
  • Mice, Transgenic
  • Motor Neurons / drug effects
  • Motor Neurons / physiology
  • Muscle Weakness / drug therapy*
  • Muscle Weakness / genetics
  • Muscle Weakness / physiopathology
  • Mutation
  • Myasthenic Syndromes, Congenital / drug therapy
  • Myasthenic Syndromes, Congenital / genetics
  • Myasthenic Syndromes, Congenital / physiopathology
  • Neuromuscular Junction / drug effects
  • Neuromuscular Junction / growth & development*
  • Neuromuscular Junction / physiology*
  • Neuromuscular Junction / ultrastructure
  • Pregnancy
  • Primary Cell Culture
  • Receptor Protein-Tyrosine Kinases / chemistry*
  • Receptor Protein-Tyrosine Kinases / genetics
  • Receptor Protein-Tyrosine Kinases / physiology*
  • Receptors, Cholinergic / metabolism

Substances

  • Glycoproteins
  • Intracellular Signaling Peptides and Proteins
  • Receptors, Cholinergic
  • WD repeat containing planar cell polarity effector
  • MuSK protein, mouse
  • Receptor Protein-Tyrosine Kinases
  • Acetylcholinesterase
  • Lithium Chloride