Dok-7 regulates neuromuscular synapse formation by recruiting Crk and Crk-L

Genes Dev. 2010 Nov 1;24(21):2451-61. doi: 10.1101/gad.1977710.

Abstract

Agrin, released by motor neurons, promotes neuromuscular synapse formation by stimulating MuSK, a receptor tyrosine kinase expressed in skeletal muscle. Phosphorylated MuSK recruits docking protein-7 (Dok-7), an adaptor protein that is expressed selectively in muscle. In the absence of Dok-7, neuromuscular synapses fail to form, and mutations that impair Dok-7 are a major cause of congenital myasthenia in humans. How Dok-7 stimulates synaptic differentiation is poorly understood. Once recruited to MuSK, Dok-7 directly stimulates MuSK kinase activity. This unusual activity of an adapter protein is mediated by the N-terminal region of Dok-7, whereas most mutations that cause congenital myasthenia truncate the C-terminal domain. Here, we demonstrate that Dok-7 also functions downstream from MuSK, and we identify the proteins that are recruited to the C-terminal domain of Dok-7. We show that Agrin stimulates phosphorylation of two tyrosine residues in the C-terminal domain of Dok-7, which leads to recruitment of two adapter proteins: Crk and Crk-L. Furthermore, we show that selective inactivation of Crk and Crk-L in skeletal muscle leads to severe defects in neuromuscular synapses in vivo, revealing a critical role for Crk and Crk-L downstream from Dok-7 in presynaptic and postsynaptic differentiation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Agrin / pharmacology
  • Animals
  • Blotting, Western
  • Cell Line
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • HEK293 Cells
  • Humans
  • Mice
  • Mice, Knockout
  • Microscopy, Confocal
  • Muscle Fibers, Skeletal / cytology
  • Muscle Fibers, Skeletal / drug effects
  • Muscle Fibers, Skeletal / metabolism
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • Muscle, Skeletal / embryology
  • Muscle, Skeletal / metabolism
  • Mutation
  • Neuromuscular Junction / metabolism*
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Phosphorylation / drug effects
  • Proto-Oncogene Proteins c-crk / genetics
  • Proto-Oncogene Proteins c-crk / metabolism*
  • Receptor Protein-Tyrosine Kinases / genetics
  • Receptor Protein-Tyrosine Kinases / metabolism
  • Receptors, Cholinergic / genetics
  • Receptors, Cholinergic / metabolism
  • Synapses / metabolism*
  • Time Factors
  • Tyrosine / genetics
  • Tyrosine / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Agrin
  • CRKL protein
  • Crk protein, mouse
  • Dok-7 protein, mouse
  • Muscle Proteins
  • Nuclear Proteins
  • Proto-Oncogene Proteins c-crk
  • Receptors, Cholinergic
  • Green Fluorescent Proteins
  • Tyrosine
  • MuSK protein, mouse
  • Receptor Protein-Tyrosine Kinases