The Onecut transcription factor HNF-6 regulates in motor neurons the formation of the neuromuscular junctions

PLoS One. 2012;7(12):e50509. doi: 10.1371/journal.pone.0050509. Epub 2012 Dec 5.

Abstract

The neuromuscular junctions are the specialized synapses whereby spinal motor neurons control the contraction of skeletal muscles. The formation of the neuromuscular junctions is controlled by a complex interplay of multiple mechanisms coordinately activated in motor nerve terminals and in their target myotubes. However, the transcriptional regulators that control in motor neurons the genetic programs involved in neuromuscular junction development remain unknown. Here, we provide evidence that the Onecut transcription factor HNF-6 regulates in motor neurons the formation of the neuromuscular junctions. Indeed, adult Hnf6 mutant mice exhibit hindlimb muscle weakness and abnormal locomotion. This results from defects of hindlimb neuromuscular junctions characterized by an abnormal morphology and defective localization of the synaptic vesicle protein synaptophysin at the motor nerve terminals. These defects are consequences of altered and delayed formation of the neuromuscular junctions in newborn mutant animals. Furthermore, we show that the expression level of numerous regulators of neuromuscular junction formation, namely agrin, neuregulin-2 and TGF-ß receptor II, is downregulated in the spinal motor neurons of Hnf6 mutant newborn animals. Finally, altered formation of neuromuscular junction-like structures in a co-culture model of wildtype myotubes with mutant embryonic spinal cord slices is rescued by recombinant agrin and neuregulin, indicating that depletion in these factors contributes to defective neuromuscular junction development in the absence of HNF-6. Thus, HNF-6 controls in spinal motor neurons a genetic program that coordinates the formation of hindlimb neuromuscular junctions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Coculture Techniques
  • DNA Primers
  • Fluorescent Antibody Technique
  • Hepatocyte Nuclear Factor 6 / physiology*
  • In Situ Hybridization
  • Locomotion
  • Mice
  • Mice, Mutant Strains
  • Microscopy, Electron
  • Motor Neurons / physiology*
  • Neuromuscular Junction / growth & development*
  • Polymerase Chain Reaction

Substances

  • DNA Primers
  • Hepatocyte Nuclear Factor 6

Grants and funding

This work was supported by the “Fonds spéciaux de recherché” (FSR) of the Université catholique de Louvain, by the Fonds de la Recherche Scientifique (F.R.S.-FNRS) including a Crédit au chercheur #1.5.085.10.F and a grant from the Fund for Scientific Medical Research #3.4.538.10.F (Belgium), by the Actions de Recherche Concertées grant #10/15-026 (Communauté française de Belgique and Académie Louvain) and by the Association Belge contre les Maladies neuro-Musculaires (ABMM asbl) (F.C.), by the Walloon Region’s Marshall Programme of Excellence (DIANE convention) (P.G.), and by the Association pour la recherche sur la SLA et les autres maladies du motoneurone (ARSIa) and the Association pour la recherche et le développment des moyens de lutte contre les maladies neurodégénératives (AREMANE) (F.R., J.P.L.). E.A. holds a specialization grant from the F.R.I.A. (Belgium). F.C. is a Research Associate of the F.R.S.-FNRS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.