Human motor units in microfluidic devices are impaired by FUS mutations and improved by HDAC6 inhibition

Stem Cell Reports. 2021 Sep 14;16(9):2213-2227. doi: 10.1016/j.stemcr.2021.03.029. Epub 2021 Apr 22.

Abstract

Neuromuscular junctions (NMJs) ensure communication between motor neurons (MNs) and muscle; however, in MN disorders, such as amyotrophic lateral sclerosis (ALS), NMJs degenerate resulting in muscle atrophy. The aim of this study was to establish a versatile and reproducible in vitro model of a human motor unit to investigate the effects of ALS-causing mutations. Therefore, we generated a co-culture of human induced pluripotent stem cell (iPSC)-derived MNs and human primary mesoangioblast-derived myotubes in microfluidic devices. A chemotactic and volumetric gradient facilitated the growth of MN neurites through microgrooves resulting in the interaction with myotubes and the formation of NMJs. We observed that ALS-causing FUS mutations resulted in reduced neurite outgrowth as well as an impaired neurite regrowth upon axotomy. NMJ numbers were likewise reduced in the FUS-ALS model. Interestingly, the selective HDAC6 inhibitor, Tubastatin A, improved the neurite outgrowth, regrowth, and NMJ morphology, prompting HDAC6 inhibition as a potential therapeutic strategy for ALS.

Keywords: FUS; HDAC6; Tubastatin A; amyotrophic lateral sclerosis; microfluidic device; neurite outgrowth; neurite regrowth; neuromuscular junction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Agrin / metabolism
  • Amyotrophic Lateral Sclerosis / etiology
  • Amyotrophic Lateral Sclerosis / metabolism
  • Amyotrophic Lateral Sclerosis / pathology
  • Biomarkers
  • Cell Culture Techniques
  • Cell Differentiation / drug effects
  • Coculture Techniques
  • Fluorescent Antibody Technique
  • Histone Deacetylase 6 / antagonists & inhibitors*
  • Histone Deacetylase Inhibitors / pharmacology*
  • Humans
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / metabolism
  • Lab-On-A-Chip Devices*
  • Laminin / metabolism
  • Microfluidic Analytical Techniques
  • Motor Neurons / cytology
  • Motor Neurons / drug effects
  • Motor Neurons / metabolism
  • Muscle Fibers, Skeletal / cytology
  • Muscle Fibers, Skeletal / drug effects
  • Muscle Fibers, Skeletal / metabolism
  • Mutation*
  • Neuromuscular Junction / drug effects
  • Neuromuscular Junction / genetics*
  • Neuromuscular Junction / physiopathology*
  • Neuronal Outgrowth / drug effects
  • RNA-Binding Protein FUS / genetics*

Substances

  • Agrin
  • Biomarkers
  • FUS protein, human
  • Histone Deacetylase Inhibitors
  • Laminin
  • RNA-Binding Protein FUS
  • HDAC6 protein, human
  • Histone Deacetylase 6