Transgenic expression of neuronal dystonin isoform 2 partially rescues the disease phenotype of the dystonia musculorum mouse model of hereditary sensory autonomic neuropathy VI

Hum Mol Genet. 2014 May 15;23(10):2694-710. doi: 10.1093/hmg/ddt663. Epub 2013 Dec 30.

Abstract

A newly identified lethal form of hereditary sensory and autonomic neuropathy (HSAN), designated HSAN-VI, is caused by a homozygous mutation in the bullous pemphigoid antigen 1 (BPAG1)/dystonin gene (DST). The HSAN-VI mutation impacts all major neuronal BPAG1/dystonin protein isoforms: dystonin-a1, -a2 and -a3. Homozygous mutations in the murine Dst gene cause a severe sensory neuropathy termed dystonia musculorum (dt). Phenotypically, dt mice are similar to HSAN-VI patients, manifesting progressive limb contractures, dystonia, dysautonomia and early postnatal death. To obtain a better molecular understanding of disease pathogenesis in HSAN-VI patients and the dt disorder, we generated transgenic mice expressing a myc-tagged dystonin-a2 protein under the regulation of the neuronal prion protein promoter on the dt(Tg4/Tg4) background, which is devoid of endogenous dystonin-a1 and -a2, but does express dystonin-a3. Restoring dystonin-a2 expression in the nervous system, particularly within sensory neurons, prevented the disorganization of organelle membranes and microtubule networks, attenuated the degeneration of sensory neuron subtypes and ameliorated the phenotype and increased life span in these mice. Despite these improvements, complete rescue was not observed likely because of inadequate expression of the transgene. Taken together, this study provides needed insight into the molecular basis of the dt disorder and other peripheral neuropathies including HSAN-VI.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carrier Proteins / genetics*
  • Carrier Proteins / metabolism
  • Cells, Cultured
  • Cytoskeletal Proteins / genetics*
  • Cytoskeletal Proteins / metabolism
  • Disease Models, Animal
  • Dystonia Musculorum Deformans / genetics
  • Dystonin
  • Ganglia, Spinal / pathology
  • Hereditary Sensory and Autonomic Neuropathies / genetics*
  • Hereditary Sensory and Autonomic Neuropathies / pathology
  • Humans
  • Intracellular Membranes / metabolism
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microtubules / metabolism
  • Muscle Spindles / metabolism
  • Muscle Spindles / pathology
  • Nerve Fibers, Myelinated / metabolism
  • Nerve Fibers, Myelinated / pathology
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism
  • Neuromuscular Junction / metabolism
  • Neuromuscular Junction / pathology
  • Phenotype
  • Proprioception
  • Sensory Receptor Cells / pathology
  • Transgenes

Substances

  • Carrier Proteins
  • Cytoskeletal Proteins
  • Dst protein, mouse
  • Dystonin
  • Nerve Tissue Proteins