Peripheral SMN restoration is essential for long-term rescue of a severe spinal muscular atrophy mouse model

Nature. 2011 Oct 5;478(7367):123-6. doi: 10.1038/nature10485.

Abstract

Spinal muscular atrophy (SMA) is a motor neuron disease and the leading genetic cause of infant mortality; it results from loss-of-function mutations in the survival motor neuron 1 (SMN1) gene. Humans have a paralogue, SMN2, whose exon 7 is predominantly skipped, but the limited amount of functional, full-length SMN protein expressed from SMN2 cannot fully compensate for a lack of SMN1. SMN is important for the biogenesis of spliceosomal small nuclear ribonucleoprotein particles, but downstream splicing targets involved in pathogenesis remain elusive. There is no effective SMA treatment, but SMN restoration in spinal cord motor neurons is thought to be necessary and sufficient. Non-central nervous system (CNS) pathologies, including cardiovascular defects, were recently reported in severe SMA mouse models and patients, reflecting autonomic dysfunction or direct effects in cardiac tissues. Here we compared systemic versus CNS restoration of SMN in a severe mouse model. We used an antisense oligonucleotide (ASO), ASO-10-27, that effectively corrects SMN2 splicing and restores SMN expression in motor neurons after intracerebroventricular injection. Systemic administration of ASO-10-27 to neonates robustly rescued severe SMA mice, much more effectively than intracerebroventricular administration; subcutaneous injections extended the median lifespan by 25 fold. Furthermore, neonatal SMA mice had decreased hepatic Igfals expression, leading to a pronounced reduction in circulating insulin-like growth factor 1 (IGF1), and ASO-10-27 treatment restored IGF1 to normal levels. These results suggest that the liver is important in SMA pathogenesis, underscoring the importance of SMN in peripheral tissues, and demonstrate the efficacy of a promising drug candidate.

Publication types

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

MeSH terms

  • Alternative Splicing / drug effects
  • Alternative Splicing / genetics
  • Animals
  • Animals, Newborn
  • Carrier Proteins / metabolism
  • Disease Models, Animal*
  • Glycoproteins / deficiency
  • Glycoproteins / metabolism
  • Growth Hormone / metabolism
  • Humans
  • Insulin-Like Growth Factor I / deficiency
  • Insulin-Like Growth Factor I / metabolism
  • Kaplan-Meier Estimate
  • Liver / metabolism
  • Longevity / drug effects
  • Mice
  • Mice, Transgenic
  • Motor Neurons / drug effects
  • Motor Neurons / metabolism
  • Motor Neurons / pathology
  • Muscular Atrophy, Spinal / genetics
  • Muscular Atrophy, Spinal / metabolism*
  • Muscular Atrophy, Spinal / pathology*
  • Muscular Atrophy, Spinal / physiopathology
  • Oligonucleotides, Antisense / administration & dosage
  • Oligonucleotides, Antisense / genetics
  • Oligonucleotides, Antisense / pharmacology
  • RNA Isoforms / analysis
  • RNA Isoforms / genetics
  • RNA, Messenger / analysis
  • RNA, Messenger / genetics
  • Rotarod Performance Test
  • Spinal Cord / cytology
  • Spinal Cord / metabolism
  • Spinal Cord / pathology
  • Survival of Motor Neuron 1 Protein / genetics
  • Survival of Motor Neuron 2 Protein / genetics
  • Survival of Motor Neuron 2 Protein / metabolism
  • Transgenes

Substances

  • Carrier Proteins
  • Glycoproteins
  • Oligonucleotides, Antisense
  • RNA Isoforms
  • RNA, Messenger
  • SMN2 protein, human
  • Smn1 protein, mouse
  • Survival of Motor Neuron 1 Protein
  • Survival of Motor Neuron 2 Protein
  • insulin-like growth factor binding protein, acid labile subunit
  • Insulin-Like Growth Factor I
  • Growth Hormone