Splicing changes in SMA mouse motoneurons and SMN-depleted neuroblastoma cells: evidence for involvement of splicing regulatory proteins

RNA Biol. 2014;11(11):1430-46. doi: 10.1080/15476286.2014.996494.

Abstract

Spinal Muscular Atrophy (SMA) is caused by deletions or mutations in the Survival Motor Neuron 1 (SMN1) gene. The second gene copy, SMN2, produces some, but not enough, functional SMN protein. SMN is essential to assemble small nuclear ribonucleoproteins (snRNPs) that form the spliceosome. However, it is not clear whether SMA is caused by defects in this function that could lead to splicing changes in all tissues, or by the impairment of an additional, less well characterized, but motoneuron-specific SMN function. We addressed the first possibility by exon junction microarray analysis of motoneurons (MNs) isolated by laser capture microdissection from a severe SMA mouse model. This revealed changes in multiple U2-dependent splicing events. Moreover, splicing appeared to be more strongly affected in MNs than in other cells. By testing mutiple genes in a model of progressive SMN depletion in NB2a neuroblastoma cells, we obtained evidence that U2-dependent splicing changes occur earlier than U12-dependent ones. As several of these changes affect genes coding for splicing regulators, this may acerbate the splicing response induced by low SMN levels and induce secondary waves of splicing alterations.

Keywords: ESE, exonic splicing enhancer; FCS, fetal calf serum; MN, motoneuron; NMD, nonsense-mediated mRNA decay; NMJ, neuromuscular junction, PCR; RT, reverse transcription; SMA, Spinal Muscular Atrophy; SMN, Survival Motor Neuron; Spinal Muscular Atrophy; TcRβ, T-cell receptor β chain; exon junction microarray; hz, heterozygote, LCM; laser capture microdissection; major spliceosome; minor spliceosome; motoneurons; neurodegerative disease; polymerase chain reaction, qPCR; real-time (quantitative) PCR; sh, short hairpin; snRNA, small nuclear ribonucleic acid; snRNP assembly; snRNP, small nuclear ribonucleoprotein; splicing; splicing regulators.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Line, Tumor
  • Cells, Cultured
  • Gene Expression Regulation*
  • Humans
  • Introns / genetics
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Motor Neurons / metabolism*
  • Muscular Atrophy, Spinal / genetics
  • Muscular Atrophy, Spinal / metabolism
  • Muscular Atrophy, Spinal / pathology
  • Neuroblastoma / genetics
  • Neuroblastoma / metabolism
  • Neuroblastoma / pathology
  • RNA Interference
  • RNA Splicing Factors
  • RNA Splicing*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • SMN Complex Proteins / genetics*
  • SMN Complex Proteins / metabolism
  • Septins / genetics
  • Septins / metabolism

Substances

  • Membrane Proteins
  • RNA Splicing Factors
  • RNA-Binding Proteins
  • Rbfox1 protein, mouse
  • SMN Complex Proteins
  • Tmem41b protein, mouse
  • Septins
  • septin 9, mouse