The spinal muscular atrophy with pontocerebellar hypoplasia gene VRK1 regulates neuronal migration through an amyloid-β precursor protein-dependent mechanism

J Neurosci. 2015 Jan 21;35(3):936-42. doi: 10.1523/JNEUROSCI.1998-14.2015.

Abstract

Spinal muscular atrophy with pontocerebellar hypoplasia (SMA-PCH) is an infantile SMA variant with additional manifestations, particularly severe microcephaly. We previously identified a nonsense mutation in Vaccinia-related kinase 1 (VRK1), R358X, as a cause of SMA-PCH. VRK1-R358X is a rare founder mutation in Ashkenazi Jews, and additional mutations in patients of different origins have recently been identified. VRK1 is a nuclear serine/threonine protein kinase known to play multiple roles in cellular proliferation, cell cycle regulation, and carcinogenesis. However, VRK1 was not known to have neuronal functions before its identification as a gene mutated in SMA-PCH. Here we show that VRK1-R358X homozygosity results in lack of VRK1 protein, and demonstrate a role for VRK1 in neuronal migration and neuronal stem cell proliferation. Using shRNA in utero electroporation in mice, we show that Vrk1 knockdown significantly impairs cortical neuronal migration, and affects the cell cycle of neuronal progenitors. Expression of wild-type human VRK1 rescues both proliferation and migration phenotypes. However, kinase-dead human VRK1 rescues only the migration impairment, suggesting the role of VRK1 in neuronal migration is partly noncatalytic. Furthermore, we found that VRK1 deficiency in human and mouse leads to downregulation of amyloid-β precursor protein (APP), a known neuronal migration gene. APP overexpression rescues the phenotype caused by Vrk1 knockdown, suggesting that VRK1 affects neuronal migration through an APP-dependent mechanism.

Keywords: APP; SMA-PCH (spinal muscular atrophy pontocerebellar hypoplasia); VRK1; neuronal migration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid beta-Protein Precursor / genetics
  • Amyloid beta-Protein Precursor / metabolism*
  • Animals
  • Cell Cycle / genetics
  • Cell Line, Tumor
  • Cell Movement / genetics*
  • Cerebellar Diseases / genetics
  • Cerebellar Diseases / metabolism
  • Cerebellar Diseases / pathology
  • Cerebellum / abnormalities*
  • Cerebellum / metabolism
  • Cerebellum / pathology
  • Cerebral Cortex / cytology
  • Cerebral Cortex / metabolism
  • Developmental Disabilities / genetics
  • Developmental Disabilities / metabolism
  • Developmental Disabilities / pathology
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Magnetic Resonance Imaging
  • Mice
  • Nervous System Malformations / genetics
  • Nervous System Malformations / metabolism*
  • Nervous System Malformations / pathology
  • Neurons / cytology*
  • Neurons / metabolism
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Spinal Muscular Atrophies of Childhood / genetics
  • Spinal Muscular Atrophies of Childhood / metabolism*
  • Spinal Muscular Atrophies of Childhood / pathology

Substances

  • Amyloid beta-Protein Precursor
  • Intracellular Signaling Peptides and Proteins
  • Protein Serine-Threonine Kinases
  • VRK1 protein, human

Supplementary concepts

  • Cerebellar Hypoplasia
  • Pontocerebellar Hypoplasia