A homozygous canonical splice acceptor site mutation in PRUNE1 is responsible for a rare childhood neurodegenerative disease in Manitoba Cree families

Am J Med Genet A. 2019 Feb;179(2):206-218. doi: 10.1002/ajmg.a.60690. Epub 2018 Dec 17.

Abstract

Autosomal recessive PRUNE1 mutations are reported to cause a severe neurodevelopmental disorder with microcephaly, hypotonia, and brain malformations. We describe clinical and neuropathological features in a cohort of nine individuals of Cree descent who, because of a founder effect, are homozygous for the same PRUNE1 mutation. They follow the course of a combined neuromuscular and neurodegenerative disease, rather than a pure failure of normal development. This cohort presented in infancy with features of lower motor neuron disease, such as hypotonia, contractures, tongue fasciculations, and feeding difficulties in the absence of congenital brain anomalies and microcephaly. A neurodegenerative course followed with onset of seizures, spasticity, and respiratory insufficiency. Muscle biopsies showed denervation/reinnervation features, nonspecific atrophy and end-stage atrophy. Autopsy findings in two patients are also described, suggesting length dependent central motor axon degeneration, peripheral motor axon degeneration, possible spinal motor neuron degeneration, and accumulation of beta amyloid precursor protein inclusions in select brainstem nuclei. Exome sequencing and homozygosity mapping identified a homozygous PRUNE1 mutation in a canonical splice site, which produces two abnormal PRUNE1 mRNA products. Based on our studies and the histopathology and phenotypic data, we provide further evidence that this disorder leads to a neurodegenerative disease affecting both the peripheral and central nervous systems and suggest that the pathogenic c.521-2A>G mutation could lead to an altered effect on tubulin dynamics.

Keywords: Cree; PRUNE1; myoclonic epilepsy; neurodegenerative; peripheral neuropathy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acid Ceramidase / genetics
  • Central Nervous System / metabolism
  • Central Nervous System / physiopathology
  • Child
  • Child, Preschool
  • Exome Sequencing
  • Female
  • Founder Effect
  • Homozygote
  • Humans
  • Infant
  • Infant, Newborn
  • Male
  • Manitoba / epidemiology
  • Microcephaly / genetics*
  • Microcephaly / physiopathology
  • Mutation
  • Neurodegenerative Diseases / genetics*
  • Neurodegenerative Diseases / pathology
  • Pedigree
  • Phenotype
  • Phosphoric Monoester Hydrolases / genetics*
  • Polymorphism, Single Nucleotide / genetics
  • RNA Splice Sites / genetics*
  • Tubulin / genetics
  • Tubulin / metabolism

Substances

  • RNA Splice Sites
  • Tubulin
  • PRUNE1 protein, human
  • Phosphoric Monoester Hydrolases
  • Acid Ceramidase