Recessive PRDM13 mutations cause fatal perinatal brainstem dysfunction with cerebellar hypoplasia and disrupt Purkinje cell differentiation

Am J Hum Genet. 2022 May 5;109(5):909-927. doi: 10.1016/j.ajhg.2022.03.010. Epub 2022 Apr 6.

Abstract

Pontocerebellar hypoplasias (PCHs) are congenital disorders characterized by hypoplasia or early atrophy of the cerebellum and brainstem, leading to a very limited motor and cognitive development. Although over 20 genes have been shown to be mutated in PCHs, a large proportion of affected individuals remains undiagnosed. We describe four families with children presenting with severe neonatal brainstem dysfunction and pronounced deficits in cognitive and motor development associated with four different bi-allelic mutations in PRDM13, including homozygous truncating variants in the most severely affected individuals. Brain MRI and fetopathological examination revealed a PCH-like phenotype, associated with major hypoplasia of inferior olive nuclei and dysplasia of the dentate nucleus. Notably, histopathological examinations highlighted a sparse and disorganized Purkinje cell layer in the cerebellum. PRDM13 encodes a transcriptional repressor known to be critical for neuronal subtypes specification in the mouse retina and spinal cord but had not been implicated, so far, in hindbrain development. snRNA-seq data mining and in situ hybridization in humans show that PRDM13 is expressed at early stages in the progenitors of the cerebellar ventricular zone, which gives rise to cerebellar GABAergic neurons, including Purkinje cells. We also show that loss of function of prdm13 in zebrafish leads to a reduction in Purkinje cells numbers and a complete absence of the inferior olive nuclei. Altogether our data identified bi-allelic mutations in PRDM13 as causing a olivopontocerebellar hypoplasia syndrome and suggest that early deregulations of the transcriptional control of neuronal fate specification could contribute to a significant number of cases.

Keywords: PRDM13; Purkinje cells; brainstem; cerebellum; inferior olive nuclei; neurodevelopment; neuronal specification; olivopontocerebellar hypoplasia; zebrafish.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Diseases* / pathology
  • Brain Stem
  • Cerebellum / abnormalities
  • Cerebellum / pathology
  • Developmental Disabilities
  • Histone-Lysine N-Methyltransferase / genetics
  • Humans
  • Mice
  • Mutation / genetics
  • Nervous System Malformations
  • Neurogenesis / genetics
  • Purkinje Cells / metabolism
  • Transcription Factors / genetics
  • Zebrafish* / metabolism

Substances

  • Transcription Factors
  • Prdm13 protein, mouse
  • Histone-Lysine N-Methyltransferase

Supplementary concepts

  • Cerebellar Hypoplasia