Loss of PHF6 causes spontaneous seizures, enlarged brain ventricles and altered transcription in the cortex of a mouse model of the Börjeson-Forssman-Lehmann intellectual disability syndrome

PLoS Genet. 2024 Oct 15;20(10):e1011428. doi: 10.1371/journal.pgen.1011428. eCollection 2024 Oct.

Abstract

Börjeson-Forssman-Lehmann syndrome (BFLS) is an X-linked intellectual disability and endocrine disorder caused by pathogenic variants of plant homeodomain finger gene 6 (PHF6). An understanding of the role of PHF6 in vivo in the development of the mammalian nervous system is required to advance our knowledge of how PHF6 mutations cause BFLS. Here, we show that PHF6 protein levels are greatly reduced in cells derived from a subset of patients with BFLS. We report the phenotypic, anatomical, cellular and molecular characterization of the brain in males and females in two mouse models of BFLS, namely loss of Phf6 in the germline and nervous system-specific deletion of Phf6. We show that loss of PHF6 resulted in spontaneous seizures occurring via a neural intrinsic mechanism. Histological and morphological analysis revealed a significant enlargement of the lateral ventricles in adult Phf6-deficient mice, while other brain structures and cortical lamination were normal. Phf6 deficient neural precursor cells showed a reduced capacity for self-renewal and increased differentiation into neurons. Phf6 deficient cortical neurons commenced spontaneous neuronal activity prematurely suggesting precocious neuronal maturation. We show that loss of PHF6 in the foetal cortex and isolated cortical neurons predominantly caused upregulation of genes, including Reln, Nr4a2, Slc12a5, Phip and ZIC family transcription factor genes, involved in neural development and function, providing insight into the molecular effects of loss of PHF6 in the developing brain.

MeSH terms

  • Animals
  • Calcinosis / genetics
  • Calcinosis / metabolism
  • Calcinosis / pathology
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / pathology
  • Disease Models, Animal
  • Face / abnormalities
  • Female
  • Fingers / abnormalities
  • Humans
  • Hypogonadism / genetics
  • Hypogonadism / metabolism
  • Hypogonadism / pathology
  • Intellectual Disability / genetics
  • Male
  • Mental Retardation, X-Linked* / genetics
  • Mental Retardation, X-Linked* / pathology
  • Mice
  • Mice, Knockout
  • Neural Stem Cells / metabolism
  • Obesity
  • Repressor Proteins* / genetics
  • Repressor Proteins* / metabolism
  • Seizures* / genetics
  • Seizures* / metabolism
  • Transcription, Genetic
  • Vestibular Diseases / genetics
  • Vestibular Diseases / pathology

Substances

  • PHF6 protein, human
  • Phf6 protein, mouse
  • Repressor Proteins

Supplementary concepts

  • Borjeson-Forssman-Lehmann syndrome

Grants and funding

This work was supported by an Australian Postgraduate Award (H.M.M.), National Health and Medical Research Council (NHMRC) Project grants (1029481 and 1084248 to A.K.V.), NHMRC Research Fellowships (1003435 [T.T.], 575512 and 1081421 [A.K.V.], 1154970 [G.K.S.] and 1155224 [J.G.], NHMRC investigator grants 1176789 [A.K.V.] and 2025645 [G.K.S.]), Independent Research Institutes Infrastructure Support Scheme from the Australian Government’s NHMRC, and a Victorian State Government Operational Infrastructure Support Grant. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.