Blood phenylalanine lowering partially reverses white matter changes in a mouse model of phenylketonuria

Mol Ther. 2025 Sep 3;33(9):4303-4319. doi: 10.1016/j.ymthe.2025.06.020. Epub 2025 Jun 14.

Abstract

Phenylketonuria (PKU) is a genetic defect caused by lack of the liver enzyme phenylalanine hydroxylase (PAH). This deficiency results in elevated blood phenylalanine (Phe) levels and neurotoxicity, which is manifested by reduced brain size, lower neurotransmitter levels, and reduced myelination. The goal of this study was to investigate brain myelination defects and their reversibility upon blood Phe lowering by analyzing the corpus callosum (CC) of adult Pahenu2 (PAH-deficient) mice. MRI and immunostaining demonstrated a significant reduction in CC volume in Pahenu2 mice. Treatment with an adeno-associated vector (AAV) encoding mouse PAH for 3.5 months improved but did not completely normalize CC volume. Total cholesterol, a major component of myelin, was unchanged in the CC of Pahenu2 mouse, while some sterol intermediates were significantly reduced by treatment. Single-nuclei transcriptomics showed an upregulation of oxidative stress-related pathways and increased expression of transthyretin, ApoE, Cst3, and Cd81 in CC in Pahenu2 mice. Normalization of blood Phe restored gene expression to levels comparable to those of heterozygous mice and was associated with the generation of differentiated myelin-producing oligodendrocyte subtypes and neuroprotective astrocytes. In summary, Pahenu2 mice showed white matter abnormalities and changes in transcriptome and sterol profiles, which were partially corrected by the normalization of blood Phe.

Keywords: AAV gene delivery; Pah(enu2) mice; brain white matter; phenylketonuria; single-cell analysis; transcriptome.

MeSH terms

  • Animals
  • Corpus Callosum / metabolism
  • Corpus Callosum / pathology
  • Dependovirus / genetics
  • Disease Models, Animal
  • Genetic Therapy
  • Genetic Vectors / administration & dosage
  • Genetic Vectors / genetics
  • Mice
  • Myelin Sheath / metabolism
  • Oligodendroglia / metabolism
  • Phenylalanine Hydroxylase* / genetics
  • Phenylalanine Hydroxylase* / metabolism
  • Phenylalanine* / blood
  • Phenylketonurias* / blood
  • Phenylketonurias* / genetics
  • Phenylketonurias* / pathology
  • Phenylketonurias* / therapy
  • White Matter* / diagnostic imaging
  • White Matter* / metabolism
  • White Matter* / pathology

Substances

  • Phenylalanine Hydroxylase
  • Phenylalanine