Learning impairments and molecular changes in the brain caused by β-catenin loss

Hum Mol Genet. 2019 Sep 1;28(17):2965-2975. doi: 10.1093/hmg/ddz115.

Abstract

Intellectual disability (ID), defined as IQ<70, occurs in 2.5% of individuals. Elucidating the underlying molecular mechanisms is essential for developing therapeutic strategies. Several of the identified genes that link to ID in humans are predicted to cause malfunction of β-catenin pathways, including mutations in CTNNB1 (β-catenin) itself. To identify pathological changes caused by β-catenin loss in the brain, we have generated a new β-catenin conditional knockout mouse (β-cat cKO) with targeted depletion of β-catenin in forebrain neurons during the period of major synaptogenesis, a critical window for brain development and function. Compared with control littermates, β-cat cKO mice display severe cognitive impairments. We tested for changes in two β-catenin pathways essential for normal brain function, cadherin-based synaptic adhesion complexes and canonical Wnt (Wingless-related integration site) signal transduction. Relative to control littermates, β-cat cKOs exhibit reduced levels of key synaptic adhesion and scaffold binding partners of β-catenin, including N-cadherin, α-N-catenin, p120ctn and S-SCAM/Magi2. Unexpectedly, the expression levels of several canonical Wnt target genes were not altered in β-cat cKOs. This lack of change led us to find that β-catenin loss leads to upregulation of γ-catenin (plakoglobin), a partial functional homolog, whose neural-specific role is poorly defined. We show that γ-catenin interacts with several β-catenin binding partners in neurons but is not able to fully substitute for β-catenin loss, likely due to differences in the N-and C-termini between the catenins. Our findings identify severe learning impairments, upregulation of γ-catenin and reductions in synaptic adhesion and scaffold proteins as major consequences of β-catenin loss.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Anxiety
  • Behavior, Animal
  • Brain / metabolism*
  • Brain / physiopathology*
  • Cognitive Dysfunction / diagnosis
  • Cognitive Dysfunction / etiology
  • Cognitive Dysfunction / psychology
  • Disease Models, Animal
  • Disease Susceptibility*
  • Gene Expression Regulation
  • Learning*
  • Mice
  • Mice, Knockout
  • Neurons / metabolism
  • Phenotype
  • Severity of Illness Index
  • Signal Transduction
  • Wnt Proteins / metabolism
  • beta Catenin / deficiency*

Substances

  • Wnt Proteins
  • beta Catenin