Betaine ameliorates schizophrenic traits by functionally compensating for KIF3-based CRMP2 transport

Cell Rep. 2021 Apr 13;35(2):108971. doi: 10.1016/j.celrep.2021.108971.

Abstract

In schizophrenia (SCZ), neurons in the brain tend to undergo gross morphological changes, but the related molecular mechanism remains largely elusive. Using Kif3b+/- mice as a model with SCZ-like behaviors, we found that a high-betaine diet can significantly alleviate schizophrenic traits related to neuronal morphogenesis and behaviors. According to a deficiency in the transport of collapsin response mediator protein 2 (CRMP2) by the KIF3 motor, we identified a significant reduction in lamellipodial dynamics in developing Kif3b+/- neurons as a cause of neurite hyperbranching. Betaine administration significantly decreases CRMP2 carbonylation, which enhances the F-actin bundling needed for proper lamellipodial dynamics and microtubule exclusion and may thus functionally compensate for KIF3 deficiency. Because the KIF3 expression levels tend to be downregulated in the human prefrontal cortex of the postmortem brains of SCZ patients, this mechanism may partly participate in human SCZ pathogenesis, which we hypothesize could be alleviated by betaine administration.

Keywords: CRMP2; KIF3; actin dynamics; betaine; carbonylation; kinesin; lamellipodia; neurite branching; schizophrenia; social interaction.

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Animals
  • Behavior, Animal / drug effects
  • Betaine / pharmacology*
  • Biological Transport
  • Diet / methods
  • Disease Models, Animal
  • Gene Expression Regulation, Developmental
  • Humans
  • Intercellular Signaling Peptides and Proteins / deficiency
  • Intercellular Signaling Peptides and Proteins / genetics*
  • Kinesins / deficiency
  • Kinesins / genetics*
  • Male
  • Mice
  • Mice, Knockout
  • Microtubules / drug effects
  • Microtubules / metabolism
  • Microtubules / ultrastructure
  • Nerve Tissue Proteins / deficiency
  • Nerve Tissue Proteins / genetics*
  • Neurons / drug effects*
  • Neurons / metabolism
  • Neurons / ultrastructure
  • Prefrontal Cortex / drug effects*
  • Prefrontal Cortex / metabolism
  • Prefrontal Cortex / pathology
  • Protein Binding
  • Protein Carbonylation
  • Pseudopodia / drug effects*
  • Pseudopodia / metabolism
  • Pseudopodia / ultrastructure
  • Schizophrenia / diet therapy*
  • Schizophrenia / genetics
  • Schizophrenia / metabolism
  • Schizophrenia / pathology

Substances

  • Actins
  • Intercellular Signaling Peptides and Proteins
  • Kif3b protein, mouse
  • Nerve Tissue Proteins
  • collapsin response mediator protein-2
  • Betaine
  • Kinesins