Patient-specific mutation of Dync1h1 in mice causes brain and behavioral deficits

Neurobiol Dis. 2024 Sep:199:106594. doi: 10.1016/j.nbd.2024.106594. Epub 2024 Jul 16.

Abstract

Aims: Cytoplasmic dynein heavy chain (DYNC1H1) is a multi-subunit protein complex that provides motor force for movement of cargo on microtubules and traffics them back to the soma. In humans, mutations along the DYNC1H1 gene result in intellectual disabilities, cognitive delays, and neurologic and motor deficits. The aim of the study was to generate a mouse model to a newly identified de novo heterozygous DYNC1H1 mutation, within a functional ATPase domain (c9052C > T(P3018S)), identified in a child with motor deficits, and intellectual disabilities.

Results: P3018S heterozygous (HET) knockin mice are viable; homozygotes are lethal. Metabolic and EchoMRI™ testing show that HET mice have a higher metabolic rate, are more active, and have less body fat compared to wildtype mice. Neurobehavioral studies show that HET mice perform worse when traversing elevated balance beams, and on the negative geotaxis test. Immunofluorescent staining shows neuronal migration abnormalities in the dorsal and lateral neocortex with heterotopia in layer I. Neuron-subtype specific transcription factors CUX1 and CTGF identified neurons from layers II/III and VI respectively in cortical layer I, and abnormal pyramidal neurons with MAP2+ dendrites projecting downward from the pial surface.

Conclusion: The HET mice are a good model for the motor deficits seen in the child, and highlights the importance of cytoplasmic dynein in the maintenance of cortical function and dendritic orientation relative to the pial surface. Our results are discussed in the context of other dynein mutant mice and in relation to clinical presentation in humans with DYNC1H1 mutations.

Keywords: Abnormal neuronal positioning; Autism spectrum disorder (ASD); Cortical layer-specific transcription factors; De novo dynein heavy chain mutation; Heterotopia; Neuronal migration defects.

MeSH terms

  • Animals
  • Brain / metabolism
  • Brain / pathology
  • Cytoplasmic Dyneins* / genetics
  • Cytoplasmic Dyneins* / metabolism
  • Disease Models, Animal
  • Humans
  • Intellectual Disability / genetics
  • Male
  • Mice
  • Mice, Transgenic
  • Mutation* / genetics
  • Neurons / metabolism
  • Neurons / pathology

Substances

  • Cytoplasmic Dyneins
  • Dync1h1 protein, mouse
  • DYNC1H1 protein, human