Loss-of-function mutation of c-Ret causes cerebellar hypoplasia in mice with Hirschsprung disease and Down's syndrome

J Biol Chem. 2021 Jan-Jun:296:100389. doi: 10.1016/j.jbc.2021.100389. Epub 2021 Feb 6.

Abstract

The c-RET proto-oncogene encodes a receptor-tyrosine kinase. Loss-of-function mutations of RET have been shown to be associated with Hirschsprung disease and Down's syndrome (HSCR-DS) in humans. DS is known to involve cerebellar hypoplasia, which is characterized by reduced cerebellar size. Despite the fact that c-Ret has been shown to be associated with HSCR-DS in humans and to be expressed in Purkinje cells (PCs) in experimental animals, there is limited information about the role of activity of c-Ret/c-RET kinase in cerebellar hypoplasia. We found that a loss-of-function mutation of c-Ret Y1062 in PCs causes cerebellar hypoplasia in c-Ret mutant mice. Wild-type mice had increased phosphorylation of c-Ret in PCs during postnatal development, while c-Ret mutant mice had postnatal hypoplasia of the cerebellum with immature neurite outgrowth in PCs and granule cells (GCs). c-Ret mutant mice also showed decreased numbers of glial fibers and mitogenic sonic hedgehog (Shh)-positive vesicles in the external germinal layer of PCs. c-Ret-mediated cerebellar hypoplasia was rescued by subcutaneous injection of a smoothened agonist (SAG) as well as by reduced expression of Patched1, a negative regulator for Shh. Our results suggest that the loss-of-function mutation of c-Ret Y1062 results in the development of cerebellar hypoplasia via impairment of the Shh-mediated development of GCs and glial fibers in mice with HSCR-DS.

Keywords: cerebellum; neurite outgrowth; neurological disease; phosphotyrosine; receptor tyrosine kinase; sonic hedgehog (Shh).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cerebellum / abnormalities*
  • Cerebellum / metabolism
  • Cerebellum / pathology
  • Developmental Disabilities / genetics
  • Developmental Disabilities / metabolism
  • Developmental Disabilities / pathology
  • Disease Models, Animal
  • Down Syndrome / complications
  • Down Syndrome / genetics*
  • Down Syndrome / metabolism
  • Down Syndrome / pathology
  • Gene Knock-In Techniques / methods
  • Hedgehog Proteins / metabolism
  • Hirschsprung Disease / complications
  • Hirschsprung Disease / genetics*
  • Hirschsprung Disease / metabolism
  • Hirschsprung Disease / pathology
  • Loss of Function Mutation*
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Nervous System Malformations / genetics*
  • Nervous System Malformations / metabolism
  • Nervous System Malformations / pathology
  • Neuroglia / metabolism
  • Neuroglia / pathology
  • Phosphorylation
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins c-ret / genetics*
  • Proto-Oncogene Proteins c-ret / metabolism
  • Purkinje Cells / metabolism
  • Purkinje Cells / pathology

Substances

  • Hedgehog Proteins
  • MAS1 protein, human
  • Proto-Oncogene Mas
  • Shh protein, mouse
  • Proto-Oncogene Proteins c-ret
  • Ret protein, mouse

Supplementary concepts

  • Cerebellar Hypoplasia