Identification of disease-relevant modulators of the SHH pathway in the developing brain

Development. 2021 Sep 1;148(17):dev199307. doi: 10.1242/dev.199307. Epub 2021 Aug 31.

Abstract

Pathogenic gene variants in humans that affect the sonic hedgehog (SHH) pathway lead to severe brain malformations with variable penetrance due to unknown modifier genes. To identify such modifiers, we established novel congenic mouse models. LRP2-deficient C57BL/6N mice suffer from heart outflow tract defects and holoprosencephaly caused by impaired SHH activity. These defects are fully rescued on a FVB/N background, indicating a strong influence of modifier genes. Applying comparative transcriptomics, we identified Pttg1 and Ulk4 as candidate modifiers upregulated in the rescue strain. Functional analyses showed that ULK4 and PTTG1, both microtubule-associated proteins, are positive regulators of SHH signaling, rendering the pathway more resilient to disturbances. In addition, we characterized ULK4 and PTTG1 as previously unidentified components of primary cilia in the neuroepithelium. The identification of genes that powerfully modulate the penetrance of genetic disturbances affecting the brain and heart is likely relevant to understanding the variability in human congenital disorders.

Keywords: Forebrain development; Heart; Holoprosencephaly; Modifier genes; Primary cilium; SHH.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / embryology*
  • Brain / metabolism
  • Cilia / metabolism
  • Disease Models, Animal
  • Genes, Modifier / physiology*
  • Heart Defects, Congenital / genetics
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism*
  • Holoprosencephaly / genetics
  • Low Density Lipoprotein Receptor-Related Protein-2 / genetics
  • Low Density Lipoprotein Receptor-Related Protein-2 / metabolism
  • Mice
  • Mutation
  • Neuroepithelial Cells / metabolism
  • Penetrance
  • Phenotype
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Securin / genetics
  • Securin / metabolism
  • Signal Transduction*

Substances

  • Hedgehog Proteins
  • Low Density Lipoprotein Receptor-Related Protein-2
  • Lrp2 protein, mouse
  • PTTG1 protein, mouse
  • Securin
  • Shh protein, mouse
  • Ulk4 protein, mouse
  • Protein Serine-Threonine Kinases