Dysregulation of the NRG1/ERBB pathway causes a developmental disorder with gastrointestinal dysmotility in humans

J Clin Invest. 2021 Mar 15;131(6):e145837. doi: 10.1172/JCI145837.

Abstract

Hirschsprung disease (HSCR) is the most frequent developmental anomaly of the enteric nervous system, with an incidence of 1 in 5000 live births. Chronic intestinal pseudo-obstruction (CIPO) is less frequent and classified as neurogenic or myogenic. Isolated HSCR has an oligogenic inheritance with RET as the major disease-causing gene, while CIPO is genetically heterogeneous, caused by mutations in smooth muscle-specific genes. Here, we describe a series of patients with developmental disorders including gastrointestinal dysmotility, and investigate the underlying molecular bases. Trio-exome sequencing led to the identification of biallelic variants in ERBB3 and ERBB2 in 8 individuals variably associating HSCR, CIPO, peripheral neuropathy, and arthrogryposis. Thorough gut histology revealed aganglionosis, hypoganglionosis, and intestinal smooth muscle abnormalities. The cell type-specific ErbB3 and ErbB2 function was further analyzed in mouse single-cell RNA sequencing data and in a conditional ErbB3-deficient mouse model, revealing a primary role for ERBB3 in enteric progenitors. The consequences of the identified variants were evaluated using quantitative real-time PCR (RT-qPCR) on patient-derived fibroblasts or immunoblot assays on Neuro-2a cells overexpressing WT or mutant proteins, revealing either decreased expression or altered phosphorylation of the mutant receptors. Our results demonstrate that dysregulation of ERBB3 or ERBB2 leads to a broad spectrum of developmental anomalies, including intestinal dysmotility.

Keywords: Development; Gastroenterology; Genetic diseases; Molecular genetics.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Animals
  • Child, Preschool
  • Developmental Disabilities / genetics*
  • Developmental Disabilities / pathology
  • Disease Models, Animal
  • Female
  • Gastrointestinal Motility / genetics
  • Hirschsprung Disease / genetics
  • Hirschsprung Disease / pathology
  • Humans
  • Infant, Newborn
  • Intestinal Pseudo-Obstruction / genetics*
  • Intestinal Pseudo-Obstruction / pathology
  • Male
  • Mice
  • Models, Molecular
  • Mutation*
  • Neuregulin-1 / genetics*
  • Pedigree
  • Phenotype
  • Pregnancy
  • Receptor, ErbB-2 / chemistry
  • Receptor, ErbB-2 / genetics*
  • Receptor, ErbB-3 / chemistry
  • Receptor, ErbB-3 / deficiency
  • Receptor, ErbB-3 / genetics*

Substances

  • NRG1 protein, human
  • Neuregulin-1
  • ERBB2 protein, human
  • ERBB3 protein, human
  • ErbB3 protein, mouse
  • Receptor, ErbB-2
  • Receptor, ErbB-3

Grants and funding

TLL fourth year PhD fellowship