Mutations in RAD21 disrupt regulation of APOB in patients with chronic intestinal pseudo-obstruction

Gastroenterology. 2015 Apr;148(4):771-782.e11. doi: 10.1053/j.gastro.2014.12.034. Epub 2015 Jan 6.

Abstract

Background & aims: Chronic intestinal pseudo-obstruction (CIPO) is characterized by severe intestinal dysmotility that mimics a mechanical subocclusion with no evidence of gut obstruction. We searched for genetic variants associated with CIPO to increase our understanding of its pathogenesis and to identify potential biomarkers.

Methods: We performed whole-exome sequencing of genomic DNA from patients with familial CIPO syndrome. Blood and lymphoblastoid cells were collected from patients and controls (individuals without CIPO); levels of messenger RNA (mRNA) and proteins were analyzed by quantitative reverse-transcription polymerase chain reaction, immunoblot, and mobility shift assays. Complementary DNAs were transfected into HEK293 cells. Expression of rad21 was suppressed in zebrafish embryos using a splice-blocking morpholino (rad21a). Gut tissues were collected and analyzed.

Results: We identified a homozygous mutation (p.622, encodes Ala>Thr) in RAD21 in patients from a consanguineous family with CIPO. Expression of RUNX1, a target of RAD21, was reduced in cells from patients with CIPO compared with controls. In zebrafish, suppression of rad21a reduced expression of runx1; this phenotype was corrected by injection of human RAD21 mRNA, but not with the mRNA from the mutated p.622 allele. rad21a Morpholino zebrafish had delayed intestinal transit and greatly reduced numbers of enteric neurons, similar to patients with CIPO. This defect was greater in zebrafish with suppressed expression of ret and rad21, indicating their interaction in the regulation of gut neurogenesis. The promoter region of APOB bound RAD21 but not RAD21 p.622 Ala>Thr; expression of wild-type RAD21 in HEK293 cells repressed expression of APOB, compared with control vector. The gut-specific isoform of APOB (APOB48) is overexpressed in sera from patients with CIPO who carry the RAD21 mutation. APOB48 also is overexpressed in sporadic CIPO in sera and gut biopsy specimens.

Conclusions: Some patients with CIPO carry mutations in RAD21 that disrupt the ability of its product to regulate genes such as RUNX1 and APOB. Reduced expression of rad21 in zebrafish, and dysregulation of these target genes, disrupts intestinal transit and the development of enteric neurons.

Keywords: Animal Model; Genetic Analysis; Intestinal Motility; Sporadic and Familial Chronic Intestinal Pseudo-obstruction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Apolipoprotein B-100 / genetics*
  • Case-Control Studies
  • Cell Cycle Proteins / genetics*
  • Chronic Disease
  • Core Binding Factor Alpha 2 Subunit / genetics*
  • DNA-Binding Proteins
  • Enteric Nervous System / metabolism*
  • Enteric Nervous System / physiopathology
  • Female
  • Gastrointestinal Motility / genetics*
  • Gene Expression Profiling
  • Gene Knockdown Techniques
  • HEK293 Cells
  • Humans
  • Intestinal Pseudo-Obstruction / genetics*
  • Intestinal Pseudo-Obstruction / physiopathology
  • Male
  • Middle Aged
  • Nuclear Proteins / genetics*
  • Phosphoproteins / genetics*
  • RNA, Messenger / genetics*
  • Sequence Analysis, DNA
  • Young Adult
  • Zebrafish
  • Zebrafish Proteins / genetics*

Substances

  • APOB protein, human
  • Apolipoprotein B-100
  • Cell Cycle Proteins
  • Core Binding Factor Alpha 2 Subunit
  • DNA-Binding Proteins
  • Nuclear Proteins
  • Phosphoproteins
  • RAD21 protein, human
  • RNA, Messenger
  • RUNX1 protein, human
  • Zebrafish Proteins
  • rad21a protein, zebrafish