Mutations in GREB1L Cause Bilateral Kidney Agenesis in Humans and Mice

Am J Hum Genet. 2017 Nov 2;101(5):803-814. doi: 10.1016/j.ajhg.2017.09.026.

Abstract

Congenital anomalies of the kidney and urinary tract (CAKUT) constitute a major cause of chronic kidney disease in children and 20% of prenatally detected anomalies. CAKUT encompass a spectrum of developmental kidney defects, including renal agenesis, hypoplasia, and cystic and non-cystic dysplasia. More than 50 genes have been reported as mutated in CAKUT-affected case subjects. However, the pathophysiological mechanisms leading to bilateral kidney agenesis (BKA) remain largely elusive. Whole-exome or targeted exome sequencing of 183 unrelated familial and/or severe CAKUT-affected case subjects, including 54 fetuses with BKA, led to the identification of 16 heterozygous variants in GREB1L (growth regulation by estrogen in breast cancer 1-like), a gene reported as a target of retinoic acid signaling. Four loss-of-function and 12 damaging missense variants, 14 being absent from GnomAD, were identified. Twelve of them were present in familial or simplex BKA-affected case subjects. Female BKA-affected fetuses also displayed uterus agenesis. We demonstrated a significant association between GREB1L variants and BKA. By in situ hybridization, we showed expression of Greb1l in the nephrogenic zone in developing mouse kidney. We generated a Greb1l knock-out mouse model by CRISPR-Cas9. Analysis at E13.5 revealed lack of kidneys and genital tract anomalies in male and female Greb1l-/- embryos and a slight decrease in ureteric bud branching in Greb1l+/- embryos. We showed that Greb1l invalidation in mIMCD3 cells affected tubulomorphogenesis in 3D-collagen culture, a phenotype rescued by expression of the wild-type human protein. This demonstrates that GREB1L plays a major role in early metanephros and genital development in mice and humans.

Keywords: 3DISCO; CAKUT; GREB1L; genital tract; heart defect; kidney agenesis; kidney development; mouse model; nephrogenesis; tubulogenesis.

MeSH terms

  • Animals
  • Child
  • Congenital Abnormalities / genetics*
  • Exome / genetics
  • Female
  • Fetus / abnormalities
  • Heterozygote
  • Humans
  • Kidney / abnormalities*
  • Kidney Diseases / congenital*
  • Kidney Diseases / genetics
  • Male
  • Membrane Proteins
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutation / genetics*
  • Neoplasm Proteins / genetics*
  • Phenotype
  • Proteins / genetics*
  • Urinary Tract / abnormalities
  • Urogenital Abnormalities / genetics

Substances

  • GREB1 protein, human
  • KIAA0575 protein, mouse
  • Membrane Proteins
  • Neoplasm Proteins
  • Proteins

Supplementary concepts

  • Hereditary renal agenesis
  • Renal Adysplasia