Retinoic acid catabolizing enzyme CYP26C1 is a genetic modifier in SHOX deficiency

EMBO Mol Med. 2016 Dec 1;8(12):1455-1469. doi: 10.15252/emmm.201606623. Print 2016 Dec.

Abstract

Mutations in the homeobox gene SHOX cause SHOX deficiency, a condition with clinical manifestations ranging from short stature without dysmorphic signs to severe mesomelic skeletal dysplasia. In rare cases, individuals with SHOX deficiency are asymptomatic. To elucidate the factors that modify disease severity/penetrance, we studied a three-generation family with SHOX deficiency. The variant p.Phe508Cys of the retinoic acid catabolizing enzyme CYP26C1 co-segregated with the SHOX variant p.Val161Ala in the affected individuals, while the SHOX mutant alone was present in asymptomatic individuals. Two further cases with SHOX deficiency and damaging CYP26C1 variants were identified in a cohort of 68 individuals with LWD The identified CYP26C1 variants affected its catabolic activity, leading to an increased level of retinoic acid. High levels of retinoic acid significantly decrease SHOX expression in human primary chondrocytes and zebrafish embryos. Individual morpholino knockdown of either gene shortens the pectoral fins, whereas depletion of both genes leads to a more severe phenotype. Together, our findings describe CYP26C1 as the first genetic modifier for SHOX deficiency.

Keywords: clinical variability; genetic modifiers; limb development; retinoic acid; skeletal dysplasia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Animals
  • Child
  • Cytochrome P450 Family 26 / genetics*
  • Cytochrome P450 Family 26 / metabolism
  • Female
  • Gene Expression Profiling
  • Genetic Predisposition to Disease*
  • Genetic Variation
  • Growth Disorders / genetics*
  • Growth Disorders / pathology*
  • Homeodomain Proteins / genetics*
  • Humans
  • Male
  • Middle Aged
  • Osteochondrodysplasias / genetics*
  • Osteochondrodysplasias / pathology*
  • Retinoic Acid 4-Hydroxylase / genetics
  • Retinoic Acid 4-Hydroxylase / metabolism
  • Sequence Analysis, DNA
  • Severity of Illness Index
  • Short Stature Homeobox Protein
  • Tretinoin / metabolism
  • Young Adult
  • Zebrafish / anatomy & histology
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism

Substances

  • Homeodomain Proteins
  • SHOX protein, human
  • Short Stature Homeobox Protein
  • Zebrafish Proteins
  • Tretinoin
  • CYP26C1 protein, human
  • Cyp26c1 protein, zebrafish
  • Cytochrome P450 Family 26
  • Retinoic Acid 4-Hydroxylase

Supplementary concepts

  • Leri-Weil syndrome