Vitamin D-Dependent Rickets Type 1 Caused by Mutations in CYP27B1 Affecting Protein Interactions With Adrenodoxin

J Clin Endocrinol Metab. 2016 Sep;101(9):3409-18. doi: 10.1210/jc.2016-2124. Epub 2016 Jul 11.

Abstract

Context: CYP27B1 converts 25-hydroxyvitamin D3 to active 1,25-dihydroxyvitamin D3, playing a vital role in calcium homeostasis and bone growth. Vitamin D-dependent rickets type 1 (VDDR-1) is a rare autosomal recessive disorder caused by mutations in CYP27B1.

Objective: The objective of the study was an enzymatic and structural analysis of mutations in a patient with calcipenic rickets. Design, Setting, Patient, and Intervention: Two siblings presented with calcipenic rickets and normal 1,25-dihydroxyvitamin D3 levels. CYP27B1 gene analysis showed compound heterozygous mutations confirming VDDR-1. We studied wild-type CYP27B1 and mutations H441Y and R459L by computational homology modeling, molecular dynamics simulations, and functional studies using a luciferase assay. The patients were successfully treated with calcitriol.

Main outcome: The main outcomes of the study were novel mutations leading to a severe loss of CYP27B1 activities for metabolism of 25-hydroxyvitamin D3.

Results: Mitochondrial cytochrome P450s require adrenodoxin (FDX1) and adrenodoxin reductase. We created models of CYP27B1-FDX1 complex, which revealed negative effects of mutations H441Y and R459L. Upon structural analysis, near-identical folds, protein contact areas, and orientations of heme/iron-sulfur cluster suggested that both mutations may destabilize the CYP27B1-FDX1 complex by negating directional interactions with adrenodoxin. This system is highly sensitive to small local changes modulating the binding/dissociation of adrenodoxin, and electron-transporting efficiency might change with mutations at the surface. Functional assays confirmed this hypothesis and showed severe loss of activity of CYP27B1 by both mutations.

Conclusions: This is the first report of mutations in CYP27B1 causing VDDR-1 by affecting protein-protein interactions with FDX1 that results in reduced CYP27B1 activities. Detailed characterization of mutations in CYP27B1 is required for understanding the novel molecular mechanisms causing VDDR-1.

Publication types

  • Case Reports

MeSH terms

  • 25-Hydroxyvitamin D3 1-alpha-Hydroxylase / genetics*
  • 25-Hydroxyvitamin D3 1-alpha-Hydroxylase / metabolism
  • Adrenodoxin / metabolism*
  • Amino Acid Sequence
  • Biomarkers / metabolism
  • Familial Hypophosphatemic Rickets / genetics*
  • Familial Hypophosphatemic Rickets / pathology*
  • Female
  • Humans
  • Infant
  • Infant, Newborn
  • Male
  • Mutation / genetics*
  • Prognosis
  • Sequence Homology, Amino Acid
  • Vitamin D / analogs & derivatives
  • Vitamin D / metabolism
  • Vitamin D Deficiency / complications

Substances

  • Biomarkers
  • dihydroxy-vitamin D3
  • Adrenodoxin
  • Vitamin D
  • 25-Hydroxyvitamin D3 1-alpha-Hydroxylase
  • CYP27B1 protein, human

Supplementary concepts

  • Vitamin D Hydroxylation-Deficient Rickets, Type 1A