Mutations near amino end of alpha1(I) collagen cause combined osteogenesis imperfecta/Ehlers-Danlos syndrome by interference with N-propeptide processing

J Biol Chem. 2005 May 13;280(19):19259-69. doi: 10.1074/jbc.M414698200. Epub 2005 Feb 22.

Abstract

Patients with OI/EDS form a distinct subset of osteogenesis imperfecta (OI) patients. In addition to skeletal fragility, they have characteristics of Ehlers-Danlos syndrome (EDS). We identified 7 children with types III or IV OI, plus severe large and small joint laxity and early progressive scoliosis. In each child with OI/EDS, we identified a mutation in the first 90 residues of the helical region of alpha1(I) collagen. These mutations prevent or delay removal of the procollagen N-propeptide by purified N-proteinase (ADAMTS-2) in vitro and in pericellular assays. The mutant pN-collagen which results is efficiently incorporated into matrix by cultured fibroblasts and osteoblasts and is prominently present in newly incorporated and immaturely cross-linked collagen. Dermal collagen fibrils have significantly reduced cross-sectional diameters, corroborating incorporation of pN-collagen into fibrils in vivo. Differential scanning calorimetry revealed that these mutant collagens are less stable than the corresponding procollagens, which is not seen with other type I collagen helical mutations. These mutations disrupt a distinct folding region of high thermal stability in the first 90 residues at the amino end of type I collagen and alter the secondary structure of the adjacent N-proteinase cleavage site. Thus, these OI/EDS collagen mutations are directly responsible for the bone fragility of OI and indirectly responsible for EDS symptoms, by interference with N-propeptide removal.

MeSH terms

  • ADAM Proteins
  • ADAMTS Proteins
  • ADAMTS4 Protein
  • Adolescent
  • Adult
  • Amino Acid Sequence
  • Calorimetry, Differential Scanning
  • Cells, Cultured
  • Child, Preschool
  • Collagen / metabolism
  • Collagen Type I / genetics*
  • Cross-Linking Reagents / pharmacology
  • DNA Mutational Analysis
  • Ehlers-Danlos Syndrome / genetics*
  • Electrophoresis, Polyacrylamide Gel
  • Extracellular Matrix / metabolism
  • Female
  • Fibroblasts / cytology
  • Hot Temperature
  • Humans
  • Infant
  • Male
  • Microscopy, Electron, Transmission
  • Molecular Sequence Data
  • Mutation*
  • Osteoblasts / metabolism
  • Osteogenesis Imperfecta / genetics*
  • Peptides / chemistry
  • Phenotype
  • Procollagen N-Endopeptidase / metabolism
  • Protein Binding
  • Protein Conformation
  • Protein Folding
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Sequence Homology, Amino Acid
  • Skin / cytology
  • Skin / metabolism
  • Time Factors

Substances

  • Collagen Type I
  • Cross-Linking Reagents
  • Peptides
  • Collagen
  • ADAM Proteins
  • ADAMTS Proteins
  • ADAMTS2 protein, human
  • Procollagen N-Endopeptidase
  • ADAMTS4 Protein