Localized chondro-ossification underlies joint dysfunction and motor deficits in the Fkbp10 mouse model of osteogenesis imperfecta

Proc Natl Acad Sci U S A. 2021 Jun 22;118(25):e2100690118. doi: 10.1073/pnas.2100690118.

Abstract

Osteogenesis imperfecta (OI) is a genetic disorder that features wide-ranging defects in both skeletal and nonskeletal tissues. Previously, we and others reported that loss-of-function mutations in FK506 Binding Protein 10 (FKBP10) lead to skeletal deformities in conjunction with joint contractures. However, the pathogenic mechanisms underlying joint dysfunction in OI are poorly understood. In this study, we have generated a mouse model in which Fkbp10 is conditionally deleted in tendons and ligaments. Fkbp10 removal substantially reduced telopeptide lysyl hydroxylation of type I procollagen and collagen cross-linking in tendons. These biochemical alterations resulting from Fkbp10 ablation were associated with a site-specific induction of fibrosis, inflammation, and ectopic chondrogenesis followed by joint deformities in postnatal mice. We found that the ectopic chondrogenesis coincided with enhanced Gli1 expression, indicating dysregulated Hedgehog (Hh) signaling. Importantly, genetic inhibition of the Hh pathway attenuated ectopic chondrogenesis and joint deformities in Fkbp10 mutants. Furthermore, Hh inhibition restored alterations in gait parameters caused by Fkbp10 loss. Taken together, we identified a previously unappreciated role of Fkbp10 in tendons and ligaments and pathogenic mechanisms driving OI joint dysfunction.

Keywords: Fkbp10; contracture; ligament; osteogenesis imperfecta; tendon.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Newborn
  • Chondrocytes / pathology*
  • Chondrogenesis / genetics
  • Collagen Type I / metabolism
  • Disease Models, Animal
  • Fibrosis
  • Gait
  • Gene Deletion
  • Gene Expression Regulation
  • Hedgehog Proteins / metabolism
  • Hydroxylation
  • Inflammation / genetics
  • Inflammation / pathology
  • Joints / pathology
  • Joints / physiopathology*
  • Ligaments / pathology
  • Lysine / metabolism
  • Mice
  • Models, Biological
  • Motor Activity*
  • Ossification, Heterotopic / complications
  • Ossification, Heterotopic / genetics
  • Ossification, Heterotopic / pathology
  • Ossification, Heterotopic / physiopathology
  • Osteogenesis Imperfecta / complications
  • Osteogenesis Imperfecta / genetics
  • Osteogenesis Imperfecta / pathology
  • Osteogenesis Imperfecta / physiopathology*
  • Osteogenesis* / genetics
  • Peptides / metabolism
  • Sequence Analysis, RNA
  • Signal Transduction
  • Tacrolimus Binding Proteins / genetics
  • Tacrolimus Binding Proteins / metabolism*
  • Tendons / pathology

Substances

  • Collagen Type I
  • Hedgehog Proteins
  • Peptides
  • collagen type I trimeric cross-linked peptide
  • Tacrolimus Binding Proteins
  • Fkbp10 protein, mouse
  • Lysine