Adamtsl2 deletion results in bronchial fibrillin microfibril accumulation and bronchial epithelial dysplasia--a novel mouse model providing insights into geleophysic dysplasia

Dis Model Mech. 2015 May;8(5):487-99. doi: 10.1242/dmm.017046. Epub 2015 Mar 11.

Abstract

Mutations in the secreted glycoprotein ADAMTSL2 cause recessive geleophysic dysplasia (GD) in humans and Musladin-Lueke syndrome (MLS) in dogs. GD is a severe, often lethal, condition presenting with short stature, brachydactyly, stiff skin, joint contractures, tracheal-bronchial stenosis and cardiac valve anomalies, whereas MLS is non-lethal and characterized by short stature and severe skin fibrosis. Although most mutations in fibrillin-1 (FBN1) cause Marfan syndrome (MFS), a microfibril disorder leading to transforming growth factor-β (TGFβ) dysregulation, domain-specific FBN1 mutations result in dominant GD. ADAMTSL2 has been previously shown to bind FBN1 and latent TGFβ-binding protein-1 (LTBP1). Here, we investigated mice with targeted Adamtsl2 inactivation as a new model for GD (Adamtsl2(-/-) mice). An intragenic lacZ reporter in these mice showed that ADAMTSL2 was produced exclusively by bronchial smooth muscle cells during embryonic lung development. Adamtsl2(-/-) mice, which died at birth, had severe bronchial epithelial dysplasia with abnormal glycogen-rich inclusions in bronchial epithelium resembling the cellular anomalies described previously in GD. An increase in microfibrils in the bronchial wall was associated with increased FBN2 and microfibril-associated glycoprotein-1 (MAGP1) staining, whereas LTBP1 staining was increased in bronchial epithelium. ADAMTSL2 was shown to bind directly to FBN2 with an affinity comparable to FBN1. The observed extracellular matrix (ECM) alterations were associated with increased bronchial epithelial TGFβ signaling at 17.5 days of gestation; however, treatment with TGFβ-neutralizing antibody did not correct the epithelial dysplasia. These investigations reveal a new function of ADAMTSL2 in modulating microfibril formation, and a previously unsuspected association with FBN2. Our studies suggest that the bronchial epithelial dysplasia accompanying microfibril dysregulation in Adamtsl2(-/-) mice cannot be reversed by TGFβ neutralization, and thus might be mediated by other mechanisms.

Keywords: ADAMTS-like protein; Connective tissue disorder; Extracellular matrix; Fibrillin microfibril; Lung development.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAMTS Proteins
  • Animals
  • Animals, Newborn
  • Bone Diseases, Developmental / metabolism
  • Bone Diseases, Developmental / pathology*
  • Bronchi / pathology*
  • Bronchi / ultrastructure
  • Cellular Microenvironment
  • Disease Models, Animal
  • Epithelium / metabolism
  • Epithelium / pathology*
  • Epithelium / ultrastructure
  • Extracellular Matrix / metabolism
  • Extracellular Matrix Proteins / metabolism*
  • Fibrillin-1
  • Fibrillin-2
  • Fibrillins
  • Gene Deletion*
  • Glycogen / metabolism
  • Limb Deformities, Congenital / metabolism
  • Limb Deformities, Congenital / pathology*
  • Mice, Inbred C57BL
  • Microfibrils / metabolism*
  • Microfilament Proteins / metabolism*
  • Protein Binding
  • Signal Transduction
  • Transforming Growth Factor beta / metabolism

Substances

  • Adamtsl2 protein, mouse
  • Extracellular Matrix Proteins
  • FBN1 protein, human
  • FBN2 protein, human
  • Fbn1 protein, mouse
  • Fbn2 protein, mouse
  • Fibrillin-1
  • Fibrillin-2
  • Fibrillins
  • Microfilament Proteins
  • Transforming Growth Factor beta
  • Glycogen
  • ADAMTS Proteins

Supplementary concepts

  • Acromicric dysplasia