Imbalanced cellular metabolism compromises cartilage homeostasis and joint function in a mouse model of mucolipidosis type III gamma

Dis Model Mech. 2020 Nov 18;13(11):dmm046425. doi: 10.1242/dmm.046425.

Abstract

Mucolipidosis type III (MLIII) gamma is a rare inherited lysosomal storage disorder caused by mutations in GNPTG encoding the γ-subunit of GlcNAc-1-phosphotransferase, the key enzyme ensuring proper intracellular location of multiple lysosomal enzymes. Patients with MLIII gamma typically present with osteoarthritis and joint stiffness, suggesting cartilage involvement. Using Gnptg knockout (Gnptgko ) mice as a model of the human disease, we showed that missorting of a number of lysosomal enzymes is associated with intracellular accumulation of chondroitin sulfate in Gnptgko chondrocytes and their impaired differentiation, as well as with altered microstructure of the cartilage extracellular matrix (ECM). We also demonstrated distinct functional and structural properties of the Achilles tendons isolated from Gnptgko and Gnptab knock-in (Gnptabki ) mice, the latter displaying a more severe phenotype resembling mucolipidosis type II (MLII) in humans. Together with comparative analyses of joint mobility in MLII and MLIII patients, these findings provide a basis for better understanding of the molecular reasons leading to joint pathology in these patients. Our data suggest that lack of GlcNAc-1-phosphotransferase activity due to defects in the γ-subunit causes structural changes within the ECM of connective and mechanosensitive tissues, such as cartilage and tendon, and eventually results in functional joint abnormalities typically observed in MLIII gamma patients. This idea was supported by a deficit of the limb motor function in Gnptgko mice challenged on a rotarod under fatigue-associated conditions, suggesting that the impaired motor performance of Gnptgko mice was caused by fatigue and/or pain at the joint.This article has an associated First Person interview with the first author of the paper.

Keywords: Cartilage; Extracellular matrix; Joints; Lysosomal enzymes; MLIII gamma; Tendon.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Achilles Tendon / pathology
  • Achilles Tendon / ultrastructure
  • Aging / pathology
  • Animals
  • Cartilage / pathology*
  • Cartilage / ultrastructure
  • Cell Differentiation
  • Chondrocytes / metabolism
  • Chondrocytes / pathology
  • Chondrocytes / ultrastructure
  • Disease Models, Animal
  • Extracellular Matrix / metabolism
  • Extracellular Matrix / ultrastructure
  • Fibrillar Collagens / metabolism
  • Homeostasis*
  • Joints / pathology*
  • Lysosomes / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Motor Activity
  • Mucolipidoses / metabolism*
  • Mucolipidoses / pathology*
  • Mucolipidoses / physiopathology
  • Transferases (Other Substituted Phosphate Groups) / metabolism

Substances

  • Fibrillar Collagens
  • Transferases (Other Substituted Phosphate Groups)

Supplementary concepts

  • Mucolipidosis III Gamma