ER procollagen storage defect without coupled unfolded protein response drives precocious arthritis

Life Sci Alliance. 2024 Jul 9;7(9):e202402842. doi: 10.26508/lsa.202402842. Print 2024 Sep.

Abstract

Collagenopathies are a group of clinically diverse disorders caused by defects in collagen folding and secretion. For example, mutations in the gene encoding collagen type-II, the primary collagen in cartilage, can lead to diverse chondrodysplasias. One example is the Gly1170Ser substitution in procollagen-II, which causes precocious osteoarthritis. Here, we biochemically and mechanistically characterize an induced pluripotent stem cell-based cartilage model of this disease, including both hetero- and homozygous genotypes. We show that Gly1170Ser procollagen-II is notably slow to fold and secrete. Instead, procollagen-II accumulates intracellularly, consistent with an endoplasmic reticulum (ER) storage disorder. Likely owing to the unique features of the collagen triple helix, this accumulation is not recognized by the unfolded protein response. Gly1170Ser procollagen-II interacts to a greater extent than wild-type with specific ER proteostasis network components, consistent with its slow folding. These findings provide mechanistic elucidation into the etiology of this disease. Moreover, the easily expandable cartilage model will enable rapid testing of therapeutic strategies to restore proteostasis in the collagenopathies.

MeSH terms

  • Animals
  • Arthritis / genetics
  • Arthritis / metabolism
  • Cartilage / metabolism
  • Cartilage / pathology
  • Chondrocytes / metabolism
  • Collagen Type II* / metabolism
  • Endoplasmic Reticulum* / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Mutation
  • Osteoarthritis / genetics
  • Osteoarthritis / metabolism
  • Osteoarthritis / pathology
  • Procollagen* / metabolism
  • Protein Folding
  • Unfolded Protein Response*

Substances

  • Procollagen
  • Collagen Type II