Positive Effects of a Young Systemic Environment and High Growth Differentiation Factor 11 Levels on Chondrocyte Proliferation and Cartilage Matrix Synthesis in Old Mice

Arthritis Rheumatol. 2020 Jul;72(7):1123-1133. doi: 10.1002/art.41230. Epub 2020 May 21.

Abstract

Objective: To investigate the effects of a young systemic environment and growth differentiation factor 11 (GDF-11) on aging cartilage.

Methods: A heterochronic parabiosis model (2-month-old mouse and 12-month-old mouse [Y/O]), an isochronic parabiosis model (12-month-old mouse and 12-month-old mouse [O/O]), and 12-month-old mice alone (O) were evaluated. Knee joints and chondrocytes from old mice were examined by radiography, histology, cell proliferation assays, immunohistochemistry, Western blotting, and quantitative reverse transcriptase-polymerase chain reaction 16 weeks after parabiosis surgery. GDF-11 was injected into 12-month-old mouse joints daily for 16 weeks. Cartilage degeneration, cell proliferation, and osteoarthritis-related gene expression were evaluated.

Results: Osteoarthritis Research Society International scores in old mice were significantly lower in the Y/O group than in the O/O and O groups (both P < 0.05). The percentage of 5-ethynyl-2'-deoxyuridine-positive chondrocytes in old mice was significantly higher in the Y/O group than in the other groups (P < 0.05). Type II collagen (CII) and SOX9 messenger RNA levels differed in cartilage from old mice in the Y/O group compared to the O/O and O groups (both P < 0.05). RUNX-2, CX, and matrix metalloproteinase 13 levels were significantly lower in cartilage from old mice in the Y/O group compared to the O/O and O groups (both P < 0.05). Similar results were obtained for protein expression levels and after GDF-11 treatment in vitro and in vivo. Phosphorylated Smad2/3 (pSmad2/3) levels were higher in the recombinant GDF-11-treated group than in the control group.

Conclusion: A young systemic environment promotes chondrocyte proliferation and cartilage matrix synthesis in old mice. GDF-11, a "young factor," contributes to these effects through the up-regulation of pSmad2/3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Aged
  • Aging / genetics*
  • Aging / metabolism
  • Aging / pathology
  • Animals
  • Arthroplasty, Replacement, Knee
  • Bone Morphogenetic Proteins / metabolism
  • Bone Morphogenetic Proteins / pharmacology*
  • Cartilage, Articular / drug effects*
  • Cartilage, Articular / metabolism
  • Cell Proliferation / drug effects*
  • Chondrocytes / drug effects*
  • Chondrocytes / metabolism
  • Collagen Type II / drug effects
  • Collagen Type II / genetics
  • Collagen Type II / metabolism
  • Collagen Type X / drug effects
  • Collagen Type X / genetics
  • Collagen Type X / metabolism
  • Core Binding Factor Alpha 1 Subunit / drug effects
  • Core Binding Factor Alpha 1 Subunit / genetics
  • Core Binding Factor Alpha 1 Subunit / metabolism
  • Extracellular Matrix / drug effects
  • Extracellular Matrix / metabolism
  • Female
  • Growth Differentiation Factors / metabolism
  • Growth Differentiation Factors / pharmacology*
  • Humans
  • In Vitro Techniques
  • Knee Joint
  • Male
  • Matrix Metalloproteinase 13 / drug effects
  • Matrix Metalloproteinase 13 / genetics
  • Matrix Metalloproteinase 13 / metabolism
  • Mice
  • Osteoarthritis, Knee / genetics*
  • Osteoarthritis, Knee / metabolism
  • Parabiosis*
  • Phosphorylation
  • RNA, Messenger / drug effects
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • SOX9 Transcription Factor / drug effects
  • SOX9 Transcription Factor / genetics
  • SOX9 Transcription Factor / metabolism
  • Smad2 Protein / drug effects
  • Smad2 Protein / metabolism
  • Smad3 Protein / drug effects
  • Smad3 Protein / metabolism
  • Stifle
  • Young Adult

Substances

  • Bone Morphogenetic Proteins
  • Collagen Type II
  • Collagen Type X
  • Core Binding Factor Alpha 1 Subunit
  • GDF11 protein, human
  • Gdf11 protein, mouse
  • Growth Differentiation Factors
  • RNA, Messenger
  • Runx2 protein, mouse
  • SOX9 Transcription Factor
  • Smad2 Protein
  • Smad3 Protein
  • Sox9 protein, mouse
  • Matrix Metalloproteinase 13
  • Mmp13 protein, mouse