Effects of long-term exercise and a high-fat diet on synovial fluid metabolomics and joint structural phenotypes in mice: an integrated network analysis

Osteoarthritis Cartilage. 2021 Nov;29(11):1549-1563. doi: 10.1016/j.joca.2021.08.008. Epub 2021 Aug 28.

Abstract

Objective: To explore how systemic factors that modify knee osteoarthritis risk are connected to 'whole-joint' structural changes by evaluating the effects of high-fat diet and wheel running exercise on synovial fluid (SF) metabolomics.

Methods: Male mice were fed a defined control or high-fat (60% kcal fat) diet from 6 to 52 weeks of age, and half the animals were housed with running wheels from 26 to 52 weeks of age (n = 9-13 per group). Joint tissue structure and osteoarthritis pathology were evaluated by histology and micro-computed tomography. Systemic metabolic and inflammatory changes were evaluated by body composition, glucose tolerance testing, and serum biomarkers. SF metabolites were analyzed by high performance-liquid chromatography mass spectrometry. We built correlation-based network models to evaluate the connectivity between systemic and local metabolic biomarkers and osteoarthritis structural pathology within each experimental group.

Results: High-fat diet caused moderate osteoarthritis, including cartilage pathology, synovitis and increased subchondral bone density. In contrast, voluntary exercise had a negligible effect on these joint structure components. 1,412 SF metabolite features were detected, with high-fat sedentary mice being the most distinct. Diet and activity uniquely altered SF metabolites attributed to amino acids, lipids, and steroids. Notably, high-fat diet increased network connections to systemic biomarkers such as interleukin-1β and glucose intolerance. In contrast, exercise increased local joint-level network connections, especially among subchondral bone features and SF metabolites.

Conclusion: Network mapping showed that obesity strengthened SF metabolite links to blood glucose and inflammation, whereas exercise strengthened SF metabolite links to subchondral bone structure.

Keywords: Exercise; Metabolomics; Obesity; Osteoarthritis; Synovial fluid; Systems biology.

Publication types

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

MeSH terms

  • Animals
  • Biomarkers / blood
  • Chemokine CCL2 / blood
  • Chondrocytes / pathology
  • Diet, High-Fat*
  • Glucose Intolerance
  • Hypertrophy
  • Interleukin-10 / blood
  • Interleukin-1beta / blood
  • Interleukin-8 / blood
  • Leptin / blood
  • Metabolomics
  • Mice
  • Mice, Inbred C57BL
  • Osteoarthritis
  • Physical Conditioning, Animal*
  • Stifle / diagnostic imaging*
  • Stifle / pathology*
  • Synovial Fluid / metabolism*
  • X-Ray Microtomography

Substances

  • Biomarkers
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Interleukin-1beta
  • Interleukin-8
  • Leptin
  • Interleukin-10