Production of RANKL by Memory B Cells: A Link Between B Cells and Bone Erosion in Rheumatoid Arthritis

Arthritis Rheumatol. 2016 Apr;68(4):805-16. doi: 10.1002/art.39489.

Abstract

Objective: Rheumatoid arthritis (RA) is a systemic autoimmune disease that often leads to joint damage. The mechanisms of bone damage in RA are complex, involving activation of bone-resorbing osteoclasts (OCs) by synoviocytes and Th17 cells. This study was undertaken to investigate whether B cells play a direct role in osteoclastogenesis through the production of RANKL, the essential cytokine for OC development.

Methods: RANKL production by total B cells or sorted B cell subpopulations in the peripheral blood and synovial tissue from healthy donors or anti-cyclic citrullinated peptide-positive patients with RA was examined by flow cytometry, real-time polymerase chain reaction, enzyme-linked immunosorbent assay, and immunohistochemical analysis. To define direct effects on osteoclastogenesis, B cells were cocultured with CD14+ monocytes, and OCs were enumerated by tartrate-resistant acid phosphatase staining.

Results: Healthy donor peripheral blood B cells were capable of expressing RANKL upon stimulation, with switched memory B cells (CD27+IgD-) having the highest propensity for RANKL production. Notably, switched memory B cells in the peripheral blood from RA patients expressed significantly more RANKL compared to healthy controls. In RA synovial fluid and tissue, memory B cells were enriched and spontaneously expressed RANKL, with some of these cells visualized adjacent to RANK+ OC precursors. Critically, B cells supported OC differentiation in vitro in a RANKL-dependent manner, and the number of OCs was higher in cultures with RA B cells than in those derived from healthy controls.

Conclusion: These findings reveal the critical importance of B cells in bone homeostasis and their likely contribution to joint destruction in RA.

Publication types

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

MeSH terms

  • Acid Phosphatase / metabolism
  • Arthritis, Rheumatoid / immunology
  • Arthritis, Rheumatoid / metabolism*
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism*
  • Bone Resorption / immunology
  • Bone Resorption / metabolism*
  • Case-Control Studies
  • Cell Differentiation / immunology*
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • Humans
  • Immunohistochemistry
  • In Vitro Techniques
  • Isoenzymes / metabolism
  • Monocytes
  • Osteoclasts / immunology
  • Osteoclasts / metabolism*
  • RANK Ligand / immunology
  • RANK Ligand / metabolism*
  • RNA, Messenger / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Synovial Fluid
  • Synovial Membrane / cytology
  • Synovial Membrane / immunology
  • Synovial Membrane / metabolism
  • Tartrate-Resistant Acid Phosphatase

Substances

  • Isoenzymes
  • RANK Ligand
  • RNA, Messenger
  • TNFSF11 protein, human
  • Acid Phosphatase
  • Tartrate-Resistant Acid Phosphatase