Osteoarthritis-associated basic calcium phosphate crystals alter immune cell metabolism and promote M1 macrophage polarization

Osteoarthritis Cartilage. 2020 May;28(5):603-612. doi: 10.1016/j.joca.2019.10.010. Epub 2019 Nov 12.

Abstract

Objective: A number of studies have demonstrated that molecules called 'alarmins' or danger-associated molecular patterns (DAMPs), contribute to inflammatory processes in the OA joint. Metabolic reprogramming of immune cells, including macrophages, is emerging as a prominent player in determining immune cell phenotype and function. The aim of this study was to investigate if basic calcium phosphate (BCP) crystals which are OA-associated DAMPs, impact on macrophage phenotype and metabolism.

Methods: Human monocyte derived macrophages were treated with BCP crystals and expression of M1 (CXCL9, CXCL10) and M2 (MRC1, CCL13)-associated markers was assessed by real-time PCR while surface maturation marker (CD40, CD80 & CD86) expression was assessed by flow cytometry. BCP induced metabolic changes were assessed by Seahorse analysis and glycolytic marker expression (hexokinase 2(HK2), Glut1 and HIF1α) was examined using real-time PCR and immunoblotting.

Results: Treatment with BCP crystals upregulated mRNA levels of CXCL9 and CXCL10 while concomitantly downregulating expression of CCL13 and MRC1. Furthermore, BCP-treated macrophages enhanced surface expression of the maturation makers, CD40, CD80 and CD86. BCP-treated cells also exhibited a shift towards glycolysis as evidenced by an increased ECAR/OCR ratio and enhanced expression of the glycolytic markers, HK2, Glut1 and HIF1α. Finally, BCP-induced macrophage activation and alarmin expression was reduced in the presence of the glycolytic inhibitor, 2-DG.

Conclusions: This study not only provides further insight into how OA-associated DAMPs impact on immune cell function, but also highlights metabolic reprogramming as a potential therapeutic target for calcium crystal-related arthropathies.

Keywords: BCP crystals; Immunometabolism; Macrophage polarization; Metabolic reprogramming.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • B7-1 Antigen / metabolism
  • B7-2 Antigen / metabolism
  • CD40 Antigens / metabolism
  • Calcium Phosphates / pharmacology*
  • Chemokine CXCL10 / drug effects
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL10 / immunology
  • Chemokine CXCL9 / drug effects
  • Chemokine CXCL9 / genetics
  • Chemokine CXCL9 / immunology
  • Cytokines / drug effects*
  • Cytokines / genetics
  • Down-Regulation
  • Glucose Transporter Type 1 / drug effects
  • Glucose Transporter Type 1 / genetics
  • Glucose Transporter Type 1 / metabolism
  • Glycolysis / drug effects*
  • Glycolysis / genetics
  • Hexokinase / drug effects
  • Hexokinase / genetics
  • Hexokinase / metabolism
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / drug effects
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Macrophage Activation
  • Macrophages / drug effects*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Membrane Glycoproteins / drug effects
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology
  • Monocyte Chemoattractant Proteins / drug effects
  • Monocyte Chemoattractant Proteins / genetics
  • Monocyte Chemoattractant Proteins / immunology
  • Osteoarthritis / genetics
  • Osteoarthritis / immunology*
  • Phenotype
  • RNA, Messenger / drug effects
  • RNA, Messenger / metabolism
  • Real-Time Polymerase Chain Reaction
  • Receptors, Immunologic / drug effects
  • Receptors, Immunologic / genetics
  • Receptors, Immunologic / immunology
  • Up-Regulation

Substances

  • B7-1 Antigen
  • B7-2 Antigen
  • CCL13 protein, human
  • CD40 Antigens
  • CXCL10 protein, human
  • CXCL9 protein, human
  • Calcium Phosphates
  • Chemokine CXCL10
  • Chemokine CXCL9
  • Cytokines
  • Glucose Transporter Type 1
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • MRC1 protein, human
  • Membrane Glycoproteins
  • Monocyte Chemoattractant Proteins
  • RNA, Messenger
  • Receptors, Immunologic
  • SLC2A1 protein, human
  • HK2 protein, human
  • Hexokinase