Serum amyloid A chemoattracts immature dendritic cells and indirectly provokes monocyte chemotaxis by induction of cooperating CC and CXC chemokines

Eur J Immunol. 2015 Jan;45(1):101-12. doi: 10.1002/eji.201444818. Epub 2014 Dec 1.

Abstract

Serum amyloid A (SAA) is an acute phase protein that is upregulated in inflammatory diseases and chemoattracts monocytes, lymphocytes, and granulocytes via its G protein-coupled receptor formyl peptide receptor like 1/formyl peptide receptor 2 (FPRL1/FPR2). Here, we demonstrated that the SAA1α isoform also chemoattracts monocyte-derived immature dendritic cells (DCs) in the Boyden and μ-slide chemotaxis assay and that its chemotactic activity for monocytes and DCs was indirectly mediated via rapid chemokine induction. Indeed, SAA1 induced significant amounts (≥5 ng/mL) of macrophage inflammatory protein-1α/CC chemokine ligand 3 (MIP-1α/CCL3) and interleukin-8/CXC chemokine ligand 8 (IL-8/CXCL8) in monocytes and DCs in a dose-dependent manner within 3 h. However, SAA1 also directly activated monocytes and DCs for signaling and chemotaxis without chemokine interference. SAA1-induced monocyte migration was nevertheless significantly prevented (60-80% inhibition) in the constant presence of desensitizing exogenous MIP-1α/CCL3, neutralizing anti-MIP-1α/CCL3 antibody, or a combination of CC chemokine receptor 1 (CCR1) and CCR5 antagonists, indicating that this endogenously produced CC chemokine was indirectly contributing to SAA1-mediated chemotaxis. Further, anti-IL-8/CXCL8 antibody neutralized SAA1-induced monocyte migration, suggesting that endogenous IL-8/CXCL8 acted in concert with MIP-1α/CCL3. This explained why SAA1 failed to synergize with exogenously added MIP-1α/CCL3 or stromal cell-derived factor-1α (SDF-1α)/CXCL12 in monocyte and DC chemotaxis. In addition to direct leukocyte activation, SAA1 induces a chemotactic cascade mediated by expression of cooperating chemokines to prolong leukocyte recruitment to the inflammatory site.

Keywords: Chemokines; Chemotaxis; DCs; Monocytes; Serum amyloid A.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Neutralizing / pharmacology
  • Cell Line
  • Chemokine CCL3 / antagonists & inhibitors
  • Chemokine CCL3 / genetics
  • Chemokine CCL3 / immunology*
  • Chemokine CXCL12 / pharmacology
  • Chemotaxis / drug effects
  • Chemotaxis / immunology
  • Dendritic Cells / cytology
  • Dendritic Cells / drug effects*
  • Dendritic Cells / immunology
  • Diffusion Chambers, Culture
  • Dose-Response Relationship, Immunologic
  • Gene Expression Regulation
  • Humans
  • Interleukin-8 / agonists
  • Interleukin-8 / antagonists & inhibitors
  • Interleukin-8 / genetics
  • Interleukin-8 / immunology*
  • Monocytes / cytology
  • Monocytes / drug effects*
  • Monocytes / immunology
  • Primary Cell Culture
  • Receptors, CCR1 / antagonists & inhibitors
  • Receptors, CCR1 / genetics
  • Receptors, CCR1 / immunology
  • Receptors, CCR5 / genetics
  • Receptors, CCR5 / immunology
  • Recombinant Proteins / pharmacology
  • Serum Amyloid A Protein / pharmacology*
  • Signal Transduction

Substances

  • Antibodies, Neutralizing
  • CCL3 protein, human
  • CCR1 protein, human
  • CCR5 protein, human
  • CXCL12 protein, human
  • Chemokine CCL3
  • Chemokine CXCL12
  • Interleukin-8
  • Receptors, CCR1
  • Receptors, CCR5
  • Recombinant Proteins
  • SAA1 protein, human
  • Serum Amyloid A Protein