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The Role of Atypical Chemoattractant Receptors in Recruiting Neutrophils into Inflamed Tissue Sites

Key findings

  • Using multiphoton intravital microscopy of mice with inflammatory arthritis, Massachusetts General Hospital researchers found that two atypical chemoattractant receptors facilitate neutrophil recruitment from the circulation into the tissue
  • Complement C5a receptor 2 (C5aR2) helped transport tissue-derived C5a into the blood vessel lumen to induce the C5aR1-mediated initial adhesion of circulating neutrophils
  • Atypical chemokine receptor 1 (ACKR1) transported CXCR2 chemokine ligands across the joint endothelium to induce CXCR2-mediated transendothelial migration of neutrophils and entry into the joint
  • Inhibition of both C5aR2 and ACKR1 may have an additive or synergistic therapeutic effect in suppressing neutrophil recruitment

A key element of inflammation is the recruitment of leukocytes across post-capillary blood vessels into the tissue. Chemoattractants acting as tissue "gatekeepers" instruct circulating leukocytes to enter specific tissue beds by inducing them to adhere to the endothelium, followed by transendothelial migration. Yet how tissue-derived chemoattractants are transported into the blood vessel lumen to induce leukocyte entry isn't well understood.

In a mouse model of arthritis, Andrew D. Luster, MD, PhD, chief of the Division of Rheumatology, Allergy and Immunology and director of the Center for Immunology and Inflammatory Diseases at Massachusetts General Hospital, and colleagues have identified a previously unknown sequential role of two atypical chemoattractant receptors, complement C5a receptor 2 (C5aR2) and atypical chemokine receptor 1 (ACKR1), in controlling the passage of neutrophils from the circulation into tissue. Their report appears in Science Immunology.

Clues from Previous Research

Dr. Luster and colleagues previously used multiphoton intravital microscopy to image neutrophil recruitment into ankle joints of living mice with immune complex–induced arthritis. Published in Science Immunology, they observed that expression of complement C5a receptor 1 (C5aR1) on neutrophils was critical for initial neutrophil adhesion and spreading on the endothelium of the joint.

Current Study

In the new study, which made use of the same mouse model of arthritis, the research team observed with intravital microscopy that C5aR2 and ACKR1 are required for neutrophil entry into the joint and the development of inflammatory arthritis. These receptors are both atypical in that they don't bind G proteins and therefore don't initiate G protein–dependent signaling.

When C5aR2 and ACKR1 collaborated with the signaling chemoattractant receptors C5aR1 and CXCR2, the following occurred:

  • C5aR2 expressed on endothelial cells transported C5a generated within the joint into the vessel lumen
  • C5a was captured on the surface of endothelial cells by heparan sulfate proteoglycans and was presented to circulating neutrophils, which initiated C5aR1-mediated adhesion of neutrophils
  • ACKR1 expressed on endothelial cells transported CXCR2 ligands produced within the joint into the lumen of the overlying blood vessel, initiating CXCR2-mediated transendothelial migration of neutrophils and entry into the joint

Potential Therapeutic Implications

C5ar2- and Ackr1-knockout mice were able to support neutrophil adhesion and transendothelial migration, but they couldn't transport tissue-derived C5a and CXCR2 chemokine ligands, respectively, to induce these processes. Therefore, inhibition of both C5aR2 and ACKR1 may prove to have an additive or synergistic effect on suppressing neutrophil recruitment.

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