Neutrophil Extracellular Traps in Autoimmunity and Allergy: Immune Complexes at Work

Vanessa Granger, Marine Peyneau, Sylvie Chollet-Martin, Luc de Chaisemartin, Vanessa Granger, Marine Peyneau, Sylvie Chollet-Martin, Luc de Chaisemartin

Abstract

Neutrophil extracellular traps (NETs) have been initially described as main actors in host defense owing to their ability to immobilize and sometimes kill microorganisms. Subsequent studies have demonstrated their implication in the pathophysiology of various diseases, due to the toxic effects of their main components on surrounding tissues. Several distinct NETosis pathways have been described in response to various triggers. Among these triggers, IgG immune complexes (IC) play an important role since they induce robust NET release upon binding to activating FcγRs on neutrophils. Few in vitro studies have documented the mechanisms of IC-induced NET release and evidence about the partners involved is controversial. In vivo, animal models and clinical studies have strongly suggested the importance of IgG IC-induced NET release for autoimmunity and anaphylaxis. In this review, we will focus on two autoimmune diseases in which NETs are undoubtedly major players, systemic lupus erythematosus (SLE), and rheumatoid arthritis (RA). We will also discuss anaphylaxis as another example of disease recently associated with IC-induced NET release. Understanding the role of IC-induced NETs in these settings will pave the way for new diagnostic tools and therapeutic strategies.

Keywords: NETs; anaphylaxis; autoimmunity; immune complexes; neutrophils.

Copyright © 2019 Granger, Peyneau, Chollet-Martin and de Chaisemartin.

Figures

Figure 1
Figure 1
Mechanisms of NET formation in autoimmunity. Autoantigen/IgG IC can bind to several FcγRs expressed at the neutrophil surface and induce their activation. In particular, NOX2 is activated and produce ROS that can in turn activate PAD4 leading to protein citrullination and chromatin decondensation. In parallel, ROS can also help MPO and NE degranulation and translocation to the nucleus contributing to chromatin unfolding. The nuclear membrane breaks down, the decondensed chromatin is released in the cytosol and becomes decorated with various cytosolic and granule-derived proteins. Finally, NETs are released exposing to the immune system a large number of autoantigens that can amplify this mechanism called lytic NETosis. In some conditions, in particular in SLE, these IC can also induce a non-lytic NOX2-independent NETosis via the production of mitochondria-derived ROS and/or DNA; in that case, neutrophils are still alive.
Figure 2
Figure 2
Mechanisms of NET formation during anaphylaxis. The classical pathway of anaphylaxis is based on histamine release by mast cells and basophils activated by the engagement of FcεRI after interaction of specific IgE with an allergen. A second pathway was recently demonstrated both in mice and human. In this pathway the allergen reacts with specific IgG and form an IC that binds to several FcγRs at the neutrophil surface and activate them. In addition to ROS and protease release, neutrophils release PAF and NETs, that could be also involved in anaphylaxis clinical manifestations.

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