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

Overview

Journal Front Immunol

Specialty Allergy & Immunology

Date 2019 Dec 19

PMID 31849989

Citations 28

Authors

Vanessa Granger

Marine Peyneau

Sylvie Chollet-Martin

Luc de Chaisemartin

Affiliations

Soon will be listed here.

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 studies have documented the mechanisms of IC-induced NET release and evidence about the partners involved is controversial. , 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.

Citing Articles

Feasibility of detecting snake envenomation biomarkers from dried blood spots.

Smith C, Brandehoff N, Pepin L, McCabe M, Castoe T, Mackessy S Anal Sci Adv. 2024; 4(1-2):26-36.

PMID: 38715579 PMC: 10989584. DOI: 10.1002/ansa.202200050.

The Role of Neutrophil Extracellular Traps in the Outcome of Malignant Epitheliomas: Significance of CA215 Involvement.

Himcinschi M, Uscatescu V, Gherghe G, Stoian I, Vlad A, Popa D Diagnostics (Basel). 2024; 14(3).

PMID: 38337844 PMC: 10855654. DOI: 10.3390/diagnostics14030328.

ATP functions as a primary alarmin in allergen-induced type 2 immunity.

OGrady S, Kita H Am J Physiol Cell Physiol. 2023; 325(5):C1369-C1386.

PMID: 37842751 PMC: 10861152. DOI: 10.1152/ajpcell.00370.2023.

NETosis: an emerging therapeutic target in renal diseases.

Juha M, Molnar A, Jakus Z, Ledo N Front Immunol. 2023; 14:1253667.

PMID: 37744367 PMC: 10514582. DOI: 10.3389/fimmu.2023.1253667.

Genome-wide association study of a semicontinuous trait: illustration of the impact of the modeling strategy through the study of Neutrophil Extracellular Traps levels.

Munsch G, Proust C, Labrouche-Colomer S, Aissi D, Boland A, Morange P NAR Genom Bioinform. 2023; 5(2):lqad062.

PMID: 37388819 PMC: 10304785. DOI: 10.1093/nargab/lqad062.

References

Barrientos L, Bignon A, Gueguen C, de Chaisemartin L, Gorges R, Sandre C . Neutrophil extracellular traps downregulate lipopolysaccharide-induced activation of monocyte-derived dendritic cells. J Immunol. 2014; 193(11):5689-98. DOI: 10.4049/jimmunol.1400586. View

Aleyd E, Al M, Tuk C, van der Laken C, van Egmond M . IgA Complexes in Plasma and Synovial Fluid of Patients with Rheumatoid Arthritis Induce Neutrophil Extracellular Traps via FcαRI. J Immunol. 2016; 197(12):4552-4559. DOI: 10.4049/jimmunol.1502353. View

Demoruelle M, Harrall K, Ho L, Purmalek M, Seto N, Rothfuss H . Anti-Citrullinated Protein Antibodies Are Associated With Neutrophil Extracellular Traps in the Sputum in Relatives of Rheumatoid Arthritis Patients. Arthritis Rheumatol. 2017; 69(6):1165-1175. PMC: 5449213. DOI: 10.1002/art.40066. View

Rocks N, Vanwinge C, Radermecker C, Blacher S, Gilles C, Maree R . Ozone-primed neutrophils promote early steps of tumour cell metastasis to lungs by enhancing their NET production. Thorax. 2019; 74(8):768-779. DOI: 10.1136/thoraxjnl-2018-211990. View

Cortjens B, van Woensel J, Bem R . Neutrophil Extracellular Traps in Respiratory Disease: guided anti-microbial traps or toxic webs?. Paediatr Respir Rev. 2016; 21:54-61. DOI: 10.1016/j.prrv.2016.03.007. View

Li P, Li M, Lindberg M, Kennett M, Xiong N, Wang Y . PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med. 2010; 207(9):1853-62. PMC: 2931169. DOI: 10.1084/jem.20100239. View

Oehmcke S, Morgelin M, Herwald H . Activation of the human contact system on neutrophil extracellular traps. J Innate Immun. 2010; 1(3):225-30. PMC: 6951039. DOI: 10.1159/000203700. View

Dicker A, Crichton M, Pumphrey E, Cassidy A, Suarez-Cuartin G, Sibila O . Neutrophil extracellular traps are associated with disease severity and microbiota diversity in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol. 2017; 141(1):117-127. PMC: 5751731. DOI: 10.1016/j.jaci.2017.04.022. View

Suzuki A, Kochi Y, Shoda H, Seri Y, Fujio K, Sawada T . Decreased severity of experimental autoimmune arthritis in peptidylarginine deiminase type 4 knockout mice. BMC Musculoskelet Disord. 2016; 17:205. PMC: 4858923. DOI: 10.1186/s12891-016-1055-2. View

10.

Chen W, Wang Q, Ke Y, Lin J . Neutrophil Function in an Inflammatory Milieu of Rheumatoid Arthritis. J Immunol Res. 2019; 2018:8549329. PMC: 6304923. DOI: 10.1155/2018/8549329. View

11.

Francis A, Bosio E, Stone S, Fatovich D, Arendts G, Macdonald S . Markers Involved in Innate Immunity and Neutrophil Activation are Elevated during Acute Human Anaphylaxis: Validation of a Microarray Study. J Innate Immun. 2018; 11(1):63-73. PMC: 6738247. DOI: 10.1159/000492301. View

12.

Aleman O, Mora N, Cortes-Vieyra R, Uribe-Querol E, Rosales C . Transforming Growth Factor-β-Activated Kinase 1 Is Required for Human FcγRIIIb-Induced Neutrophil Extracellular Trap Formation. Front Immunol. 2016; 7:277. PMC: 4947870. DOI: 10.3389/fimmu.2016.00277. View

13.

Jeremic I, Djuric O, Nikolic M, Vlajnic M, Nikolic A, Radojkovic D . Neutrophil extracellular traps-associated markers are elevated in patients with systemic lupus erythematosus. Rheumatol Int. 2019; 39(11):1849-1857. DOI: 10.1007/s00296-019-04426-1. View

14.

Beutier H, Hechler B, Godon O, Wang Y, Gillis C, de Chaisemartin L . Platelets expressing IgG receptor FcγRIIA/CD32A determine the severity of experimental anaphylaxis. Sci Immunol. 2018; 3(22). DOI: 10.1126/sciimmunol.aan5997. View

15.

Odqvist L, Jevnikar Z, Riise R, Oberg L, Rhedin M, Leonard D . Genetic variations in A20 DUB domain provide a genetic link to citrullination and neutrophil extracellular traps in systemic lupus erythematosus. Ann Rheum Dis. 2019; 78(10):1363-1370. PMC: 6788882. DOI: 10.1136/annrheumdis-2019-215434. View

16.

Garcia-Romo G, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z . Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med. 2011; 3(73):73ra20. PMC: 3143837. DOI: 10.1126/scitranslmed.3001201. View

17.

Makrygiannakis D, Hermansson M, Ulfgren A, Nicholas A, Zendman A, Eklund A . Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann Rheum Dis. 2008; 67(10):1488-92. DOI: 10.1136/ard.2007.075192. View

18.

Wang S, Xie T, Sun S, Wang K, Liu B, Wu X . DNase-1 Treatment Exerts Protective Effects in a Rat Model of Intestinal Ischemia-Reperfusion Injury. Sci Rep. 2018; 8(1):17788. PMC: 6290768. DOI: 10.1038/s41598-018-36198-2. View

19.

Ebrahimi F, Giaglis S, Hahn S, Blum C, Baumgartner C, Kutz A . Markers of neutrophil extracellular traps predict adverse outcome in community-acquired pneumonia: secondary analysis of a randomised controlled trial. Eur Respir J. 2018; 51(4). DOI: 10.1183/13993003.01389-2017. View

20.

Chen K, Nishi H, Travers R, Tsuboi N, Martinod K, Wagner D . Endocytosis of soluble immune complexes leads to their clearance by FcγRIIIB but induces neutrophil extracellular traps via FcγRIIA in vivo. Blood. 2012; 120(22):4421-31. PMC: 3507149. DOI: 10.1182/blood-2011-12-401133. View