Heterogeneous NLRP3 inflammasome signature in circulating myeloid cells as a biomarker of COVID-19 severity

Blood Advances - Tập 5 - Trang 1523-1534 - 2021
Johan Courjon1,2, Océane Dufies1, Alexandre Robert1,3, Laurent Bailly2,4, Cédric Torre1, David Chirio2, Julie Contenti2, Sébastien Vitale1,2, Céline Loubatier1, Anne Doye1, Christelle Pomares-Estran1,2, Géraldine Gonfrier2, Romain Lotte1,2, Patrick Munro1, Orane Visvikis1, Jean Dellamonica2, Valérie Giordanengo1,2, Michel Carles2, Laurent Yvan-Charvet1, Stoyan Ivanov1
1Université Côte d'Azur, Inserm, C3M, Nice, France
2Université Côte d'Azur, CHU Nice, Nice, France
3Service de Médecine Intensive Réanimation, Centre Hospitalier de Cannes, Cannes, France
4Public Health Department, University Hospital of Nice, Université Côte d’Azur, Nice, France

Tóm tắt

Abstract

Dysregulated immune response is the key factor leading to unfavorable coronavirus disease 2019 (COVID-19) outcome. Depending on the pathogen-associated molecular pattern, the NLRP3 inflammasome can play a crucial role during innate immunity activation. To date, studies describing the NLRP3 response during severe acute respiratory syndrome coronavirus 2 infection in patients are lacking. We prospectively monitored caspase-1 activation levels in peripheral myeloid cells from healthy donors and patients with mild to critical COVID-19. The caspase-1 activation potential in response to NLRP3 inflammasome stimulation was opposed between nonclassical monocytes and CD66b+CD16dim granulocytes in severe and critical COVID-19 patients. Unexpectedly, the CD66b+CD16dim granulocytes had decreased nigericin-triggered caspase-1 activation potential associated with an increased percentage of NLRP3 inflammasome impaired immature neutrophils and a loss of eosinophils in the blood. In patients who recovered from COVID-19, nigericin-triggered caspase-1 activation potential in CD66b+CD16dim cells was restored and the proportion of immature neutrophils was similar to control. Here, we reveal that NLRP3 inflammasome activation potential differs among myeloid cells and could be used as a biomarker of a COVID-19 patient’s evolution. This assay could be a useful tool to predict patient outcome. This trial was registered at www.clinicaltrials.gov as #NCT04385017.


Tài liệu tham khảo

Li, 2020, Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia, N Engl J Med, 382, 1199, 10.1056/NEJMoa2001316

Jamilloux, 2020, Should we stimulate or suppress immune responses in COVID-19? Cytokine and anti-cytokine interventions, Autoimmun Rev, 19, 102567, 10.1016/j.autrev.2020.102567

Iwasaki, 2015, Control of adaptive immunity by the innate immune system, Nat Immunol, 16, 343, 10.1038/ni.3123

Medzhitov, 2009, Approaching the asymptote: 20 years later, Immunity, 30, 766, 10.1016/j.immuni.2009.06.004

Takeuchi, 2009, Innate immunity to virus infection, Immunol Rev, 227, 75, 10.1111/j.1600-065X.2008.00737.x

Chow, 2018, RIG-I and other RNA sensors in antiviral immunity, Annu Rev Immunol, 36, 667, 10.1146/annurev-immunol-042617-053309

Huang, 2020, Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China, Lancet, 395, 497, 10.1016/S0140-6736(20)30183-5

Wen, 2020, Immune cell profiling of COVID-19 patients in the recovery stage by single-cell sequencing [published correction appears in Cell Discov. 2020;6:41], Cell Discov, 6, 31, 10.1038/s41421-020-0168-9

Vabret, 2020, Advancing scientific knowledge in times of pandemics, Nat Rev Immunol, 20, 338, 10.1038/s41577-020-0319-0

Chen, 2019, Severe acute respiratory syndrome coronavirus viroporin 3a activates the NLRP3 inflammasome, Front Microbiol, 10, 50, 10.3389/fmicb.2019.00050

Merad, 2020, Pathological inflammation in patients with COVID-19: a key role for monocytes and macrophages [published corrections appear in Nat Rev Immunol. 2020;20(7):448], Nat Rev Immunol, 20, 355, 10.1038/s41577-020-0331-4

Deftereos, 2020, The Greek study in the effects of colchicine in COvid-19 complications prevention (GRECCO-19 study): rationale and study design, Hellenic J Cardiol, 61, 42, 10.1016/j.hjc.2020.03.002

Parisi, 2020, Precision medicine in COVID-19: IL-1β a potential target, JACC Basic Transl Sci, 5, 543, 10.1016/j.jacbts.2020.04.006

Cheong, 2020, Anti-malarial drug, artemisinin and its derivatives for the treatment of respiratory diseases, Pharmacol Res, 158, 104901, 10.1016/j.phrs.2020.104901

Rodrigues, 2021, Inflammasomes are activated in response to SARS-CoV-2 infection and are associated with COVID-19 severity in patients, J Exp Med, 218, e20201707, 10.1084/jem.20201707

Ferreira

AC

, SoaresVC, de Azevedo-QuintanilhaIG, et al

SARS-CoV-2 induces inflammasome-dependent pyroptosis and downmodulation of HLA-DR in human monocytes.

www.medrxiv.org/content/10.1101/2020.08.25.20182055v2. Accessed 10 January 2021.

World Health Organization (WHO), 2020, Clinical Management of COVID-19: Interim Guidance

Frat, 2015, High-flow oxygen through nasal cannula in acute hypoxemic respiratory failure, N Engl J Med, 372, 2185, 10.1056/NEJMoa1503326

Martínez-García, 2019, P2X7 receptor induces mitochondrial failure in monocytes and compromises NLRP3 inflammasome activation during sepsis, Nat Commun, 10, 2711, 10.1038/s41467-019-10626-x

Zhao, 2020, Longitudinal COVID-19 profiling associates IL-1RA and IL-10 with disease severity and RANTES with mild disease, JCI Insight, 5, e139834, 10.1172/jci.insight.139834

Groslambert, 2018, Spotlight on the NLRP3 inflammasome pathway, J Inflamm Res, 11, 359, 10.2147/JIR.S141220

Grieshaber-Bouyer, 2019, Neutrophil heterogeneity as therapeutic opportunity in immune-mediated disease, Front Immunol, 10, 346, 10.3389/fimmu.2019.00346

Cavalli, 2020, Interleukin-1 blockade with high-dose anakinra in patients with COVID-19, acute respiratory distress syndrome, and hyperinflammation: a retrospective cohort study, Lancet Rheumatol, 2, e325, 10.1016/S2665-9913(20)30127-2

Pillay, 2010, Functional heterogeneity and differential priming of circulating neutrophils in human experimental endotoxemia, J Leukoc Biol, 88, 211, 10.1189/jlb.1209793

Vitte, 2020, A granulocytic signature identifies COVID-19 and its severity, J Infect Dis, 222, 1985, 10.1093/infdis/jiaa591

Immunological Genome Project, 2020, ImmGen at 15, Nat Immunol, 21, 700, 10.1038/s41590-020-0687-4

Wilk, 2020, A single-cell atlas of the peripheral immune response in patients with severe COVID-19, Nat Med, 26, 1070, 10.1038/s41591-020-0944-y