NFκB and NLRP3/NLRC4 inflammasomes regulate differentiation, activation and functional properties of monocytes in response to distinct SARS-CoV-2 proteins.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
07 Mar 2024
07 Mar 2024
Historique:
received:
14
04
2023
accepted:
22
02
2024
medline:
8
3
2024
pubmed:
8
3
2024
entrez:
7
3
2024
Statut:
epublish
Résumé
Increased recruitment of transitional and non-classical monocytes in the lung during SARS-CoV-2 infection is associated with COVID-19 severity. However, whether specific innate sensors mediate the activation or differentiation of monocytes in response to different SARS-CoV-2 proteins remain poorly characterized. Here, we show that SARS-CoV-2 Spike 1 but not nucleoprotein induce differentiation of monocytes into transitional or non-classical subsets from both peripheral blood and COVID-19 bronchoalveolar lavage samples in a NFκB-dependent manner, but this process does not require inflammasome activation. However, NLRP3 and NLRC4 differentially regulated CD86 expression in monocytes in response to Spike 1 and Nucleoprotein, respectively. Moreover, monocytes exposed to Spike 1 induce significantly higher proportions of Th1 and Th17 CD4 + T cells. In contrast, monocytes exposed to Nucleoprotein reduce the degranulation of CD8 + T cells from severe COVID-19 patients. Our study provides insights in the differential impact of innate sensors in regulating monocytes in response to different SARS-CoV-2 proteins, which might be useful to better understand COVID-19 immunopathology and identify therapeutic targets.
Identifiants
pubmed: 38453949
doi: 10.1038/s41467-024-46322-8
pii: 10.1038/s41467-024-46322-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2100Subventions
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : CIBERINFECC
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : CIBERINFECC
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : CIBERINFECC
Organisme : Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III)
ID : CIBERCV
Organisme : Ministry of Economy and Competitiveness | Agencia Estatal de Investigación (Spanish Agencia Estatal de Investigación)
ID : PID2021-127899OB-I00
Organisme : Ministry of Economy and Competitiveness | Agencia Estatal de Investigación (Spanish Agencia Estatal de Investigación)
ID : PID2021-127899OB-I00
Organisme : Comunidad de Madrid
ID : Inmunovacter REACT-UE
Organisme : Comunidad de Madrid
ID : INMUNOVACTER REACT-EU
Organisme : Comunidad de Madrid
ID : INMUNOVACTER REACT-EU
Organisme : Ministerio de Economía y Competitividad (Ministry of Economy and Competitiveness)
ID : PDC2021-121719-I00
Organisme : Ministerio de Economía y Competitividad (Ministry of Economy and Competitiveness)
ID : PID-2020-120412RB-I00
Informations de copyright
© 2024. The Author(s).
Références
Ruan, Q., Yang, K., Wang, W., Jiang, L. & Song, J. Clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China. Intensive Care Med. 46, 846–848 (2020).
doi: 10.1007/s00134-020-05991-x
Guan, W. J. et al. Clinical characteristics of coronavirus disease 2019 in China. N. Engl. J. Med. 382, 1708–1720 (2020).
doi: 10.1056/NEJMoa2002032
Huang, C. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395, 497–506 (2020).
doi: 10.1016/S0140-6736(20)30183-5
Makarova, Y. A. et al. Atherosclerosis, cardiovascular disorders and COVID-19: comorbid pathogenesis. Diagnostics (Basel) 13, 478 (2023).
doi: 10.3390/diagnostics13030478
Deng, S. Q. & Peng, H. J. Characteristics of and public health responses to the coronavirus disease 2019 outbreak in China. J. Clin. Med. 9, 575 (2020).
doi: 10.3390/jcm9020575
Augello, M., Bono, V., Rovito, R., Tincati, C. & Marchetti, G. Immunologic interplay between HIV/AIDS and COVID-19: adding fuel to the flames? Curr. HIV/AIDS Rep. 20, 51–75 (2023).
Goldman, J. D., Robinson, P. C., Uldrick, T. S. & Ljungman, P. COVID-19 in immunocompromised populations: implications for prognosis and repurposing of immunotherapies. J. Immunother. Cancer 9, e002630 (2021).
doi: 10.1136/jitc-2021-002630
Lakota, K. et al. COVID-19 in association with development, course, and treatment of systemic autoimmune rheumatic diseases. Front. Immunol. 11, 611318 (2020).
doi: 10.3389/fimmu.2020.611318
Zhang, Q., Bastard, P., Cobat, A. & Casanova, J. L. Human genetic and immunological determinants of critical COVID-19 pneumonia. Nature 603, 587–598 (2022).
doi: 10.1038/s41586-022-04447-0
Bastard, P. et al. Autoantibodies against type I IFNs in patients with life-threatening COVID-19. Science 370, eabd4585 (2020).
doi: 10.1126/science.abd4585
Escobedo, R. A., Singh, D. K. & Kaushal, D. Understanding COVID-19: from dysregulated immunity to vaccination status Quo. Front. Immunol. 12, 765349 (2021).
doi: 10.3389/fimmu.2021.765349
Gu, R., Mao, T., Lu, Q., Tianjiao Su, T. & Wang, J. Myeloid dysregulation and therapeutic intervention in COVID-19. Semin. Immunol. 55, 101524 (2021).
doi: 10.1016/j.smim.2021.101524
Reddy, M. A. et al. Opposing actions of c-ets/PU.1 and c-myb protooncogene products in regulating the macrophage-specific promoters of the human and mouse colony-stimulating factor-1 receptor (c-fms) genes. J. Exp. Med. 180, 2309–2319 (1994).
doi: 10.1084/jem.180.6.2309
Ziegler-Heitbrock, L. et al. Nomenclature of monocytes and dendritic cells in blood. Blood 116, e74–80 (2010).
doi: 10.1182/blood-2010-02-258558
Collin, M., McGovern, N. & Muzlifah, H. Human dendritic cell subsets. Immunology 140, 22–30 (2013).
doi: 10.1111/imm.12117
Wong, K. L. et al. The three human monocyte subsets: implications for health and disease. Immunol. Res. 53, 41–57 (2012).
doi: 10.1007/s12026-012-8297-3
Wong, K. L. et al. Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood J. Am. Soc. Hematol. 118, e16–e31 (2011).
Schmidl, C. et al. Transcription and enhancer profiling in human monocyte subsets. Blood 123, e90–9 (2014).
doi: 10.1182/blood-2013-02-484188
Shi, C. & Pamer, E. G. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11, 762–774 (2011).
doi: 10.1038/nri3070
Iijima, N., Mattei, L. M. & Iwasaki, A. Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc. Natl. Acad. Sci. USA 108, 284–289 (2011).
doi: 10.1073/pnas.1005201108
Sánchez-Cerrillo, I. et al. COVID-19 severity associates with pulmonary redistribution of CD1c+ DCs and inflammatory transitional and nonclassical monocytes. J. Clin. Investig. 130, 6290–6300 (2020).
doi: 10.1172/JCI140335
Schulte-Schrepping, J. et al. Severe COVID-19 is marked by a dysregulated myeloid cell compartment. Cell 182, 1419–1440.e23 (2020).
doi: 10.1016/j.cell.2020.08.001
Visintin, A. et al. Regulation of Toll-like receptors in human monocytes and dendritic cells. J. Immunol. 166, 249–255 (2001).
doi: 10.4049/jimmunol.166.1.249
Belge, K.-U. et al. The proinflammatory CD14 CD16 DR monocytes are a major source of TNF. J. Immunol. 168, 3536–3542 (2002).
doi: 10.4049/jimmunol.168.7.3536
Zhao, Y. et al. SARS-CoV-2 spike protein interacts with and activates TLR41. Cell Res. 31, 818–820 (2021).
doi: 10.1038/s41422-021-00495-9
Aboudounya, M. M. & Heads, R. J. COVID-19 and toll-like receptor 4 (TLR4): SARS-CoV-2 may bind and activate TLR4 to increase ACE2 expression, facilitating entry and causing hyperinflammation. Mediators Inflamm. 2021, 8874339 (2021).
doi: 10.1155/2021/8874339
Andersson, U., Ottestad, W. & Tracey, K. J. Extracellular HMGB1: a therapeutic target in severe pulmonary inflammation including COVID-19? Mol. Med. 26, 42 (2020).
doi: 10.1186/s10020-020-00172-4
Theobald, S. J. et al. Long-lived macrophage reprogramming drives spike protein-mediated inflammasome activation in COVID-19. EMBO Mol. Med. 13, e14150 (2021).
doi: 10.15252/emmm.202114150
Si Ming, M. Inflammasomes in the gastrointestinal tract: infection, cancer and gut microbiota homeostasis. Nat. Rev. Gastroenterol. Hepatol. 15, 721–737 (2018).
doi: 10.1038/s41575-018-0054-1
Strowig, T., Henao-Mejia, J., Elinav, E. & Flavell, R. Inflammasomes in health and disease. Nature 481, 278–286 (2012).
doi: 10.1038/nature10759
Sandall, C. F., Ziehr, B. K. & MacDonald, J. A. ATP-binding and hydrolysis in inflammasome activation. Molecules 25, 4572 (2020).
doi: 10.3390/molecules25194572
Mendonça, R., Silveira, A. A., Conran, N. Red cell DAMPs and inflammation. Inflamm. Res. 65, 665–678 (2016).
Kinra, M., Nampoothiri, M., Arora, D. & Mudgal, J. Reviewing the importance of TLR-NLRP3-pyroptosis pathway and mechanism of experimental NLRP3 inflammasome inhibitors. Scand. J. Immunol. 95, e13124 (2022).
doi: 10.1111/sji.13124
Duncan, J. A. & Canna, S. W. The NLRC 4 inflammasome. Immunol. Rev. 281, 115–123 (2018).
doi: 10.1111/imr.12607
Delgado-Arévalo, C. et al. NLRC4-mediated activation of CD1c+ DC contributes to perpetuation of synovitis in rheumatoid arthritis. JCI Insight 7, e152886 (2022).
doi: 10.1172/jci.insight.152886
Zhao, J. et al. Airway memory CD4(+) T cells mediate protective immunity against emerging respiratory coronaviruses. Immunity 44, 1379–1391 (2016).
doi: 10.1016/j.immuni.2016.05.006
Ziegler-Heitbrock, L. The CD14 CD16 blood monocytes: their role in infection and inflammation. J. Leukoc. Biol. 81, 584–592 (2007).
doi: 10.1189/jlb.0806510
Channappanavar, R., Fett, C., Zhao, J., Meyerholz, D. K. & Perlman, S. Virus-specific memory CD8 T cells provide substantial protection from lethal severe acute respiratory syndrome coronavirus infection. J. Virol. 88, 11034–11044 (2014).
doi: 10.1128/JVI.01505-14
Mahmoud Salehi Khesht, A. et al. Different T cell related immunological profiles in COVID-19 patients compared to healthy controls. Int. Immunopharmacol. 97, 107828 (2021).
doi: 10.1016/j.intimp.2021.107828
Vallejo, A., Vizcarra, P., Quereda, C., Moreno, A. & Casado, J. L. IFN-γ(+) cell response and IFN-γ release concordance after in vitro SARS-CoV-2 stimulation. Eur. J. Clin. Investig. 51, e13636 (2021).
doi: 10.1111/eci.13636
Pacha, O., Sallman, M. A. & Evans, S. E. COVID-19: a case for inhibiting IL-17? Nat. Rev. Immunol. 20, 345–346 (2020).
doi: 10.1038/s41577-020-0328-z
Zhao, Y. et al. Clonal expansion and activation of tissue-resident memory-like Th17 cells expressing GM-CSF in the lungs of severe COVID-19 patients. Sci. Immunol. 6, eabf6692 (2021).
doi: 10.1126/sciimmunol.abf6692
Grau-Expósito, J. et al. Peripheral and lung resident memory T cell responses against SARS-CoV-2. Nat. Commun. 12, 3010 (2021).
doi: 10.1038/s41467-021-23333-3
Zhou, Y. et al. Pathogenic T-cells and inflammatory monocytes incite inflammatory storms in severe COVID-19 patients. Natl. Sci. Rev. 7, 998–1002 (2020).
doi: 10.1093/nsr/nwaa041
Kuri-Cervantes, L. et al. Comprehensive mapping of immune perturbations associated with severe COVID-19. Sci. Immunol. 5, eabd7114 (2020).
doi: 10.1126/sciimmunol.abd7114
Grau-Expósito, J. et al. Peripheral and lung resident memory T cell responses against SARS-CoV-2. Nat. Commun. 12, 1–17 (2021).
doi: 10.1038/s41467-021-23333-3
Zheng, M. et al. Functional exhaustion of antiviral lymphocytes in COVID-19 patients. Cell. Mol. Immunol. 17, 533–535 (2020).
doi: 10.1038/s41423-020-0402-2
Cheon, I. S. et al. Immune signatures underlying post-acute COVID-19 lung sequelae. Sci. Immunol. 6, eabk1741 (2021).
doi: 10.1126/sciimmunol.abk1741
Oja, A. E. et al. Divergent SARS-CoV-2-specific T- and B-cell responses in severe but not mild COVID-19 patients. Eur. J. Immunol. 50, 1998–2012 (2020).
doi: 10.1002/eji.202048908
Rajan, J. V., Warren, S. E., Miao, E. A. & Aderem, A. Activation of the NLRP3 inflammasome by intracellular poly I:C. FEBS Lett. 584, 4627–4632 (2010).
doi: 10.1016/j.febslet.2010.10.036
Silveira, T. N. & Zamboni, D. S. Pore formation triggered by Legionella spp. is an Nlrc4 inflammasome-dependent host cell response that precedes pyroptosis. Infect. Immun. 78, 1403–1413 (2010).
doi: 10.1128/IAI.00905-09
Jiang, Z. et al. Poly(I-C)-induced Toll-like receptor 3 (TLR3)-mediated activation of NFkappa B and MAP kinase is through an interleukin-1 receptor-associated kinase (IRAK)-independent pathway employing the signaling components TLR3-TRAF6-TAK1-TAB2-PKR. J. Biol. Chem. 278, 16713–16719 (2003).
doi: 10.1074/jbc.M300562200
Hayashi, F. et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099–1103 (2001).
doi: 10.1038/35074106
Pan, Z. K. et al. Bacterial LPS up-regulated TLR3 expression is critical for antiviral response in human monocytes: evidence for negative regulation by CYLD. Int. Immunol. 23, 357–364 (2011).
doi: 10.1093/intimm/dxr019
Zhu, Q. & Kanneganti, T. D. Cutting edge: distinct regulatory mechanisms control proinflammatory cytokines IL-18 and IL-1β. J. Immunol. 198, 4210–4215 (2017).
doi: 10.4049/jimmunol.1700352
Juliana, C. et al. Anti-inflammatory compounds parthenolide and Bay 11-7082 are direct inhibitors of the inflammasome. J. Biol. Chem. 285, 9792–9802 (2010).
doi: 10.1074/jbc.M109.082305
Zhang, D., Qiu, L., Jin, X., Guo, Z. & Guo, C. Nuclear factor-kappaB inhibition by parthenolide potentiates the efficacy of Taxol in non-small cell lung cancer in vitro and in vivo. Mol. Cancer Res. 7, 1139–1149 (2009).
doi: 10.1158/1541-7786.MCR-08-0410
Liu, H. R. et al. Antiproliferative activity of the total saponin of Solanum lyratum Thunb in Hela cells by inducing apoptosis. Pharmazie 63, 836–842 (2008).
Coll, R. C. et al. A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat. Med. 21, 248–255 (2015).
doi: 10.1038/nm.3806
Eisfeld, H. S. et al. Viral glycoproteins induce NLRP3 inflammasome activation and pyroptosis in macrophages. Viruses 13, 2076 (2021).
doi: 10.3390/v13102076
Pan, P. et al. SARS-CoV-2 N protein promotes NLRP3 inflammasome activation to induce hyperinflammation. Nat. Commun. 12, 4664 (2021).
doi: 10.1038/s41467-021-25015-6
de Almeida, L. et al. Identification of immunomodulatory drugs that inhibit multiple inflammasomes and impair SARS-CoV-2 infection. Sci. Adv. 8, eabo5400 (2022).
doi: 10.1126/sciadv.abo5400
Esparcia-Pinedo, L. et al. CD4+ T cell immune specificity changes after vaccination in healthy and COVID-19 convalescent subjects. Front. Immunol. 12, 755891 (2021).
doi: 10.3389/fimmu.2021.755891
Wu, J. et al. Immunological profiling of COVID-19 patients with pulmonary sequelae. mBio 12, e0159921 (2021).
doi: 10.1128/mBio.01599-21
Piñero, D. J., Hu, J., Cook, B. M., Scaduto, R. C. Jr. & Connor, J. R. Interleukin-1beta increases binding of the iron regulatory protein and the synthesis of ferritin by increasing the labile iron pool. Biochim. Biophys. Acta 1497, 279–288 (2000).
doi: 10.1016/S0167-4889(00)00066-5
Guo, S. et al. The NLRP3 inflammasome and IL-1β accelerate immunologically mediated pathology in experimental viral fulminant hepatitis. PLoS Pathog. 11, e1005155 (2015).
doi: 10.1371/journal.ppat.1005155
Haist, K. C., Burrack, K. S., Davenport, B. J. & Morrison, T. E. Inflammatory monocytes mediate control of acute alphavirus infection in mice. PLoS Pathog. 13, e1006748 (2017).
doi: 10.1371/journal.ppat.1006748
Auffray, C., Sieweke, M. H. & Geissmann, F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27, 669–692 (2009).
doi: 10.1146/annurev.immunol.021908.132557
Lim, J. K. et al. Chemokine receptor Ccr2 is critical for monocyte accumulation and survival in West Nile virus encephalitis. J. Immunol. 186, 471–478 (2011).
doi: 10.4049/jimmunol.1003003
Peters, W. et al. Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 98, 7958–7963 (2001).
doi: 10.1073/pnas.131207398
Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79–91 (2013).
doi: 10.1016/j.immuni.2012.12.001
Patel, A. A. et al. The fate and lifespan of human monocyte subsets in steady state and systemic inflammation. J. Exp. Med. 214, 1913–1923 (2017).
doi: 10.1084/jem.20170355
Tak, T. et al. Circulatory and maturation kinetics of human monocyte subsets in vivo. Blood 130, 1474–1477 (2017).
doi: 10.1182/blood-2017-03-771261
Dosch, S. F., Mahajan, S. D. & Collins, A. R. SARS coronavirus spike protein-induced innate immune response occurs via activation of the NF-kappaB pathway in human monocyte macrophages in vitro. Virus Res. 142, 19–27 (2009).
doi: 10.1016/j.virusres.2009.01.005
Vijay-Kumar, M., Carvalho, F. A., Aitken, J. D., Fifadara, N. H. & Gewirtz, A. T. TLR5 or NLRC4 is necessary and sufficient for promotion of humoral immunity by flagellin. Eur. J. Immunol. 40, 3528–3534 (2010).
doi: 10.1002/eji.201040421
Bahrami, M., Kamalinejad, M., Latifi, S. A., Seif, F. & Dadmehr, M. Cytokine storm in COVID-19 and parthenolide: Preclinical evidence. Phytother. Res. 34, 2429–2430 (2020).
doi: 10.1002/ptr.6776
Carlisi, D. et al. Parthenolide and its soluble analogues: multitasking compounds with antitumor properties. Biomedicines 10, 514 (2022).
doi: 10.3390/biomedicines10020514
Sánchez-Tarjuelo, R. et al. The TLR4-MyD88 signaling axis regulates lung monocyte differentiation pathways in response to streptococcus pneumoniae. Front. Immunol. 11, 2120 (2020).
doi: 10.3389/fimmu.2020.02120
Sefik, E. et al. Inflammasome activation in infected macrophages drives COVID-19 pathology. Nature 606, 585–593 (2022).
doi: 10.1038/s41586-022-04802-1
Akinosoglou, K. et al. Efficacy and safety of early soluble urokinase plasminogen receptor plasma-guided anakinra treatment of COVID-19 pneumonia: A subgroup analysis of the SAVE-MORE randomised trial. EClinicalMedicine 56, 101785 (2023).
doi: 10.1016/j.eclinm.2022.101785
Dahms, K. et al. Anakinra for the treatment of COVID-19 patients: a systematic review and meta-analysis. Eur. J. Med. Res. 28, 100 (2023).
doi: 10.1186/s40001-023-01072-z
Kyriazopoulou, E. et al. Early treatment of COVID-19 with anakinra guided by soluble urokinase plasminogen receptor plasma levels: a double-blind, randomized controlled phase 3 trial. Nat. Med. 27, 1752–1760 (2021).
doi: 10.1038/s41591-021-01499-z
D’Alonzo, D., De Fenza, M. & Pavone, V. COVID-19 and pneumonia: a role for the uPA/uPAR system. Drug Discov. Today 25, 1528–1534 (2020).
doi: 10.1016/j.drudis.2020.06.013
Huet, T. et al. Anakinra for severe forms of COVID-19: a cohort study. Lancet Rheumatol. 2, e393–e400 (2020).
doi: 10.1016/S2665-9913(20)30164-8
Naveed, Z. et al. Anakinra treatment efficacy in reduction of inflammatory biomarkers in COVID-19 patients: a meta-analysis. J. Clin. Lab. Anal. 36, e24434 (2022).
doi: 10.1002/jcla.24434
Bertoni, A. et al. Spontaneous NLRP3 inflammasome-driven IL-1-β secretion is induced in severe COVID-19 patients and responds to anakinra treatment. J. Allergy Clin. Immunol. 150, 796–805 (2022).
doi: 10.1016/j.jaci.2022.05.029
Bellino, S. COVID-19 treatments approved in the European Union and clinical recommendations for the management of non-hospitalized and hospitalized patients. Ann. Med. 54, 2856–2860 (2022).
doi: 10.1080/07853890.2022.2133162
Shapiro, L., Scherger, S., Franco-Paredes, C., Gharamti, A. & Henao-Martinez, A. F. Anakinra authorized to treat severe coronavirus disease 2019; Sepsis breakthrough or time to reflect? Front. Microbiol. 14, 1250483 (2023).
doi: 10.3389/fmicb.2023.1250483
Wang, C. et al. NLRP3 inflammasome activation triggers gasdermin D-independent inflammation. Sci. Immunol. 6, eabj3859 (2021).
doi: 10.1126/sciimmunol.abj3859
Pan, P. et al. SARS-CoV-2 N protein promotes NLRP3 inflammasome activation to induce hyperinflammation. Nat. Commun. 12, 1–17 (2021).
Yang, J., Wise, L. & Fukuchi, K. I. TLR4 cross-talk with NLRP3 inflammasome and complement signaling pathways in Alzheimer’s disease. Front. Immunol. 11, 724 (2020).
doi: 10.3389/fimmu.2020.00724
Gurung, P. et al. Chronic TLR stimulation controls NLRP3 inflammasome activation through IL-10 mediated regulation of NLRP3 expression and Caspase-8 activation. Sci. Rep. 5, 14488 (2015).
doi: 10.1038/srep14488
Yilmaz, O. et al. ATP-dependent activation of an inflammasome in primary gingival epithelial cells infected by Porphyromonas gingivalis. Cell. Microbiol. 12, 188–198 (2010).
doi: 10.1111/j.1462-5822.2009.01390.x
Naseer, N. et al. Salmonella enterica serovar Typhimurium induces NAIP/NLRC4- and NLRP3/ASC-independent, Caspase-4-dependent inflammasome activation in human intestinal epithelial cells. Infect. Immun. 90, e0066321 (2022).
doi: 10.1128/iai.00663-21
Zhu, W., Chen, P., Wang, K. & Xing, X. The effect of transpyloric enteral nutrition on inflammatory response and prognosis for patients with Corona Virus Disease-19 in intensive care unit: A STROBE compliant study. Medicine 101, e31294 (2022).
doi: 10.1097/MD.0000000000031294
Planès, R. et al. Human NLRP1 is a sensor of pathogenic coronavirus 3CL proteases in lung epithelial cells. Mol. Cell 82, 2385–2400.e9 (2022).
doi: 10.1016/j.molcel.2022.04.033
Setaro, A. C. & Gaglia, M. M. All hands on deck: SARS-CoV-2 proteins that block early anti-viral interferon responses. Curr. Res. Virol. Sci. 2, 100015 (2021).
doi: 10.1016/j.crviro.2021.100015
Shang, J. et al. Severe acute respiratory syndrome coronavirus 2 for physicians: molecular characteristics and host immunity (Review). Mol. Med. Rep. 23, 262 (2021).
doi: 10.3892/mmr.2021.11901
Wong, L. R. et al. Middle East respiratory syndrome coronavirus ORF8b accessory protein suppresses type I IFN expression by impeding HSP70-dependent activation of IRF3 kinase IKKε. J. Immunol. 205, 1564–1579 (2020).
doi: 10.4049/jimmunol.1901489
Snell, L. M. et al. Overcoming CD4 Th1 cell fate restrictions to sustain antiviral CD8 T cells and control persistent virus infection. Cell Rep. 16, 3286–3296 (2016).
doi: 10.1016/j.celrep.2016.08.065
Szabo, S. J. et al. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655–669 (2000).
doi: 10.1016/S0092-8674(00)80702-3
Huaux, F., Liu, T., McGarry, B., Ullenbruch, M. & Phan, S. H. Dual roles of IL-4 in lung injury and fibrosis. J. Immunol. 170, 2083–2092 (2003).
doi: 10.4049/jimmunol.170.4.2083
Renu, K. et al. The role of Interleukin-4 in COVID-19 associated male infertility–A hypothesis. J. Reprod. Immunol. 142, 103213 (2020).
doi: 10.1016/j.jri.2020.103213
Ewer, K. J. et al. T cell and antibody responses induced by a single dose of ChAdOx1 nCoV-19 (AZD1222) vaccine in a phase 1/2 clinical trial. Nat. Med. 27, 270–278 (2021).
doi: 10.1038/s41591-020-01194-5
Luzina, I. G., Todd, N. W., Iacono, A. T. & Atamas, S. P. Roles of T lymphocytes in pulmonary fibrosis. J. Leukoc. Biol. 83, 237–244 (2008).
doi: 10.1189/jlb.0707504
Hirahara, K., Aoki, A. & Nakayama, T. Pathogenic helper T cells. Allergol. Int. 70, 169–173 (2021).
doi: 10.1016/j.alit.2021.02.001
Nakayama, T. et al. CD4+ T cells in inflammatory diseases: pathogenic T-helper cells and the CD69-Myl9 system. Int. Immunol. 33, 699–704 (2021).
doi: 10.1093/intimm/dxab053
Xie, M., Cheng, B., Ding, Y., Wang, C. & Chen, J. Correlations of IL-17 and NF-κB gene polymorphisms with susceptibility and prognosis in acute respiratory distress syndrome in a Chinese population. Biosci. Rep. 39, BSR20181987 (2019).
doi: 10.1042/BSR20181987
Martínez-Fleta, P. et al. A differential signature of circulating miRNAs and cytokines between COVID-19 and community-acquired pneumonia uncovers novel physiopathological mechanisms of COVID-19. Front. Immunol. 12, 815651 (2021).
doi: 10.3389/fimmu.2021.815651
Schleier, L. et al. Non-classical monocyte homing to the gut via α4β7 integrin mediates macrophage-dependent intestinal wound healing. Gut 69, 252–263 (2020).
doi: 10.1136/gutjnl-2018-316772
Ożańska, A., Szymczak, D. & Rybka, J. Pattern of human monocyte subpopulations in health and disease. Scand. J. Immunol. 92, e12883 (2020).
doi: 10.1111/sji.12883
Dutertre, C. A. et al. Pivotal role of M-DC8 monocytes from viremic HIV-infected patients in TNFα overproduction in response to microbial products. Blood J. Am. Soc. Hematol. 120, 2259–2268 (2012).
Kapellos, T. S. et al. Human monocyte subsets and phenotypes in major chronic inflammatory diseases. Front. Immunol. 10, 2035 (2019).
doi: 10.3389/fimmu.2019.02035
Lei, L. et al. The phenotypic changes of γδ T cells in COVID-19 patients. J. Cell. Mol. Med. 24, 11603–11606 (2020).
doi: 10.1111/jcmm.15620
Hirsch, J., Uzun, G., Zlamal, J., Singh, A. & Bakchoul, T. Platelet-neutrophil interaction in COVID-19 and vaccine-induced thrombotic thrombocytopenia. Front. Immunol. 14, 1186000 (2023).
doi: 10.3389/fimmu.2023.1186000
Cesta, M. C. et al. Neutrophil activation and neutrophil extracellular traps (NETs) in COVID-19 ARDS and immunothrombosis. Eur. J. Immunol. 53, e2250010 (2023).
doi: 10.1002/eji.202250010
Alamri, A., Fisk, D., Upreti, D. & Kung, S. K. P. A missing link: engagements of dendritic cells in the pathogenesis of SARS-CoV-2 infections. Int J. Mol. Sci. 22, 1118 (2021).
doi: 10.3390/ijms22031118
Mansourabadi, A. H. et al. B lymphocytes in COVID-19: a tale of harmony and discordance. Arch. Virol. 168, 148 (2023).
doi: 10.1007/s00705-023-05773-y
Diao B. et al. Reduction and functional exhaustion of T cells in patients with coronavirus disease 2019 (COVID-19). Front. Immunol. 11, 827 (2020).
Gozzi-Silva, S. C. et al. Generation of cytotoxic T cells and dysfunctional CD8 T cells in severe COVID-19 patients. Cells 11, 3359 (2022).
doi: 10.3390/cells11213359
Pereira-Manfro, W. F. et al. Expression of TIGIT, PD-1 and HLA-DR/CD38 markers on CD8-T cells of children and adolescents infected with HIV and uninfected controls. Rev. Inst. Med. Trop. Sao Paulo 65, e14 (2023).
doi: 10.1590/s1678-9946202365014