Autocrine vitamin D signaling switches off pro-inflammatory programs of T


Journal

Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354

Informations de publication

Date de publication:
01 2022
Historique:
received: 23 07 2020
accepted: 26 10 2021
pubmed: 13 11 2021
medline: 12 1 2022
entrez: 12 11 2021
Statut: ppublish

Résumé

The molecular mechanisms governing orderly shutdown and retraction of CD4

Identifiants

pubmed: 34764490
doi: 10.1038/s41590-021-01080-3
pii: 10.1038/s41590-021-01080-3
pmc: PMC7612139
mid: EMS137571
doi:

Substances chimiques

BACH2 protein, human 0
Basic-Leucine Zipper Transcription Factors 0
IFNG protein, human 0
IL10 protein, human 0
Receptors, Calcitriol 0
STAT3 Transcription Factor 0
STAT3 protein, human 0
VDR protein, human 0
Interleukin-10 130068-27-8
Vitamin D 1406-16-2
Complement C3a 80295-42-7
Complement C3b 80295-43-8
Interferon-gamma 82115-62-6
25-Hydroxyvitamin D3 1-alpha-Hydroxylase EC 1.14.15.18
CYP27B1 protein, human EC 1.14.15.18
JNK Mitogen-Activated Protein Kinases EC 2.7.11.24

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

62-74

Subventions

Organisme : British Heart Foundation
ID : RG/13/12/30395
Pays : United Kingdom
Organisme : Wellcome Trust (Wellcome)
ID : 097261/Z/11/Z
Organisme : U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (NHLBI)
ID : ZIA/Hl006223
Organisme : Crohn's and Colitis Foundation (Crohn's & Colitis Foundation)
ID : CCFA no. 3765
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (National Institute of Diabetes & Digestive & Kidney Diseases)
ID : DK12262401A1
Organisme : NIDDK NIH HHS
ID : R01 DK122624
Pays : United States
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : FR 3851/2-1
Organisme : U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (NHLBI)
ID : ZIA/HL006193
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (National Institute of Diabetes & Digestive & Kidney Diseases)
ID : ZIA/DK075149
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : ZIA/AI00117
Organisme : British Heart Foundation (BHF)
ID : RG/13/12/30395
Organisme : NIGMS NIH HHS
ID : R35 GM138283
Pays : United States
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R35GM138283
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : ZIA/AI001175
Organisme : U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (NHLBI)
ID : ZIA/Hl00622

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2021. This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.

Références

RECOVERY Collaborative Group et al.Dexamethasone in hospitalized patients with COVID-19. New Engl. J. Med. 384, 693–704 (2020).
doi: 10.1056/NEJMoa2021436
Gazzinelli, R. T. et al. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4
pubmed: 8752931 doi: 10.4049/jimmunol.157.2.798
Noris, M. & Remuzzi, G. Overview of complement activation and regulation. Semin. Nephrol. 33, 479–492 (2013).
pubmed: 24161035 pmcid: 3820029 doi: 10.1016/j.semnephrol.2013.08.001
Merle, N. S., Church, S. E., Fremeaux-Bacchi, V. & Roumenina, L. T. Complement system part I – molecular mechanisms of activation and regulation. Front. Immunol. 6, 262 (2015).
pubmed: 26082779 pmcid: 4451739 doi: 10.3389/fimmu.2015.00262
Robbins, R. A., Russ, W. D., Rasmussen, J. K. & Clayton, M. M. Activation of the complement system in the adult respiratory distress syndrome 1–4. Am. Rev. Respir. Dis. 135, 651–658 (1987).
pubmed: 3826891
Ohta, R. et al. Serum concentrations of complement anaphylatoxins and proinflammatory mediators in patients with 2009 H1N1 influenza. Microbiol. Immunol. 55, 191–198 (2011).
pubmed: 21244468 doi: 10.1111/j.1348-0421.2011.00309.x
Carvelli, J. et al. Association of COVID-19 inflammation with activation of the C5a–C5aR1 axis. Nature https://doi.org/10.1038/s41586-020-2600-6 (2020).
Sinkovits, G. et al. Complement overactivation and consumption predicts in-hospital mortality in SARS-CoV-2 infection. Front. Immunol. 12, 663187 (2021).
pubmed: 33841446 pmcid: 8027327 doi: 10.3389/fimmu.2021.663187
Ramlall, V. et al. Immune complement and coagulation dysfunction in adverse outcomes of SARS-CoV-2 infection. Nat. Med. 26, 1609–1615 (2020).
pubmed: 32747830 pmcid: 7809634 doi: 10.1038/s41591-020-1021-2
Rockx, B. et al. Early upregulation of acute respiratory distress syndrome-associated cytokines promotes lethal disease in an aged-mouse model of severe acute respiratory syndrome coronavirus infection. J. Virol. 83, 7062–7074 (2009).
pubmed: 19420084 pmcid: 2704758 doi: 10.1128/JVI.00127-09
Mastaglio, S. et al. The first case of COVID-19 treated with the complement C3 inhibitor AMY-101. Clin. Immunol. 215, 108450 (2020).
pubmed: 32360516 pmcid: 7189192 doi: 10.1016/j.clim.2020.108450
Liszewski, M. K. et al. Intracellular complement activation sustains T cell homeostasis and mediates effector differentiation. Immunity 39, 1143–1157 (2013).
pubmed: 24315997 pmcid: 3865363 doi: 10.1016/j.immuni.2013.10.018
Yan, B. et al. SARS-CoV-2 drives JAK1/2-dependent local complement hyperactivation. Sci. Immunol. 6, eabg0833 (2021).
pubmed: 33827897 pmcid: 8139422 doi: 10.1126/sciimmunol.abg0833
West, E. E., Kolev, M. & Kemper, C. Complement and the regulation of T cell responses. Annu Rev. Immunol. 36, 309–338 (2018).
pubmed: 29677470 pmcid: 7478175 doi: 10.1146/annurev-immunol-042617-053245
Break, T. J. et al. Aberrant type 1 immunity drives susceptibility to mucosal fungal infections. Science 371, eaay5731 (2021).
pubmed: 33446526 pmcid: 8326743 doi: 10.1126/science.aay5731
Cardone, J. et al. Complement regulator CD46 temporally regulates cytokine production by conventional and unconventional T cells. Nat. Immunol. 11, 862–871 (2010).
pubmed: 20694009 pmcid: 4011020 doi: 10.1038/ni.1917
Yamshchikov, A., Desai, N., Blumberg, H., Ziegler, T. & Tangpricha, V. Vitamin D for treatment and prevention of infectious diseases: a systematic review of randomized controlled trials. Endocr. Pr. 15, 438–449 (2009).
doi: 10.4158/EP09101.ORR
Holick, M. F. Vitamin D deficiency. N. Engl. J. Med. 357, 266–281 (2007).
pubmed: 17634462 doi: 10.1056/NEJMra070553
Akbar, M. R., Wibowo, A., Pranata, R. & Setiabudiawan, B. Low serum 25-hydroxyvitamin D (vitamin D) level is associated with susceptibility to COVID-19, severity, and mortality: a systematic review and meta-analysis. Front. Nutr. 8, 660420 (2021).
pubmed: 33855042 pmcid: 8039288 doi: 10.3389/fnut.2021.660420
Zhao, J. et al. Airway memory CD4(
pubmed: 27287409 pmcid: 4917442 doi: 10.1016/j.immuni.2016.05.006
Lucas, C. et al. Longitudinal analyses reveal immunological misfiring in severe COVID-19. Nature 584, 463–469 (2020).
pubmed: 32717743 pmcid: 7477538 doi: 10.1038/s41586-020-2588-y
Kolev, M. et al. Diapedesis-induced integrin signaling via LFA-1 facilitates tissue immunity by inducing intrinsic complement C3 expression in immune cells. Immunity 52, 513–527 (2020).
pubmed: 32187519 pmcid: 7111494 doi: 10.1016/j.immuni.2020.02.006
Magro, C. et al. Complement-associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: a report of five cases. Transl. Res. 220, 1–13 (2020).
pubmed: 32299776 pmcid: 7158248 doi: 10.1016/j.trsl.2020.04.007
Grifoni, A. et al. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell 181, 1489–1501 (2020).
pubmed: 32473127 pmcid: 7237901 doi: 10.1016/j.cell.2020.05.015
Sigmundsdottir, H. et al. DCs metabolize sunlight-induced vitamin D3 to ‘program’ T cell attraction to the epidermal chemokine CCL27. Nat. Immunol. 8, 285–293 (2007).
pubmed: 17259988 doi: 10.1038/ni1433
Veldman, C. M., Cantorna, M. T. & DeLuca, H. F. Expression of 1,25-dihydroxyvitamin D3 receptor in the immune system. Arch. Biochem. Biophys. 374, 334–338 (2000).
pubmed: 10666315 doi: 10.1006/abbi.1999.1605
Chen, D.-J. et al. Altered microRNAs expression in T cells of patients with SLE involved in the lack of vitamin D. Oncotarget 8, 62099–62110 (2017).
pubmed: 28977929 pmcid: 5617489 doi: 10.18632/oncotarget.19062
Jeffery, L. E. et al. 1,25-Dihydroxyvitamin D3 and IL-2 combine to inhibit T cell production of inflammatory cytokines and promote development of regulatory T cells expressing CTLA-4 and FoxP3. J. Immunol. 183, 5458–5467 (2009).
pubmed: 19843932 doi: 10.4049/jimmunol.0803217
Barrat, F. J. et al. In vitro generation of interleukin 10-producing regulatory CD4
pubmed: 11877483 pmcid: 2193760 doi: 10.1084/jem.20011629
Gagliani, N. et al. Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells. Nat. Med. 19, 739–746 (2013).
pubmed: 23624599 doi: 10.1038/nm.3179
Hunter, C. A. & Jones, S. A. IL-6 as a keystone cytokine in health and disease. Nat. Immunol. 16, 448–457 (2015).
pubmed: 25898198 doi: 10.1038/ni.3153
Abani, O. et al. Tocilizumab in patients admitted to hospital with COVID-19 (RECOVERY): a randomised, controlled, open-label, platform trial. Lancet 397, 1637–1645 (2021).
doi: 10.1016/S0140-6736(21)00676-0
Stumhofer, J. S. et al. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat. Immunol. 8, 1363–1371 (2007).
pubmed: 17994025 doi: 10.1038/ni1537
Jin, J.-O., Han, X. & Yu, Q. Interleukin-6 induces the generation of IL-10-producing Tr1 cells and suppresses autoimmune tissue inflammation. J. Autoimmun. 40, 28–44 (2013).
pubmed: 22921334 doi: 10.1016/j.jaut.2012.07.009
Bettelli, E. et al. Reciprocal developmental pathways for the generation of pathogenic effector T
pubmed: 16648838 doi: 10.1038/nature04753
Afzali, B. et al. BACH2 immunodeficiency illustrates an association between super-enhancers and haploinsufficiency. Nat. Immunol. 18, 813–823 (2017).
pubmed: 28530713 pmcid: 5593426 doi: 10.1038/ni.3753
Whyte, W. A. et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153, 307–319 (2013).
pubmed: 23582322 pmcid: 3653129 doi: 10.1016/j.cell.2013.03.035
Roychoudhuri, R. et al. BACH2 represses effector programs to stabilize T(reg)-mediated immune homeostasis. Nature 498, 506–510 (2013).
pubmed: 23728300 pmcid: 3710737 doi: 10.1038/nature12199
Povoleri, G. A. M. et al. Human retinoic acid–regulated CD161
pubmed: 30397350 pmcid: 6474659 doi: 10.1038/s41590-018-0230-z
Playford, M. P. et al. Serum active 1,25(OH)2D, but not inactive 25(OH)D vitamin D levels are associated with cardiometabolic and cardiovascular disease risk in psoriasis. Atherosclerosis 289, 44–50 (2019).
pubmed: 31450013 pmcid: 7428835 doi: 10.1016/j.atherosclerosis.2019.08.006
Armstrong, A. W. & Read, C. Pathophysiology, clinical presentation, and treatment of psoriasis. JAMA 323, 1945–1960 (2020).
pubmed: 32427307 doi: 10.1001/jama.2020.4006
Ghannam, A., Fauquert, J.-L., Thomas, C., Kemper, C. & Drouet, C. Human complement C3 deficiency: T
pubmed: 24321396 doi: 10.1016/j.molimm.2013.11.010
Schedel, M. et al. 1,25D3 prevents CD8
pubmed: 26750596 pmcid: 4712703 doi: 10.1038/ncomms10213
Song, J. et al. Vitamin D receptor restricts T helper 2-biased inflammation in the heart. Cardiovasc. Res. 114, 870–879 (2018).
pubmed: 29444238 doi: 10.1093/cvr/cvy034
Bohmann, D. et al. Human proto-oncogene c-jun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1. Science 238, 1386–1392 (1987).
pubmed: 2825349 doi: 10.1126/science.2825349
Tian, S. et al. Meta-analysis derived (MAD) transcriptome of psoriasis defines the ‘core’ pathogenesis of disease. PLoS ONE 7, e44274 (2012).
pubmed: 22957057 pmcid: 3434204 doi: 10.1371/journal.pone.0044274
Franke, A. et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn’s disease susceptibility loci. Nat. Genet. 42, 1118–1125 (2010).
pubmed: 21102463 pmcid: 3299551 doi: 10.1038/ng.717
Yegorov, S., Bromage, S., Boldbaatar, N. & Ganmaa, D. Effects of vitamin D supplementation and seasonality on circulating cytokines in adolescents: analysis of data from a feasibility trial in Mongolia. Front. Nutr. 6, 166 (2019).
pubmed: 31709259 pmcid: 6819500 doi: 10.3389/fnut.2019.00166
Turksen, K., Kupper, T., Degenstein, L., Williams, I. & Fuchs, E. Interleukin 6: insights to its function in skin by overexpression in transgenic mice. Proc. Natl Acad. Sci. USA 89, 5068–5072 (1992).
pubmed: 1375756 pmcid: 49230 doi: 10.1073/pnas.89.11.5068
Lin, Z., Kondo, T., Ishida, Y., Takayasu, T. & Mukaida, N. Essential involvement of IL-6 in the skin wound-healing process as evidenced by delayed wound healing in IL‐6‐deficient mice. J. Leukoc. Biol. 73, 713–721 (2003).
pubmed: 12773503 doi: 10.1189/jlb.0802397
Wendling, D., Letho-Gyselinck, H., Guillot, X. & Prati, C. Psoriasis onset with tocilizumab treatment for rheumatoid arthritis. J. Rheumatol. 39, 657–657 (2012).
pubmed: 22383356 doi: 10.3899/jrheum.111166
Nogues, X. et al. Calcifediol treatment and COVID-19-related outcomes. J. Clin. Endocrinol. Metab. 106, dgab405 (2021).
doi: 10.1210/clinem/dgab405
Alcala-Diaz, J. F. et al. Calcifediol treatment and hospital mortality due to COVID-19: a cohort study. Nutrients 13, 1760 (2021).
pubmed: 34064175 pmcid: 8224356 doi: 10.3390/nu13061760
Kolev, M. et al. Complement regulates nutrient influx and metabolic reprogramming during T
pubmed: 26084023 pmcid: 4518498 doi: 10.1016/j.immuni.2015.05.024
Skene, P. J., Henikoff, J. G. & Henikoff, S. Targeted in situ genome-wide profiling with high efficiency for low cell numbers. Nat. Protoc. 13, 1006–1019 (2018).
pubmed: 29651053 doi: 10.1038/nprot.2018.015
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286 pmcid: 3322381 doi: 10.1038/nmeth.1923
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Zhang, Y. et al. Model-based analysis of ChIP-seq (MACS). Genome Biol. 9, R137 (2008).
pubmed: 18798982 pmcid: 2592715 doi: 10.1186/gb-2008-9-9-r137
Zhu, Q., Liu, N., Orkin, S. H. & Yuan, G.-C. CUT&RUNTools: a flexible pipeline for CUT&RUN processing and footprint analysis. Genome Biol. 20, 192 (2019).
pubmed: 31500663 pmcid: 6734249 doi: 10.1186/s13059-019-1802-4
Ramírez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160–W165 (2016).
pubmed: 27079975 pmcid: 4987876 doi: 10.1093/nar/gkw257
Kaya-Okur, H. S. et al. CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat. Commun. 10, 1930 (2019).
pubmed: 31036827 pmcid: 6488672 doi: 10.1038/s41467-019-09982-5
Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinf. 12, 323 (2011).
doi: 10.1186/1471-2105-12-323
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
pubmed: 19910308 doi: 10.1093/bioinformatics/btp616
Liao, M. et al. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19. Nat. Med. 26, 842–844 (2020).
pubmed: 32398875 doi: 10.1038/s41591-020-0901-9
Reyfman, P. A. et al. Single-cell transcriptomic analysis of human lung provides insights into the pathobiology of pulmonary fibrosis. Am. J. Resp. Crit. Care 199, 1517–1536 (2019).
doi: 10.1164/rccm.201712-2410OC
Tirosh, I. et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189–196 (2016).
pubmed: 27124452 pmcid: 4944528 doi: 10.1126/science.aad0501
Stuart, T. et al. Comprehensive Integration of single-cell data. Cell 177, 1888–1902 (2019).
pubmed: 31178118 pmcid: 6687398 doi: 10.1016/j.cell.2019.05.031
Wilk, A. J. et al. A single-cell atlas of the peripheral immune response in patients with severe COVID-19. Nat. Med. 26, 1070–1076 (2020).
pubmed: 32514174 pmcid: 7382903 doi: 10.1038/s41591-020-0944-y
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517 pmcid: 1239896 doi: 10.1073/pnas.0506580102
Liberzon, A. et al. Molecular signatures database (MSigDB) 3.0. Bioinformatics 27, 1739–1740 (2011).
pubmed: 21546393 pmcid: 3106198 doi: 10.1093/bioinformatics/btr260
Liberzon, A. et al. The molecular signatures database hallmark gene set collection. Cell Syst. 1, 417–425 (2015).
pubmed: 26771021 pmcid: 4707969 doi: 10.1016/j.cels.2015.12.004
Stubbington, M. J. et al. An atlas of mouse CD4
pubmed: 25886751 pmcid: 4384382 doi: 10.1186/s13062-015-0045-x
Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003).
pubmed: 14597658 pmcid: 403769 doi: 10.1101/gr.1239303
Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009).
pubmed: 19541911 pmcid: 2752132 doi: 10.1101/gr.092759.109

Auteurs

Daniel Chauss (D)

Immunoregulation Section, Kidney Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), National Institutes of Health, Bethesda, MD, USA.

Tilo Freiwald (T)

Immunoregulation Section, Kidney Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), National Institutes of Health, Bethesda, MD, USA.
Medic Clinic III, Department of Nephrology, University Hospital Frankfurt, Goethe-University, Frankfurt, Germany.

Reuben McGregor (R)

Immunoregulation Section, Kidney Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), National Institutes of Health, Bethesda, MD, USA.
Department of Molecular Medicine and Pathology, School of Medical Sciences, The University of Auckland, Auckland, New Zealand.

Bingyu Yan (B)

Department of Biochemistry, Purdue University, West Lafayette, IN, USA.

Luopin Wang (L)

Department of Computer Science, Purdue University, West Lafayette, IN, USA.

Estefania Nova-Lamperti (E)

Molecular and Translational Immunology Laboratory, Department of Clinical Biochemistry and Immunology, Faculty of Pharmacy, Universidad de Concepcion, Concepcion, Chile.

Dhaneshwar Kumar (D)

Immunoregulation Section, Kidney Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), National Institutes of Health, Bethesda, MD, USA.
Department of Computer Science, Purdue University, West Lafayette, IN, USA.

Zonghao Zhang (Z)

Department of Agricultural and Biological Engineering, Purdue University, West Lafayette, IN, USA.

Heather Teague (H)

Laboratory of Inflammation & Cardiometabolic Diseases, Cardiovascular Branch, National Heart, Lung, and Blood Institute (NHLBI), National Institutes of Health, Bethesda, MD, USA.

Erin E West (EE)

Complement and Inflammation Research Section, National Heart, Lung, and Blood Institute (NHLBI), National Institutes of Health, Bethesda, MD, USA.

Kevin M Vannella (KM)

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health, Bethesda, MD, USA.
Emerging Pathogens Section, Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA.

Marcos J Ramos-Benitez (MJ)

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health, Bethesda, MD, USA.
Emerging Pathogens Section, Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA.

Jack Bibby (J)

Complement and Inflammation Research Section, National Heart, Lung, and Blood Institute (NHLBI), National Institutes of Health, Bethesda, MD, USA.

Audrey Kelly (A)

Peter Gorer Department of Immunobiology, School of Immunology and Microbial Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.

Amna Malik (A)

Department of Medicine, Imperial College London, London, UK.

Alexandra F Freeman (AF)

Laboratory of Clinical Immunology & Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health, Bethesda, MD, USA.

Daniella M Schwartz (DM)

Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health, Bethesda, MD, USA.

Didier Portilla (D)

Immunoregulation Section, Kidney Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), National Institutes of Health, Bethesda, MD, USA.
Division of Nephrology and the Center for Immunity, Inflammation and Regenerative Medicine, University of Virginia, Charlottesville, VA, USA.

Daniel S Chertow (DS)

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health, Bethesda, MD, USA.
Emerging Pathogens Section, Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA.

Susan John (S)

Peter Gorer Department of Immunobiology, School of Immunology and Microbial Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.

Paul Lavender (P)

Peter Gorer Department of Immunobiology, School of Immunology and Microbial Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.

Claudia Kemper (C)

Complement and Inflammation Research Section, National Heart, Lung, and Blood Institute (NHLBI), National Institutes of Health, Bethesda, MD, USA.
Institute for Systemic Inflammation Research, University of Lübeck, Lübeck, Germany.

Giovanna Lombardi (G)

Peter Gorer Department of Immunobiology, School of Immunology and Microbial Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.

Nehal N Mehta (NN)

Laboratory of Inflammation & Cardiometabolic Diseases, Cardiovascular Branch, National Heart, Lung, and Blood Institute (NHLBI), National Institutes of Health, Bethesda, MD, USA.

Nichola Cooper (N)

Department of Medicine, Imperial College London, London, UK.

Michail S Lionakis (MS)

Fungal Pathogenesis Section, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health, Bethesda, MD, USA.

Arian Laurence (A)

Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Majid Kazemian (M)

Department of Biochemistry, Purdue University, West Lafayette, IN, USA. kazemian@purdue.edu.
Department of Computer Science, Purdue University, West Lafayette, IN, USA. kazemian@purdue.edu.

Behdad Afzali (B)

Immunoregulation Section, Kidney Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), National Institutes of Health, Bethesda, MD, USA. behdad.afzali@nih.gov.

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