Autoantibodies against chemokines post-SARS-CoV-2 infection correlate with disease course.
Journal
Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
received:
11
07
2022
accepted:
27
01
2023
medline:
3
4
2023
pubmed:
7
3
2023
entrez:
6
3
2023
Statut:
ppublish
Résumé
Infection with severe acute respiratory syndrome coronavirus 2 associates with diverse symptoms, which can persist for months. While antiviral antibodies are protective, those targeting interferons and other immune factors are associated with adverse coronavirus disease 2019 (COVID-19) outcomes. Here we discovered that antibodies against specific chemokines were omnipresent post-COVID-19, were associated with favorable disease outcome and negatively correlated with the development of long COVID at 1 yr post-infection. Chemokine antibodies were also present in HIV-1 infection and autoimmune disorders, but they targeted different chemokines compared with COVID-19. Monoclonal antibodies derived from COVID-19 convalescents that bound to the chemokine N-loop impaired cell migration. Given the role of chemokines in orchestrating immune cell trafficking, naturally arising chemokine antibodies may modulate the inflammatory response and thus bear therapeutic potential.
Identifiants
pubmed: 36879067
doi: 10.1038/s41590-023-01445-w
pii: 10.1038/s41590-023-01445-w
pmc: PMC10063443
mid: EMS172243
doi:
Substances chimiques
Autoantibodies
0
Chemokines
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
604-611Subventions
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : P01-AI138938
Organisme : Swiss National Science Foundation
ID : 198431
Pays : Switzerland
Organisme : Wellcome Trust
ID : 201369
Pays : United Kingdom
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : U01-AI151698
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : U19-AI111825
Commentaires et corrections
Type : UpdateOf
Type : CommentIn
Informations de copyright
© 2023. The Author(s).
Références
Mehandru, S. & Merad, M. Pathological sequelae of long-haul COVID. Nat. Immunol. 23, 194–202 (2022).
doi: 10.1038/s41590-021-01104-y
pubmed: 35105985
pmcid: 9127978
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
pubmed: 31986264
pmcid: 7159299
Blomberg, B. et al. Long COVID in a prospective cohort of home-isolated patients. Nat. Med. 27, 1607–1613 (2021).
doi: 10.1038/s41591-021-01433-3
pubmed: 34163090
pmcid: 8440190
Nalbandian, A. et al. Post-acute COVID-19 syndrome. Nat. Med. 27, 601–615 (2021).
doi: 10.1038/s41591-021-01283-z
pubmed: 33753937
pmcid: 8893149
Merad, M., Blish, C. A., Sallusto, F. & Iwasaki, A. The immunology and immunopathology of COVID-19. Science 375, 1122–1127 (2022).
doi: 10.1126/science.abm8108
pubmed: 35271343
Phetsouphanh, C. et al. Immunological dysfunction persists for 8 months following initial mild-to-moderate SARS-CoV-2 infection. Nat. Immunol. 23, 210–216 (2022).
doi: 10.1038/s41590-021-01113-x
pubmed: 35027728
Cervia, C. et al. Immunoglobulin signature predicts risk of post-acute COVID-19 syndrome. Nat. Commun. 13, 446 (2022).
doi: 10.1038/s41467-021-27797-1
pubmed: 35078982
pmcid: 8789854
Proal, A. D. & VanElzakker, M. B. Long COVID or post-acute sequelae of COVID-19 (PASC): an overview of biological factors that may contribute to persistent symptoms. Front. Microbiol. 12, 698169 (2021).
doi: 10.3389/fmicb.2021.698169
pubmed: 34248921
pmcid: 8260991
Chen, K. et al. Chemokines in homeostasis and diseases. Cell. Mol. Immunol. 15, 324–334 (2018).
doi: 10.1038/cmi.2017.134
pubmed: 29375126
pmcid: 6052829
Blanco-Melo, D. et al. Imbalanced host response to SARS-CoV-2 drives development of COVID-19. Cell 181, 1036–1045.e1039 (2020).
doi: 10.1016/j.cell.2020.04.026
pubmed: 32416070
pmcid: 7227586
Liao, M. et al. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19. Nat. Med. 26, 842–844 (2020).
doi: 10.1038/s41591-020-0901-9
pubmed: 32398875
Paludan, S. R. & Mogensen, T. H. Innate immunological pathways in COVID-19 pathogenesis. Sci. Immunol. 7, eabm5505 (2022).
doi: 10.1126/sciimmunol.abm5505
pubmed: 34995097
Khalil, B. A., Elemam, N. M. & Maghazachi, A. A. Chemokines and chemokine receptors during COVID-19 infection. Comput. Struct. Biotechnol. J. 19, 976–988 (2021).
doi: 10.1016/j.csbj.2021.01.034
pubmed: 33558827
pmcid: 7859556
Lucas, C. et al. Longitudinal analyses reveal immunological misfiring in severe COVID-19. Nature 584, 463–469 (2020).
doi: 10.1038/s41586-020-2588-y
pubmed: 32717743
pmcid: 7477538
COMBAT-Consortium. A blood atlas of COVID-19 defines hallmarks of disease severity and specificity. Cell 185, 916–938.e958 (2022).
doi: 10.1016/j.cell.2022.01.012
Su, Y. et al. Multi-omics resolves a sharp disease-state shift between mild and moderate COVID-19. Cell 183, 1479–1495.e1420 (2020).
doi: 10.1016/j.cell.2020.10.037
pubmed: 33171100
pmcid: 7598382
Rendeiro, A. F. et al. The spatial landscape of lung pathology during COVID-19 progression. Nature 593, 564–569 (2021).
doi: 10.1038/s41586-021-03475-6
pubmed: 33780969
pmcid: 8204801
Wendisch, D. et al. SARS-CoV-2 infection triggers profibrotic macrophage responses and lung fibrosis. Cell 184, 6243–6261.e6227 (2021).
doi: 10.1016/j.cell.2021.11.033
pubmed: 34914922
pmcid: 8626230
Bastard, P. et al. Autoantibodies neutralizing type I IFNs are present in ~4% of uninfected individuals over 70 years old and account for ~20% of COVID-19 deaths. Sci. Immunol. 6, eabl4340 (2021).
doi: 10.1126/sciimmunol.abl4340
pubmed: 34413139
pmcid: 8521484
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
pubmed: 32972996
pmcid: 7857397
Chang, S. E. et al. New-onset IgG autoantibodies in hospitalized patients with COVID-19. Nat. Commun. 12, 5417 (2021).
doi: 10.1038/s41467-021-25509-3
pubmed: 34521836
pmcid: 8440763
Zuo, Y. et al. Prothrombotic autoantibodies in serum from patients hospitalized with COVID-19. Sci. Transl. Med. 12, eabd3876 (2020).
doi: 10.1126/scitranslmed.abd3876
pubmed: 33139519
pmcid: 7724273
van der Wijst, M. G. P. et al. Type I interferon autoantibodies are associated with systemic immune alterations in patients with COVID-19. Sci. Transl. Med. 13, eabh2624 (2021).
doi: 10.1126/scitranslmed.abh2624
pubmed: 34429372
pmcid: 8601717
Woodruff, M. C. et al. Dysregulated naive B cells and de novo autoreactivity in severe COVID-19. Nature 611, 139–147 (2022).
doi: 10.1038/s41586-022-05273-0
pubmed: 36044993
pmcid: 9630115
Wang, E. Y. et al. Diverse functional autoantibodies in patients with COVID-19. Nature 595, 283–288 (2021).
doi: 10.1038/s41586-021-03631-y
pubmed: 34010947
Crump, M. P. et al. Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J. 16, 6996–7007 (1997).
doi: 10.1093/emboj/16.23.6996
pubmed: 9384579
pmcid: 1170303
Robbiani, D. F. et al. Convergent antibody responses to SARS-CoV-2 in convalescent individuals. Nature 584, 437–442 (2020).
doi: 10.1038/s41586-020-2456-9
pubmed: 32555388
pmcid: 7442695
Gaebler, C. et al. Evolution of antibody immunity to SARS-CoV-2. Nature 591, 639–644 (2021).
doi: 10.1038/s41586-021-03207-w
pubmed: 33461210
pmcid: 8221082
Gonzalez-Quintela, A. et al. Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin. Exp. Immunol. 151, 42–50 (2008).
doi: 10.1111/j.1365-2249.2007.03545.x
pubmed: 18005364
pmcid: 2276914
Su, Y. et al. Multiple early factors anticipate post-acute COVID-19 sequelae. Cell 185, 881–895.e820 (2022).
doi: 10.1016/j.cell.2022.01.014
pubmed: 35216672
pmcid: 8786632
Browne, S. K. & Holland, S. M. Anticytokine autoantibodies in infectious diseases: pathogenesis and mechanisms. Lancet Infect. Dis. 10, 875–885 (2010).
doi: 10.1016/S1473-3099(10)70196-1
pubmed: 21109174
Garcia, D. & Erkan, D. Diagnosis and management of the antiphospholipid syndrome. N. Engl. J. Med. 378, 2010–2021 (2018).
doi: 10.1056/NEJMra1705454
pubmed: 29791828
Mantovani, A. et al. Long Covid: where we stand and challenges ahead. Cell Death Differ. 29, 1891–1900 (2022).
pubmed: 36071155
pmcid: 9449925
Mouquet, H. & Nussenzweig, M. C. Polyreactive antibodies in adaptive immune responses to viruses. Cell. Mol. Life Sci. 69, 1435–1445 (2012).
doi: 10.1007/s00018-011-0872-6
pubmed: 22045557
Ercolini, A. M. & Miller, S. D. The role of infections in autoimmune disease. Clin. Exp. Immunol. 155, 1–15 (2009).
doi: 10.1111/j.1365-2249.2008.03834.x
pubmed: 19076824
pmcid: 2665673
Suurmond, J. & Diamond, B. Autoantibodies in systemic autoimmune diseases: specificity and pathogenicity. J. Clin. Invest. 125, 2194–2202 (2015).
doi: 10.1172/JCI78084
pubmed: 25938780
pmcid: 4497746
Baden, L. R. et al. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N. Engl. J. Med. 384, 403–416 (2021).
doi: 10.1056/NEJMoa2035389
pubmed: 33378609
Polack, F. P. et al. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N. Engl. J. Med. 383, 2603–2615 (2020).
doi: 10.1056/NEJMoa2034577
pubmed: 33301246
Cecchinato, V. et al. Impairment of CCR6
doi: 10.4049/jimmunol.1600568
pubmed: 27895171
Stravalaci, M. et al. Recognition and inhibition of SARS-CoV-2 by humoral innate immunity pattern recognition molecules. Nat. Immunol. 23, 275–286 (2022).
doi: 10.1038/s41590-021-01114-w
pubmed: 35102342
Bello-Rivero, I. et al. Characterization of the immunoreactivity of anti-interferon alpha antibodies in myasthenia gravis patients. Epitope mapping. J. Autoimmun. 23, 63–73 (2004).
doi: 10.1016/j.jaut.2004.03.013
pubmed: 15236754
Shrock, E. et al. Viral epitope profiling of COVID-19 patients reveals cross-reactivity and correlates of severity. Science 370, eabd4250 (2020).
doi: 10.1126/science.abd4250
pubmed: 32994364
pmcid: 7857405
Clark-Lewis, I., Vo, L., Owen, P. & Anderson, J. Chemical synthesis, purification, and folding of C-X-C and C-C chemokines. Methods Enzymol. 287, 233–250 (1997).
doi: 10.1016/S0076-6879(97)87018-8
pubmed: 9330326
Moepps, B. & Thelen, M. Monitoring scavenging activity of chemokine receptors. Methods Enzymol. 570, 87–118 (2016).
doi: 10.1016/bs.mie.2015.11.003
pubmed: 26921943
De Gasparo, R. et al. Bispecific IgG neutralizes SARS-CoV-2 variants and prevents escape in mice. Nature 593, 424–428 (2021).
doi: 10.1038/s41586-021-03461-y
pubmed: 33767445
Ogilvie, P., Bardi, G., Clark-Lewis, I., Baggiolini, M. & Uguccioni, M. Eotaxin is a natural antagonist for CCR2 and an agonist for CCR5. Blood 97, 1920–1924 (2001).
doi: 10.1182/blood.V97.7.1920
pubmed: 11264152
Zaslaver, A., Feniger-Barish, R. & Ben-Baruch, A. Actin filaments are involved in the regulation of trafficking of two closely related chemokine receptors, CXCR1 and CXCR2. J. Immunol. 166, 1272–1284 (2001).
doi: 10.4049/jimmunol.166.2.1272
pubmed: 11145710
Loetscher, M. et al. TYMSTR, a putative chemokine receptor selectively expressed in activated T cells, exhibits HIV-1 coreceptor function. Curr. Biol. 7, 652–660 (1997).
doi: 10.1016/S0960-9822(06)00292-2
pubmed: 9285716
Uguccioni, M., D’Apuzzo, M., Loetscher, M., Dewald, B. & Baggiolini, M. Actions of the chemotactic cytokines MCP-1, MCP-2, MCP-3, RANTES, MIP-1α and MIP-1β on human monocytes. Eur. J. Immunol. 25, 64–68 (1995).
doi: 10.1002/eji.1830250113
pubmed: 7531149
Robbiani, D. F. et al. Recurrent potent human neutralizing antibodies to Zika virus in brazil and Mexico. Cell 169, 597–609.e511 (2017).
doi: 10.1016/j.cell.2017.04.024
pubmed: 28475892
pmcid: 5492969
Tiller, T. et al. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329, 112–124 (2008).
doi: 10.1016/j.jim.2007.09.017
pubmed: 17996249
von Boehmer, L. et al. Sequencing and cloning of antigen-specific antibodies from mouse memory B cells. Nat. Protoc. 11, 1908–1923 (2016).
doi: 10.1038/nprot.2016.102
Ye, J., Ma, N., Madden, T. L. & Ostell, J. M. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res. 41, W34–W40 (2013).
doi: 10.1093/nar/gkt382
pubmed: 23671333
pmcid: 3692102
Gupta, N. T. et al. Change-O: a toolkit for analyzing large-scale B cell immunoglobulin repertoire sequencing data. Bioinformatics 31, 3356–3358 (2015).
doi: 10.1093/bioinformatics/btv359
pubmed: 26069265
pmcid: 4793929
Schmidt, F. et al. Measuring SARS-CoV-2 neutralizing antibody activity using pseudotyped and chimeric viruses. J. Exp. Med. 217, e20201181 (2020).
doi: 10.1084/jem.20201181
pubmed: 32692348
pmcid: 7372514
Zheng, Y. et al. Structure of CC chemokine receptor 2 with orthosteric and allosteric antagonists. Nature 540, 458–461 (2016).
doi: 10.1038/nature20605
pubmed: 27926736
pmcid: 5159191
Shaik, M. M. et al. Structural basis of coreceptor recognition by HIV-1 envelope spike. Nature 565, 318–323 (2019).
doi: 10.1038/s41586-018-0804-9
pubmed: 30542158
Wasilko, D. J. et al. Structural basis for chemokine receptor CCR6 activation by the endogenous protein ligand CCL20. Nat. Commun. 11, 3031 (2020).
doi: 10.1038/s41467-020-16820-6
pubmed: 32541785
pmcid: 7295996
Waterhouse, A. et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 46, W296–W303 (2018).
doi: 10.1093/nar/gky427
pubmed: 29788355
pmcid: 6030848
Blaszczyk, J. et al. Complete crystal structure of monocyte chemotactic protein-2, a CC chemokine that interacts with multiple receptors. Biochemistry 39, 14075–14081 (2000).
doi: 10.1021/bi0009340
pubmed: 11087354