Autoantibodies in COVID‐19 correlate with antiviral humoral responses and distinct immune signatures

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Abstract

Background

Several autoimmune features occur during coronavirus disease 2019 (COVID‐19), with possible implications for disease course, immunity, and autoimmune pathology. In this study, we longitudinally screened for clinically relevant systemic autoantibodies to assess their prevalence, temporal trajectory, and association with immunity, comorbidities, and severity of COVID‐19.

Methods

We performed highly sensitive indirect immunofluorescence assays to detect antinuclear antibodies (ANA) and antineutrophil cytoplasmic antibodies (ANCA), along with serum proteomics and virome‐wide serological profiling in a multicentric cohort of 175 COVID‐19 patients followed up to 1 year after infection, eleven vaccinated individuals, and 41 unexposed controls.

Results

Compared with healthy controls, similar prevalence and patterns of ANA were present in patients during acute COVID‐19 and recovery. However, the paired analysis revealed a subgroup of patients with transient presence of certain ANA patterns during acute COVID‐19. Furthermore, patients with severe COVID‐19 exhibited a high prevalence of ANCA during acute disease. These autoantibodies were quantitatively associated with higher SARS‐CoV‐2‐specific antibody titers in COVID‐19 patients and in vaccinated individuals, thus linking autoantibody production to increased antigen‐specific humoral responses. Notably, the qualitative breadth of antibodies cross‐reactive with other coronaviruses was comparable in ANA‐positive and ANA‐negative individuals during acute COVID‐19. In autoantibody‐positive patients, multiparametric characterization demonstrated an inflammatory signature during acute COVID‐19 and alterations of the B‐cell compartment after recovery.

Conclusion

Highly sensitive indirect immunofluorescence assays revealed transient autoantibody production during acute SARS‐CoV‐2 infection, while the presence of autoantibodies in COVID‐19 patients correlated with increased antiviral humoral immune responses and inflammatory immune signatures.

Abstract

In a multicentric cohort of 175 COVID‐19 patients, 11 vaccinated individuals, and 41 unexposed controls, we measured ANA and ANCA, along with serum proteomics and virome‐wide serological profiling. Paired analysis revealed the transient presence of ANA patterns and ANCA during acute COVID‐19. The presence of autoantibodies correlated with increased virus‐specific humoral immune responses and a proinflammatory immune signature.

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Most cited references 58

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Clinical Characteristics of Coronavirus Disease 2019 in China

Wei-jie Guan, Zheng-yi Ni, Yu Hu … (2020)

Abstract Background Since December 2019, when coronavirus disease 2019 (Covid-19) emerged in Wuhan city and rapidly spread throughout China, data have been needed on the clinical characteristics of the affected patients. Methods We extracted data regarding 1099 patients with laboratory-confirmed Covid-19 from 552 hospitals in 30 provinces, autonomous regions, and municipalities in mainland China through January 29, 2020. The primary composite end point was admission to an intensive care unit (ICU), the use of mechanical ventilation, or death. Results The median age of the patients was 47 years; 41.9% of the patients were female. The primary composite end point occurred in 67 patients (6.1%), including 5.0% who were admitted to the ICU, 2.3% who underwent invasive mechanical ventilation, and 1.4% who died. Only 1.9% of the patients had a history of direct contact with wildlife. Among nonresidents of Wuhan, 72.3% had contact with residents of Wuhan, including 31.3% who had visited the city. The most common symptoms were fever (43.8% on admission and 88.7% during hospitalization) and cough (67.8%). Diarrhea was uncommon (3.8%). The median incubation period was 4 days (interquartile range, 2 to 7). On admission, ground-glass opacity was the most common radiologic finding on chest computed tomography (CT) (56.4%). No radiographic or CT abnormality was found in 157 of 877 patients (17.9%) with nonsevere disease and in 5 of 173 patients (2.9%) with severe disease. Lymphocytopenia was present in 83.2% of the patients on admission. Conclusions During the first 2 months of the current outbreak, Covid-19 spread rapidly throughout China and caused varying degrees of illness. Patients often presented without fever, and many did not have abnormal radiologic findings. (Funded by the National Health Commission of China and others.)

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Pathophysiology, Transmission, Diagnosis, and Treatment of Coronavirus Disease 2019 (COVID-19): A Review

W. Joost Wiersinga, Andrew Rhodes, Allen Cheng … (2020)

The coronavirus disease 2019 (COVID-19) pandemic, due to the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has caused a worldwide sudden and substantial increase in hospitalizations for pneumonia with multiorgan disease. This review discusses current evidence regarding the pathophysiology, transmission, diagnosis, and management of COVID-19.

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Autoantibodies against type I IFNs in patients with life-threatening COVID-19

Paul Bastard, Lindsey B. Rosen, Qian Zhang … (2021)

The genetics underlying severe COVID-19 The immune system is complex and involves many genes, including those that encode cytokines known as interferons (IFNs). Individuals that lack specific IFNs can be more susceptible to infectious diseases. Furthermore, the autoantibody system dampens IFN response to prevent damage from pathogen-induced inflammation. Two studies now examine the likelihood that genetics affects the risk of severe coronavirus disease 2019 (COVID-19) through components of this system (see the Perspective by Beck and Aksentijevich). Q. Zhang et al. used a candidate gene approach and identified patients with severe COVID-19 who have mutations in genes involved in the regulation of type I and III IFN immunity. They found enrichment of these genes in patients and conclude that genetics may determine the clinical course of the infection. Bastard et al. identified individuals with high titers of neutralizing autoantibodies against type I IFN-α2 and IFN-ω in about 10% of patients with severe COVID-19 pneumonia. These autoantibodies were not found either in infected people who were asymptomatic or had milder phenotype or in healthy individuals. Together, these studies identify a means by which individuals at highest risk of life-threatening COVID-19 can be identified. Science, this issue p. eabd4570, p. eabd4585; see also p. 404

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Author and article information

Contributors

Onur Boyman:

ORCID: https://orcid.org/0000-0001-8279-5545

onur.boyman@uzh.ch

Journal

Journal ID (nlm-ta): Allergy

Journal ID (iso-abbrev): Allergy

Journal ID (doi): 10.1111/(ISSN)1398-9995

Journal ID (publisher-id): ALL

Title: Allergy

Publisher: John Wiley and Sons Inc. (Hoboken )

ISSN (Print): 0105-4538

ISSN (Electronic): 1398-9995

Publication date (Electronic): 08 April 2022

Publication date PMC-release: 08 April 2022

Electronic Location Identifier: 10.1111/all.15302

Affiliations

[ ¹ ] Department of Immunology University Hospital Zurich Zurich Switzerland

[ ² ] Science for Life Laboratory Department of Women's and Children's Health Karolinska Institutet Solna Sweden

[ ³ ] Clinic for Internal Medicine Hirslanden Klinik St. Anna Lucerne Switzerland

[ ⁴ ] Department of Medicine Limmattal Hospital Schlieren Switzerland

[ ⁵ ] Clinic for Internal Medicine City Hospital Triemli Zurich Zurich Switzerland

[ ⁶ ] Pediatric Rheumatology Karolinska University Hospital Solna Sweden

[ ⁷ ] Department of Immunology and Inflammation Imperial College London London UK

[ ⁸ ] Faculty of Medicine University of Zurich Zurich Switzerland

Author notes

[*] [* ] Correspondence

Onur Boyman, Department of Immunology, University Hospital Zurich, Schmelzbergstrasse 26, 8091 Zurich, Switzerland.

Email: onur.boyman@ 123456uzh.ch

Author information

Patrick Taeschler https://orcid.org/0000-0003-0522-7629

Carlo Cervia https://orcid.org/0000-0001-7120-8739

Yves Zurbuchen https://orcid.org/0000-0001-5387-9950

Sara Hasler https://orcid.org/0000-0001-7357-9090

Christian Pou https://orcid.org/0000-0003-3932-788X

Ziyang Tan https://orcid.org/0000-0002-7205-4978

Sarah Adamo https://orcid.org/0000-0002-6161-3156

Miro E. Raeber https://orcid.org/0000-0003-2609-0246

Esther Bächli https://orcid.org/0000-0003-4887-7576

Alain Rudiger https://orcid.org/0000-0001-7943-7624

Melina Stüssi‐Helbling https://orcid.org/0000-0002-7896-6644

Lars C. Huber https://orcid.org/0000-0001-5378-4716

Petter Brodin https://orcid.org/0000-0002-8103-0046

Jakob Nilsson https://orcid.org/0000-0001-5091-8133

Elsbeth Probst‐Müller https://orcid.org/0000-0002-9046-4196

Onur Boyman https://orcid.org/0000-0001-8279-5545

Article

Publisher ID: ALL15302

DOI: 10.1111/all.15302

PMC ID: 9111424

PubMed ID: 35364615

SO-VID: 078945b1-db63-4c5f-b5e2-949784ff5c46

License:

This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

History

Date revision received : 08 March 2022

Date received : 10 February 2022

Date accepted : 20 March 2022

Page count

Figures: 7, Tables: 2, Pages: 16, Words: 8845

Funding

Funded by: Universitätsspital Zürich

Funded by: Gottfried und Julia Bangerter‐Rhyner‐Stiftung , doi 10.13039/501100005688;

Funded by: Universität Zürich

Funded by: Schweizerische Akademie der Medizinischen Wissenschaften , doi 10.13039/501100008485;

Funded by: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Funded by: Digitalization Initiative of the Zurich Higher Education Institutions

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details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.6 mode:remove_FC converted:17.05.2022

ScienceOpen disciplines: Immunology

Keywords: antinuclear antibodies,autoantibodies,covid‐19,sars‐cov‐2,virscan

Data availability:

ScienceOpen disciplines: Immunology

Keywords: antinuclear antibodies, autoantibodies, covid‐19, sars‐cov‐2, virscan

Autoantibodies in COVID‐19 correlate with antiviral humoral responses and distinct immune signatures

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Abstract

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Conclusion

Abstract

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Novel Coronavirus Disease COVID-19

Most cited references 58

Clinical Characteristics of Coronavirus Disease 2019 in China

Pathophysiology, Transmission, Diagnosis, and Treatment of Coronavirus Disease 2019 (COVID-19): A Review

Autoantibodies against type I IFNs in patients with life-threatening COVID-19

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