Cited by 504interferon and immune responsesCOVID-19 Clinical Research StudiesSARS-CoV-2 and COVID-19 Research

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Untuned antiviral immunity in COVID-19 revealed by temporal type I/III interferon patterns and flu comparison

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Galani, Ioanna-Evdokia, Rovina, Nikoletta, Lampropoulou, Vicky, Triantafyllia, Vasiliki, Manioudaki, Maria, Pavlos, Eleftherios, Koukaki, Evangelia, Fragkou, Paraskevi C., Panou, Vasiliki, Rapti, Vasiliki, Koltsida, Ourania, Mentis, Andreas, Koulouris, Nikolaos, Tsiodras, Sotirios, Koutsoukou, Antonia, Andreakos, Evangelos·2021·Nature Immunology

DOI 10.1038/s41590-020-00840-x

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Abstract

A central paradigm of immunity is that interferon (IFN)-mediated antiviral responses precede pro-inflammatory ones, optimizing host protection and minimizing collateral damage 1,2. Here, we report that for coronavirus disease 2019 (COVID-19) this paradigm does not apply. By investigating temporal IFN and inflammatory cytokine patterns in 32 moderate-to-severe patients with COVID-19 hospitalized for pneumonia and longitudinally followed for the development of respiratory failure and death, we reveal that IFN-λ and type I IFN production were both diminished and delayed, induced only in a fraction of patients as they became critically ill. On the contrary, pro-inflammatory cytokines such as tumor necrosis factor (TNF), interleukin (IL)-6 and IL-8 were produced before IFNs in all patients and persisted for a prolonged time. This condition was reflected in blood transcriptomes wherein prominent IFN signatures were only seen in critically ill patients who also exhibited augmented inflammation. By comparison, in 16 patients with influenza (flu) hospitalized for pneumonia with similar clinicopathological characteristics to those of COVID-19 and 24 nonhospitalized patients with flu with milder symptoms, IFN-λ and type I IFN were robustly induced earlier, at higher levels and independently of disease severity, whereas pro-inflammatory cytokines were only acutely produced. Notably, higher IFN-λ concentrations in patients with COVID-19 correlated with lower viral load in bronchial aspirates and faster viral clearance and a higher IFN-λ to type I IFN ratio correlated with improved outcome for critically ill patients. Moreover, altered cytokine patterns in patients with COVID-19 correlated with longer hospitalization and higher incidence of critical disease and mortality compared to flu. These data point to an untuned antiviral response in COVID-19, contributing to persistent viral presence, hyperinflammation and respiratory failure.

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Authors: Galani, I.-E., Rovina, N., Lampropoulou, V., Triantafyllia, V., Manioudaki, M., Pavlos, E., Koukaki, E., Fragkou, P. C., Panou, V., Rapti, V., Koltsida, O., Mentis, A., Koulouris, N., Tsiodras, S., Koutsoukou, A., & Andreakos, E.
Affiliations: Biomedical Research Foundation of the Academy of Athens (GR)
National and Kapodistrian University of Athens (GR)
Sotiria General Hospital (GR)
Pasteur Hellenic Institute (GR)
Corresponding author: Andreakos, Evangelos
ORCID: Galani, Ioanna-Evdokia
Rovina, Nikoletta
Lampropoulou, Vicky
Triantafyllia, Vasiliki
Koukaki, Evangelia
Fragkou, Paraskevi C.
Panou, Vasiliki
Rapti, Vasiliki
Koulouris, Nikolaos
Tsiodras, Sotirios
Koutsoukou, Antonia
Andreakos, Evangelos
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2020-12-04
Volume: 22
Issue: 1
Pages: 32-40
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/s41590-020-00840-x
OpenAlex: W3107596380
Cited by: 503
References: 41
Citations by year: 2026: 22 · 2025: 46 · 2024: 58 · 2023: 91 · 2022: 156 · 2021: 128 · 2020: 1
FWCI: 32.87
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Immunology (publishedVersion)
medRxiv (acceptedVersion)
PubMed (publishedVersion)
Funders: EC | Horizon 2020 Framework Programme (779295, 767015)
Janssen Pharmaceuticals
Topics: Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Keywords: COVID-19 pandemic, SARS-CoV-2, influenza, type I interferon, interferon lambda, antiviral immunity, inflammatory cytokines, interleukin-6, TNF-α, interleukin-8, hyperinflammation, viral load, viral clearance, respiratory failure, mortality, blood transcriptome, cytokine dynamics
MeSH terms: COVID-19, SARS-CoV-2, Interferon Lambda, Humans, Immunity, Inflammation, Influenza, Human, Interferon Type I, Interferons, Length of Stay, Prognosis, Gene Expression, Cytokines, Disease Progression, Viral Load, Gene Expression Profiling

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Untuned antiviral immunity in COVID-19 revealed by temporal type I/III interferon patterns and flu comparison

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