Protective immune trajectories in early viral containment of non-pneumonic SARS-CoV-2 infection

Kami Pekayvaz; Alexander Leunig; Rainer Kaiser; Markus Joppich; Sophia Brambs; Aleksandar Janjic; Oliver Popp; Daniel Nixdorf; Valeria Fumagalli; Nora Schmidt; Vivien Polewka; Afra Anjum; Viktoria Knottenberg; Luke Eivers; Lucas E. Wange; Christoph Gold; Marieluise Kirchner; Maximilian Muenchhoff; Johannes C. Hellmuth; Clemens Scherer; Raquel Rubio-Acero; Tabea Eser; Flora Deák; Kerstin Puchinger; Niklas Kuhl; Andreas Linder; Kathrin Saar; Lukas Tomas; Christian Schulz; Andreas Wieser; Wolfgang Enard; Inge Kroidl; Christof Geldmacher; Michael von Bergwelt-Baildon; Oliver T. Keppler; Mathias Munschauer; Matteo Iannacone; Ralf Zimmer; Philipp Mertins; Norbert Hubner; Michael Hoelscher; Steffen Massberg; Konstantin Stark; Leo Nicolai

doi:10.1038/s41467-022-28508-0

Protective immune trajectories in early viral containment of non-pneumonic SARS-CoV-2 infection

Kami Pekayvaz^*
, Alexander Leunig
, Rainer Kaiser
, Markus Joppich
, Sophia Brambs
, Aleksandar Janjic
, Oliver Popp
, Daniel Nixdorf
, Valeria Fumagalli
, Nora Schmidt
, Vivien Polewka
, Afra Anjum
, Viktoria Knottenberg
, Luke Eivers
, Lucas E. Wange
, Christoph Gold
, Marieluise Kirchner
, Maximilian Muenchhoff
, Johannes C. Hellmuth
, Clemens Scherer

Raquel Rubio-Acero, Tabea Eser, Flora Deák, Kerstin Puchinger, Niklas Kuhl, Andreas Linder, Kathrin Saar, Lukas Tomas, Christian Schulz, Andreas Wieser, Wolfgang Enard, Inge Kroidl, Christof Geldmacher, Michael von Bergwelt-Baildon, Oliver T. Keppler, Mathias Munschauer, Matteo Iannacone, Ralf Zimmer, Philipp Mertins, Norbert Hubner, Michael Hoelscher, Steffen Massberg, Konstantin Stark^*, Leo Nicolai^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

21 Scopus citations

Abstract

The antiviral immune response to SARS-CoV-2 infection can limit viral spread and prevent development of pneumonic COVID-19. However, the protective immunological response associated with successful viral containment in the upper airways remains unclear. Here, we combine a multi-omics approach with longitudinal sampling to reveal temporally resolved protective immune signatures in non-pneumonic and ambulatory SARS-CoV-2 infected patients and associate specific immune trajectories with upper airway viral containment. We see a distinct systemic rather than local immune state associated with viral containment, characterized by interferon stimulated gene (ISG) upregulation across circulating immune cell subsets in non-pneumonic SARS-CoV2 infection. We report reduced cytotoxic potential of Natural Killer (NK) and T cells, and an immune-modulatory monocyte phenotype associated with protective immunity in COVID-19. Together, we show protective immune trajectories in SARS-CoV2 infection, which have important implications for patient prognosis and the development of immunomodulatory therapies.

Original language	English
Article number	1018
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-28508-0
State	Published - Dec 2022
Externally published	Yes

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Pekayvaz, K., Leunig, A., Kaiser, R., Joppich, M., Brambs, S., Janjic, A., Popp, O., Nixdorf, D., Fumagalli, V., Schmidt, N., Polewka, V., Anjum, A., Knottenberg, V., Eivers, L., Wange, L. E., Gold, C., Kirchner, M., Muenchhoff, M., Hellmuth, J. C., ... Nicolai, L. (2022). Protective immune trajectories in early viral containment of non-pneumonic SARS-CoV-2 infection. Nature Communications, 13(1), Article 1018. https://doi.org/10.1038/s41467-022-28508-0

@article{b23748dc072846d8a01590fde973d6bd,

title = "Protective immune trajectories in early viral containment of non-pneumonic SARS-CoV-2 infection",

abstract = "The antiviral immune response to SARS-CoV-2 infection can limit viral spread and prevent development of pneumonic COVID-19. However, the protective immunological response associated with successful viral containment in the upper airways remains unclear. Here, we combine a multi-omics approach with longitudinal sampling to reveal temporally resolved protective immune signatures in non-pneumonic and ambulatory SARS-CoV-2 infected patients and associate specific immune trajectories with upper airway viral containment. We see a distinct systemic rather than local immune state associated with viral containment, characterized by interferon stimulated gene (ISG) upregulation across circulating immune cell subsets in non-pneumonic SARS-CoV2 infection. We report reduced cytotoxic potential of Natural Killer (NK) and T cells, and an immune-modulatory monocyte phenotype associated with protective immunity in COVID-19. Together, we show protective immune trajectories in SARS-CoV2 infection, which have important implications for patient prognosis and the development of immunomodulatory therapies.",

author = "Kami Pekayvaz and Alexander Leunig and Rainer Kaiser and Markus Joppich and Sophia Brambs and Aleksandar Janjic and Oliver Popp and Daniel Nixdorf and Valeria Fumagalli and Nora Schmidt and Vivien Polewka and Afra Anjum and Viktoria Knottenberg and Luke Eivers and Wange, \{Lucas E.\} and Christoph Gold and Marieluise Kirchner and Maximilian Muenchhoff and Hellmuth, \{Johannes C.\} and Clemens Scherer and Raquel Rubio-Acero and Tabea Eser and Flora De{\'a}k and Kerstin Puchinger and Niklas Kuhl and Andreas Linder and Kathrin Saar and Lukas Tomas and Christian Schulz and Andreas Wieser and Wolfgang Enard and Inge Kroidl and Christof Geldmacher and \{von Bergwelt-Baildon\}, Michael and Keppler, \{Oliver T.\} and Mathias Munschauer and Matteo Iannacone and Ralf Zimmer and Philipp Mertins and Norbert Hubner and Michael Hoelscher and Steffen Massberg and Konstantin Stark and Leo Nicolai",

note = "Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1038/s41467-022-28508-0",

language = "English",

volume = "13",

journal = "Nature Communications",

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Pekayvaz, K, Leunig, A, Kaiser, R, Joppich, M, Brambs, S, Janjic, A, Popp, O, Nixdorf, D, Fumagalli, V, Schmidt, N, Polewka, V, Anjum, A, Knottenberg, V, Eivers, L, Wange, LE, Gold, C, Kirchner, M, Muenchhoff, M, Hellmuth, JC, Scherer, C, Rubio-Acero, R, Eser, T, Deák, F, Puchinger, K, Kuhl, N, Linder, A, Saar, K, Tomas, L, Schulz, C, Wieser, A, Enard, W, Kroidl, I, Geldmacher, C, von Bergwelt-Baildon, M, Keppler, OT, Munschauer, M, Iannacone, M, Zimmer, R, Mertins, P, Hubner, N, Hoelscher, M, Massberg, S, Stark, K & Nicolai, L 2022, 'Protective immune trajectories in early viral containment of non-pneumonic SARS-CoV-2 infection', Nature Communications, vol. 13, no. 1, 1018. https://doi.org/10.1038/s41467-022-28508-0

TY - JOUR

T1 - Protective immune trajectories in early viral containment of non-pneumonic SARS-CoV-2 infection

AU - Pekayvaz, Kami

AU - Leunig, Alexander

AU - Kaiser, Rainer

AU - Joppich, Markus

AU - Brambs, Sophia

AU - Janjic, Aleksandar

AU - Popp, Oliver

AU - Nixdorf, Daniel

AU - Fumagalli, Valeria

AU - Schmidt, Nora

AU - Polewka, Vivien

AU - Anjum, Afra

AU - Knottenberg, Viktoria

AU - Eivers, Luke

AU - Wange, Lucas E.

AU - Gold, Christoph

AU - Kirchner, Marieluise

AU - Muenchhoff, Maximilian

AU - Hellmuth, Johannes C.

AU - Scherer, Clemens

AU - Rubio-Acero, Raquel

AU - Eser, Tabea

AU - Deák, Flora

AU - Puchinger, Kerstin

AU - Kuhl, Niklas

AU - Linder, Andreas

AU - Saar, Kathrin

AU - Tomas, Lukas

AU - Schulz, Christian

AU - Wieser, Andreas

AU - Enard, Wolfgang

AU - Kroidl, Inge

AU - Geldmacher, Christof

AU - von Bergwelt-Baildon, Michael

AU - Keppler, Oliver T.

AU - Munschauer, Mathias

AU - Iannacone, Matteo

AU - Zimmer, Ralf

AU - Mertins, Philipp

AU - Hubner, Norbert

AU - Hoelscher, Michael

AU - Massberg, Steffen

AU - Stark, Konstantin

AU - Nicolai, Leo

PY - 2022/12

Y1 - 2022/12

N2 - The antiviral immune response to SARS-CoV-2 infection can limit viral spread and prevent development of pneumonic COVID-19. However, the protective immunological response associated with successful viral containment in the upper airways remains unclear. Here, we combine a multi-omics approach with longitudinal sampling to reveal temporally resolved protective immune signatures in non-pneumonic and ambulatory SARS-CoV-2 infected patients and associate specific immune trajectories with upper airway viral containment. We see a distinct systemic rather than local immune state associated with viral containment, characterized by interferon stimulated gene (ISG) upregulation across circulating immune cell subsets in non-pneumonic SARS-CoV2 infection. We report reduced cytotoxic potential of Natural Killer (NK) and T cells, and an immune-modulatory monocyte phenotype associated with protective immunity in COVID-19. Together, we show protective immune trajectories in SARS-CoV2 infection, which have important implications for patient prognosis and the development of immunomodulatory therapies.

AB - The antiviral immune response to SARS-CoV-2 infection can limit viral spread and prevent development of pneumonic COVID-19. However, the protective immunological response associated with successful viral containment in the upper airways remains unclear. Here, we combine a multi-omics approach with longitudinal sampling to reveal temporally resolved protective immune signatures in non-pneumonic and ambulatory SARS-CoV-2 infected patients and associate specific immune trajectories with upper airway viral containment. We see a distinct systemic rather than local immune state associated with viral containment, characterized by interferon stimulated gene (ISG) upregulation across circulating immune cell subsets in non-pneumonic SARS-CoV2 infection. We report reduced cytotoxic potential of Natural Killer (NK) and T cells, and an immune-modulatory monocyte phenotype associated with protective immunity in COVID-19. Together, we show protective immune trajectories in SARS-CoV2 infection, which have important implications for patient prognosis and the development of immunomodulatory therapies.

UR - https://www.scopus.com/pages/publications/85125156047

U2 - 10.1038/s41467-022-28508-0

DO - 10.1038/s41467-022-28508-0

M3 - Article

C2 - 35197461

AN - SCOPUS:85125156047

SN - 2041-1723

VL - 13

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 1018

ER -

Protective immune trajectories in early viral containment of non-pneumonic SARS-CoV-2 infection

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