IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28508-0.html
   My bibliography  Save this article

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

Author

Listed:
  • Kami Pekayvaz

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance)

  • Alexander Leunig

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance)

  • Rainer Kaiser

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance)

  • Markus Joppich

    (Ludwig-Maximilian Universität München)

  • Sophia Brambs

    (University Hospital, LMU Munich)

  • Aleksandar Janjic

    (Ludwig-Maximilians University Munich)

  • Oliver Popp

    (Max Delbrück Center for Molecular Medicine (MDC) and Berlin Institute of Health (BIH))

  • Daniel Nixdorf

    (Gene Center, LMU Munich
    University Hospital, LMU Munich)

  • Valeria Fumagalli

    (IRCCS San Raffaele Scientific Institute
    Vita-Salute San Raffaele University)

  • Nora Schmidt

    (Helmholtz-Center for Infection Research)

  • Vivien Polewka

    (University Hospital, LMU Munich)

  • Afra Anjum

    (University Hospital, LMU Munich)

  • Viktoria Knottenberg

    (University Hospital, LMU Munich)

  • Luke Eivers

    (University Hospital, LMU Munich)

  • Lucas E. Wange

    (Ludwig-Maximilians University Munich)

  • Christoph Gold

    (University Hospital, LMU Munich)

  • Marieluise Kirchner

    (Max Delbrück Center for Molecular Medicine (MDC) and Berlin Institute of Health (BIH))

  • Maximilian Muenchhoff

    (Faculty of Medicine, LMU München
    Partner Site Munich
    University Hospital, LMU Munich)

  • Johannes C. Hellmuth

    (University Hospital, LMU Munich
    University Hospital, LMU Munich)

  • Clemens Scherer

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance
    University Hospital, LMU Munich)

  • Raquel Rubio-Acero

    (Partner Site Munich
    University Hospital Ludwig-Maximilian University Munich)

  • Tabea Eser

    (Partner Site Munich
    University Hospital Ludwig-Maximilian University Munich)

  • Flora Deák

    (Partner Site Munich
    University Hospital Ludwig-Maximilian University Munich)

  • Kerstin Puchinger

    (University Hospital Ludwig-Maximilian University Munich)

  • Niklas Kuhl

    (University Hospital Ludwig-Maximilian University Munich
    University Hospital, LMU Munich)

  • Andreas Linder

    (University Hospital Ludwig-Maximilian University Munich
    University Hospital, LMU Munich)

  • Kathrin Saar

    (Max Delbrück Center for Molecular Medicine (MDC) and Berlin Institute of Health (BIH)
    DZHK (German Centre for Cardiovascular Research))

  • Lukas Tomas

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance)

  • Christian Schulz

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance)

  • Andreas Wieser

    (Partner Site Munich
    University Hospital Ludwig-Maximilian University Munich)

  • Wolfgang Enard

    (Ludwig-Maximilians University Munich)

  • Inge Kroidl

    (Partner Site Munich
    University Hospital Ludwig-Maximilian University Munich)

  • Christof Geldmacher

    (Partner Site Munich
    University Hospital Ludwig-Maximilian University Munich)

  • Michael Bergwelt-Baildon

    (University Hospital, LMU Munich
    University Hospital, LMU Munich)

  • Oliver T. Keppler

    (Faculty of Medicine, LMU München
    Partner Site Munich
    University Hospital, LMU Munich)

  • Mathias Munschauer

    (Helmholtz-Center for Infection Research)

  • Matteo Iannacone

    (IRCCS San Raffaele Scientific Institute
    Vita-Salute San Raffaele University
    IRCCS San Raffaele Scientific Institute)

  • Ralf Zimmer

    (Ludwig-Maximilian Universität München)

  • Philipp Mertins

    (Max Delbrück Center for Molecular Medicine (MDC) and Berlin Institute of Health (BIH))

  • Norbert Hubner

    (Max Delbrück Center for Molecular Medicine (MDC) and Berlin Institute of Health (BIH)
    DZHK (German Centre for Cardiovascular Research))

  • Michael Hoelscher

    (Partner Site Munich
    University Hospital Ludwig-Maximilian University Munich)

  • Steffen Massberg

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance)

  • Konstantin Stark

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance)

  • Leo Nicolai

    (University Hospital, LMU Munich
    partner site Munich Heart Alliance)

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.

Suggested Citation

  • Kami Pekayvaz & Alexander Leunig & Rainer Kaiser & Markus Joppich & Sophia Brambs & Aleksandar Janjic & Oliver Popp & Daniel Nixdorf & Valeria Fumagalli & Nora Schmidt & Vivien Polewka & Afra Anjum & , 2022. "Protective immune trajectories in early viral containment of non-pneumonic SARS-CoV-2 infection," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28508-0
    DOI: 10.1038/s41467-022-28508-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28508-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28508-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. John W. Schoggins & Sam J. Wilson & Maryline Panis & Mary Y. Murphy & Christopher T. Jones & Paul Bieniasz & Charles M. Rice, 2011. "A diverse range of gene products are effectors of the type I interferon antiviral response," Nature, Nature, vol. 472(7344), pages 481-485, April.
    2. Peng Zhou & Xing-Lou Yang & Xian-Guang Wang & Ben Hu & Lei Zhang & Wei Zhang & Hao-Rui Si & Yan Zhu & Bei Li & Chao-Lin Huang & Hui-Dong Chen & Jing Chen & Yun Luo & Hua Guo & Ren-Di Jiang & Mei-Qin L, 2020. "Addendum: A pneumonia outbreak associated with a new coronavirus of probable bat origin," Nature, Nature, vol. 588(7836), pages 6-6, December.
    3. Peng Zhou & Xing-Lou Yang & Xian-Guang Wang & Ben Hu & Lei Zhang & Wei Zhang & Hao-Rui Si & Yan Zhu & Bei Li & Chao-Lin Huang & Hui-Dong Chen & Jing Chen & Yun Luo & Hua Guo & Ren-Di Jiang & Mei-Qin L, 2020. "A pneumonia outbreak associated with a new coronavirus of probable bat origin," Nature, Nature, vol. 579(7798), pages 270-273, March.
    4. Alexis J. Combes & Tristan Courau & Nicholas F. Kuhn & Kenneth H. Hu & Arja Ray & William S. Chen & Nayvin W. Chew & Simon J. Cleary & Divyashree Kushnoor & Gabriella C. Reeder & Alan Shen & Jessica T, 2021. "Global absence and targeting of protective immune states in severe COVID-19," Nature, Nature, vol. 591(7848), pages 124-130, March.
    5. Shin-ichi Koizumi & Daiki Sasaki & Tsung-Han Hsieh & Naoyuki Taira & Nana Arakaki & Shinichi Yamasaki & Ke Wang & Shukla Sarkar & Hiroki Shirahata & Mio Miyagi & Hiroki Ishikawa, 2018. "JunB regulates homeostasis and suppressive functions of effector regulatory T cells," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    6. Oliver H. Tam & Alexei A. Aravin & Paula Stein & Angelique Girard & Elizabeth P. Murchison & Sihem Cheloufi & Emily Hodges & Martin Anger & Ravi Sachidanandam & Richard M. Schultz & Gregory J. Hannon, 2008. "Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes," Nature, Nature, vol. 453(7194), pages 534-538, May.
    7. Jose Ordovas-Montanes & Daniel F. Dwyer & Sarah K. Nyquist & Kathleen M. Buchheit & Marko Vukovic & Chaarushena Deb & Marc H. Wadsworth & Travis K. Hughes & Samuel W. Kazer & Eri Yoshimoto & Katherine, 2018. "Allergic inflammatory memory in human respiratory epithelial progenitor cells," Nature, Nature, vol. 560(7720), pages 649-654, August.
    8. Alexis J. Combes & Tristan Courau & Nicholas F. Kuhn & Kenneth H. Hu & Arja Ray & William S. Chen & Nayvin W. Chew & Simon J. Cleary & Divyashree Kushnoor & Gabriella C. Reeder & Alan Shen & Jessica T, 2021. "Publisher Correction: Global absence and targeting of protective immune states in severe COVID-19," Nature, Nature, vol. 596(7872), pages 8-8, August.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jun-Yu Si & Yuan-Mei Chen & Ye-Hui Sun & Meng-Xue Gu & Mei-Ling Huang & Lu-Lu Shi & Xiao Yu & Xiao Yang & Qing Xiong & Cheng-Bao Ma & Peng Liu & Zheng-Li Shi & Huan Yan, 2024. "Sarbecovirus RBD indels and specific residues dictating multi-species ACE2 adaptiveness," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. NGO, Hoang Anh & HOANG, Thai Nam, 2020. "A Rolling Optimized Nonlinear Grey Bernoulli Model RONGBM(1,1) and application in predicting total COVID-19 cases," OSF Preprints 6y95m_v1, Center for Open Science.
    3. Graziella Orrù & Ciro Conversano & Eleonora Malloggi & Francesca Francesconi & Rebecca Ciacchini & Angelo Gemignani, 2020. "Neurological Complications of COVID-19 and Possible Neuroinvasion Pathways: A Systematic Review," IJERPH, MDPI, vol. 17(18), pages 1-18, September.
    4. Britton Boras & Rhys M. Jones & Brandon J. Anson & Dan Arenson & Lisa Aschenbrenner & Malina A. Bakowski & Nathan Beutler & Joseph Binder & Emily Chen & Heather Eng & Holly Hammond & Jennifer Hammond , 2021. "Preclinical characterization of an intravenous coronavirus 3CL protease inhibitor for the potential treatment of COVID19," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    5. Susanne Kessler & Bradly Burke & Geoffroy Andrieux & Jan Schinköthe & Lea Hamberger & Johannes Kacza & Shijun Zhan & Clara Reasoner & Taru S. Dutt & Maria Kaukab Osman & Marcela Henao-Tamayo & Julian , 2024. "Deciphering bat influenza H18N11 infection dynamics in male Jamaican fruit bats on a single-cell level," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Yongzhu Xiong & Yunpeng Wang & Feng Chen & Mingyong Zhu, 2020. "Spatial Statistics and Influencing Factors of the COVID-19 Epidemic at Both Prefecture and County Levels in Hubei Province, China," IJERPH, MDPI, vol. 17(11), pages 1-26, May.
    7. Eugene Song & Jae-Eun Lee & Seola Kwon, 2021. "Effect of Public Empathy with Infection-Control Guidelines on Infection-Prevention Attitudes and Behaviors: Based on the Case of COVID-19," IJERPH, MDPI, vol. 18(24), pages 1-18, December.
    8. Jaeyong Lee & Calem Kenward & Liam J. Worrall & Marija Vuckovic & Francesco Gentile & Anh-Tien Ton & Myles Ng & Artem Cherkasov & Natalie C. J. Strynadka & Mark Paetzel, 2022. "X-ray crystallographic characterization of the SARS-CoV-2 main protease polyprotein cleavage sites essential for viral processing and maturation," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    9. Xu, Baochang & Li, Sihui & Afzal, Ayesha & Mirza, Nawazish & Zhang, Meng, 2022. "The impact of financial development on environmental sustainability: A European perspective," Resources Policy, Elsevier, vol. 78(C).
    10. Nur Hannani Bi Rahman & Shazmin Shareena A. Azis & Ibrahim Sipan, 2021. "COVID-19: Standard Operating Procedure Improvement For Green Office Building Using Indoor Environmental Quality," LARES lares-2021-4dqg, Latin American Real Estate Society (LARES).
    11. Eduardo Gutiérrez-Abejón & Eduardo Tamayo & Débora Martín-García & F. Javier Álvarez & Francisco Herrera-Gómez, 2020. "Clinical Profile, Treatment and Predictors during the First COVID-19 Wave: A Population-Based Registry Analysis from Castile and Leon Hospitals," IJERPH, MDPI, vol. 17(24), pages 1-15, December.
    12. Meriem Bekliz & Kenneth Adea & Pauline Vetter & Christiane S. Eberhardt & Krisztina Hosszu-Fellous & Diem-Lan Vu & Olha Puhach & Manel Essaidi-Laziosi & Sophie Waldvogel-Abramowski & Caroline Stephan , 2022. "Neutralization capacity of antibodies elicited through homologous or heterologous infection or vaccination against SARS-CoV-2 VOCs," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    13. Maria de Lourdes Aguiar-Oliveira & Aline Campos & Aline R. Matos & Caroline Rigotto & Adriana Sotero-Martins & Paulo F. P. Teixeira & Marilda M. Siqueira, 2020. "Wastewater-Based Epidemiology (WBE) and Viral Detection in Polluted Surface Water: A Valuable Tool for COVID-19 Surveillance—A Brief Review," IJERPH, MDPI, vol. 17(24), pages 1-19, December.
    14. Daiki Yamaguchi & Odgerel Chimed-Ochir & Yui Yumiya & Eisaku Kishita & Tomoyuki Akita & Junko Tanaka & Tatsuhiko Kubo, 2024. "Potential Risk Factors to COVID-19 Severity: Comparison of SARS-CoV-2 Delta- and Omicron-Dominant Periods," IJERPH, MDPI, vol. 21(3), pages 1-11, March.
    15. Dunbar, Kwamie, 2022. "Impact of the COVID-19 event on U.S. banks’ financial soundness," Research in International Business and Finance, Elsevier, vol. 59(C).
    16. Jian Rong & Achi Haider & Troels E. Jeppesen & Lee Josephson & Steven H. Liang, 2023. "Radiochemistry for positron emission tomography," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    17. Cecilia A. Sánchez & Hongying Li & Kendra L. Phelps & Carlos Zambrana-Torrelio & Lin-Fa Wang & Peng Zhou & Zheng-Li Shi & Kevin J. Olival & Peter Daszak, 2022. "A strategy to assess spillover risk of bat SARS-related coronaviruses in Southeast Asia," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    18. Sarwan Ali & Babatunde Bello & Murray Patterson, 2023. "Solvent Accessibility of Coronaviridae Spike Proteins through the Lens of Information Gain," J, MDPI, vol. 6(2), pages 1-12, April.
    19. Agata Jabłońska-Trypuć & Marcin Makuła & Maria Włodarczyk-Makuła & Elżbieta Wołejko & Urszula Wydro & Lluis Serra-Majem & Józefa Wiater, 2022. "Inanimate Surfaces as a Source of Hospital Infections Caused by Fungi, Bacteria and Viruses with Particular Emphasis on SARS-CoV-2," IJERPH, MDPI, vol. 19(13), pages 1-22, July.
    20. Alice Latinne & Ben Hu & Kevin J. Olival & Guangjian Zhu & Li-Biao Zhang & Hongying Li & Aleksei A. Chmura & Hume E. Field & Carlos Zambrana-Torrelio & Jonathan H. Epstein & Bei Li & Wei Zhang & Lin-F, 2024. "Origin and cross-species transmission of bat coronaviruses in China," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28508-0. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.