Quantitative multiorgan proteomics of fatal COVID‐19 uncovers tissue‐specific effects beyond inflammation

Abstract SARS‐CoV‐2 may directly and indirectly damage lung tissue and other host organs, but there are few system‐wide, untargeted studies of these effects on the human body. Here, we developed a parallelized mass spectrometry (MS) proteomics workflow enabling the rapid, quantitative analysis of hu...

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Main Authors: Lisa Schweizer, Tina Schaller, Maximilian Zwiebel, Özge Karayel, Johannes Bruno Müller‐Reif, Wen‐Feng Zeng, Sebastian Dintner, Thierry M Nordmann, Klaus Hirschbühl, Bruno Märkl, Rainer Claus, Matthias Mann
Format: Article
Language:English
Published: Springer Nature 2023-07-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202317459
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author Lisa Schweizer
Tina Schaller
Maximilian Zwiebel
Özge Karayel
Johannes Bruno Müller‐Reif
Wen‐Feng Zeng
Sebastian Dintner
Thierry M Nordmann
Klaus Hirschbühl
Bruno Märkl
Rainer Claus
Matthias Mann
author_facet Lisa Schweizer
Tina Schaller
Maximilian Zwiebel
Özge Karayel
Johannes Bruno Müller‐Reif
Wen‐Feng Zeng
Sebastian Dintner
Thierry M Nordmann
Klaus Hirschbühl
Bruno Märkl
Rainer Claus
Matthias Mann
author_sort Lisa Schweizer
collection DOAJ
description Abstract SARS‐CoV‐2 may directly and indirectly damage lung tissue and other host organs, but there are few system‐wide, untargeted studies of these effects on the human body. Here, we developed a parallelized mass spectrometry (MS) proteomics workflow enabling the rapid, quantitative analysis of hundreds of virus‐infected FFPE tissues. The first layer of response to SARS‐CoV‐2 in all tissues was dominated by circulating inflammatory molecules. Beyond systemic inflammation, we differentiated between systemic and true tissue‐specific effects to reflect distinct COVID‐19‐associated damage patterns. Proteomic changes in the lungs resembled those of diffuse alveolar damage (DAD) in non‐COVID‐19 patients. Extensive organ‐specific changes were also evident in the kidneys, liver, and lymphatic and vascular systems. Secondary inflammatory effects in the brain were related to rearrangements in neurotransmitter receptors and myelin degradation. These MS‐proteomics‐derived results contribute substantially to our understanding of COVID‐19 pathomechanisms and suggest strategies for organ‐specific therapeutic interventions.
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institution Kabale University
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publishDate 2023-07-01
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spelling doaj-art-901eda2487d34885bb7571aa2ad46f4e2025-08-20T03:46:25ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842023-07-0115912110.15252/emmm.202317459Quantitative multiorgan proteomics of fatal COVID‐19 uncovers tissue‐specific effects beyond inflammationLisa Schweizer0Tina Schaller1Maximilian Zwiebel2Özge Karayel3Johannes Bruno Müller‐Reif4Wen‐Feng Zeng5Sebastian Dintner6Thierry M Nordmann7Klaus Hirschbühl8Bruno Märkl9Rainer Claus10Matthias Mann11Department of Proteomics and Signal Transduction, Max Planck Institute of BiochemistryPathology, Medical Faculty, University of AugsburgDepartment of Proteomics and Signal Transduction, Max Planck Institute of BiochemistryDepartment of Proteomics and Signal Transduction, Max Planck Institute of BiochemistryDepartment of Proteomics and Signal Transduction, Max Planck Institute of BiochemistryDepartment of Proteomics and Signal Transduction, Max Planck Institute of BiochemistryPathology, Medical Faculty, University of AugsburgDepartment of Proteomics and Signal Transduction, Max Planck Institute of BiochemistryHematology and Oncology, Medical Faculty, University of AugsburgPathology, Medical Faculty, University of AugsburgPathology, Medical Faculty, University of AugsburgDepartment of Proteomics and Signal Transduction, Max Planck Institute of BiochemistryAbstract SARS‐CoV‐2 may directly and indirectly damage lung tissue and other host organs, but there are few system‐wide, untargeted studies of these effects on the human body. Here, we developed a parallelized mass spectrometry (MS) proteomics workflow enabling the rapid, quantitative analysis of hundreds of virus‐infected FFPE tissues. The first layer of response to SARS‐CoV‐2 in all tissues was dominated by circulating inflammatory molecules. Beyond systemic inflammation, we differentiated between systemic and true tissue‐specific effects to reflect distinct COVID‐19‐associated damage patterns. Proteomic changes in the lungs resembled those of diffuse alveolar damage (DAD) in non‐COVID‐19 patients. Extensive organ‐specific changes were also evident in the kidneys, liver, and lymphatic and vascular systems. Secondary inflammatory effects in the brain were related to rearrangements in neurotransmitter receptors and myelin degradation. These MS‐proteomics‐derived results contribute substantially to our understanding of COVID‐19 pathomechanisms and suggest strategies for organ‐specific therapeutic interventions.https://doi.org/10.15252/emmm.202317459COVID‐19mass spectrometrypathologyproteomicsvirus
spellingShingle Lisa Schweizer
Tina Schaller
Maximilian Zwiebel
Özge Karayel
Johannes Bruno Müller‐Reif
Wen‐Feng Zeng
Sebastian Dintner
Thierry M Nordmann
Klaus Hirschbühl
Bruno Märkl
Rainer Claus
Matthias Mann
Quantitative multiorgan proteomics of fatal COVID‐19 uncovers tissue‐specific effects beyond inflammation
EMBO Molecular Medicine
COVID‐19
mass spectrometry
pathology
proteomics
virus
title Quantitative multiorgan proteomics of fatal COVID‐19 uncovers tissue‐specific effects beyond inflammation
title_full Quantitative multiorgan proteomics of fatal COVID‐19 uncovers tissue‐specific effects beyond inflammation
title_fullStr Quantitative multiorgan proteomics of fatal COVID‐19 uncovers tissue‐specific effects beyond inflammation
title_full_unstemmed Quantitative multiorgan proteomics of fatal COVID‐19 uncovers tissue‐specific effects beyond inflammation
title_short Quantitative multiorgan proteomics of fatal COVID‐19 uncovers tissue‐specific effects beyond inflammation
title_sort quantitative multiorgan proteomics of fatal covid 19 uncovers tissue specific effects beyond inflammation
topic COVID‐19
mass spectrometry
pathology
proteomics
virus
url https://doi.org/10.15252/emmm.202317459
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