Systemic cytokines drive conserved severity-associated myeloid responses across bacterial and viral infections

Abstract Both bacterial and viral infections can trigger an overwhelming host response, leading to immunopathology and organ dysfunction. Multiple studies have reported dysregulated myeloid cell states in patients with bacterial sepsis or severe SARS-CoV-2 infection. However, their relevance to vira...

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Main Authors: Kimberly Kajihara, Donghong Yan, Gretchen L. Seim, Hannah Little-Hooy, Jing Kang, Cynthia Chen, Marco De Simone, Tim Delemarre, Spyros Darmanis, Haridha Shivram, Rebecca N. Bauer, Carrie M. Rosenberger, Sharookh B. Kapadia, Min Xu, Miguel Reyes
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-08407-y
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author Kimberly Kajihara
Donghong Yan
Gretchen L. Seim
Hannah Little-Hooy
Jing Kang
Cynthia Chen
Marco De Simone
Tim Delemarre
Spyros Darmanis
Haridha Shivram
Rebecca N. Bauer
Carrie M. Rosenberger
Sharookh B. Kapadia
Min Xu
Miguel Reyes
author_facet Kimberly Kajihara
Donghong Yan
Gretchen L. Seim
Hannah Little-Hooy
Jing Kang
Cynthia Chen
Marco De Simone
Tim Delemarre
Spyros Darmanis
Haridha Shivram
Rebecca N. Bauer
Carrie M. Rosenberger
Sharookh B. Kapadia
Min Xu
Miguel Reyes
author_sort Kimberly Kajihara
collection DOAJ
description Abstract Both bacterial and viral infections can trigger an overwhelming host response, leading to immunopathology and organ dysfunction. Multiple studies have reported dysregulated myeloid cell states in patients with bacterial sepsis or severe SARS-CoV-2 infection. However, their relevance to viral infections other than COVID-19, the factors driving their induction, and their role in tissue injury remain poorly understood. Here, we performed a multi-cohort analysis of single cell and bulk transcriptomic data from 1845 patients across 25 studies. Our meta-analysis revealed a conserved severity-associated gene signature pointing to emergency myelopoiesis (EM) and increased IL1R2 expression in monocytes and neutrophils from patients with bacterial sepsis, COVID-19, and influenza. Analysis of tocilizumab-treated COVID-19 patients showed that IL-6 signaling blockade partially reduces this signature and results in a compensatory increase in G-CSF. To validate the role of these cytokines in vivo, we used a mouse model of influenza infection that recapitulates severity-associated increases in IL1R2+ monocytes and IL1R2hi neutrophils, and demonstrate that combined IL-6 and G-CSF blockade inhibits their production. Our study demonstrates the cooperative role of G-CSF and IL-6 in driving the production of severity-associated IL1R2+ myeloid cells and highlights the link between myeloid dysregulation and tissue injury during severe infection.
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spelling doaj-art-ec4a89f83ba54c4facfd2faf7d023fd92025-08-20T04:02:55ZengNature PortfolioCommunications Biology2399-36422025-07-018111110.1038/s42003-025-08407-ySystemic cytokines drive conserved severity-associated myeloid responses across bacterial and viral infectionsKimberly Kajihara0Donghong Yan1Gretchen L. Seim2Hannah Little-Hooy3Jing Kang4Cynthia Chen5Marco De Simone6Tim Delemarre7Spyros Darmanis8Haridha Shivram9Rebecca N. Bauer10Carrie M. Rosenberger11Sharookh B. Kapadia12Min Xu13Miguel Reyes14Department of Infectious Diseases, GenentechDepartment of Translational Immunology, GenentechDepartment of Infectious Diseases, GenentechDepartment of Translational Immunology, GenentechDepartment of Translational Immunology, GenentechDepartment of Microchemistry, Proteomics, Lipidomics and Next-Generation Sequencing, GenentechDepartment of Microchemistry, Proteomics, Lipidomics and Next-Generation Sequencing, GenentechDepartment of Immunology and Regenerative Medicine, GenentechDepartment of Microchemistry, Proteomics, Lipidomics and Next-Generation Sequencing, GenentechDepartment of Translational Medicine, GenentechDepartment of Translational Medicine, GenentechDepartment of Immunology and Regenerative Medicine, GenentechDepartment of Infectious Diseases, GenentechDepartment of Translational Immunology, GenentechDepartment of Infectious Diseases, GenentechAbstract Both bacterial and viral infections can trigger an overwhelming host response, leading to immunopathology and organ dysfunction. Multiple studies have reported dysregulated myeloid cell states in patients with bacterial sepsis or severe SARS-CoV-2 infection. However, their relevance to viral infections other than COVID-19, the factors driving their induction, and their role in tissue injury remain poorly understood. Here, we performed a multi-cohort analysis of single cell and bulk transcriptomic data from 1845 patients across 25 studies. Our meta-analysis revealed a conserved severity-associated gene signature pointing to emergency myelopoiesis (EM) and increased IL1R2 expression in monocytes and neutrophils from patients with bacterial sepsis, COVID-19, and influenza. Analysis of tocilizumab-treated COVID-19 patients showed that IL-6 signaling blockade partially reduces this signature and results in a compensatory increase in G-CSF. To validate the role of these cytokines in vivo, we used a mouse model of influenza infection that recapitulates severity-associated increases in IL1R2+ monocytes and IL1R2hi neutrophils, and demonstrate that combined IL-6 and G-CSF blockade inhibits their production. Our study demonstrates the cooperative role of G-CSF and IL-6 in driving the production of severity-associated IL1R2+ myeloid cells and highlights the link between myeloid dysregulation and tissue injury during severe infection.https://doi.org/10.1038/s42003-025-08407-y
spellingShingle Kimberly Kajihara
Donghong Yan
Gretchen L. Seim
Hannah Little-Hooy
Jing Kang
Cynthia Chen
Marco De Simone
Tim Delemarre
Spyros Darmanis
Haridha Shivram
Rebecca N. Bauer
Carrie M. Rosenberger
Sharookh B. Kapadia
Min Xu
Miguel Reyes
Systemic cytokines drive conserved severity-associated myeloid responses across bacterial and viral infections
Communications Biology
title Systemic cytokines drive conserved severity-associated myeloid responses across bacterial and viral infections
title_full Systemic cytokines drive conserved severity-associated myeloid responses across bacterial and viral infections
title_fullStr Systemic cytokines drive conserved severity-associated myeloid responses across bacterial and viral infections
title_full_unstemmed Systemic cytokines drive conserved severity-associated myeloid responses across bacterial and viral infections
title_short Systemic cytokines drive conserved severity-associated myeloid responses across bacterial and viral infections
title_sort systemic cytokines drive conserved severity associated myeloid responses across bacterial and viral infections
url https://doi.org/10.1038/s42003-025-08407-y
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