Transcriptomic analysis reveals shared deregulated neutrophil responses in COVID-19 and idiopathic pulmonary fibrosis

Abstract Background Coronavirus disease 2019 (COVID-19) is a respiratory disease linked with deregulated immune responses, leading to hyperinflammation, acute respiratory distress syndrome, and pulmonary fibrosis, often with fatal outcomes. Neutrophils play a central role in COVID-19 pathogenesis, w...

Full description

Saved in:
Bibliographic Details
Main Authors: Georgios Divolis, Evgenia Synolaki, Rodoula Tringidou, Argyrios Tzouvelekis, Dimitrios T. Boumpas, Panagiotis Skendros, Ioanna-Evdokia Galani
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Respiratory Research
Subjects:
Online Access:https://doi.org/10.1186/s12931-025-03180-2
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849691388150546432
author Georgios Divolis
Evgenia Synolaki
Rodoula Tringidou
Argyrios Tzouvelekis
Dimitrios T. Boumpas
Panagiotis Skendros
Ioanna-Evdokia Galani
author_facet Georgios Divolis
Evgenia Synolaki
Rodoula Tringidou
Argyrios Tzouvelekis
Dimitrios T. Boumpas
Panagiotis Skendros
Ioanna-Evdokia Galani
author_sort Georgios Divolis
collection DOAJ
description Abstract Background Coronavirus disease 2019 (COVID-19) is a respiratory disease linked with deregulated immune responses, leading to hyperinflammation, acute respiratory distress syndrome, and pulmonary fibrosis, often with fatal outcomes. Neutrophils play a central role in COVID-19 pathogenesis, with elevated peripheral blood neutrophil counts correlating with disease severity. Despite extensive research, the molecular processes associated with neutrophil hyperactivation in COVID-19 remain elusive. Methods To investigate the molecular signatures underlying neutrophil-driven pathology, we conducted transcriptome analysis in neutrophils isolated from the peripheral blood of COVID-19 patients versus healthy individuals. To evaluate the specificity of identified neutrophil signatures in COVID-19, we extended our transcriptomic analysis to neutrophils from patients with idiopathic pulmonary fibrosis (IPF), a non-infectious fibrotic lung disease. Additionally, immunofluorescence staining was performed on lung biopsy specimens from IPF patients to validate transcriptomic findings at the tissue level. Results Our analysis revealed significant transcriptional changes in COVID-19 neutrophils, particularly in pathways involved in immune regulation, inflammation, and antiviral responses. Additionally, pathways associated with autophagy and chromatin remodeling were upregulated, while translation-related processes were suppressed, indicating an increased predisposition for neutrophil extracellular trap (NET) release. This neutrophil transcriptional signature in COVID-19 appears to be associated with the previously reported deregulation of the Activin/Follistatin system in the periphery. Notably, a comparative transcriptomic analysis with neutrophils isolated from IPF patients revealed the induction of substantially overlapping inflammatory processes, suggesting common deregulated responses in COVID-19 and IPF. Consistently, significant NET formation, a hallmark of COVID-19-related inflammation, was observed within lung biopsies from IPF patients. Conclusion By delineating both shared and disease-specific molecular pathways, our findings validate the critical role of neutrophils in COVID-19 and IPF pathophysiology, highlighting their involvement in balancing the inflammatory response across diverse lung diseases.
format Article
id doaj-art-585c8ffaa7b446df9c59382ae07fee5e
institution DOAJ
issn 1465-993X
language English
publishDate 2025-06-01
publisher BMC
record_format Article
series Respiratory Research
spelling doaj-art-585c8ffaa7b446df9c59382ae07fee5e2025-08-20T03:21:02ZengBMCRespiratory Research1465-993X2025-06-0126111810.1186/s12931-025-03180-2Transcriptomic analysis reveals shared deregulated neutrophil responses in COVID-19 and idiopathic pulmonary fibrosisGeorgios Divolis0Evgenia Synolaki1Rodoula Tringidou2Argyrios Tzouvelekis3Dimitrios T. Boumpas4Panagiotis Skendros5Ioanna-Evdokia Galani6Center for Clinical, Experimental Surgery and Translational Research, Biomedical Research Foundation Academy of Athens (BRFAA)Center for Clinical, Experimental Surgery and Translational Research, Biomedical Research Foundation Academy of Athens (BRFAA)Department of Pathology, ‘Sotiria’ General Hospital of Chest DiseasesDivision of Respiratory Medicine, Medical School, University of PatrasCenter for Clinical, Experimental Surgery and Translational Research, Biomedical Research Foundation Academy of Athens (BRFAA)Laboratory of Molecular Hematology, Department of Medicine, Democritus University of ThraceCenter for Basic Research, BRFAAAbstract Background Coronavirus disease 2019 (COVID-19) is a respiratory disease linked with deregulated immune responses, leading to hyperinflammation, acute respiratory distress syndrome, and pulmonary fibrosis, often with fatal outcomes. Neutrophils play a central role in COVID-19 pathogenesis, with elevated peripheral blood neutrophil counts correlating with disease severity. Despite extensive research, the molecular processes associated with neutrophil hyperactivation in COVID-19 remain elusive. Methods To investigate the molecular signatures underlying neutrophil-driven pathology, we conducted transcriptome analysis in neutrophils isolated from the peripheral blood of COVID-19 patients versus healthy individuals. To evaluate the specificity of identified neutrophil signatures in COVID-19, we extended our transcriptomic analysis to neutrophils from patients with idiopathic pulmonary fibrosis (IPF), a non-infectious fibrotic lung disease. Additionally, immunofluorescence staining was performed on lung biopsy specimens from IPF patients to validate transcriptomic findings at the tissue level. Results Our analysis revealed significant transcriptional changes in COVID-19 neutrophils, particularly in pathways involved in immune regulation, inflammation, and antiviral responses. Additionally, pathways associated with autophagy and chromatin remodeling were upregulated, while translation-related processes were suppressed, indicating an increased predisposition for neutrophil extracellular trap (NET) release. This neutrophil transcriptional signature in COVID-19 appears to be associated with the previously reported deregulation of the Activin/Follistatin system in the periphery. Notably, a comparative transcriptomic analysis with neutrophils isolated from IPF patients revealed the induction of substantially overlapping inflammatory processes, suggesting common deregulated responses in COVID-19 and IPF. Consistently, significant NET formation, a hallmark of COVID-19-related inflammation, was observed within lung biopsies from IPF patients. Conclusion By delineating both shared and disease-specific molecular pathways, our findings validate the critical role of neutrophils in COVID-19 and IPF pathophysiology, highlighting their involvement in balancing the inflammatory response across diverse lung diseases.https://doi.org/10.1186/s12931-025-03180-2NeutrophilsCOVID-19Viral infectionIdiopathic pulmonary fibrosisNETosisRNA Sequencing
spellingShingle Georgios Divolis
Evgenia Synolaki
Rodoula Tringidou
Argyrios Tzouvelekis
Dimitrios T. Boumpas
Panagiotis Skendros
Ioanna-Evdokia Galani
Transcriptomic analysis reveals shared deregulated neutrophil responses in COVID-19 and idiopathic pulmonary fibrosis
Respiratory Research
Neutrophils
COVID-19
Viral infection
Idiopathic pulmonary fibrosis
NETosis
RNA Sequencing
title Transcriptomic analysis reveals shared deregulated neutrophil responses in COVID-19 and idiopathic pulmonary fibrosis
title_full Transcriptomic analysis reveals shared deregulated neutrophil responses in COVID-19 and idiopathic pulmonary fibrosis
title_fullStr Transcriptomic analysis reveals shared deregulated neutrophil responses in COVID-19 and idiopathic pulmonary fibrosis
title_full_unstemmed Transcriptomic analysis reveals shared deregulated neutrophil responses in COVID-19 and idiopathic pulmonary fibrosis
title_short Transcriptomic analysis reveals shared deregulated neutrophil responses in COVID-19 and idiopathic pulmonary fibrosis
title_sort transcriptomic analysis reveals shared deregulated neutrophil responses in covid 19 and idiopathic pulmonary fibrosis
topic Neutrophils
COVID-19
Viral infection
Idiopathic pulmonary fibrosis
NETosis
RNA Sequencing
url https://doi.org/10.1186/s12931-025-03180-2
work_keys_str_mv AT georgiosdivolis transcriptomicanalysisrevealssharedderegulatedneutrophilresponsesincovid19andidiopathicpulmonaryfibrosis
AT evgeniasynolaki transcriptomicanalysisrevealssharedderegulatedneutrophilresponsesincovid19andidiopathicpulmonaryfibrosis
AT rodoulatringidou transcriptomicanalysisrevealssharedderegulatedneutrophilresponsesincovid19andidiopathicpulmonaryfibrosis
AT argyriostzouvelekis transcriptomicanalysisrevealssharedderegulatedneutrophilresponsesincovid19andidiopathicpulmonaryfibrosis
AT dimitriostboumpas transcriptomicanalysisrevealssharedderegulatedneutrophilresponsesincovid19andidiopathicpulmonaryfibrosis
AT panagiotisskendros transcriptomicanalysisrevealssharedderegulatedneutrophilresponsesincovid19andidiopathicpulmonaryfibrosis
AT ioannaevdokiagalani transcriptomicanalysisrevealssharedderegulatedneutrophilresponsesincovid19andidiopathicpulmonaryfibrosis