ArticleCell2023
Epigenetic memory of coronavirus infection in innate immune cells and their progenitors.
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Article in Cell, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 188 papers, 1 of them a synthesis that pooled it.
0numbers the graph read from it
0cells of the map it votes in
188citing papers in PubMed, 1 pooled it
41.6field-weighted citation impact, top 1% of its field
What it found
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The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.
The trial behind it
Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.
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Who cites it
188 citing papers in PubMed, 1 synthesis or guideline pooled it, 253 citations in OpenAlex.
- Mucosal immune response in biology, disease prevention and treatment.Signal transduction and targeted therapy · 2025Pooled it
- Meplazumab, a CD147 antibody, for severe COVID-19: a double-blind, randomized, placebo-controlled, phase 3 clinical trial.Signal transduction and targeted therapy · 2025Trial
- Mitochondria-Derived Vesicles and Inflammatory Profiles of Adults with Long COVID Supplemented with Red Beetroot Juice: Secondary Analysis of a Randomized Controlled Trial.International journal of molecular sciences · 2025Trial
- Circulating hematopoietic stem/progenitor cell subsets contribute to human hematopoietic homeostasis.Blood · 2024Trial
- Review
- Monocytes in pneumonia: Functional plasticity and innate memory (Review).International journal of molecular medicine · 2026Review
- NS1-Induced PARP1 Phase Transitions Prolongs Host Transcriptional Pausing to Promote Influenza A Virus Replication.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2026Article
- Targeting BIRC6 rejuvenates hematopoietic stem cell aging and immunosenescence.Signal transduction and targeted therapy · 2026Article
- Drugging trained immunity: immunometabolic and epigenetic control of maladaptive inflammatory memory in chronic inflammatory diseases.Immunologic research · 2026Review
- Trained immunity: New insights into pathogenesis and therapeutic targets in diabetes and diabetic complications.Genes & diseases · 2026Review
- Trained immunity links hematopoietic stem cell aging to aging-associated inflammation.Nature aging · 2026Article
- Innate Immune Memory Responses in Organ Transplantation.Arteriosclerosis, thrombosis, and vascular biology · 2026Review
- A multicenter retrospective study on severe complications of acute otitis media and sinusitis in healthy children in the context of covid pandemic - CAOS-kids.Scientific reports · 2026Article
- Glucagon-like peptide-1 receptor agonist prevents pulmonary fibrosis following acute COVID-19 infection associated with type 2 diabetes.Journal of virology · 2026Article
- Metabolic-epigenetic crosstalk in innate immune cell plasticity within the tumor microenvironment.Experimental & molecular medicine · 2026Review
- Innate Immune Reprogramming Mediated by Endogenous Retroelement Dysregulation Drives Multiple Sclerosis Progression.Annals of clinical and translational neurology · 2026Article
- Review
- Article
- Brain endothelial cells orchestrate a neuroprotective antiviral state in the CNS in response to peripheral viral pattern sensing.Immunity · 2026Article
- Dysregulated myelopoiesis and enhanced glutaminase-dependent neutrophil survival in preclinical obesity.ImmunoHorizons · 2026Article
128 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
55 authors at 10 institutions in 4 countries.
Jin-Gyu CheongDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Immunology and Microbial Pathogenesis Program, Weill Cornell Medicine, New York, NY 10065, USA.
Arjun RavishankarDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Siddhartha SharmaThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
Christopher N ParkhurstDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Simon A GrassmannImmunology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Claire K WingertImmunology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Paoline LaurentHSS Research Institute, Hospital for Special Surgery, New York, NY 10021, USA.
Sai MaGene Regulation Observatory, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02142, USA.
Lucinda PaddockDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Isabella C MirandaDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Emin Onur KarakaslarThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA; Leiden University Medical Center (LUMC), Leiden, The Netherlands.
Djamel Nehar-BelaidThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
Asa ThibodeauThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
Michael J BaleDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Immunology and Microbial Pathogenesis Program, Weill Cornell Medicine, New York, NY 10065, USA.
Vinay K KarthaGene Regulation Observatory, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02142, USA.
Jim K YeeDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Minh Y MaysDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Chenyang JiangDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Andrew W DamanDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Immunology and Microbial Pathogenesis Program, Weill Cornell Medicine, New York, NY 10065, USA.
Alexia Martinez de PazDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Dughan AhimovicDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Immunology and Microbial Pathogenesis Program, Weill Cornell Medicine, New York, NY 10065, USA.
Victor RamosThe Rockefeller University, New York, NY 10065, USA.
Alexander LercherThe Rockefeller University, New York, NY 10065, USA.
Erik NielsenDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Department of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Sergio Alvarez-MulettDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Ling ZhengDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Andrew EarlGene Regulation Observatory, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02142, USA.
Alisha YallowitzDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Lexi RobbinsDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Elyse LaFondNYU Langone Health, New York, NY 10016, USA.
Karissa L WeidmanDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Sabrina Racine-BrzostekDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
He S YangDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
David R PriceDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Louise LeyreImmunology and Microbial Pathogenesis Program, Weill Cornell Medicine, New York, NY 10065, USA.
André F RendeiroInstitute for Computational Biomedicine, Weill Cornell Medicine, New York, NY 10065, USA; Caryl and Israel Englander Institute for Precision Medicine, Weill Cornell Medicine, New York, NY 10065, USA; CeMM Research Center for Molecular Medicine, Austrian Academy of Sciences, 1090 Vienna, Austria.
Hiranmayi RavichandranCaryl and Israel Englander Institute for Precision Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY 10065, USA.
Junbum KimInstitute for Computational Biomedicine, Weill Cornell Medicine, New York, NY 10065, USA.
Alain C BorczukDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Department of Pathology and Laboratory Medicine, Northwell Health, Greenvale, NY 11548, USA.
Charles M RiceThe Rockefeller University, New York, NY 10065, USA.
R Brad JonesDepartment of Medicine, Division of Infectious Diseases, Weill Cornell Medicine, New York, NY 10065, USA; Department of Microbiology and Immunology, Weill Cornell Medicine, New York, NY 10065, USA.
Edward J SchenckDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Robert J KanerDepartment of Genetic Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Amy ChadburnDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Zhen ZhaoDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Virginia PascualDepartment of Pediatrics, Gale and Ira Drukier Institute for Children's Health, Weill Cornell Medicine, New York, NY 10065, USA.
Olivier ElementoInstitute for Computational Biomedicine, Weill Cornell Medicine, New York, NY 10065, USA; Caryl and Israel Englander Institute for Precision Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Robert E SchwartzDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Jason D BuenrostroGene Regulation Observatory, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02142, USA.
Rachel E NiecDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA; The Rockefeller University, New York, NY 10065, USA.
Franck J BarratImmunology and Microbial Pathogenesis Program, Weill Cornell Medicine, New York, NY 10065, USA; HSS Research Institute, Hospital for Special Surgery, New York, NY 10021, USA; Department of Microbiology and Immunology, Weill Cornell Medicine, New York, NY 10065, USA.
Lindsay LiefDepartment of Medicine, Weill Cornell Medicine, New York, NY 10065, USA.
Joseph C SunImmunology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Duygu UcarThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA; Institute for Systems Genomics, University of Connecticut Health Center, Farmington, CT, USA. Electronic address: duygu.ucar@jax.org.
Steven Z JosefowiczDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY 10065, USA; Immunology and Microbial Pathogenesis Program, Weill Cornell Medicine, New York, NY 10065, USA. Electronic address: szj2001@med.cornell.edu.
Cornell University · USBroad Institute · USJackson Laboratory · USMemorial Sloan Kettering Cancer Center · USRockefeller University · USHospital for Special Surgery · USAustrian Academy of Sciences · ATLeiden University Medical Center · NLNorthwell Health · USNYU Langone Health · US
Funding
X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI SELWYN M VICKERS · 1985 to 2026
$347.4MClinical and Translational Science AwardUL1TR001873 · NCATS · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI REILLY, MUREDACH P · 2016 to 2025
$99.0MDisparities in COVID Disease Severity and Outcomes in New York CityUL1TR002384 · NCATS · WEILL MEDICAL COLL OF CORNELL UNIV · PI JULIANNE L IMPERATO-MCGINLEY · 2017 to 2026
$86.2MStructure, Function, and Dynamics of Macro-molecular Complexes that Execute and Regulate Genome FunctionRM1GM139738 · NIGMS · CORNELL UNIVERSITY · PI Thomas George Wade Graham, Steven Zvi Josefowicz · 2021 to 2026
$14.4MPrincipal ProjectU19AI144301 · NIAID · WEILL MEDICAL COLL OF CORNELL UNIV · PI DAVID CHARLES LYDEN · 2019 to 2026
$9.9MHistone Variant H3.3 as a Transcription Rheostat in the Immune SystemR01AI148416 · NIAID · WEILL MEDICAL COLL OF CORNELL UNIV · PI Steven Zvi Josefowicz · 2020 to 2026
$4.6MTracking SARS-CoV-2 one molecule at a time: Spatiotemporal investigation of coronavirus replication dynamics and host response in single cells in vitro and in vivoR01AI161444 · NIAID · ROCKEFELLER UNIVERSITY · PI Charles M Rice · 2022 to 2026
$3.1MHigh-resolution single cell profiling of vaccine responsiveness in the elderlyR01AI142086 · NIAID · JACKSON LABORATORY · PI UCAR, DUYGU · 2019 to 2023
$2.9MOptimization of the engineered 3D hepatic microenvironment enhances pluripotent stem cell derived hepatocyteR01DK121072 · NIDDK · WEILL MEDICAL COLL OF CORNELL UNIV · PI SCHWARTZ, ROBERT E · 2020 to 2024
$2.6MRole of plasmacytoid dendritic cells in autoimmunityR01AI132447 · NIAID · HOSPITAL FOR SPECIAL SURGERY · PI BARRAT, FRANCK · 2018 to 2022
$2.2MMSK Computational Biology Summer ProgramR25CA233208 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI Michael F. Berger, Yaihara Myriam Fortis-Santiago · 2019 to 2026
$1.8MMicrobial Regulation of Microglial FunctionK08MH130773 · NIMH · WEILL MEDICAL COLL OF CORNELL UNIV · PI PARKHURST, CHRISTOPHER NEAL · 2022 to 2025
$782kNCATS NIH HHS UL1 TR001873NCATS NIH HHS UL1 TR002384NCI NIH HHS P30 CA008748NCI NIH HHS R25 CA233208NIAID NIH HHS R01 AI132447NIAID NIH HHS R01 AI142086NIAID NIH HHS R01 AI148416NIAID NIH HHS R01 AI161444NIAID NIH HHS U19 AI144301NIDDK NIH HHS R01 DK121072NIGMS NIH HHS RM1 GM139738NIMH NIH HHS K08 MH130773
Abstract
Inflammation can trigger lasting phenotypes in immune and non-immune cells. Whether and how human infections and associated inflammation can form innate immune memory in hematopoietic stem and progenitor cells (HSPC) has remained unclear. We found that circulating HSPC, enriched from peripheral blood, captured the diversity of bone marrow HSPC, enabling investigation of their epigenomic reprogramming following coronavirus disease 2019 (COVID-19). Alterations in innate immune phenotypes and epigenetic programs of HSPC persisted for months to 1 year following severe COVID-19 and were associated with distinct transcription factor (TF) activities, altered regulation of inflammatory programs, and durable increases in myelopoiesis. HSPC epigenomic alterations were conveyed, through differentiation, to progeny innate immune cells. Early activity of IL-6 contributed to these persistent phenotypes in human COVID-19 and a mouse coronavirus infection model. Epigenetic reprogramming of HSPC may underlie altered immune function following infection and be broadly relevant, especially for millions of COVID-19 survivors.
Indexed as
COVID-19Epigenetic MemoryPost-Acute COVID-19 SyndromeAnimalsCell DifferentiationDisease Models, AnimalHematopoietic Stem CellsHumansInflammationMiceMonocytesTrained ImmunityCOVID-19epigenetic memoryepigenomehematopoietic stem and progenitor cellsIL-6monocytesPASCperipheral blood mononuclear cell progenitor input enrichmentpost-acute sequelae SARS-CoV-2 infectionsingle-celltrained immunitytranscriptome
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