ArticleNature cancer2024
Unique structural configuration of EV-DNA primes Kupffer cell-mediated antitumor immunity to prevent metastatic progression.
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Article in Nature cancer, 2024. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 25 papers.
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25citing papers in PubMed
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Who cites it
25 citing papers in PubMed.
- Metastasis enables immunogenicity through migrasome-mediated antigen release.Nature immunology · 2026Article
- Extracellular vesicles shape tumourigenesis: from signalling networks to systemic progression.Cancer metastasis reviews · 2026Review
- Extracellular vesicle proteins monitor and interfere with CLDN18.2-targeted CAR-T cell and antibody therapies against gastrointestinal cancers.Nature communications · 2026Article
- Advancing the applications of liquid biopsies in oncology.Nature reviews. Genetics · 2026Review
- Single-cell multiomics reveals exosome-mediated reprogramming and clonotypic remodeling of T cells in triple-negative breast cancer.Signal transduction and targeted therapy · 2026Article
- Kupffer cells in liver homeostasis and disease: from immune sentinels to metabolic gatekeepers.Nature reviews. Immunology · 2026Review
- Extracellular vesicles in solid tumors: from tumor ecology to engineered therapeutics.Molecular cancer · 2026Review
- Emerging biomodels to understand the pathophysiology of sepsis and evaluate new therapeutic strategies targeting extracellular histones.Materials today. Bio · 2026Review
- Extracellular Vesicles in the Biology and Liquid Biopsy Diagnostics of Pediatric High-Grade Glioma - Emerging Findings and Opportunities.Journal of extracellular biology · 2026Review
- Activated T cell extracellular vesicle DNA transfer enhances antigen presentation and anti-tumor immunity.Cancer cell · 2026Article
- Systemic Propagation of STING Signalling via Generation of Large Extracellular Vesicles.Journal of extracellular vesicles · 2026Article
- Glioblastoma Cells Expressing Oncogenic EGFR Release Multiple Extracellular Vesicle Subpopulations Positive or Negative for EGFR.Journal of extracellular biology · 2026Article
- Proteomic Profiling of Human Extracellular Vesicles Reveals Diagnostic Biomarkers for Colon Adenocarcinoma.Journal of extracellular vesicles · 2026Article
- Circulating Tumour DNA and Extracellular Vesicle-Associated DNA as Biomarkers for Cancer Detection: A Systematic Review and Meta-Analysis.Journal of extracellular biology · 2026Article
- Mechanisms of tumor-derived extracellular vesicle-mediated immunometabolic reprogramming and immunotherapeutic resistance.Molecular cancer · 2026Review
- 80 years of extracellular vesicles: from discovery to clinical translation.Extracellular vesicles and circulating nucleic acids · 2026Review
- Navigating the Tumor Microenvironment in Colorectal Liver Metastasis: Barriers to Therapy and Emerging Opportunities.Oncology research · 2026Review
- Clinical relevance of extracellular vesicles in cancer - therapeutic and diagnostic potential.Nature reviews. Clinical oncology · 2025Review
- Tertiary lymphoid structures in cancer: spatiotemporal heterogeneity, immune orchestration, and translational opportunities.Journal of hematology & oncology · 2025Review
- Liver metastasis of colorectal cancer: Mechanism and clinical therapy (Review).Oncology reports · 2025Review
Corrections and comments
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Authors and funding
39 authors.
Inbal WortzelChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0003-4321-1230
Yura Seo *Yonsei Cancer Center, Division of Medical Oncology, Department of Internal Medicine, Graduate School of Medical Science, Brain Korea 21 FOUR Project, Yonsei University College of Medicine, Seoul, Republic of Korea.ORCID http://orcid.org/0009-0004-8830-0442
Ife Akano *Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Lee ShaashuaChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0002-6240-1649
Gabriel Cardial TobiasChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0001-9488-2566
Jakob HebertChemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID http://orcid.org/0000-0003-2243-1445
Kyung-A KimYonsei Cancer Center, Division of Medical Oncology, Department of Internal Medicine, Graduate School of Medical Science, Brain Korea 21 FOUR Project, Yonsei University College of Medicine, Seoul, Republic of Korea.
DooA KimYonsei Cancer Center, Division of Medical Oncology, Department of Internal Medicine, Graduate School of Medical Science, Brain Korea 21 FOUR Project, Yonsei University College of Medicine, Seoul, Republic of Korea.ORCID http://orcid.org/0009-0009-3843-1344
Shani DrorChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0002-9909-8110
Yanshen LiuChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0009-0001-0586-9667
Griffin Campbell AzrakChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0009-0003-3633-2904
Michele CioffiChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0003-4180-5369
Kofi Ennu JohnsonChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.
Tammy HennikaChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0001-9264-6498
Meshulam Zisha TwerskiChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.
Alexis KushnerChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0009-0006-0719-3425
Robert MathChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0009-0004-5443-7520
Yoon Dae HanDepartment of Surgery, Yonsei University College of Medicine, Seoul, Republic of Korea.
Dai Hoon HanDepartment of Surgery, Yonsei University College of Medicine, Seoul, Republic of Korea.ORCID http://orcid.org/0000-0003-2787-7876
Minsun JungDepartment of Pathology, Yonsei University College of Medicine, Seoul, Republic of Korea.ORCID http://orcid.org/0000-0002-8701-4282
Juyeong ParkYonsei Cancer Center, Division of Medical Oncology, Department of Internal Medicine, Graduate School of Medical Science, Brain Korea 21 FOUR Project, Yonsei University College of Medicine, Seoul, Republic of Korea.
Soonmyung PaikYonsei Cancer Center, Division of Medical Oncology, Department of Internal Medicine, Graduate School of Medical Science, Brain Korea 21 FOUR Project, Yonsei University College of Medicine, Seoul, Republic of Korea.ORCID http://orcid.org/0000-0001-9688-6480
Jeon-Soo ShinDepartment of Microbiology, Brain Korea 21 FOUR Project for Medical Science, Yonsei University College of Medicine, Seoul, Republic of Korea.ORCID http://orcid.org/0000-0002-8294-3234
Min Goo LeeDepartment of Pharmacology, Yonsei University College of Medicine, Seoul, Republic of Korea.ORCID http://orcid.org/0000-0001-7436-012X
Marco Vincenzo RussoGene Editing and Screening Core Facility, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID http://orcid.org/0000-0002-5148-1305
Daniel ZakheimGene Editing and Screening Core Facility, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Jesse BarnesGene Editing and Screening Core Facility, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID http://orcid.org/0009-0007-1066-5961
Sunjoy MehtaGene Editing and Screening Core Facility, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Katia ManovaChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.
Robert E SchwartzDivision of Gastroenterology and Hepatology, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0002-5417-5995
Basant Kumar ThakurDepartment of Pediatrics III, University Hospital Essen, Essen, Germany.ORCID http://orcid.org/0000-0001-7013-7895
Nancy BoudreauChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.
Irina MateiChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0002-5712-8430
Haiying ZhangChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0002-7158-2373
Simone SidoliDepartment of Biochemistry, Albert Einstein College of Medicine, New York, NY, USA.ORCID http://orcid.org/0000-0001-9073-6641
Jacqueline BrombergDepartment of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA. bromberj@mskcc.org.ORCID http://orcid.org/0000-0002-7957-9339
Yael DavidChemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA. davidshy@mskcc.org.ORCID http://orcid.org/0000-0003-1696-0025
Han Sang KimChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA. modeerfhs@yuhs.ac.ORCID http://orcid.org/0000-0002-6504-9927
David LydenChildren's Cancer and Blood Foundation Laboratories, Departments of Pediatrics, and Cell and Developmental Biology, Drukier Institute for Children's Health, Meyer Cancer Center, Weill Cornell Medicine, New York, NY, USA. dcl2001@med.cornell.edu.ORCID http://orcid.org/0000-0003-0193-4131
Funding
X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI Hongbiao Carl Lekaye · 1985 to 2026
$347.4MPancreatic Cancer Detection ConsortiumU01CA210240 · NCI · UNIVERSITY OF NEBRASKA MEDICAL CENTER · PI Michael A. Hollingsworth · 2017 to 2026
$12.9MTranslating Stress Response Targeted Therapy for B-Cell LymphomasP50CA192937 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI DALLA-FAVERA, RICCARDO, ZELENETZ, ANDREW D. · 2016 to 2020
$10.9MSystemic regulation of metastasisR35CA232093 · NCI · WEILL MEDICAL COLL OF CORNELL UNIV · PI LYDEN, DAVID CHARLES · 2018 to 2024
$7.0MTumor-derived extracellular vesicles in the pre-metastatic niche.R01CA207983 · NCI · CHILDREN'S HOSPITAL OF LOS ANGELES · PI Yves A DeClerck · 2017 to 2026
$5.6MDevelopment and application of asymmetric-flow field-flow (AF4) technology in fractionation and characterization of exosome subpopulations and novel nanoveiscles in pancreatic cancer modelR01CA218513 · NCI · WEILL MEDICAL COLL OF CORNELL UNIV · PI Jacob Geri, DAVID CHARLES LYDEN · 2017 to 2026
$4.3MDefining neoantigen immunodominance for antigen selection and biomarker discovery in human pancreatic cancer immunotherapyU01CA224175 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI BALACHANDRAN, VINOD P, LEACH, STEVEN D · 2017 to 2021
$3.1MCharacterization and Functional Analysis of Breast Cancer Secreted Exosomes in MaU01CA169538 · NCI · WEILL MEDICAL COLL OF CORNELL UNIV · PI BISSELL, MINA, LYDEN, DAVID CHARLES · 2012 to 2016
$2.9MInvestigating histone glycation as a new dynamic epigenetic markR35GM138386 · NIGMS · SLOAN-KETTERING INST CAN RESEARCH · PI DAVID-SHTERNBERG, YAEL E · 2020 to 2024
$2.2MCenter for Strategic Scientific Initiatives, National Cancer Institute (NCI Center for Strategic Scientific Initiatives) CA218513Korea Health Industry Development Institute (KHIDI) HI19C1330Ministry of Trade, Industry and Energy (Ministry of Trade, Industry and Energy, Korea) 20012443NCI NIH HHS P30 CA008748NCI NIH HHS P50 CA192937NCI NIH HHS R01 CA207983NCI NIH HHS R01 CA218513NCI NIH HHS R35 CA232093NCI NIH HHS U01 CA169538NCI NIH HHS U01 CA210240NCI NIH HHS U01 CA224175NIGMS NIH HHS R35 GM138386U.S. Department of Health & Human Services | NIH | National Cancer Institute (NCI) CA224175 (D.L.), CA210240 (D.L.), CA232093 (D.L.), CA207983 (D.L.), CA169538 (D.L.) and CA218513Worldwide Cancer Research 23-0105
Abstract
Extracellular vesicles (EVs) transport biomolecules that mediate intercellular communication. We previously showed that EVs contain DNA (EV-DNA) representing the entire genome. However, the mechanism of genomic EV-DNA packaging and its role in cancer remain elusive. We now demonstrate that EV-DNA is predominantly localized on the vesicle surface and associated with uniquely modified and cleaved histones. Moreover, a genome-wide clustered regularly interspaced short palindromic repeats knockout screen revealed that immune developmental pathways and genes, including apoptotic peptidase activating factor 1 (APAF1) and neutrophil cytosolic factor 1 (NCF1), regulate EV-DNA packaging. Furthermore, in colorectal cancer models, uptake of EV-DNA by pre-metastatic liver Kupffer cells (KCs) activated DNA damage responses. This activation rewired KC cytokine production and promoted the formation of tertiary lymphoid structures, thereby suppressing liver metastasis. Conversely, loss of APAF1 decreased EV-DNA packaging and promoted liver metastasis. Importantly, colorectal cancer biopsy EV-DNA secretion could serve as a predictive biomarker for postoperative metastasis. Taken together, our findings indicate that uniquely chromatinized EV-DNA induces antitumor immunity.
Indexed as
Colorectal NeoplasmsExtracellular VesiclesKupffer CellsLiver NeoplasmsAnimalsApoptotic Protease-Activating Factor 1Cell Line, TumorDisease ProgressionDNADNA DamageHumansMaleMiceNeoplasm MetastasisAPAF1 protein, humanApoptotic Protease-Activating Factor 1DNA
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