ArticleCell2017
Enhancer Reprogramming Promotes Pancreatic Cancer Metastasis.
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Article in Cell, 2017. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 313 papers.
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313citing papers in PubMed
40.4field-weighted citation impact, top 1% of its field
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313 citing papers in PubMed, 481 citations in OpenAlex.
- Tissue-derived extracellular matrix hydrogels instruct epigenetic adaptation in metastatic colonization.Bioactive materials · 2027Article
- METTL1-mediated m7G modification of valine tRNAs drives metabolic adaptation in pancreatic ductal adenocarcinoma cells.The Journal of clinical investigation · 2026Article
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- Epigenetic reprogramming of lineage switching in cancer.FEBS letters · 2026Review
- Hypoxia-induced metastatic heterogeneity in pancreatic cancer.Nature communications · 2026Article
- Activation of KIT signaling promotes early tumorigenesis through the AP-1 pathway in APC/TP53 double-knockout human colon organoids.Cell death & disease · 2026Article
- KMT2D depletion promotes KRAS-induced pancreatic carcinogenesis independent of TP53.The Journal of biological chemistry · 2026Article
- BCR::ABL1-Induced Enhancer Reprogramming Uncovers Hypersensitivity of Ph+B-ALL Cells to Enhancer-Targeting Drugs.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2026Article
- Trans-histone crosstalk establishes distinct H3K79 methylation zones with differential transcriptional functions.Nucleic acids research · 2026Article
- Review
- A KLF5's domino effect drives metastatic pancreatic cancer.Molecular cancer · 2026Article
- Generation of a comprehensive epigenomic atlas in clear cell renal cell carcinoma informs kidney cancer progression and heritability.Cell reports · 2026Article
- The application of experimental models for the drug discovery for digestive tumors.Molecular cancer · 2026Review
- ERRα-KDM5C restrains STING enhancer activity to modulate type I interferon signaling in breast cancer progression.Cell death & disease · 2026Article
- CRISPR screen of human pancreatic cancer xenografts identifies a KLF5 proliferation vulnerability through epigenetic modifiers NCAPD2 and MTHFD1.Molecular cancer · 2026Article
- DNMT3A p.R882C driven proliferation and anti-apoptotic effects in pancreatic cancer cells.Scientific reports · 2026Article
- Metabolites beyond metabolism: Exploring their atypical roles in protein modification and signaling transduction.Chinese medical journal · 2026Review
- Enhancer-dependent gene regulation in space, time, and malignancies.International journal of cancer · 2026Review
- Systemic control of HNF1B-driven redox homeostasis by N6-adenosine methylation.Nucleic acids research · 2026Article
- Molecular mechanisms of KMT2C alterations in gastrointestinal cancers: enhancer network destabilization, lineage plasticity, and clinical translation.Frontiers in immunology · 2026Review
253 more citing papers are in PubMed but not listed here.
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Authors and funding
24 authors at 6 institutions in 1 country.
Jae-Seok RoeCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Chang-Il HwangCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
Tim D D SomervilleCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Joseph P MilazzoCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Eun Jung LeeCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
Brandon Da SilvaCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
Laura MaiorinoCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Hervé TiriacCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
C Megan YoungCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
Koji MiyabayashiCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
Dea FilippiniCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
Brianna CreightonCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
Richard A BurkhartDivision of Hepatobiliary and Pancreatic Surgery, Department of Surgery, Johns Hopkins Hospital, Baltimore, MD 21287, USA.
Jonathan M BuscagliaDivision of Gastroenterology & Hepatology, Stony Brook University School of Medicine, Stony Brook, NY 11790, USA.
Edward J KimDivision of Hematology/Oncology, UC Davis Medical Center, Sacramento, CA 95817, USA.
Jean L GremDepartment of Medicine, University of Nebraska Medical Center, Omaha, NE 68198, USA.
Audrey J LazenbyDepartment of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, NE 68198, USA.
James A GrunkemeyerEppley Institute for Research in Cancer and Allied Diseases, Fred & Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, NE 68198, USA.
Michael A HollingsworthEppley Institute for Research in Cancer and Allied Diseases, Fred & Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, NE 68198, USA.
Paul M GrandgenettEppley Institute for Research in Cancer and Allied Diseases, Fred & Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, NE 68198, USA.
Mikala EgebladCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Youngkyu ParkCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA.
David A TuvesonCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY 11724, USA. Electronic address: dtuveson@cshl.edu.
Christopher R VakocCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA. Electronic address: vakoc@cshl.edu.
Cold Spring Harbor Laboratory · USLustgarten Foundation · USUniversity of Nebraska Medical Center · USJohns Hopkins Hospital · USStony Brook University · USUniversity of California Davis Medical Center · US
Funding
Single-Cell Biology Shared ResourceP30CA045508 · NCI · COLD SPRING HARBOR LABORATORY · PI John Edward Moses · 1987 to 2026
$118.9MVIRAL TRANSACTIVATIONP01CA013106 · NCI · COLD SPRING HARBOR LABORATORY · PI William Richard McCombie · 1985 to 2026
$116.8MStaff InvestigatorsP30CA093373 · NCI · UNIVERSITY OF CALIFORNIA DAVIS · PI Laura Marcu · 2002 to 2026
$84.9MTissue CoreP50CA127297 · NCI · UNIVERSITY OF NEBRASKA MEDICAL CENTER · PI HOLLINGSWORTH, MICHAEL A. · 2008 to 2018
$17.1MTranslational Research Enhancement CoreP30DK089502 · NIDDK · JOHNS HOPKINS UNIVERSITY · PI ZACHOS, NICHOLAS CONSTANTINE · 2011 to 2020
$12.0MUAB / UMN SPORE in Pancreatic CancerP50CA101955 · NCI · UNIVERSITY OF ALABAMA AT BIRMINGHAM · PI BUCHSBAUM, DONALD J · 2010 to 2014
$11.1MCOMPUTATIONAL AND FUNCTIONAL APPROACHES TO VALIDATING CANCER GENOME TARGETSU01CA168409 · NCI · COLD SPRING HARBOR LABORATORY · PI POWERS, SCOTT · 2012 to 2016
$7.3MClinical and Laboratory Research Training for Surgical OncologistsT32CA126607 · NCI · JOHNS HOPKINS UNIVERSITY · PI CAMERON, ANDREW M. · 2008 to 2024
$6.0MNrf2 Regulation of Ductal Pancreatic Cancer Etiology and Treatment ResponseR01CA188134 · NCI · COLD SPRING HARBOR LABORATORY · PI TUVESON, DAVID A · 2017 to 2021
$3.0M(PQA-4) Organoid Omics To Detect And Defeat Ductal Pancreatic CancerR01CA190092 · NCI · COLD SPRING HARBOR LABORATORY · PI TUVESON, DAVID A · 2014 to 2017
$2.2MPreclinical Models for Cancer Therapeutic DevelopmentR50CA211506 · NCI · COLD SPRING HARBOR LABORATORY · PI PARK, YOUNGKYU · 2016 to 2025
$2.1MIntegrated Translational Cancer Science CenterU10CA180944 · NCI · COLD SPRING HARBOR LABORATORY · PI BAKER, LAURENCE HOWARD, LIU, EDISON TAK-BUN · 2014 to 2018
$2.0MNCI NIH HHS F32 CA180717NCI NIH HHS P01 CA013106NCI NIH HHS P20 CA192994NCI NIH HHS P20 CA192996NCI NIH HHS P30 CA045508NCI NIH HHS P30 CA093373NCI NIH HHS P50 CA101955NCI NIH HHS P50 CA127297NCI NIH HHS R01 CA188134NCI NIH HHS R01 CA190092NCI NIH HHS R50 CA211462NCI NIH HHS R50 CA211506NCI NIH HHS T32 CA126607NCI NIH HHS U01 CA168409NCI NIH HHS U10 CA180944NIDDK NIH HHS P30 DK089502
Abstract
Pancreatic ductal adenocarcinoma (PDA) is one of the most lethal human malignancies, owing in part to its propensity for metastasis. Here, we used an organoid culture system to investigate how transcription and the enhancer landscape become altered during discrete stages of disease progression in a PDA mouse model. This approach revealed that the metastatic transition is accompanied by massive and recurrent alterations in enhancer activity. We implicate the pioneer factor FOXA1 as a driver of enhancer activation in this system, a mechanism that renders PDA cells more invasive and less anchorage-dependent for growth in vitro, as well as more metastatic in vivo. In this context, FOXA1-dependent enhancer reprogramming activates a transcriptional program of embryonic foregut endoderm. Collectively, our study implicates enhancer reprogramming, FOXA1 upregulation, and a retrograde developmental transition in PDA metastasis.
Indexed as
Enhancer Elements, GeneticGene Expression Regulation, NeoplasticAdenocarcinomaAnimalsCarcinoma, Pancreatic DuctalCell Line, TumorDisease Models, AnimalEpigenomicsFemaleGene Expression ProfilingHepatocyte Nuclear Factor 3-alphaHumansMaleMiceMice, Inbred C57BLNeoplasm MetastasisFOXA1 protein, humanFoxa1 protein, mouseHepatocyte Nuclear Factor 3-alphaenhancerFOXA1metastasisorganoidpancreatic cancerpancreatic ductal adenocarcinoma
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