ArticleCell systems2024
PanIN and CAF transitions in pancreatic carcinogenesis revealed with spatial data integration.
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Article in Cell systems, 2024. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 50 papers.
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Who cites it
50 citing papers in PubMed.
- Gemcitabine and nab-paclitaxel with or without the VDR agonist paricalcitol for metastatic pancreatic cancer: a randomized, multiarm, run-in phase trial.Nature cancer · 2026Trial
- Periductal Fibroblast Density Defines Lymphocyte Exclusion via a CD44-Dependent Stromal Checkpoint in Pancreatic Cancer.Cancer immunology research · 2026Article
- 3D multi-omics tumour atlases: from technology to biology and clinical translation.Nature reviews. Cancer · 2026Review
- Asynchronous Evolution of Epithelium and Stroma Differentiates Precursor Lesions from Pancreatic Cancer.Cancer discovery · 2026Article
- Unveiling the role of spatial transcriptomics in the analysis of the tumor immune microenvironment (Review).International journal of molecular medicine · 2026Review
- Article
- Review
- Article
- Spatially resolved tissue architecture and computational pathology in pancreatic cancer.Experimental & molecular medicine · 2026Review
- Cancer-Associated Fibroblasts Promote Epithelial-Mesenchymal Transition and Classical to Basal Subtype Shift in Pancreatic Cancer.Cancer research · 2026Article
- Trimodal, uncertainty-guided whole-slide framework for genome-scale spatial expression and image-only virtual perturbation in cancer cohorts.Genome medicine · 2026Article
- D3aist: data-driven detection of atypical interactions in spatial transcriptomics.BMC genomics · 2026Article
- Eosinophil diversity and function: emerging insights into subtypes and therapeutic targets.Cell death discovery · 2026Review
- CODAvision: best practices and a user-friendly interface for rapid, customizable segmentation of medical images.Nature protocols · 2026Review
- AI-Powered Deep Visual Proteomics Reveals Critical Molecular Transitions in Pancreatic Cancer Precursors.Cancer discovery · 2026Article
- Quantitative 3D histology reveals localized immune remodeling during early pancreatic cancer progression.Cell press blue · 2026Article
- Progress and challenges in the development of advanced pancreatic cancer organoids.Journal of experimental & clinical cancer research : CR · 2026Review
- Decoding the CAF-TAM axis: multi-omics dissection and therapeutic targeting of stromal-immune crosstalk in the tumor microenvironment.Cell death & disease · 2026Review
- Molecular subtypes in pancreatic cancer: from academic promise to clinical reality.Molecular cancer · 2026Review
- Deep Learning Enabled 3D Multi-Omic Analysis Reveals Molecular Signatures of Heterogeneous Response to Chemotherapy in Pancreatic Cancer.bioRxiv : the preprint server for biology · 2026Article
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Authors and funding
27 authors.
Alexander T F BellDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Jacob T MitchellDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Genetic Medicine, Johns Hopkins School of Medicine, Baltimore, MD, USA.
Ashley L KiemenDepartment of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, MD, USA; Department of Pathology, Johns Hopkins School of Medicine, Baltimore, MD, USA.
Melissa LymanDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Kohei FujikuraDepartment of Pathology, Johns Hopkins School of Medicine, Baltimore, MD, USA.
Jae W LeeDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Pathology, Johns Hopkins School of Medicine, Baltimore, MD, USA.
Erin CoyneDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Sarah M ShinDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Sushma NagarajDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Atul DeshpandeDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Pei-Hsun WuDepartment of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, MD, USA.
Dimitrios N SidiropoulosDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Cellular and Molecular Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Rossin ErbeDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Genetic Medicine, Johns Hopkins School of Medicine, Baltimore, MD, USA.
Jacob Stern10x Genomics, Pleasanton, CA, USA.
Rena Chan10x Genomics, Pleasanton, CA, USA.
Stephen Williams10x Genomics, Pleasanton, CA, USA.
James M Chell10x Genomics, Pleasanton, CA, USA.
Lauren CiottiDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Jacquelyn W ZimmermanDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; The Skip Viragh Center for Clinical and Translational Research, Baltimore, MD, USA.
Denis WirtzDepartment of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, MD, USA; Department of Materials Science and Engineering, The Johns Hopkins University, Baltimore, MD, USA; Johns Hopkins Physical Sciences - Oncology Center, The Johns Hopkins University, Baltimore, MD, USA.
Won Jin HoDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; The Skip Viragh Center for Clinical and Translational Research, Baltimore, MD, USA.
Neeha ZaidiDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; The Skip Viragh Center for Clinical and Translational Research, Baltimore, MD, USA.
Elizabeth ThompsonDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Pathology, Johns Hopkins School of Medicine, Baltimore, MD, USA; The Skip Viragh Center for Clinical and Translational Research, Baltimore, MD, USA.
Elizabeth M JaffeeDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; The Skip Viragh Center for Clinical and Translational Research, Baltimore, MD, USA.
Laura D WoodDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Pathology, Johns Hopkins School of Medicine, Baltimore, MD, USA; The Skip Viragh Center for Clinical and Translational Research, Baltimore, MD, USA.
Elana J FertigDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Applied Mathematics and Statistics, Whiting School of Engineering, Johns Hopkins University, Baltimore, MD, USA; The Skip Viragh Center for Clinical and Translational Research, Baltimore, MD, USA. Electronic address: ejfertig@jhmi.edu.
Luciane T KagoharaDepartment of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Bloomberg Kimmel Immunology Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA; The Skip Viragh Center for Clinical and Translational Research, Baltimore, MD, USA. Electronic address: ltsukam1@jhmi.edu.
Funding
Tumor Antigens for Individual Signatures and TherapyP50CA062924 · NCI · JOHNS HOPKINS UNIVERSITY · PI THOMPSON, ELIZABETH D · 1993 to 2022
$54.6MTransforming Human Pancreatic Cancer Into An Immunologic DiseaseP01CA247886 · NCI · JOHNS HOPKINS UNIVERSITY · PI JAFFEE, ELIZABETH M. · 2021 to 2025
$12.7MTech Core 2U54CA268083 · NCI · JOHNS HOPKINS UNIVERSITY · PI Denis Wirtz, Laura DeLong Wood · 2022 to 2026
$10.2MThe Role of Physical Cues in Collective Cell InvasionU54CA210173 · NCI · JOHNS HOPKINS UNIVERSITY · PI WIRTZ, DENIS · 2016 to 2020
$9.9MIntegrating bioinformatics into multiscale models for hepatocellular carcinomaU01CA212007 · NCI · JOHNS HOPKINS UNIVERSITY · PI EWALD, ANDREW JOSEF, FERTIG, ELANA · 2018 to 2022
$3.2MValidation of Nuclear Morphology as a Biomarker of Aging and Aging-Related PhenotypesU01AG060903 · NIA · JOHNS HOPKINS UNIVERSITY · PI WIRTZ, DENIS · 2018 to 2022
$3.1MInterrogation of the Impact of Selection on the Evolution of Human PancreaticCancer Precursor LesionsU01CA271273 · NCI · JOHNS HOPKINS UNIVERSITY · PI Elana Fertig, Rachel Karchin · 2022 to 2026
$2.8MMutant KRAS targeted vaccines for the interception of pancreatic cancer developmentR37CA292056 · NCI · JOHNS HOPKINS UNIVERSITY · PI Neeha Zaidi · 2024 to 2026
$2.0MSingle-cell and imaging data integration software to spatially resolve the tumor microenvironmentU01CA253403 · NCI · JOHNS HOPKINS UNIVERSITY · PI FERTIG, ELANA · 2020 to 2022
$1.2MNeoantigen-Targeted Vaccines in Combination with Immune Checkpoint Inhibitors for Pancreatic CancerK08CA248624 · NCI · JOHNS HOPKINS UNIVERSITY · PI ZAIDI, NEEHA · 2021 to 2025
$1.1MDetermining Dendritic Cell Responses to Vaccine-based Immunotherapy in PDAC at Single Cell Resolution.F31CA268724 · NCI · JOHNS HOPKINS UNIVERSITY · PI SIDIROPOULOS, DIMITRIOS N · 2022 to 2023
$67kInvestigation of Immunotherapy-induced Alterations to Cellular Communication Networks in Pancreatic Ductal AdenocarcinomaF31CA284525 · NCI · JOHNS HOPKINS UNIVERSITY · PI MITCHELL, JACOB THOMAS · 2024 to 2024
$42kNCI NIH HHS F31 CA268724NCI NIH HHS F31 CA284525NCI NIH HHS K08 CA248624NCI NIH HHS P01 CA247886NCI NIH HHS P50 CA062924NCI NIH HHS R37 CA292056NCI NIH HHS U01 CA212007NCI NIH HHS U01 CA253403NCI NIH HHS U01 CA271273NCI NIH HHS U54 CA210173NCI NIH HHS U54 CA268083NIA NIH HHS U01 AG060903
Abstract
This study introduces a new imaging, spatial transcriptomics (ST), and single-cell RNA-sequencing integration pipeline to characterize neoplastic cell state transitions during tumorigenesis. We applied a semi-supervised analysis pipeline to examine premalignant pancreatic intraepithelial neoplasias (PanINs) that can develop into pancreatic ductal adenocarcinoma (PDAC). Their strict diagnosis on formalin-fixed and paraffin-embedded (FFPE) samples limited the single-cell characterization of human PanINs within their microenvironment. We leverage whole transcriptome FFPE ST to enable the study of a rare cohort of matched low-grade (LG) and high-grade (HG) PanIN lesions to track progression and map cellular phenotypes relative to single-cell PDAC datasets. We demonstrate that cancer-associated fibroblasts (CAFs), including antigen-presenting CAFs, are located close to PanINs. We further observed a transition from CAF-related inflammatory signaling to cellular proliferation during PanIN progression. We validate these findings with single-cell high-dimensional imaging proteomics and transcriptomics technologies. Altogether, our semi-supervised learning framework for spatial multi-omics has broad applicability across cancer types to decipher the spatiotemporal dynamics of carcinogenesis.
Indexed as
Cancer-Associated FibroblastsCarcinogenesisCarcinoma, Pancreatic DuctalPancreatic NeoplasmsCarcinoma in SituGene Expression Regulation, NeoplasticHumansSingle-Cell AnalysisTranscriptomeTumor Microenvironmentimaging mass cytometrymachine learningmulti-omicspancreatic adenocarcinomapancreatic intraepithelial neoplasiaspatial transcriptomicstransfer learningVisiumXenium
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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the Socratic graph.