ArticleCell2023
Molecular cartography uncovers evolutionary and microenvironmental dynamics in sporadic colorectal tumors.
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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 76 papers.
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76citing papers in PubMed
11.7field-weighted citation impact, top 1% of its field
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Who cites it
76 citing papers in PubMed, 76 citations in OpenAlex.
- Unique circulating miRNAome signatures captured with distinct molecular states in Lynch syndrome and sporadic colorectal cancer.Molecular oncology · 2026Article
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- Colorectal Cancer: Epidemiology, Risk Factors, Signaling Pathways, Clinical Features, Screening, Diagnosis, and Management.MedComm · 2026Review
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- Supermeres Containing the Discoidin Domain Receptor 1 Extracellular Domain Promote Collagen Alignment and Immune Exclusion in Microsatellite-Stable Colorectal Cancer.Cancer research communications · 2026Article
- Spatiotemporal lineage tracing reveals the dynamic spatial architecture of tumor growth and metastasis.Nature genetics · 2026Article
- Advances in single-cell and spatial multi-omics for plant development and stress responses.Plant diversity · 2026Review
- Lineage plasticity driven by GATA6 loss fuels colorectal cancer metastasis.Cell stem cell · 2026Article
- 3D pathology-guided microdissection.Nature methods · 2026Article
- Pathophysiology of colitis-associated colorectal cancer.Nature reviews. Gastroenterology & hepatology · 2026Review
- Cancer Heterogeneity and Cancer Cell Plasticity: Molecular Mechanisms and Precision Therapy.MedComm · 2026Review
- Notch3/4 Knockdown Inhibits Colon Adenocarcinoma Progression by Suppressing Tumor Cell Activity and Orchestrating VEGFA-Dependent Tumor Immune Microenvironment.Cancer medicine · 2026Article
- NICD3 mediates pro-angiogenic effects through SMAD3/TGFBI axis in colorectal cancer.Cell death & disease · 2026Article
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- Single-cell analysis identifies dysregulated cell type-specific gene programs and intercellular crosstalk underlying colorectal cancer.NPJ precision oncology · 2026Article
- Pan-cancer analysis of spatial transcriptomics reveals heterogeneous tumor spatial microenvironment.Cell reports. Medicine · 2026Article
- A comprehensive survey of computer vision methods for spatial transcriptomics.Briefings in bioinformatics · 2026Review
- Heterogeneous Intermediate Phenotypes of Cancer Cells with Varying Ki-67-Positivity Rates, Including Histologically HCC-like and NEC-like Cells, in Liver MiNEN.International journal of molecular sciences · 2026Article
- Transforming growth factor β induced as a novel secreted immune checkpoint counterinhibiting human tumor-associated T cells.Journal for immunotherapy of cancer · 2026Article
- Article
16 more citing papers are in PubMed but not listed here.
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Authors and funding
33 authors at 4 institutions in 1 country.
Cody N HeiserProgram in Chemical and Physical Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA; Epithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Alan J SimmonsEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Frank RevettaDepartment of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Eliot T McKinleyEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Marisol A Ramirez-SolanoDepartment of Biostatistics and Center for Quantitative Sciences, Vanderbilt University Medical Center, Nashville, TN 37235, USA.
Jiawei WangEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Harsimran KaurProgram in Chemical and Physical Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA; Epithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Justin ShaoEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Computer Science, Vanderbilt University, Nashville, TN 37235, USA.
Gregory D AyersDepartment of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Yu WangDepartment of Biostatistics and Center for Quantitative Sciences, Vanderbilt University Medical Center, Nashville, TN 37235, USA.
Sarah E GlassEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Naila TasneemEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Zhengyi ChenProgram in Chemical and Physical Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA; Epithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Yan QinIncendia Therapeutics, Inc., Boston, MA 02135, USA.
William KimEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Andrea RolongEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Bob ChenProgram in Chemical and Physical Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA; Epithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Paige N VegaEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Julia L DrewesDepartment of Medicine, Division of Infectious Diseases, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Nicholas O MarkhamEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Nabil SalehEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Fotis NikolosDepartment of Urology, Neal Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA.
Simon VandekarDepartment of Biostatistics and Center for Quantitative Sciences, Vanderbilt University Medical Center, Nashville, TN 37235, USA.
Angela L JonesVanderbilt Technologies for Advanced Genomics, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
M Kay WashingtonDepartment of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Joseph T RolandEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Surgery, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Keith S ChanDepartment of Urology, Neal Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA.
Thomas SchürpfIncendia Therapeutics, Inc., Boston, MA 02135, USA.
Cynthia L SearsDepartment of Medicine, Division of Infectious Diseases, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Qi LiuDepartment of Biostatistics and Center for Quantitative Sciences, Vanderbilt University Medical Center, Nashville, TN 37235, USA.
Martha J ShrubsoleDepartment of Medicine, Division of Epidemiology, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
Robert J CoffeyEpithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA. Electronic address: robert.coffey@vumc.org.
Ken S LauProgram in Chemical and Physical Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA; Epithelial Biology Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA; Department of Surgery, Vanderbilt University Medical Center, Nashville, TN 37232, USA; Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA. Electronic address: ken.s.lau@vanderbilt.edu.
Vanderbilt University · USVanderbilt University Medical Center · USHouston Methodist · USJohns Hopkins University · US
Funding
Tumor Immunology and Microenvironment Research ProgramP30CA068485 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI Ben Ho Park · 1995 to 2026
$172.8MTranslational Analysis CoreP30DK058404 · NIDDK · VANDERBILT UNIVERSITY MEDICAL CENTER · PI MARY Kay WASHINGTON · 2002 to 2026
$29.9MVanderbilt-Ingram Cancer Center SPORE in Gastrointestinal CancerP50CA236733 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI STEPHEN W. FESIK · 2019 to 2026
$19.6MVanderbilt Mouse Metabolic Physiology CenterU24DK059637 · NIDDK · VANDERBILT UNIVERSITY · PI WASSERMAN, DAVID H · 2001 to 2015
$14.9MRoles for Supermeres in CRC ProgressionP01CA229123 · NCI · VANDERBILT UNIVERSITY · PI Alissa M Weaver · 2020 to 2026
$12.9MTennessee Valley Cooperative Human Tissue NetworkUM1CA183727 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI MARY Kay WASHINGTON · 2014 to 2026
$12.6MMolecular, Cellular and Tissue Characterization UnitU2CCA233291 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI COFFEY, ROBERT J., SHRUBSOLE, MARTHA J. · 2018 to 2023
$12.2MShaping the Microenvironment by DPEP1 Facilitates Adenoma ProgressionU54CA274367 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI Ken S Lau, Martha J. Shrubsole · 2022 to 2026
$9.7MIntegrated approach to study early and late events in colonic neoplasia: mouse to manR35CA197570 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI Robert J. Coffey · 2017 to 2026
$9.4MTraining Program in Stem Cell and Regenerative Developmental BiologyT32HD007502 · NICHD · VANDERBILT UNIVERSITY · PI WRIGHT, CHRISTOPHER V · 1997 to 2022
$5.4MTuft cell heterogeneity in function, lineage, and structure in ileal inflammatory diseaseR01DK103831 · NIDDK · VANDERBILT UNIVERSITY · PI LAU, KEN S · 2016 to 2024
$4.4MDiet, Genetics, Epigenetics and Colorectal Adenoma Risk.K07CA122451 · NCI · VANDERBILT UNIVERSITY · PI SHRUBSOLE, MARTHA J. · 2007 to 2011
$655kNCI NIH HHS K07 CA122451NCI NIH HHS P01 CA229123NCI NIH HHS P30 CA068485NCI NIH HHS P50 CA236733NCI NIH HHS R35 CA197570NCI NIH HHS U2C CA233291NCI NIH HHS U54 CA274367NCI NIH HHS UM1 CA183727NICHD NIH HHS T32 HD007502NIDDK NIH HHS F31 DK127687NIDDK NIH HHS P30 DK058404NIDDK NIH HHS R01 DK103831NIDDK NIH HHS U24 DK059637
Abstract
Colorectal cancer exhibits dynamic cellular and genetic heterogeneity during progression from precursor lesions toward malignancy. Analysis of spatial multi-omic data from 31 human colorectal specimens enabled phylogeographic mapping of tumor evolution that revealed individualized progression trajectories and accompanying microenvironmental and clonal alterations. Phylogeographic mapping ordered genetic events, classified tumors by their evolutionary dynamics, and placed clonal regions along global pseudotemporal progression trajectories encompassing the chromosomal instability (CIN+) and hypermutated (HM) pathways. Integrated single-cell and spatial transcriptomic data revealed recurring epithelial programs and infiltrating immune states along progression pseudotime. We discovered an immune exclusion signature (IEX), consisting of extracellular matrix regulators DDR1, TGFBI, PAK4, and DPEP1, that charts with CIN+ tumor progression, is associated with reduced cytotoxic cell infiltration, and shows prognostic value in independent cohorts. This spatial multi-omic atlas provides insights into colorectal tumor-microenvironment co-evolution, serving as a resource for stratification and targeted treatments.
Indexed as
Colorectal NeoplasmsMicrosatellite InstabilityTumor MicroenvironmentChromosomal InstabilityDisease ProgressionGene Expression ProfilingHumansMutationp21-Activated KinasesPhylogenyPrognosisp21-Activated KinasesPAK4 protein, humancolorectal cancerimmune exclusionmicrosatellite instabilitymultiplex imagingmutationsspatial transcriptomicsstem cellstumor evolutiontumor progression
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