ArticleCell2022
Lineage tracing reveals the phylodynamics, plasticity, and paths of tumor evolution.
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Article in Cell, 2022. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 227 papers.
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227citing papers in PubMed
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Who cites it
227 citing papers in PubMed.
- Reframing cancer therapy through tumor plasticity.Nature cancer · 2026Review
- Cell plasticity in cancer and therapy resistance.Experimental & molecular medicine · 2026Review
- Decoding epithelial-mesenchymal transitions with multi-omics.Nature reviews. Genetics · 2026Review
- Lineage identity governs oncogene dependence in mouse NSCLC models of KRAS inhibitor resistance.Nature genetics · 2026Article
- Computational approaches for multimodal lineage tracing.Nature reviews. Genetics · 2026Review
- Phylogenetic and phylodynamic approaches to understanding the evolution of non-small cell lung cancer using single-cell sequencing.Oncogene · 2026Article
- Quantitative dissection of the metastatic cascade at single colony resolution.Research square · 2026Article
- A single-cell lens into the co-evolution of genotypes and phenotypes in cancer.Nature reviews. Cancer · 2026Review
- Programmable promoter editing for precise control of transgene expression.Nature biotechnology · 2026Article
- Spatial omics illuminates tumor heterogeneity.Cell reports methods · 2026Review
- Translational insights and clinical challenges of targeting cancer stem cells.Signal transduction and targeted therapy · 2026Review
- Genomic repeats for single-cell molecular recording.bioRxiv : the preprint server for biology · 2026Article
- SPACE-seq integrates spatial transcriptomics and lineage tracing in native tissues.Cell stem cell · 2026Article
- Spatio-DARLIN enables robust and efficient in situ lineage tracing in mice at single-cell resolution.Nature methods · 2026Article
- The Great Escape: the systems biology of endocrine resistance and lineage plasticity.Endocrine-related cancer · 2026Review
- Deciphering lung cancer at high resolution: a narrative review of applications of single-cell and spatial transcriptomics sequencing.Translational lung cancer research · 2026Review
- Phylogeography of Bone Metastasis: Clonal Evolution, Skeletal Niche Adaptation, and Clinical Implications.International journal of molecular sciences · 2026Review
- Comprehensive benchmarking of RNA velocity methods across single-cell datasets.Genome biology · 2026Article
- Multiple distinct metastatic cell states are induced by epithelial-mesenchymal plasticity.bioRxiv : the preprint server for biology · 2026Article
- Tumor evolution: signaling pathways, molecular mechanisms and therapeutic targets.Signal transduction and targeted therapy · 2026Review
167 more citing papers are in PubMed but not listed here.
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Authors and funding
23 authors.
Dian YangDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Matthew G JonesDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Biological and Medical Informatics Graduate Program, University of California, San Francisco, San Francisco, CA 94158, USA; Integrative Program in Quantitative Biology, University of California, San Francisco, San Francisco, CA 94158, USA; Center for Computational Biology, University of California, Berkeley, Berkeley, CA 94720, USA; David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Santiago NaranjoDavid H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
William M RideoutDavid H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Kyung Hoi Joseph MinWhitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Electrical Engineering and Computer Science, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Raymond HoDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Wei WuDepartment of Medicine, University of California, San Francisco, San Francisco, CA 94158, USA; Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA 94158, USA.
Joseph M ReplogleDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Medical Scientist Training Program, University of California, San Francisco, San Francisco, CA 94158, USA; Tetrad Graduate Program, University of California, San Francisco, San Francisco, CA 94158, USA.
Jennifer L PageCell and Genome Engineering Core, University of California San Francisco, San Francisco, CA 94158, USA.
Jeffrey J QuinnDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Felix HornsDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA.
Xiaojie QiuDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA.
Michael Z ChenWhitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Medical Scientist Training Program, Harvard Medical School, Boston, MA 02115, USA.
William A Freed-PastorDavid H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA.
Christopher S McGinnisTetrad Graduate Program, University of California, San Francisco, San Francisco, CA 94158, USA; Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA.
David M PattersonDepartment of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA.
Zev J GartnerDepartment of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA; Chan Zuckerberg BioHub Investigator, University of California, San Francisco, San Francisco, CA 94158, USA; Center for Cellular Construction, University of California, San Francisco, San Francisco, CA 94158, USA.
Eric D ChowDepartment of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA; Center for Advanced Technology, University of California, San Francisco, San Francisco, CA 94158, USA.
Trever G BivonaDepartment of Medicine, University of California, San Francisco, San Francisco, CA 94158, USA; Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA 94158, USA.
Michelle M ChanLewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544, USA; Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA.
Nir YosefCenter for Computational Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Chan Zuckerberg BioHub Investigator, University of California, San Francisco, San Francisco, CA 94158, USA; Department of Electrical Engineering and Computer Science, University of California Berkeley, Berkeley, CA 94720, USA; Ragon Institute of Massachusetts General Hospital, MIT and Harvard University, Cambridge, MA, USA. Electronic address: niryosef@berkeley.edu.
Tyler JacksDavid H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02142, USA. Electronic address: tjacks@mit.edu.
Jonathan S WeissmanDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02142, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02142, USA. Electronic address: weissman@wi.mit.edu.
Funding
VIRUS PRODUCTION COREP30CA014051 · NCI · MASSACHUSETTS INSTITUTE OF TECHNOLOGY · PI MATTHEW G. VANDER HEIDEN · 1985 to 2026
$93.9MMedical Scientist Training ProgramT32GM007753 · NIGMS · HARVARD UNIVERSITY (MEDICAL SCHOOL) · PI WALENSKY, LOREN DAVID · 1985 to 2021
$50.0MPRE-DOCTORAL TRAINING IN THE BIOLOGICAL SCIENCEST32GM007287 · NIGMS · MASSACHUSETTS INSTITUTE OF TECHNOLOGY · PI BELL, STEPHEN P., KEATING, AMY E · 1985 to 2019
$40.8MCenter for Genomic Editing and Recording: Development and Application of Next-Generation Genome and Epigenome Editing Methods to Advance the Study and Treatment of Human DiseaseRM1HG009490 · NHGRI · WHITEHEAD INSTITUTE FOR BIOMEDICAL RES · PI Brittany S. Adamson, Martin Joseph Ankrah Aryee · 2017 to 2026
$22.7MUCSF Project 1U54CA224081 · NCI · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI Jing Wang · 2017 to 2026
$12.9MThe Cancer Target Discovery and Development Network at UCSFU01CA217882 · NCI · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI BANDYOPADHYAY, SOURAV, BIVONA, TREVER G · 2017 to 2021
$5.2MBay Area Cancer Target Discovery and DevelopmentU01CA272546 · NCI · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI Sourav Bandyopadhyay, Trever G Bivona · 2022 to 2026
$4.8MCharacterization of YAP as a rational companion target in lung cancerR01CA204302 · NCI · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI Trever G Bivona · 2017 to 2026
$3.7MRational Combined Inhibition of NF-kB and EGFR to Optimize Lung Cancer TreatmentR01CA169338 · NCI · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI BIVONA, TREVER G · 2013 to 2023
$3.4M(PQ7) Defining a new mode of RAS signaling in cancer from cytoplasmic protein granulesR01CA231300 · NCI · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI BIVONA, TREVER G, HUANG, BO · 2019 to 2023
$2.3MOptimizing biologically-based rational polytherapy in ALK+ lung cancerR01CA211052 · NCI · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI BIVONA, TREVER G · 2017 to 2021
$1.8MProfiling chromatin-associated long noncoding RNAs in numerous biological contextsF32GM125247 · NIGMS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI QUINN, JEFFREY JEROME · 2017 to 2019
$179kHoward Hughes Medical InstituteNCI NIH HHS F31 CA257349NCI NIH HHS P30 CA014051NCI NIH HHS R01 CA169338NCI NIH HHS R01 CA204302NCI NIH HHS R01 CA211052NCI NIH HHS R01 CA231300NCI NIH HHS U01 CA217882NCI NIH HHS U01 CA272546NCI NIH HHS U54 CA224081NHGRI NIH HHS RM1 HG009490NIGMS NIH HHS F32 GM125247NIGMS NIH HHS F32 GM128366NIGMS NIH HHS T32 GM007287NIGMS NIH HHS T32 GM007753NINDS NIH HHS F31 NS115380
Abstract
Tumor evolution is driven by the progressive acquisition of genetic and epigenetic alterations that enable uncontrolled growth and expansion to neighboring and distal tissues. The study of phylogenetic relationships between cancer cells provides key insights into these processes. Here, we introduced an evolving lineage-tracing system with a single-cell RNA-seq readout into a mouse model of Kras;Trp53(KP)-driven lung adenocarcinoma and tracked tumor evolution from single-transformed cells to metastatic tumors at unprecedented resolution. We found that the loss of the initial, stable alveolar-type2-like state was accompanied by a transient increase in plasticity. This was followed by the adoption of distinct transcriptional programs that enable rapid expansion and, ultimately, clonal sweep of stable subclones capable of metastasizing. Finally, tumors develop through stereotypical evolutionary trajectories, and perturbing additional tumor suppressors accelerates progression by creating novel trajectories. Our study elucidates the hierarchical nature of tumor evolution and, more broadly, enables in-depth studies of tumor progression.
Indexed as
NeoplasmsAnimalsExome SequencingGenes, rasMicePhylogenyfitnessgenetically engineered mouse modellineage tracinglung cancerphylogeneticsplasticitysingle celltranscriptome heterogeneitytumor evolution
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