ArticleDevelopmental cell2021
Cooperation between melanoma cell states promotes metastasis through heterotypic cluster formation.
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Article in Developmental cell, 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 55 papers.
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55 citing papers in PubMed, 95 citations in OpenAlex.
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Authors and funding
29 authors at 10 institutions in 3 countries.
Nathaniel R CampbellWeill Cornell/Rockefeller Memorial Sloan Kettering Tri-Institutional MD-PhD Program, New York, NY 10065, USA; Computational and Systems Biology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA; Cancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Anjali RaoInstitute for Computational Medicine, NYU Grossman School of Medicine, New York, NY 10016, USA.
Miranda V HunterCancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Magdalena K SznurkowskaDepartment of Biology, Institute of Molecular Health Sciences, Swiss Federal Institute of Technology (ETH) Zurich, 8093 Zurich, Switzerland.
Luzia BrikerDepartment of Dermatology, University of Zürich Hospital, University of Zürich, Zurich, Switzerland.
Maomao ZhangCancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Maayan BaronInstitute for Computational Medicine, NYU Grossman School of Medicine, New York, NY 10016, USA.
Silja HeilmannComputational and Systems Biology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Maxime DeforetComputational and Systems Biology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Colin KennyDepartment of Anatomy and Cell Biology, University of Iowa, Iowa City, IA 52242, USA.
Lorenza P FerrettiDepartment of Dermatology, University of Zürich Hospital, University of Zürich, Zurich, Switzerland; Department of Molecular Mechanisms of Disease, University of Zürich, Zurich, Switzerland.
Ting-Hsiang HuangCancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Sarah PerleeCancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Manik GargEuropean Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Hinxton, Cambridgeshire, UK.
Jérémie NsengimanaLeeds Institute of Medical Research at St. James's, University of Leeds School of Medicine, Leeds, UK.
Massimo SainiDepartment of Biology, Institute of Molecular Health Sciences, Swiss Federal Institute of Technology (ETH) Zurich, 8093 Zurich, Switzerland.
Emily MontalCancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Mohita TagoreCancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Julia Newton-BishopLeeds Institute of Medical Research at St. James's, University of Leeds School of Medicine, Leeds, UK.
Mark R MiddletonOxford NIHR Biomedical Research Centre and Department of Oncology, University of Oxford, Oxford, UK.
Pippa CorrieCambridge Cancer Centre, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK.
David J AdamsExperimental Cancer Genetics, the Wellcome Sanger Institute, Hinxton, Cambridgeshire, UK.
Roy RabbieCambridge Cancer Centre, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK; Experimental Cancer Genetics, the Wellcome Sanger Institute, Hinxton, Cambridgeshire, UK.
Nicola AcetoDepartment of Biology, Institute of Molecular Health Sciences, Swiss Federal Institute of Technology (ETH) Zurich, 8093 Zurich, Switzerland.
Mitchell P LevesqueDepartment of Dermatology, University of Zürich Hospital, University of Zürich, Zurich, Switzerland.
Robert A CornellDepartment of Anatomy and Cell Biology, University of Iowa, Iowa City, IA 52242, USA.
Itai YanaiInstitute for Computational Medicine, NYU Grossman School of Medicine, New York, NY 10016, USA.
Joao B XavierComputational and Systems Biology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA. Electronic address: xavierj@mskcc.org.
Richard M WhiteCancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA. Electronic address: whiter@mskcc.org.
Memorial Sloan Kettering Cancer Center · USETH Zurich · CHUniversity of Zurich · CHCambridge University Hospitals NHS Foundation Trust · GBUniversity of Iowa · USUniversity of Leeds · GBEuropean Bioinformatics Institute · GBOxford BioMedica (United Kingdom) · GBTri-Institutional PhD Program in Chemical Biology · USWellcome Sanger Institute · GB
Funding
X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI Hongbiao Carl Lekaye · 1985 to 2026
$347.4MWeill Cornell/Rockefeller/Sloan-Kettering MST ProgramT32GM007739 · NIGMS · WEILL MEDICAL COLL OF CORNELL UNIV · PI HSU, KATHARINE C · 1985 to 2023
$51.1MTraining and Career Development CoreU54CA132378 · NCI · CITY COLLEGE OF NEW YORK · PI Bao Q Vuong · 2008 to 2026
$28.9MTraining and Career Development and Education CoreU54CA137788 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI ADRIANA ESPINOSA, FRANCESCA M GANY · 2008 to 2026
$28.1MGenetic Epidermiology of MelanomaR01CA083115 · NCI · UNIVERSITY OF PENNSYLVANIA · PI BISHOP, DAVID TIMOTHY, ELDER, DAVID ERIC · 2001 to 2017
$13.0MRegulation of the Melanocyte Lineage by the AP2 Transcription Factor FamilyR01AR062547 · NIAMS · UNIVERSITY OF WASHINGTON · PI CORNELL, ROBERT AARON · 2013 to 2022
$3.8MDissecting the complexity of metastasis with mathematical models and quantitative experiments with in zebrafishR01CA229215 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI WHITE, RICHARD MARK, XAVIER, JOAO · 2018 to 2022
$3.1MEvolutionary dynamics of melanoma metastasisDP2CA186572 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI WHITE, RICHARD MARK · 2013 to 2013
$2.7MInvestigating cancer metabolism and its potential for therapeutic interventionK00CA223016 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI MONTAL, EMILY DINA · 2019 to 2022
$391kDissecting the Ecology of Metastasis in a Zebrafish Model: Trade-Offs of Size and Diversity in Circulating Tumor Cell ClustersF30CA220954 · NCI · WEILL MEDICAL COLL OF CORNELL UNIV · PI CAMPBELL, NATHANIEL R · 2018 to 2021
$194kCancer Research UK 8466Cancer Research UK C2195/A8466Cancer Research UK C588/A10721Cancer Research UK C588/A19167Cancer Research UK C7535/A6408Cancer Research UK C8216/A6129Medical Research Council MR/M019012/1Medical Research Council MR/V000292/1NCI NIH HHS DP2 CA186572NCI NIH HHS F30 CA220954NCI NIH HHS K00 CA223016NCI NIH HHS P30 CA008748NCI NIH HHS R01 CA083115NCI NIH HHS R01 CA229215NCI NIH HHS U54 CA132378NCI NIH HHS U54 CA137788NIAMS NIH HHS R01 AR062547NIGMS NIH HHS T32 GM007739
Abstract
Melanomas can have multiple coexisting cell states, including proliferative (PRO) versus invasive (INV) subpopulations that represent a "go or grow" trade-off; however, how these populations interact is poorly understood. Using a combination of zebrafish modeling and analysis of patient samples, we show that INV and PRO cells form spatially structured heterotypic clusters and cooperate in the seeding of metastasis, maintaining cell state heterogeneity. INV cells adhere tightly to each other and form clusters with a rim of PRO cells. Intravital imaging demonstrated cooperation in which INV cells facilitate dissemination of less metastatic PRO cells. We identified the TFAP2 neural crest transcription factor as a master regulator of clustering and PRO/INV states. Isolation of clusters from patients with metastatic melanoma revealed a subset with heterotypic PRO-INV clusters. Our data suggest a framework for the co-existence of these two divergent cell populations, in which heterotypic clusters promote metastasis via cell-cell cooperation.
Indexed as
Cluster AnalysisAnimalsGene Expression Regulation, NeoplasticMelanomaNeoplasm MetastasisNeoplastic Cells, CirculatingNeural CrestZebrafishcirculating tumor cell clusterclustercooperationmelanomametastasisTFAP2zebrafish
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