A cellular hierarchy in melanoma uncouples growth and metastasis.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
10 2022
Historique:
received: 01 07 2020
accepted: 17 08 2022
pubmed: 22 9 2022
medline: 12 10 2022
entrez: 21 9 2022
Statut: ppublish

Résumé

Although melanoma is notorious for its high degree of heterogeneity and plasticity

Identifiants

pubmed: 36131018
doi: 10.1038/s41586-022-05242-7
pii: 10.1038/s41586-022-05242-7
pmc: PMC10439739
mid: NIHMS1922523
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

190-198

Subventions

Organisme : Medical Research Council
ID : MC_PC_17230
Pays : United Kingdom
Organisme : NIDDK NIH HHS
ID : R01 DK056645
Pays : United States
Organisme : Wellcome Trust
ID : 219478/Z/19/Z
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : P30 CA013696
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom

Commentaires et corrections

Type : ErratumIn
Type : CommentIn

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Rambow, F., Marine, J. C. & Goding, C. R. Melanoma plasticity and phenotypic diversity: therapeutic barriers and opportunities. Genes Dev. 33, 1295–1318 (2019).
Arozarena, I. & Wellbrock, C. Phenotype plasticity as enabler of melanoma progression and therapy resistance. Nat. Rev. Cancer 19, 377–391 (2019).
Gulati, G. S. et al. Single-cell transcriptional diversity is a hallmark of developmental potential. Science 367, 405–411 (2020).
pubmed: 31974247 pmcid: 7694873 doi: 10.1126/science.aax0249
Rambow, F. et al. Toward minimal residual disease-directed therapy in melanoma. Cell 174, 843–855 (2018).
pubmed: 30017245 doi: 10.1016/j.cell.2018.06.025
Tirosh, I. et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189–196 (2016).
pubmed: 27124452 pmcid: 4944528 doi: 10.1126/science.aad0501
Wouters, J. et al. Robust gene expression programs underlie recurrent cell states and phenotype switching in melanoma. Nat. Cell Biol. 22, 986–998 (2020).
pubmed: 32753671 doi: 10.1038/s41556-020-0547-3
Patton, E. E. et al. Melanoma models for the next generation of therapies. Cancer Cell 39, 610–631 (2021).
Ackermann, J. et al. Metastasizing melanoma formation caused by expression of activated N-Ras
pubmed: 15899789 doi: 10.1158/0008-5472.CAN-04-2970
Serrano, M. et al. Role of the INK4a locus in tumor suppression and cell mortality. Cell 85, 27–37 (1996).
pubmed: 8620534 doi: 10.1016/S0092-8674(00)81079-X
Tirosh, I. et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189–196 (2016).
pubmed: 27124452 pmcid: 4944528 doi: 10.1126/science.aad0501
Jerby-Arnon, L. et al. A cancer cell program promotes T cell exclusion and resistance to checkpoint blockade. Cell 175, 984–997 (2018).
pubmed: 30388455 pmcid: 6410377 doi: 10.1016/j.cell.2018.09.006
Rambow, F. et al. New functional signatures for understanding melanoma biology from tumor cell lineage-specific analysis. Cell Rep. 13, 840–853 (2015).
pubmed: 26489459 pmcid: 5970542 doi: 10.1016/j.celrep.2015.09.037
Sade-Feldman, M. et al. Defining T cell states associated with response to checkpoint immunotherapy in melanoma. Cell 175, 998–1013 (2018).
pubmed: 30388456 pmcid: 6641984 doi: 10.1016/j.cell.2018.10.038
Fan, J. et al. Linking transcriptional and genetic tumor heterogeneity through allele analysis of single-cell RNA-seq data. Genome Research 28, 1217–1227 (2018).
pubmed: 29898899 pmcid: 6071640 doi: 10.1101/gr.228080.117
Goding, C. R. & Arnheiter, H. MITF—the first 25 years. Genes Dev. 33, 983–1007 (2019).
Hoek, K. S. & Goding, C. R. Cancer stem cells versus phenotype-switching in melanoma. Pigment Cell Melanoma Res. 23, 746–759 (2010).
Aibar, S. et al. SCENIC: single-cell regulatory network inference and clustering. Nat. Methods 14, 1083–1086 (2017).
pubmed: 28991892 pmcid: 5937676 doi: 10.1038/nmeth.4463
Soldatov, R. et al. Spatiotemporal structure of cell fate decisions in murine neural crest. Science 364, eaas9536 (2019).
pubmed: 31171666 doi: 10.1126/science.aas9536
Kerosuo, L. & Bronner, M. E. cMyc regulates the size of the premigratory neural crest stem cell pool. Cell Rep. 17, 2648–2659 (2016).
pubmed: 27926868 pmcid: 5726515 doi: 10.1016/j.celrep.2016.11.025
Tsoi, J. et al. Multi-stage differentiation defines melanoma subtypes with differential vulnerability to drug-induced iron-dependent oxidative stress. Cancer Cell 33, 890–904 (2018).
pubmed: 29657129 pmcid: 5953834 doi: 10.1016/j.ccell.2018.03.017
Köhler, C. et al. Mouse cutaneous melanoma induced by mutant BRaf arises from expansion and dedifferentiation of mature pigmented melanocytes. Cell Stem Cell 21, 679–693 (2017).
pubmed: 29033351 doi: 10.1016/j.stem.2017.08.003
Pozniak, J. et al. A TCF4/BRD4-dependent regulatory network confers cross-resistance to targeted and immune checkpoint therapy in melanoma. Preprint at bioRxiv https://doi.org/10.1101/2022.08.11.502598 (2022).
Snippert, H. J. et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134–144 (2010).
pubmed: 20887898 doi: 10.1016/j.cell.2010.09.016
Reeves, M. Q., Kandyba, E., Harris, S., Del Rosario, R. & Balmain, A. Multicolour lineage tracing reveals clonal dynamics of squamous carcinoma evolution from initiation to metastasis. Nat. Cell Biol. 20, 699–709 (2018).
pubmed: 29802408 pmcid: 6400587 doi: 10.1038/s41556-018-0109-0
Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902 (2019).
pubmed: 31178118 pmcid: 6687398 doi: 10.1016/j.cell.2019.05.031
Chen, A. et al. Spatiotemporal transcriptomic atlas of mouse organogenesis using DNA nanoball-patterned arrays. Cell 185, 1777–1792 (2022).
pubmed: 35512705 doi: 10.1016/j.cell.2022.04.003
Calabrese, C. et al. A perivascular niche for brain tumor stem cells. Cancer Cell 11, 69–82 (2007).
pubmed: 17222791 doi: 10.1016/j.ccr.2006.11.020
Browaeys, R., Saelens, W. & Saeys, Y. NicheNet: modeling intercellular communication by linking ligands to target genes. Nat. Methods 17, 159–162 (2020).
pubmed: 31819264 doi: 10.1038/s41592-019-0667-5
Jin, S. et al. Inference and analysis of cell-cell communication using CellChat. Nat. Commun. 12, 1088 (2021).
pubmed: 33597522 pmcid: 7889871 doi: 10.1038/s41467-021-21246-9
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517 pmcid: 1239896 doi: 10.1073/pnas.0506580102
Wei, K. et al. Notch signalling drives synovial fibroblast identity and arthritis pathology. Nature 582, 259–264 (2020).
pubmed: 32499639 pmcid: 7841716 doi: 10.1038/s41586-020-2222-z
Takano, S. et al. Prrx1 isoform switching regulates pancreatic cancer invasion and metastatic colonization. Genes Dev. 30, 233–247 (2016).
pubmed: 26773005 pmcid: 4719312 doi: 10.1101/gad.263327.115
Ocaña, O. H. et al. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 22, 709–724 (2012).
pubmed: 23201163 doi: 10.1016/j.ccr.2012.10.012
Hoek, K. S. et al. In vivo switching of human melanoma cells between proliferative and invasive states. Cancer Res. 68, 650–656 (2008).
pubmed: 18245463 doi: 10.1158/0008-5472.CAN-07-2491
Verfaillie, A. et al. Decoding the regulatory landscape of melanoma reveals TEADS as regulators of the invasive cell state. Nat. Commun. https://doi.org/10.1038/ncomms7683 (2015).
Widmer, D. S. et al. Systematic classification of melanoma cells by phenotype-specific gene expression mapping. Pigment Cell Melanoma Res. 25, 343–353 (2012).
pubmed: 22336146 doi: 10.1111/j.1755-148X.2012.00986.x
Kawanami, A., Matsushita, T., Chan, Y. Y. & Murakami, S. Mice expressing GFP and CreER in osteochondro progenitor cells in the periosteum. Biochem. Biophys. Res. Commun. 386, 477–482 (2009).
pubmed: 19538944 pmcid: 2742350 doi: 10.1016/j.bbrc.2009.06.059
Boiko, A. D. et al. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 466, 133–137 (2010).
pubmed: 20596026 pmcid: 2898751 doi: 10.1038/nature09161
Roesch, A. et al. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141, 583–594 (2010).
pubmed: 20478252 pmcid: 2882693 doi: 10.1016/j.cell.2010.04.020
Schatton, T. et al. Identification of cells initiating human melanomas. Nature 451, 345–349 (2008).
pubmed: 18202660 pmcid: 3660705 doi: 10.1038/nature06489
Quintana, E. et al. Efficient tumour formation by single human melanoma cells. Nature 456, 593–598 (2008).
pubmed: 19052619 pmcid: 2597380 doi: 10.1038/nature07567
Stemmler, M. P., Eccles, R. L., Brabletz, S. & Brabletz, T. Non-redundant functions of EMT transcription factors. Nat. Cell Biol. 21, 102–112 (2019).
Bosenberg, M. et al. Characterization of melanocyte-specific inducible Cre recombinase transgenic mice. Genesis 44, 262–267 (2006).
pubmed: 16676322 doi: 10.1002/dvg.20205
Krimpenfort, P., Quon, K. C., Mooi, W. J., Loonstra, A. & Berns, A. Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature 413, 83–86 (2001).
pubmed: 11544530 doi: 10.1038/35092584
Dankort, D. et al. Braf
pubmed: 19282848 pmcid: 2705918 doi: 10.1038/ng.356
Maria Bosisio, F. et al. Functional heterogeneity of lymphocytic patterns in primary melanoma dissected through single-cell multiplexing. eLife https://doi.org/10.7554/eLife.53008 (2020).
Susaki, E. A. et al. Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell 157, 726–739 (2014).
pubmed: 24746791 doi: 10.1016/j.cell.2014.03.042
Frankish, A. et al. GENCODE reference annotation for the human and mouse genomes. Nucleic Acids Res. 47, D766–D773 (2019).
pubmed: 30357393 doi: 10.1093/nar/gky955
Yates, A. D. et al. Ensembl 2020. Nucleic Acids Res. 48, D682–D688 (2020).
pubmed: 31691826
Marçais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764–770 (2011).
pubmed: 21217122 pmcid: 3051319 doi: 10.1093/bioinformatics/btr011
Gans, J. D. & Wolinsky, M. Improved assay-dependent searching of nucleic acid sequence databases. Nucleic Acids Res. 36, e74 (2008).
pubmed: 18515842 pmcid: 2475610 doi: 10.1093/nar/gkn301
Rodriguez, J. M. et al. APPRIS 2017: principal isoforms for multiple gene sets. Nucleic Acids Res. 46, D213–D217 (2018).
pubmed: 29069475 doi: 10.1093/nar/gkx997
Bankhead, P. et al. QuPath: open source software for digital pathology image analysis. Sci. Rep. 7, 16878 (2017).
pubmed: 29203879 pmcid: 5715110 doi: 10.1038/s41598-017-17204-5
Schmidt, U., Weigert, M., Broaddus, C. & Myers, G. Cell detection with star-convex polygons. In Proc. Medical Image Computing and Computer Assisted Intervention—MICCAI 2018 (eds Frangi, A. et al.) Vol. 11071, 265–273 (Springer, 2018).
McGinnis, C. S., Murrow, L. M. & Gartner, Z. J. DoubletFinder: doublet detection in single-cell RNA sequencing data using artificial nearest neighbors. Cell Syst. 8, 329–337 (2019).
pubmed: 30954475 pmcid: 6853612 doi: 10.1016/j.cels.2019.03.003
Korsunsky, I. et al. Fast, sensitive and accurate integration of single-cell data with Harmony. Nat. Methods 16, 1289–1296 (2019).
pubmed: 31740819 pmcid: 6884693 doi: 10.1038/s41592-019-0619-0
Rousseeuw, P. J. Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J. Comput. Appl. Math. 20, 53–65 (1987).
doi: 10.1016/0377-0427(87)90125-7
Oren, Y. et al. Cycling cancer persister cells arise from lineages with distinct programs. Nature 596, 576–582 (2021).
pubmed: 34381210 pmcid: 9209846 doi: 10.1038/s41586-021-03796-6
Guzmán, C., Bagga, M., Kaur, A., Westermarck, J. & Abankwa, D. ColonyArea: an ImageJ plugin to automatically quantify colony formation in clonogenic assays. PLoS ONE 9, e92444 (2014).
pubmed: 24647355 pmcid: 3960247 doi: 10.1371/journal.pone.0092444

Auteurs

Panagiotis Karras (P)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Ignacio Bordeu (I)

Department of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, UK.
The Wellcome Trust/CRUK Gurdon Institute, University of Cambridge, Cambridge, UK.
Departamento de Física, Facultad de Ciencias Físicas y Matemáticas, Universidad de Chile, Santiago, Chile.

Joanna Pozniak (J)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Ada Nowosad (A)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Cecilia Pazzi (C)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Nina Van Raemdonck (N)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Ewout Landeloos (E)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Yannick Van Herck (Y)

Department of General Medical Oncology, UZ Leuven, Leuven, Belgium.

Dennis Pedri (D)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Greet Bervoets (G)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Samira Makhzami (S)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Jia Hui Khoo (JH)

BGI-Shenzhen, Shenzhen, China.

Benjamin Pavie (B)

VIB BioImaging Core, VIB Center for Brain and Disease Research, Leuven, Belgium.
VIB Bioimaging Core, VIB Center for Inflammation Research, Ghent, Belgium.
Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium.

Jochen Lamote (J)

FACS Expertise Center, Center for Cancer Biology, VIB, Leuven, Belgium.

Oskar Marin-Bejar (O)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Michael Dewaele (M)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium.
Department of Oncology, KU Leuven, Leuven, Belgium.

Han Liang (H)

BGI-Shenzhen, Shenzhen, China.

Xingju Zhang (X)

BGI-Shenzhen, Shenzhen, China.

Yichao Hua (Y)

Department of Oncology, KU Leuven, Leuven, Belgium.
Laboratory of Tumor Microenvironment and Therapeutic Resistance, Center for Cancer Biology, VIB, Leuven, Belgium.

Jasper Wouters (J)

Center for Brain & Disease Research, VIB-KU Leuven, Leuven, Belgium.
Department of Human Genetics, KU Leuven, Leuven, Belgium.

Robin Browaeys (R)

Data Mining and Modeling for Biomedicine Group, VIB Center for Inflammation Research, Ghent, Belgium.
Department of Applied Mathematics, Computer Science and Statistics, Ghent University, Ghent, Belgium.

Gabriele Bergers (G)

Department of Oncology, KU Leuven, Leuven, Belgium.
Laboratory of Tumor Microenvironment and Therapeutic Resistance, Center for Cancer Biology, VIB, Leuven, Belgium.

Yvan Saeys (Y)

Data Mining and Modeling for Biomedicine Group, VIB Center for Inflammation Research, Ghent, Belgium.
Department of Applied Mathematics, Computer Science and Statistics, Ghent University, Ghent, Belgium.

Francesca Bosisio (F)

Laboratory for Translational Cell and Tissue Research, Department of Imaging and Pathology, KU Leuven, Leuven, Belgium.

Joost van den Oord (J)

Laboratory for Translational Cell and Tissue Research, Department of Imaging and Pathology, KU Leuven, Leuven, Belgium.

Diether Lambrechts (D)

Laboratory of Translational Genetics, Center for Cancer Biology, VIB, Leuven, Belgium.
Laboratory of Translational Genetics, Center for Human Genetics, KU Leuven, Leuven, Belgium.

Anil K Rustgi (AK)

Herbert Irving Comprehensive Center, Columbia University Irving Medical Center, New York, USA.

Oliver Bechter (O)

Department of General Medical Oncology, UZ Leuven, Leuven, Belgium.

Cedric Blanpain (C)

Laboratory of Stem Cells and Cancer, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Benjamin D Simons (BD)

Department of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, UK.
The Wellcome Trust/CRUK Gurdon Institute, University of Cambridge, Cambridge, UK.
Wellcome Trust-MRC Stem Cell Institute, University of Cambridge, Cambridge, UK.

Florian Rambow (F)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium. florian.rambow@kuleuven.vib.be.
Department of Oncology, KU Leuven, Leuven, Belgium. florian.rambow@kuleuven.vib.be.
Department of Applied Computational Cancer Research, Institute for AI in Medicine (IKIM), University Hospital Essen, Essen, Germany. florian.rambow@kuleuven.vib.be.
University Duisburg-Essen, Essen, Germany. florian.rambow@kuleuven.vib.be.
German Cancer Consortium (DKTK), partner site Essen, Essen, Germany. florian.rambow@kuleuven.vib.be.

Jean-Christophe Marine (JC)

Laboratory for Molecular Cancer Biology, Center for Cancer Biology, VIB, Leuven, Belgium. jeanchristophe.marine@kuleuven.vib.be.
Department of Oncology, KU Leuven, Leuven, Belgium. jeanchristophe.marine@kuleuven.vib.be.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH