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A cellular hierarchy in melanoma uncouples growth and metastasis

Panagiotis Karras, Ignacio Bordeu, Joanna Pozniak, Ada Nowosad, Cecilia Pazzi, Nina Van Raemdonck, Ewout Landeloos, Yannick Van Herck, Dennis Pedri, Greet Bervoets, et al.
(2022) NATURE. 610(7930). p.190-198
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Abstract
Although melanoma is notorious for its high degree of heterogeneity and plasticity(1,2), the origin and magnitude of cell-state diversity remains poorly understood. Equally, it is unclear whether growth and metastatic dissemination are supported by overlapping or distinct melanoma subpopulations. Here, by combining mouse genetics, single-cell and spatial transcriptomics, lineage tracing and quantitative modelling, we provide evidence of a hierarchical model of tumour growth that mirrors the cellular and molecular logic underlying the cell-fate specification and differentiation of the embryonic neural crest. We show that tumorigenic competence is associated with a spatially localized perivascular niche, a phenotype acquired through an intercellular communication pathway established by endothelial cells. Consistent with a model in which only a fraction of cells are fated to fuel growth, temporal single-cell tracing of a population of melanoma cells with a mesenchymal-like state revealed that these cells do not contribute to primary tumour growth but, instead, constitute a pool of metastatic initiating cells that switch cell identity while disseminating to secondary organs. Our data provide a spatially and temporally resolved map of the diversity and trajectories of melanoma cell states and suggest that the ability to support growth and metastasis are limited to distinct pools of cells. The observation that these phenotypic competencies can be dynamically acquired after exposure to specific niche signals warrant the development of therapeutic strategies that interfere with the cancer cell reprogramming activity of such microenvironmental cues.
Keywords
CELLS, EXPRESSION, DIVERSITY, STATES

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MLA
Karras, Panagiotis, et al. “A Cellular Hierarchy in Melanoma Uncouples Growth and Metastasis.” NATURE, vol. 610, no. 7930, 2022, pp. 190–98, doi:10.1038/s41586-022-05242-7.
APA
Karras, P., Bordeu, I., Pozniak, J., Nowosad, A., Pazzi, C., Van Raemdonck, N., … Marine, J.-C. (2022). A cellular hierarchy in melanoma uncouples growth and metastasis. NATURE, 610(7930), 190–198. https://doi.org/10.1038/s41586-022-05242-7
Chicago author-date
Karras, Panagiotis, Ignacio Bordeu, Joanna Pozniak, Ada Nowosad, Cecilia Pazzi, Nina Van Raemdonck, Ewout Landeloos, et al. 2022. “A Cellular Hierarchy in Melanoma Uncouples Growth and Metastasis.” NATURE 610 (7930): 190–98. https://doi.org/10.1038/s41586-022-05242-7.
Chicago author-date (all authors)
Karras, Panagiotis, Ignacio Bordeu, Joanna Pozniak, Ada Nowosad, Cecilia Pazzi, Nina Van Raemdonck, Ewout Landeloos, Yannick Van Herck, Dennis Pedri, Greet Bervoets, Samira Makhzami, Jia Hui Khoo, Benjamin Pavie, Jochen Lamote, Oskar Marin-Bejar, Michael Dewaele, Han Liang, Xingju Zhang, Yichao Hua, Jasper Wouters, Robin Browaeys, Gabriele Bergers, Yvan Saeys, Francesca Bosisio, Joost van den Oord, Diether Lambrechts, Anil K. Rustgi, Oliver Bechter, Cedric Blanpain, Benjamin D. Simons, Florian Rambow, and Jean-Christophe Marine. 2022. “A Cellular Hierarchy in Melanoma Uncouples Growth and Metastasis.” NATURE 610 (7930): 190–198. doi:10.1038/s41586-022-05242-7.
Vancouver
1.
Karras P, Bordeu I, Pozniak J, Nowosad A, Pazzi C, Van Raemdonck N, et al. A cellular hierarchy in melanoma uncouples growth and metastasis. NATURE. 2022;610(7930):190–8.
IEEE
[1]
P. Karras et al., “A cellular hierarchy in melanoma uncouples growth and metastasis,” NATURE, vol. 610, no. 7930, pp. 190–198, 2022.
@article{8771129,
  abstract     = {{Although melanoma is notorious for its high degree of heterogeneity and plasticity(1,2), the origin and magnitude of cell-state diversity remains poorly understood. Equally, it is unclear whether growth and metastatic dissemination are supported by overlapping or distinct melanoma subpopulations. Here, by combining mouse genetics, single-cell and spatial transcriptomics, lineage tracing and quantitative modelling, we provide evidence of a hierarchical model of tumour growth that mirrors the cellular and molecular logic underlying the cell-fate specification and differentiation of the embryonic neural crest. We show that tumorigenic competence is associated with a spatially localized perivascular niche, a phenotype acquired through an intercellular communication pathway established by endothelial cells. Consistent with a model in which only a fraction of cells are fated to fuel growth, temporal single-cell tracing of a population of melanoma cells with a mesenchymal-like state revealed that these cells do not contribute to primary tumour growth but, instead, constitute a pool of metastatic initiating cells that switch cell identity while disseminating to secondary organs. Our data provide a spatially and temporally resolved map of the diversity and trajectories of melanoma cell states and suggest that the ability to support growth and metastasis are limited to distinct pools of cells. The observation that these phenotypic competencies can be dynamically acquired after exposure to specific niche signals warrant the development of therapeutic strategies that interfere with the cancer cell reprogramming activity of such microenvironmental cues.}},
  author       = {{Karras, Panagiotis and Bordeu, Ignacio and Pozniak, Joanna and Nowosad, Ada and Pazzi, Cecilia and Van Raemdonck, Nina and Landeloos, Ewout and Van Herck, Yannick and Pedri, Dennis and Bervoets, Greet and Makhzami, Samira and Khoo, Jia Hui and Pavie, Benjamin and Lamote, Jochen and Marin-Bejar, Oskar and Dewaele, Michael and Liang, Han and Zhang, Xingju and Hua, Yichao and Wouters, Jasper and Browaeys, Robin and Bergers, Gabriele and Saeys, Yvan and Bosisio, Francesca and van den Oord, Joost and Lambrechts, Diether and Rustgi, Anil K. and Bechter, Oliver and Blanpain, Cedric and Simons, Benjamin D. and Rambow, Florian and Marine, Jean-Christophe}},
  issn         = {{0028-0836}},
  journal      = {{NATURE}},
  keywords     = {{CELLS,EXPRESSION,DIVERSITY,STATES}},
  language     = {{eng}},
  number       = {{7930}},
  pages        = {{190--198}},
  title        = {{A cellular hierarchy in melanoma uncouples growth and metastasis}},
  url          = {{http://doi.org/10.1038/s41586-022-05242-7}},
  volume       = {{610}},
  year         = {{2022}},
}
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