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The impact of food availability on tumorigenesis is evolutionarily conserved

The inability to control cell proliferation results in the formation of tumors in many multicellular lineages. Nonetheless, little is known about the extent of conservation of the biological traits and ecological factors that promote or inhibit tumorigenesis across the metazoan tree. Particularly, c...

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Autores principales: Tissot, Sophie, Guimard, Lena, Meliani, Jordan, Boutry, Justine, Dujon, Antoine M., Capp, Jean-Pascal, Tökölyi, Jácint, Biro, Peter A., Beckmann, Christa, Fontenille, Laura, Do Khoa, Nam, Hamede, Rodrigo, Roche, Benjamin, Ujvari, Beata, Nedelcu, Aurora M., Thomas, Frédéric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10645767/
https://www.ncbi.nlm.nih.gov/pubmed/37963956
http://dx.doi.org/10.1038/s41598-023-46896-1
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author Tissot, Sophie
Guimard, Lena
Meliani, Jordan
Boutry, Justine
Dujon, Antoine M.
Capp, Jean-Pascal
Tökölyi, Jácint
Biro, Peter A.
Beckmann, Christa
Fontenille, Laura
Do Khoa, Nam
Hamede, Rodrigo
Roche, Benjamin
Ujvari, Beata
Nedelcu, Aurora M.
Thomas, Frédéric
author_facet Tissot, Sophie
Guimard, Lena
Meliani, Jordan
Boutry, Justine
Dujon, Antoine M.
Capp, Jean-Pascal
Tökölyi, Jácint
Biro, Peter A.
Beckmann, Christa
Fontenille, Laura
Do Khoa, Nam
Hamede, Rodrigo
Roche, Benjamin
Ujvari, Beata
Nedelcu, Aurora M.
Thomas, Frédéric
author_sort Tissot, Sophie
collection PubMed
description The inability to control cell proliferation results in the formation of tumors in many multicellular lineages. Nonetheless, little is known about the extent of conservation of the biological traits and ecological factors that promote or inhibit tumorigenesis across the metazoan tree. Particularly, changes in food availability have been linked to increased cancer incidence in humans, as an outcome of evolutionary mismatch. Here, we apply evolutionary oncology principles to test whether food availability, regardless of the multicellular lineage considered, has an impact on tumorigenesis. We used two phylogenetically unrelated model systems, the cnidarian Hydra oligactis and the fish Danio rerio, to investigate the impact of resource availability on tumor occurrence and progression. Individuals from healthy and tumor-prone lines were placed on four diets that differed in feeding frequency and quantity. For both models, frequent overfeeding favored tumor emergence, while lean diets appeared more protective. In terms of tumor progression, high food availability promoted it, whereas low resources controlled it, but without having a curative effect. We discuss our results in light of current ideas about the possible conservation of basic processes governing cancer in metazoans (including ancestral life history trade-offs at the cell level) and in the framework of evolutionary medicine.
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spelling pubmed-106457672023-11-14 The impact of food availability on tumorigenesis is evolutionarily conserved Tissot, Sophie Guimard, Lena Meliani, Jordan Boutry, Justine Dujon, Antoine M. Capp, Jean-Pascal Tökölyi, Jácint Biro, Peter A. Beckmann, Christa Fontenille, Laura Do Khoa, Nam Hamede, Rodrigo Roche, Benjamin Ujvari, Beata Nedelcu, Aurora M. Thomas, Frédéric Sci Rep Article The inability to control cell proliferation results in the formation of tumors in many multicellular lineages. Nonetheless, little is known about the extent of conservation of the biological traits and ecological factors that promote or inhibit tumorigenesis across the metazoan tree. Particularly, changes in food availability have been linked to increased cancer incidence in humans, as an outcome of evolutionary mismatch. Here, we apply evolutionary oncology principles to test whether food availability, regardless of the multicellular lineage considered, has an impact on tumorigenesis. We used two phylogenetically unrelated model systems, the cnidarian Hydra oligactis and the fish Danio rerio, to investigate the impact of resource availability on tumor occurrence and progression. Individuals from healthy and tumor-prone lines were placed on four diets that differed in feeding frequency and quantity. For both models, frequent overfeeding favored tumor emergence, while lean diets appeared more protective. In terms of tumor progression, high food availability promoted it, whereas low resources controlled it, but without having a curative effect. We discuss our results in light of current ideas about the possible conservation of basic processes governing cancer in metazoans (including ancestral life history trade-offs at the cell level) and in the framework of evolutionary medicine. Nature Publishing Group UK 2023-11-14 /pmc/articles/PMC10645767/ /pubmed/37963956 http://dx.doi.org/10.1038/s41598-023-46896-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Tissot, Sophie
Guimard, Lena
Meliani, Jordan
Boutry, Justine
Dujon, Antoine M.
Capp, Jean-Pascal
Tökölyi, Jácint
Biro, Peter A.
Beckmann, Christa
Fontenille, Laura
Do Khoa, Nam
Hamede, Rodrigo
Roche, Benjamin
Ujvari, Beata
Nedelcu, Aurora M.
Thomas, Frédéric
The impact of food availability on tumorigenesis is evolutionarily conserved
title The impact of food availability on tumorigenesis is evolutionarily conserved
title_full The impact of food availability on tumorigenesis is evolutionarily conserved
title_fullStr The impact of food availability on tumorigenesis is evolutionarily conserved
title_full_unstemmed The impact of food availability on tumorigenesis is evolutionarily conserved
title_short The impact of food availability on tumorigenesis is evolutionarily conserved
title_sort impact of food availability on tumorigenesis is evolutionarily conserved
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10645767/
https://www.ncbi.nlm.nih.gov/pubmed/37963956
http://dx.doi.org/10.1038/s41598-023-46896-1
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