Parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomas

Abstract Cancer development requires an evolutionary transformation from mammalian cells fully regulated by and integrated into multicellular tissue to cancer cells  that, as single cell protists, are individually subject to Darwinian selection. Through genetic and epigenetic mechanisms of inheritan...

Full description

Saved in:
Bibliographic Details
Main Authors: Robert A. Gatenby, Jamie K. Teer, Kenneth Y. Tsai, Joel S. Brown
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-08123-7
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849730850113978368
author Robert A. Gatenby
Jamie K. Teer
Kenneth Y. Tsai
Joel S. Brown
author_facet Robert A. Gatenby
Jamie K. Teer
Kenneth Y. Tsai
Joel S. Brown
author_sort Robert A. Gatenby
collection DOAJ
description Abstract Cancer development requires an evolutionary transformation from mammalian cells fully regulated by and integrated into multicellular tissue to cancer cells  that, as single cell protists, are individually subject to Darwinian selection. Through genetic and epigenetic mechanisms of inheritance, the evolving cancer phenotype must acquire independence from host controls, downregulate differentiated functions that benefit the host but not individual cells, and generate phenotypic traits that increase fitness in the context of the selection forces within the local microenvironment. Here, we investigate this  evolutionary transition in breast (BRCA) and lung (LUAD, without EGFR, KRAS or BRAF driver mutations) adenocarcinomas using bulk mutation and expression data from the TCGA database. We define evolution selection for genes and molecular pathways based on 1) changes in gene expression compared to normal tissue, and 2) significantly larger or smaller observed mutation rates compared to those expected based on the gene size. We find BRCA and LUAD disable different genes and gene pathways associated with tissue-specific signaling and differentiated functions but promote common molecular pathways associated with cell cycle, cell-cell interactions, cytoskeleton, voltage gated ion channels, and microenvironmental niche construction. Thus, tissue-specific parallel evolution in early cancer development is followed by convergence to a common cancer phenotype.
format Article
id doaj-art-bb19bbb120814bfd998a03eef3c73afb
institution DOAJ
issn 2399-3642
language English
publishDate 2025-05-01
publisher Nature Portfolio
record_format Article
series Communications Biology
spelling doaj-art-bb19bbb120814bfd998a03eef3c73afb2025-08-20T03:08:44ZengNature PortfolioCommunications Biology2399-36422025-05-018111410.1038/s42003-025-08123-7Parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomasRobert A. Gatenby0Jamie K. Teer1Kenneth Y. Tsai2Joel S. Brown3Cancer Biology and Evolution ProgramBiostatistics and Bioinformatics DepartmentCancer Biology and Evolution ProgramCancer Biology and Evolution ProgramAbstract Cancer development requires an evolutionary transformation from mammalian cells fully regulated by and integrated into multicellular tissue to cancer cells  that, as single cell protists, are individually subject to Darwinian selection. Through genetic and epigenetic mechanisms of inheritance, the evolving cancer phenotype must acquire independence from host controls, downregulate differentiated functions that benefit the host but not individual cells, and generate phenotypic traits that increase fitness in the context of the selection forces within the local microenvironment. Here, we investigate this  evolutionary transition in breast (BRCA) and lung (LUAD, without EGFR, KRAS or BRAF driver mutations) adenocarcinomas using bulk mutation and expression data from the TCGA database. We define evolution selection for genes and molecular pathways based on 1) changes in gene expression compared to normal tissue, and 2) significantly larger or smaller observed mutation rates compared to those expected based on the gene size. We find BRCA and LUAD disable different genes and gene pathways associated with tissue-specific signaling and differentiated functions but promote common molecular pathways associated with cell cycle, cell-cell interactions, cytoskeleton, voltage gated ion channels, and microenvironmental niche construction. Thus, tissue-specific parallel evolution in early cancer development is followed by convergence to a common cancer phenotype.https://doi.org/10.1038/s42003-025-08123-7
spellingShingle Robert A. Gatenby
Jamie K. Teer
Kenneth Y. Tsai
Joel S. Brown
Parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomas
Communications Biology
title Parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomas
title_full Parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomas
title_fullStr Parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomas
title_full_unstemmed Parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomas
title_short Parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomas
title_sort parallel and convergent dynamics in the evolution of primary breast and lung adenocarcinomas
url https://doi.org/10.1038/s42003-025-08123-7
work_keys_str_mv AT robertagatenby parallelandconvergentdynamicsintheevolutionofprimarybreastandlungadenocarcinomas
AT jamiekteer parallelandconvergentdynamicsintheevolutionofprimarybreastandlungadenocarcinomas
AT kennethytsai parallelandconvergentdynamicsintheevolutionofprimarybreastandlungadenocarcinomas
AT joelsbrown parallelandconvergentdynamicsintheevolutionofprimarybreastandlungadenocarcinomas