Genome-level selection in tumors as a universal marker of resistance to therapy

Abstract Tumor evolution is shaped by selective pressures imposed by physiological factors as the tumor naturally progresses to colonize local and distant tissues, as well as by therapy. However, the distinction between these two types of pressures and their impact on tumor evolution remain elusive,...

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Main Authors: Erez Persi, Praneeth R. Sudalagunta, Yuri I. Wolf, Rafael R. Canevarolo, Mehdi Damaghi, Kenneth H. Shain, Ariosto S. Silva, Eugene V. Koonin
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-61709-x
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author Erez Persi
Praneeth R. Sudalagunta
Yuri I. Wolf
Rafael R. Canevarolo
Mehdi Damaghi
Kenneth H. Shain
Ariosto S. Silva
Eugene V. Koonin
author_facet Erez Persi
Praneeth R. Sudalagunta
Yuri I. Wolf
Rafael R. Canevarolo
Mehdi Damaghi
Kenneth H. Shain
Ariosto S. Silva
Eugene V. Koonin
author_sort Erez Persi
collection DOAJ
description Abstract Tumor evolution is shaped by selective pressures imposed by physiological factors as the tumor naturally progresses to colonize local and distant tissues, as well as by therapy. However, the distinction between these two types of pressures and their impact on tumor evolution remain elusive, mainly, due to extensive intra-tumor heterogeneity. To disentangle the effects of these selective pressures, we analyze data from diverse cohorts of patients, of both treated and untreated cancers. We find that, despite the wide variation across patients, the selection strength on tumor genomes in individual patients is stable and largely unaffected by tumor progression in the primary settings, with some cancer-specific signatures detectable in the progression to metastases. However, we identify a nearly universal shift toward neutral evolution in tumors that resist treatment and demonstrate that this regime is associated with worse prognosis. We validate these findings on both published and original datasets. We suggest that monitoring the selection regime during cancer treatment can assist clinical decision-making in many cases.
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publisher Nature Portfolio
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series Nature Communications
spelling doaj-art-8ed8ac8f67874300a0c858f476ad75c52025-08-20T03:43:11ZengNature PortfolioNature Communications2041-17232025-07-0116111510.1038/s41467-025-61709-xGenome-level selection in tumors as a universal marker of resistance to therapyErez Persi0Praneeth R. Sudalagunta1Yuri I. Wolf2Rafael R. Canevarolo3Mehdi Damaghi4Kenneth H. Shain5Ariosto S. Silva6Eugene V. Koonin7Computational Biology Branch, Division of Intramural Research, National Library of Medicine, National Institutes of HealthDepartment of Metabolism and Physiology, H. Lee Moffitt Cancer Center and Research InstituteComputational Biology Branch, Division of Intramural Research, National Library of Medicine, National Institutes of HealthDepartment of Metabolism and Physiology, H. Lee Moffitt Cancer Center and Research InstituteDepartment of Pathology, School of Medicine, Stony Brook UniversityDepartments of Malignant Hematology and Molecular Medicine, H. Lee Moffitt Cancer Center and Research InstituteDepartment of Metabolism and Physiology, H. Lee Moffitt Cancer Center and Research InstituteComputational Biology Branch, Division of Intramural Research, National Library of Medicine, National Institutes of HealthAbstract Tumor evolution is shaped by selective pressures imposed by physiological factors as the tumor naturally progresses to colonize local and distant tissues, as well as by therapy. However, the distinction between these two types of pressures and their impact on tumor evolution remain elusive, mainly, due to extensive intra-tumor heterogeneity. To disentangle the effects of these selective pressures, we analyze data from diverse cohorts of patients, of both treated and untreated cancers. We find that, despite the wide variation across patients, the selection strength on tumor genomes in individual patients is stable and largely unaffected by tumor progression in the primary settings, with some cancer-specific signatures detectable in the progression to metastases. However, we identify a nearly universal shift toward neutral evolution in tumors that resist treatment and demonstrate that this regime is associated with worse prognosis. We validate these findings on both published and original datasets. We suggest that monitoring the selection regime during cancer treatment can assist clinical decision-making in many cases.https://doi.org/10.1038/s41467-025-61709-x
spellingShingle Erez Persi
Praneeth R. Sudalagunta
Yuri I. Wolf
Rafael R. Canevarolo
Mehdi Damaghi
Kenneth H. Shain
Ariosto S. Silva
Eugene V. Koonin
Genome-level selection in tumors as a universal marker of resistance to therapy
Nature Communications
title Genome-level selection in tumors as a universal marker of resistance to therapy
title_full Genome-level selection in tumors as a universal marker of resistance to therapy
title_fullStr Genome-level selection in tumors as a universal marker of resistance to therapy
title_full_unstemmed Genome-level selection in tumors as a universal marker of resistance to therapy
title_short Genome-level selection in tumors as a universal marker of resistance to therapy
title_sort genome level selection in tumors as a universal marker of resistance to therapy
url https://doi.org/10.1038/s41467-025-61709-x
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