The theory of massively repeated evolution and full identifications of cancer-driving nucleotides (CDNs)

Tumorigenesis, like most complex genetic traits, is driven by the joint actions of many mutations. At the nucleotide level, such mutations are cancer-driving nucleotides (CDNs). The full sets of CDNs are necessary, and perhaps even sufficient, for the understanding and treatment of each cancer patie...

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Main Authors: Lingjie Zhang, Tong Deng, Zhongqi Liufu, Xueyu Liu, Bingjie Chen, Zheng Hu, Chenli Liu, Miles E Tracy, Xuemei Lu, Hai-Jun Wen, Chung-I Wu
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
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Online Access:https://elifesciences.org/articles/99340
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author Lingjie Zhang
Tong Deng
Zhongqi Liufu
Xueyu Liu
Bingjie Chen
Zheng Hu
Chenli Liu
Miles E Tracy
Xuemei Lu
Hai-Jun Wen
Chung-I Wu
author_facet Lingjie Zhang
Tong Deng
Zhongqi Liufu
Xueyu Liu
Bingjie Chen
Zheng Hu
Chenli Liu
Miles E Tracy
Xuemei Lu
Hai-Jun Wen
Chung-I Wu
author_sort Lingjie Zhang
collection DOAJ
description Tumorigenesis, like most complex genetic traits, is driven by the joint actions of many mutations. At the nucleotide level, such mutations are cancer-driving nucleotides (CDNs). The full sets of CDNs are necessary, and perhaps even sufficient, for the understanding and treatment of each cancer patient. Currently, only a small fraction of CDNs is known as most mutations accrued in tumors are not drivers. We now develop the theory of CDNs on the basis that cancer evolution is massively repeated in millions of individuals. Hence, any advantageous mutation should recur frequently and, conversely, any mutation that does not is either a passenger or deleterious mutation. In the TCGA cancer database (sample size n=300–1000), point mutations may recur in i out of n patients. This study explores a wide range of mutation characteristics to determine the limit of recurrences (i*) driven solely by neutral evolution. Since no neutral mutation can reach i*=3, all mutations recurring at i≥3 are CDNs. The theory shows the feasibility of identifying almost all CDNs if n increases to 100,000 for each cancer type. At present, only <10% of CDNs have been identified. When the full sets of CDNs are identified, the evolutionary mechanism of tumorigenesis in each case can be known and, importantly, gene targeted therapy will be far more effective in treatment and robust against drug resistance.
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spelling doaj-art-17c84fcf8253415d97b5a9761f06d7eb2025-08-20T02:49:39ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.99340The theory of massively repeated evolution and full identifications of cancer-driving nucleotides (CDNs)Lingjie Zhang0https://orcid.org/0000-0002-6506-4457Tong Deng1Zhongqi Liufu2Xueyu Liu3Bingjie Chen4Zheng Hu5https://orcid.org/0000-0003-1552-0060Chenli Liu6Miles E Tracy7Xuemei Lu8https://orcid.org/0000-0001-6044-6002Hai-Jun Wen9https://orcid.org/0000-0001-8676-1254Chung-I Wu10https://orcid.org/0000-0001-7263-4238State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China; State Key Laboratory of Genetic Resources and Evolution/Yunnan Key Laboratory of Biodiversity Information, Kunming Institute of Zoology, The Chinese Academy of Sciences, Kunming, ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China; GMU-GIBH Joint School of Life Sciences, Guangzhou Medical University, Guangzhou, ChinaCAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Genetic Resources and Evolution/Yunnan Key Laboratory of Biodiversity Information, Kunming Institute of Zoology, The Chinese Academy of Sciences, Kunming, ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China; Innovation Center for Evolutionary Synthetic Biology, Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China; Innovation Center for Evolutionary Synthetic Biology, Sun Yat-sen University, Guangzhou, China; Department of Ecology and Evolution, University of Chicago, Chicago, United StatesTumorigenesis, like most complex genetic traits, is driven by the joint actions of many mutations. At the nucleotide level, such mutations are cancer-driving nucleotides (CDNs). The full sets of CDNs are necessary, and perhaps even sufficient, for the understanding and treatment of each cancer patient. Currently, only a small fraction of CDNs is known as most mutations accrued in tumors are not drivers. We now develop the theory of CDNs on the basis that cancer evolution is massively repeated in millions of individuals. Hence, any advantageous mutation should recur frequently and, conversely, any mutation that does not is either a passenger or deleterious mutation. In the TCGA cancer database (sample size n=300–1000), point mutations may recur in i out of n patients. This study explores a wide range of mutation characteristics to determine the limit of recurrences (i*) driven solely by neutral evolution. Since no neutral mutation can reach i*=3, all mutations recurring at i≥3 are CDNs. The theory shows the feasibility of identifying almost all CDNs if n increases to 100,000 for each cancer type. At present, only <10% of CDNs have been identified. When the full sets of CDNs are identified, the evolutionary mechanism of tumorigenesis in each case can be known and, importantly, gene targeted therapy will be far more effective in treatment and robust against drug resistance.https://elifesciences.org/articles/99340cancer evolutioncancer driverspoint mutations
spellingShingle Lingjie Zhang
Tong Deng
Zhongqi Liufu
Xueyu Liu
Bingjie Chen
Zheng Hu
Chenli Liu
Miles E Tracy
Xuemei Lu
Hai-Jun Wen
Chung-I Wu
The theory of massively repeated evolution and full identifications of cancer-driving nucleotides (CDNs)
eLife
cancer evolution
cancer drivers
point mutations
title The theory of massively repeated evolution and full identifications of cancer-driving nucleotides (CDNs)
title_full The theory of massively repeated evolution and full identifications of cancer-driving nucleotides (CDNs)
title_fullStr The theory of massively repeated evolution and full identifications of cancer-driving nucleotides (CDNs)
title_full_unstemmed The theory of massively repeated evolution and full identifications of cancer-driving nucleotides (CDNs)
title_short The theory of massively repeated evolution and full identifications of cancer-driving nucleotides (CDNs)
title_sort theory of massively repeated evolution and full identifications of cancer driving nucleotides cdns
topic cancer evolution
cancer drivers
point mutations
url https://elifesciences.org/articles/99340
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