Ultra-Sensitive TP53 Sequencing for Cancer Detection Reveals Progressive Clonal Selection in Normal Tissue over a Century of Human Lifespan
High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to i...
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| Published in | Cell reports (Cambridge) Vol. 28; no. 1; pp. 132 - 144.e3 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
02.07.2019
Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to identify TP53 mutations in uterine lavage. However, in addition to tumor DNA, we also detect low-frequency TP53 mutations in nearly all lavages from women with and without cancer. These mutations increase with age and share the selection traits of clonal TP53 mutations commonly found in human tumors. We show that low-frequency TP53 mutations exist in multiple healthy tissues, from newborn to centenarian, and progressively increase in abundance and pathogenicity with older age across tissue types. Our results illustrate that subclonal cancer evolutionary processes are a ubiquitous part of normal human aging, and great care must be taken to distinguish tumor-derived from age-associated mutations in high-sensitivity clinical cancer diagnostics.
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•Ovarian cancer can be detected by ultra-accurate sequencing of uterine lavage DNA•However, low-frequency TP53 mutations also exist in normal tissue of healthy women•TP53 mutations are increasingly selected for with age, revealing somatic evolution•Age-associated, cancer-like mutations challenge specificity for cancer detection
Salk et al. demonstrate that ultra-sensitive DNA sequencing to identify TP53 mutations among cells shed into uterine fluid shows potential for minimally invasive ovarian cancer detection. Yet they also reveal ubiquitous age-related accumulations of cancer-like TP53 mutations in the normal tissues of healthy women. This highlights an important challenge of using tumor driver mutations for cancer screening. |
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| AbstractList | High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to identify TP53 mutations in uterine lavage. However, in addition to tumor DNA, we also detect low-frequency TP53 mutations in nearly all lavages from women with and without cancer. These mutations increase with age and share the selection traits of clonal TP53 mutations commonly found in human tumors. We show that low-frequency TP53 mutations exist in multiple healthy tissues, from newborn to centenarian, and progressively increase in abundance and pathogenicity with older age across tissue types. Our results illustrate that subclonal cancer evolutionary processes are a ubiquitous part of normal human aging, and great care must be taken to distinguish tumor-derived from age-associated mutations in high-sensitivity clinical cancer diagnostics. : Salk et al. demonstrate that ultra-sensitive DNA sequencing to identify TP53 mutations among cells shed into uterine fluid shows potential for minimally invasive ovarian cancer detection. Yet they also reveal ubiquitous age-related accumulations of cancer-like TP53 mutations in the normal tissues of healthy women. This highlights an important challenge of using tumor driver mutations for cancer screening. Keywords: Duplex Sequencing, next-generation sequencing, TP53, clonal evolution, early detection, somatic mutations, high-grade serous ovarian cancer, uterine lavage, aging, gynecologic oncology High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to identify TP53 mutations in uterine lavage. However, in addition to tumor DNA, we also detect low-frequency TP53 mutations in nearly all lavages from women with and without cancer. These mutations increase with age and share the selection traits of clonal TP53 mutations commonly found in human tumors. We show that low-frequency TP53 mutations exist in multiple healthy tissues, from newborn to centenarian, and progressively increase in abundance and pathogenicity with older age across tissue types. Our results illustrate that subclonal cancer evolutionary processes are a ubiquitous part of normal human aging, and great care must be taken to distinguish tumor-derived from age-associated mutations in high-sensitivity clinical cancer diagnostics. [Display omitted] •Ovarian cancer can be detected by ultra-accurate sequencing of uterine lavage DNA•However, low-frequency TP53 mutations also exist in normal tissue of healthy women•TP53 mutations are increasingly selected for with age, revealing somatic evolution•Age-associated, cancer-like mutations challenge specificity for cancer detection Salk et al. demonstrate that ultra-sensitive DNA sequencing to identify TP53 mutations among cells shed into uterine fluid shows potential for minimally invasive ovarian cancer detection. Yet they also reveal ubiquitous age-related accumulations of cancer-like TP53 mutations in the normal tissues of healthy women. This highlights an important challenge of using tumor driver mutations for cancer screening. High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to identify TP53 mutations in uterine lavage. However, in addition to tumor DNA, we also detect low-frequency TP53 mutations in nearly all lavages from women with and without cancer. These mutations increase with age and share the selection traits of clonal TP53 mutations commonly found in human tumors. We show that low-frequency TP53 mutations exist in multiple healthy tissues, from newborn to centenarian, and progressively increase in abundance and pathogenicity with older age across tissue types. Our results illustrate that subclonal cancer evolutionary processes are a ubiquitous part of normal human aging, and great care must be taken to distinguish tumor-derived from age-associated mutations in high-sensitivity clinical cancer diagnostics. Salk et al. demonstrate that ultra-sensitive DNA sequencing to identify TP53 mutations among cells shed into uterine fluid shows potential for minimally invasive ovarian cancer detection. Yet they also reveal ubiquitous age-related accumulations of cancer-like TP53 mutations in the normal tissues of healthy women. This highlights an important challenge of using tumor driver mutations for cancer screening. High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to identify TP53 mutations in uterine lavage. However, in addition to tumor DNA, we also detect low-frequency TP53 mutations in nearly all lavages from women with and without cancer. These mutations increase with age and share the selection traits of clonal TP53 mutations commonly found in human tumors. We show that low-frequency TP53 mutations exist in multiple healthy tissues, from newborn to centenarian, and progressively increase in abundance and pathogenicity with older age across tissue types. Our results illustrate that subclonal cancer evolutionary processes are a ubiquitous part of normal human aging, and great care must be taken to distinguish tumor-derived from age-associated mutations in high-sensitivity clinical cancer diagnostics. High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to identify TP53 mutations in uterine lavage. However, in addition to tumor DNA, we also detect low-frequency TP53 mutations in nearly all lavages from women with and without cancer. These mutations increase with age and share the selection traits of clonal TP53 mutations commonly found in human tumors. We show that low-frequency TP53 mutations exist in multiple healthy tissues, from newborn to centenarian, and progressively increase in abundance and pathogenicity with older age across tissue types. Our results illustrate that subclonal cancer evolutionary processes are a ubiquitous part of normal human aging, and great care must be taken to distinguish tumor-derived from age-associated mutations in high-sensitivity clinical cancer diagnostics.High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to identify TP53 mutations in uterine lavage. However, in addition to tumor DNA, we also detect low-frequency TP53 mutations in nearly all lavages from women with and without cancer. These mutations increase with age and share the selection traits of clonal TP53 mutations commonly found in human tumors. We show that low-frequency TP53 mutations exist in multiple healthy tissues, from newborn to centenarian, and progressively increase in abundance and pathogenicity with older age across tissue types. Our results illustrate that subclonal cancer evolutionary processes are a ubiquitous part of normal human aging, and great care must be taken to distinguish tumor-derived from age-associated mutations in high-sensitivity clinical cancer diagnostics. High-accuracy next-generation DNA sequencing promises a paradigm shift in early cancer detection by enabling the identification of mutant cancer molecules in minimally invasive body fluid samples. We demonstrate 80% sensitivity for ovarian cancer detection using ultra-accurate Duplex Sequencing to identify TP53 mutations in uterine lavage. However, in addition to tumor DNA, we also detect low-frequency TP53 mutations in nearly all lavages from women with and without cancer. These mutations increase with age and share the selection traits of clonal TP53 mutations commonly found in human tumors. We show that low-frequency TP53 mutations exist in multiple healthy tissues, from newborn to centenarian, and progressively increase in abundance and pathogenicity with older age across tissue types. Our results illustrate that subclonal cancer evolutionary processes are a ubiquitous part of normal human aging, and great care must be taken to distinguish tumor-derived from age-associated mutations in high-sensitivity clinical cancer diagnostics. |
| Author | Loubet-Senear, Kaitlyn Vanderstichele, Adriaan Emond, Mary J. Horvat, Reinhard Loeb, Lawrence A. Zeillinger, Robert Salk, Jesse J. Higgins, Jacob E. Risques, Rosa Ana Baker, Kathryn T. Maritschnegg, Elisabeth Valentine, Charles C. Soussi, Thierry Williams, Lindsey N. Loter, Emily Tretiakova, Maria Speiser, Paul Nachmanson, Daniela |
| AuthorAffiliation | 1 Department of Medicine, Division of Medical Oncology, University of Washington, Seattle, WA 98195, USA 5 Department of Pathology, Medical University of Vienna, Vienna, Austria 6 Department of Gynecologic Oncology, Leuven Cancer Institute, University Hospitals Leuven, Katholieke Universiteit, Leuven, Belgium 8 Department of Pathology, Seattle Children’s Hospital, Seattle, WA 98105, USA 14 Present address: Bioinformatics and Systems Biology Graduate Program, University of California, San Diego, La Jolla, CA, USA 12 Present address: Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, USA 7 Department of Statistics, University of Washington, Seattle, WA 98195, USA 3 Department of Pathology, University of Washington, Seattle, WA 98195, USA 9 Sorbonne Université, UPMC Université Paris 06, 75005 Paris, France 10 Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden 2 TwinStrand Biosciences, Seattle, WA 98121, USA 13 Present address: VIB-KU Leuven Cente |
| AuthorAffiliation_xml | – name: 16 Lead Contact – name: 4 Molecular Oncology Group, Department of Obstetrics and Gynecology, Comprehensive Cancer Center-Gynecologic Cancer Unit, Medical University of Vienna, Vienna, Austria – name: 10 Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden – name: 12 Present address: Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, USA – name: 2 TwinStrand Biosciences, Seattle, WA 98121, USA – name: 13 Present address: VIB-KU Leuven Center for Brain and Disease Research, Leuven, Belgium – name: 11 INSERM, U1138, Centre de Recherche des Cordeliers, Paris, France – name: 6 Department of Gynecologic Oncology, Leuven Cancer Institute, University Hospitals Leuven, Katholieke Universiteit, Leuven, Belgium – name: 9 Sorbonne Université, UPMC Université Paris 06, 75005 Paris, France – name: 15 Present address: Knight Cancer Institute, Oregon Health and Science University, Portland, OR, USA – name: 3 Department of Pathology, University of Washington, Seattle, WA 98195, USA – name: 8 Department of Pathology, Seattle Children’s Hospital, Seattle, WA 98105, USA – name: 1 Department of Medicine, Division of Medical Oncology, University of Washington, Seattle, WA 98195, USA – name: 7 Department of Statistics, University of Washington, Seattle, WA 98195, USA – name: 14 Present address: Bioinformatics and Systems Biology Graduate Program, University of California, San Diego, La Jolla, CA, USA – name: 5 Department of Pathology, Medical University of Vienna, Vienna, Austria |
| Author_xml | – sequence: 1 givenname: Jesse J. surname: Salk fullname: Salk, Jesse J. organization: Department of Medicine, Division of Medical Oncology, University of Washington, Seattle, WA 98195, USA – sequence: 2 givenname: Kaitlyn surname: Loubet-Senear fullname: Loubet-Senear, Kaitlyn organization: Department of Pathology, University of Washington, Seattle, WA 98195, USA – sequence: 3 givenname: Elisabeth surname: Maritschnegg fullname: Maritschnegg, Elisabeth organization: Molecular Oncology Group, Department of Obstetrics and Gynecology, Comprehensive Cancer Center-Gynecologic Cancer Unit, Medical University of Vienna, Vienna, Austria – sequence: 4 givenname: Charles C. surname: Valentine fullname: Valentine, Charles C. organization: TwinStrand Biosciences, Seattle, WA 98121, USA – sequence: 5 givenname: Lindsey N. surname: Williams fullname: Williams, Lindsey N. organization: TwinStrand Biosciences, Seattle, WA 98121, USA – sequence: 6 givenname: Jacob E. surname: Higgins fullname: Higgins, Jacob E. organization: TwinStrand Biosciences, Seattle, WA 98121, USA – sequence: 7 givenname: Reinhard surname: Horvat fullname: Horvat, Reinhard organization: Department of Pathology, Medical University of Vienna, Vienna, Austria – sequence: 8 givenname: Adriaan surname: Vanderstichele fullname: Vanderstichele, Adriaan organization: Department of Gynecologic Oncology, Leuven Cancer Institute, University Hospitals Leuven, Katholieke Universiteit, Leuven, Belgium – sequence: 9 givenname: Daniela surname: Nachmanson fullname: Nachmanson, Daniela organization: Department of Pathology, University of Washington, Seattle, WA 98195, USA – sequence: 10 givenname: Kathryn T. surname: Baker fullname: Baker, Kathryn T. organization: Department of Pathology, University of Washington, Seattle, WA 98195, USA – sequence: 11 givenname: Mary J. surname: Emond fullname: Emond, Mary J. organization: Department of Statistics, University of Washington, Seattle, WA 98195, USA – sequence: 12 givenname: Emily surname: Loter fullname: Loter, Emily organization: Department of Pathology, Seattle Children’s Hospital, Seattle, WA 98105, USA – sequence: 13 givenname: Maria surname: Tretiakova fullname: Tretiakova, Maria organization: Department of Pathology, University of Washington, Seattle, WA 98195, USA – sequence: 14 givenname: Thierry surname: Soussi fullname: Soussi, Thierry organization: Sorbonne Université, UPMC Université Paris 06, 75005 Paris, France – sequence: 15 givenname: Lawrence A. surname: Loeb fullname: Loeb, Lawrence A. organization: Department of Pathology, University of Washington, Seattle, WA 98195, USA – sequence: 16 givenname: Robert surname: Zeillinger fullname: Zeillinger, Robert organization: Molecular Oncology Group, Department of Obstetrics and Gynecology, Comprehensive Cancer Center-Gynecologic Cancer Unit, Medical University of Vienna, Vienna, Austria – sequence: 17 givenname: Paul surname: Speiser fullname: Speiser, Paul organization: Molecular Oncology Group, Department of Obstetrics and Gynecology, Comprehensive Cancer Center-Gynecologic Cancer Unit, Medical University of Vienna, Vienna, Austria – sequence: 18 givenname: Rosa Ana orcidid: 0000-0002-0291-1858 surname: Risques fullname: Risques, Rosa Ana email: rrisques@uw.edu organization: Department of Pathology, University of Washington, Seattle, WA 98195, USA |
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| Keywords | somatic mutations uterine lavage next-generation sequencing high-grade serous ovarian cancer TP53, clonal evolution Duplex Sequencing gynecologic oncology early detection aging clonal evolution TP53 |
| Language | English |
| License | This is an open access article under the CC BY license. Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved. Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS J..J.S., R.Z., P.S., E.M., and R.A.R. designed the study; E.M., E.L., R.H., and A.V. procured the samples; J.J.S., K.L.-S., E.M., J.E.H., M.T., and L.N.W. processed the samples; J.J.S., C.C.V., D.N., K.T.B., T.S., and R.A.R. contributed to the data analysis and visualization; M.J.E. and R.A.R. performed the statistical analyses; L.A.L., R.Z., and P.S. contributed expertise and invaluable critical discussion; J.J.S. and R.A.R. wrote the article. |
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| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | Cell reports (Cambridge) |
| PublicationTitleAlternate | Cell Rep |
| PublicationYear | 2019 |
| Publisher | Elsevier Inc Elsevier |
| Publisher_xml | – name: Elsevier Inc – name: Elsevier |
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| SubjectTerms | Adult Aged Aged, 80 and over aging Aging - genetics Biochemistry, Molecular Biology Cancer Cell-Free Nucleic Acids - genetics Clonal Evolution - genetics Databases, Genetic DNA, Neoplasm - genetics Duplex Sequencing early detection Female Genomics gynecologic oncology high-grade serous ovarian cancer High-Throughput Nucleotide Sequencing Humans Infant, Newborn Life Sciences Middle Aged Mutation next-generation sequencing Ovarian Neoplasms - diagnosis Ovarian Neoplasms - genetics Ovarian Neoplasms - pathology Selection, Genetic Sequence Analysis, DNA somatic mutations TP53, clonal evolution Tumor Suppressor Protein p53 - genetics uterine lavage Uterus - metabolism |
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| Title | Ultra-Sensitive TP53 Sequencing for Cancer Detection Reveals Progressive Clonal Selection in Normal Tissue over a Century of Human Lifespan |
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