Cited by 1,993Acute Myeloid Leukemia ResearchCancer Genomics and DiagnosticsChromatin Remodeling and Cancer

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Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing

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Ding, Li, Ley, Timothy J., Larson, David E., Miller, Christopher A., Koboldt, Daniel C., Welch, John S., Ritchey, Julie K., Young, Margaret A., Lamprecht, Tamara, McLellan, Michael D., McMichael, Joshua F., Wallis, John W., Lu, Charles, Shen, Dong, Harris, Christopher C., Dooling, David J., Fulton, Robert S., Fulton, Lucinda L., Chen, Ken, Schmidt, Heather, Kalicki-Veizer, Joelle, Magrini, Vincent J., Cook, Lisa, McGrath, Sean D., Vickery, Tammi L., Wendl, Michael C., Heath, Sharon, Watson, Mark A., Link, Daniel C., Tomasson, Michael H., Shannon, William D., Payton, Jacqueline E., Kulkarni, Shashikant, Westervelt, Peter, Walter, Matthew J., Graubert, Timothy A., Mardis, Elaine R., Wilson, Richard K., DiPersio, John F.·2012·Nature

DOI 10.1038/nature10738PMC PMC3267864

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Abstract

The sequencing of AML genomes of eight patients before and after relapse reveals two major patterns of clonal evolution, with chemotherapy appearing to have a role in both patterns. Many patients with acute myeloid leukaemia (AML) achieve remission, but it is often short-lived and the returned disease is usually refractory to therapy. Genome sequencing of eight patients with AML before and after relapse reveals two major patterns of tumour cell evolution. The founding clone survives chemotherapy in all patients, and, in one clonal pattern, it acquires new mutations and expands at relapse. In the other, a subclone surviving from the original tumour expands and then acquires new mutations. Comparisons of relapse-specific and primary tumour mutations point to an increase in transversions, implying DNA damage caused by cytotoxic chemotherapy. This work demonstrates that the AML genome in an individual patient presents a moving target, and highlights the importance of striving to eradicate both the founding clone and all of its subclones. Most patients with acute myeloid leukaemia (AML) die from progressive disease after relapse, which is associated with clonal evolution at the cytogenetic level1,2 . To determine the mutational spectrum associated with relapse, we sequenced the primary tumour and relapse genomes from eight AML patients, and validated hundreds of somatic mutations using deep sequencing; this allowed us to define clonality and clonal evolution patterns precisely at relapse. In addition to discovering novel, recurrently mutated genes (for example, WAC, SMC3, DIS3, DDX41 and DAXX) in AML, we also found two major clonal evolution patterns during AML relapse: (1) the founding clone in the primary tumour gained mutations and evolved into the relapse clone, or (2) a subclone of the founding clone survived initial therapy, gained additional mutations and expanded at relapse. In all cases, chemotherapy failed to eradicate the founding clone. The comparison of relapse-specific versus primary tumour mutations in all eight cases revealed an increase in transversions, probably due to DNA damage caused by cytotoxic chemotherapy. These data demonstrate that AML relapse is associated with the addition of new mutations and clonal evolution, which is shaped, in part, by the chemotherapy that the patients receive to establish and maintain remissions.

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The Sequence Alignment/Map format and SAMtools
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Authors: Ding, L., Ley, T. J., Larson, D. E., Miller, C. A., Koboldt, D. C., Welch, J. S., Ritchey, J. K., Young, M. A., Lamprecht, T., McLellan, M. D., McMichael, J. F., Wallis, J. W., Lu, C., Shen, D., Harris, C. C., Dooling, D. J., Fulton, R. S., Fulton, L. L., Chen, K., Schmidt, H., Kalicki-Veizer, J., Magrini, V. J., Cook, L., McGrath, S. D., Vickery, T. L., Wendl, M. C., Heath, S., Watson, M. A., Link, D. C., Tomasson, M. H., Shannon, W. D., Payton, J. E., Kulkarni, S., Westervelt, P., Walter, M. J., Graubert, T. A., Mardis, E. R., Wilson, R. K., & DiPersio, J. F.
Affiliations: Washington University in St. Louis (US)
Corresponding author: Ley, Timothy J.
ORCID: Ding, Li
Ley, Timothy J.
Larson, David E.
Miller, Christopher A.
Koboldt, Daniel C.
Welch, John S.
Ritchey, Julie K.
McLellan, Michael D.
McMichael, Joshua F.
Lu, Charles
Shen, Dong
Fulton, Robert S.
Fulton, Lucinda L.
Chen, Ken
Magrini, Vincent J.
McGrath, Sean D.
Vickery, Tammi L.
Wendl, Michael C.
Heath, Sharon
Watson, Mark A.
Link, Daniel C.
Tomasson, Michael H.
Payton, Jacqueline E.
Kulkarni, Shashikant
Walter, Matthew J.
Graubert, Timothy A.
Mardis, Elaine R.
Wilson, Richard K.
DiPersio, John F.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-01
Volume: 481
Issue: 7382
Pages: 506-510
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature10738
PMC: PMC3267864
OpenAlex: W2093144236
Cited by: 1,993
References: 30
Citations by year: 2026: 55 · 2025: 50 · 2024: 61 · 2023: 74 · 2022: 116 · 2021: 138 · 2020: 134 · 2019: 151 · 2018: 155 · 2017: 160 · 2016: 197 · 2015: 192 · 2014: 210 · 2013: 182 · 2012: 118
FWCI: 149.48
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/3.0/ (tdm)
Locations: Nature (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Foundation for Barnes-Jewish Hospital (00335-0505-02)
National Human Genome Research Institute (U54HG003079, HG003079, NHGRI U54 HG003079)
National Cancer Institute (PO1CA101937, CA101937, P01CA101937)
Topics: Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords: acute myeloid leukemia, relapse, clonal evolution, somatic mutations, subclones, chemotherapy-induced DNA damage, transversions, recurrently mutated genes, WAC, SMC3, DIS3, DDX41, DAXX, clonality
MeSH terms: Antineoplastic Agents, Clone Cells, DNA Damage, DNA Mutational Analysis, Humans, Recurrence, Reproducibility of Results, Leukemia, Myeloid, Acute, Genome, Human, Mutagenesis, Genes, Neoplasm, High-Throughput Nucleotide Sequencing, Clonal Evolution

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Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing

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