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The Origin and Evolution of Mutations in Acute Myeloid Leukemia
Open accessAbstract
Most mutations in cancer genomes are thought to be acquired after the initiating event, which may cause genomic instability and drive clonal evolution. However, for acute myeloid leukemia (AML), normal karyotypes are common, and genomic instability is unusual. To better understand clonal evolution in AML, we sequenced the genomes of M3-AML samples with a known initiating event (PML-RARA) versus the genomes of normal karyotype M1-AML samples and the exomes of hematopoietic stem/progenitor cells (HSPCs) from healthy people. Collectively, the data suggest that most of the mutations found in AML genomes are actually random events that occurred in HSPCs before they acquired the initiating mutation; the mutational history of that cell is "captured" as the clone expands. In many cases, only one or two additional, cooperating mutations are needed to generate the malignant founding clone. Cells from the founding clone can acquire additional cooperating mutations, yielding subclones that can contribute to disease progression and/or relapse.
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“Mice lacking Msh2, the key component of both the MutSα and MutSβ complexes that mediate DNA MMR, display a genetic phenotype that closely mimics the spectrum of mutations found in aging human HSCs and in patients with myeloid leukemia (transition mutations and small insertions and deletions) 26, 27.”
From Minimal PU.1 reduction induces a preleukemic state and promotes development of acute myeloid leukemia (2015) · cites this paper as [27]
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“Recent studies in patients with AML have confirmed the functional importance and clinical significance of preleukemic stem cell populations as the cellular origin of leukemia-initiating cells in human disease27, 48.”
From Minimal PU.1 reduction induces a preleukemic state and promotes development of acute myeloid leukemia (2015) · cites this paper as [27]
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“The study of somatic mutations with standard whole-genome sequencing requires isolating clonal groups of cells recently derived from a single cell8,13,14.”
From Somatic mutation rates scale with lifespan across mammals (2022) · cites this paper as [13]
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“Hematopoietic stem cells (HSCs) randomly acquire somatic mutations with age (1).”
From Txnip Enhances Fitness of Dnmt3a -Mutant Hematopoietic Stem Cells via p21 (2022) · cites this paper as [1]
In the citing paper
“Interestingly, during human aging, mutations accumulate in the genome of blood cells and C-to-T mutations are the most prevalent (Welch et al., 2012).”
From The Aging Epigenome (2016) · cites this paper as Welch et al., 2012
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“As each HSC acquires ~1 exonic mutation per decade of life 3,”
From Clonal hematopoiesis in human aging and disease (2019) · cites this paper as [3]
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“Like most cancers, AML generally results from several driver mutations that occur sequentially in the same clone over time 3.”
From Clonal hematopoiesis in human aging and disease (2019) · cites this paper as [3]
In the citing paper
“Aging is associated with a steady increase in the number of somatic mutations in virtually all tissues 1–5.”
From Clonal hematopoiesis in human aging and disease (2019) · cites this paper as [3]
In the citing paper
“We recently reported that individual HSPCs accumulate somatic mutations as a function of age, such that by age 50, there are on average 5 coding gene mutations per HSPC11.”
From Role of TP53 mutations in the origin and evolution of therapy-related acute myeloid leukaemia (2015) · cites this paper as [11]
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Metadata
- Authors
- Welch, J. S., Ley, T. J., Link, D. C., Miller, C. A., Larson, D. E., Koboldt, D. C., Wartman, L. D., Lamprecht, T. L., Liu, F., Xia, J., Kandoth, C., Fulton, R. S., McLellan, M. D., Dooling, D. J., Wallis, J. W., Chen, K., Harris, C. C., Schmidt, H. K., Kalicki-Veizer, J. M., Lu, C., Zhang, Q., Lin, L., O’Laughlin, M. D., McMichael, J. F., Delehaunty, K. D., Fulton, L. A., Magrini, V. J., McGrath, S. D., Demeter, R. T., Vickery, T. L., Hundal, J., Cook, L. L., Swift, G. W., Reed, J. P., Alldredge, P. A., Wylie, T. N., Walker, J. R., Watson, M. A., Heath, S. E., Shannon, W. D., Varghese, N., Nagarajan, R., Payton, J. E., Baty, J. D., Kulkarni, S., Klco, J. M., Tomasson, M. H., Westervelt, P., Walter, M. J., Graubert, T. A., DiPersio, J. F., Ding, L., Mardis, E. R., & Wilson, R. K.
- Affiliations
- Washington University in St. Louis (US)
- The University of Texas MD Anderson Cancer Center (US)
- Corresponding author
- Ley, Timothy J.
- ORCID
- Welch, John S.
- Ley, Timothy J.
- Link, Daniel C.
- Miller, Christopher A.
- Larson, David E.
- Koboldt, Daniel C.
- Wartman, Lukas D.
- Liu, Fulu
- Xia, Jun
- Kandoth, Cyriac
- Fulton, Robert S.
- McLellan, Michael D.
- Chen, Ken
- Lu, Charles
- Lin, Ling
- O’Laughlin, Michelle D.
- McMichael, Joshua F.
- Magrini, Vincent J.
- McGrath, Sean D.
- Vickery, Tammi L.
- Hundal, Jasreet
- Cook, Lisa L.
- Wylie, Todd N.
- Walker, Jason R.
- Watson, Mark A.
- Heath, Sharon E.
- Payton, Jacqueline E.
- Kulkarni, Shashikant
- Klco, Jeffery M.
- Tomasson, Michael H.
- Walter, Matthew J.
- Graubert, Timothy A.
- DiPersio, John F.
- Ding, Li
- Mardis, Elaine R.
- Wilson, Richard K.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2012-07
- Volume
- 150
- Issue
- 2
- Pages
- 264-278
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3407563
- OpenAlex
- W2012753533
- Cited by
- 1,575
- References
- 85
- Citations by year
- 2026: 31 · 2025: 60 · 2024: 68 · 2023: 87 · 2022: 95 · 2021: 125 · 2020: 128 · 2019: 134 · 2018: 116 · 2017: 120 · 2016: 130 · 2015: 141 · 2014: 184 · 2013: 134 · 2012: 19
- FWCI
- 101.78
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 384 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R00HL103975, K99HL103975)
- National Human Genome Research Institute (U54HG003079)
- National Cancer Institute (P30 CA 91842, R01CA083962, P01CA101937, P30CA091842)
- 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 › Retinoids in leukemia and cellular processes
- Keywords
- acute myeloid leukemia, clonal evolution, hematopoietic stem and progenitor cells, PML-RARA fusion, normal karyotype, cooperating mutations, subclonal evolution, disease progression, relapse, genomic instability
- MeSH terms
- Adult, Aged, DNA Mutational Analysis, Female, Hematopoietic Stem Cells, Humans, Male, Middle Aged, Mutation, Recurrence, Skin, Leukemia, Myeloid, Acute, Oncogene Proteins, Fusion, Disease Progression, Genome-Wide Association Study, Young Adult, Clonal Evolution
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