Tet2 loss leads to hypermutagenicity in haematopoietic stem/progenitor cells
Open accessAbstract
TET2 is a dioxygenase that catalyses multiple steps of 5-methylcytosine oxidation. Although TET2 mutations frequently occur in various types of haematological malignancies, the mechanism by which they increase risk for these cancers remains poorly understood. Here we show that Tet2−/− mice develop spontaneous myeloid, T- and B-cell malignancies after long latencies. Exome sequencing of Tet2−/− tumours reveals accumulation of numerous mutations, including Apc, Nf1, Flt3, Cbl, Notch1 and Mll2, which are recurrently deleted/mutated in human haematological malignancies. Single-cell-targeted sequencing of wild-type and premalignant Tet2−/− Lin−c-Kit+ cells shows higher mutation frequencies in Tet2−/− cells. We further show that the increased mutational burden is particularly high at genomic sites that gained 5-hydroxymethylcytosine, where TET2 normally binds. Furthermore, TET2-mutated myeloid malignancy patients have significantly more mutational events than patients with wild-type TET2. Thus, Tet2 loss leads to hypermutagenicity in haematopoietic stem/progenitor cells, suggesting a novel TET2 loss-mediated mechanism of haematological malignancy pathogenesis.
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Sanger sequencing analysis of key regulatory and coding regions of Spi1 excluded mice harboring acquired DNA lesions that may further compromise PU.1 regulation in compound mutant animals.
“Because TET2 deficiency has been associatated with increased DNA lesions (30), we performed Sanger sequencing analysis of the key regulatory and coding regions of the PU.1 encoding gene (Spi1) and excluded the mice that harbored acquired DNA lesions, which may further compromise PU.1 regulation in compound mutant animals (Supplementary Fig. S1B; Supplementary Table S1).”
From PU.1-Dependent Enhancer Inhibition Separates <i>Tet2</i> -Deficient Hematopoiesis from Malignant Transformation (2022) · cites this paper as [30]
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TET2 mutation as prototypic clonal hematopoiesis lesion
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Impact of DNA methylation programming on normal and pre-leukemic hematopoiesis
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“Because TET2 deficiency has been associatated with increased DNA lesions (30), we performed Sanger sequencing analysis of the key regulatory and coding regions of the PU.”
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TET2 truncating mutations predict a worse outcome in blastic plasmacytoid dendritic cell neoplasm
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p300 suppresses the transition of myelodysplastic syndromes to acute myeloid leukemia
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Self-citationClonal Hematopoiesis of Indeterminate Potential as a Novel Risk Factor for Donor-Derived Leukemia
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TET-dioxygenase deficiency in oncogenesis and its targeting for tumor-selective therapeutics
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TET2 mutations as a part of DNA dioxygenase deficiency in myelodysplastic syndromes
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The Interactome between Metabolism and Gene Mutations in Myeloid Malignancies
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TET2 deficiency promotes MDS-associated leukemogenesis
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Loss of Tet2 affects platelet function but not coagulation in mice
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Clonal hematopoiesis and bone marrow inflammation
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Characteristics of myeloid sarcoma in mice and patients with TET2 deficiency
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Ten-Eleven-Translocation Genes in Cancer
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The role of epigenetic modifications in hematological cancers
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Retinoic acid and ascorbate synergize to suppress myeloid leukemia via TET2 activation
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Epigenetic Abnormalities in Acute Myeloid Leukemia and Leukemia Stem Cells
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Tet2 is a tumor suppressor in the preleukemic phase of T-cell acute lymphoblastic leukemia
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Id1 promotes clonal hematopoiesis in mice with Tet2 loss of function
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- Authors
- Pan, F., Wingo, T. S., Zhao, Z., Gao, R., Makishima, H., Qu, G., Lin, L., Yu, M., Ortega, J. R., Wang, J., Nazha, A., Chen, L., Yao, B., Liu, C., Chen, S., Weeks, O., Ni, H., Phillips, B. L., Huang, S., Wang, J., He, C., Li, G.-M., Radivoyevitch, T., Aifantis, I., Maciejewski, J. P., Yang, F.-C., Jin, P., & Xu, M.
- Affiliations
- University of Miami (US)
- United States Department of Veterans Affairs (US)
- Tianjin Medical University Cancer Institute and Hospital (CN)
- Cleveland Clinic (US)
- Emory University (US)
- University of Chicago (US)
- University of Southern California (US)
- Indiana University Indianapolis (US)
- Florida International University (US)
- University of Illinois Chicago (US)
- University of Florida (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Jin, Peng
- Xu, Mingjiang
- ORCID
- Venue
- Nature Communications
- Published
- 2017-04-25
- Volume
- 8
- Issue
- 1
- Pages
- 15102-15102
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC5414116
- OpenAlex
- W2608857438
- Cited by
- 117
- References
- 45
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 10 · 2023: 12 · 2022: 17 · 2021: 15 · 2020: 19 · 2019: 20 · 2018: 7 · 2017: 5
- FWCI
- 10.75
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Florida International University Digital Commons (Florida International University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- IUScholarWorks (Indiana University) (submittedVersion, cc-by-nc-nd)
- Funders
- U.S. Department of Veterans Affairs (BX001820, IK2 BX001820)
- National Natural Science Foundation of China (81670102, 81629001)
- National Institutes of Health (NS05163, HL112294)
- Japan Society for the Promotion of Science (16H05338, 26221308)
- National Heart, Lung, and Blood Institute (R01HL112294)
- National Cancer Institute (R01CA172408, K12CA076917, P30CA016087)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK110108)
- National Institute of Neurological Disorders and Stroke (R01NS079625)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD073162)
- 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 › Epigenetics and DNA Methylation
- Keywords
- TET2, 5-methylcytosine oxidation, 5-hydroxymethylcytosine, hematopoietic stem and progenitor cells, mutational burden, hematologic malignancies, myeloid neoplasms, T-cell malignancies, B-cell malignancies, mutational hotspots
- MeSH terms
- Exome Sequencing, DNA Demethylation, Aged, Animals, DNA Mutational Analysis, DNA-Binding Proteins, Hematopoietic Stem Cells, Humans, Proto-Oncogene Proteins, Gene Expression Regulation, Neoplastic, Mutagenesis, Mice, Knockout, Hematologic Neoplasms, RNA, Small Interfering, Epigenesis, Genetic, 5-Methylcytosine, Cell Line, Tumor, Dioxygenases, Mice, Single-Cell Analysis, Mutation Rate
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