PreprintCited by 1,040Epigenetics and DNA MethylationGenomics and Chromatin DynamicsCancer-related gene regulation

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Role of TET enzymes in DNA methylation, development, and cancer

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Rasmussen, Kasper Dindler, Helin, Kristian·2016·Genes & Development

DOI 10.1101/gad.276568.115PMC PMC4826392

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Abstract

The pattern of DNA methylation at cytosine bases in the genome is tightly linked to gene expression, and DNA methylation abnormalities are often observed in diseases. The ten eleven translocation (TET) enzymes oxidize 5-methylcytosines (5mCs) and promote locus-specific reversal of DNA methylation. TET genes, and especially TET2 , are frequently mutated in various cancers, but how the TET proteins contribute to prevent the onset and maintenance of these malignancies is largely unknown. Here, we highlight recent advances in understanding the physiological function of the TET proteins and their role in regulating DNA methylation and transcription. In addition, we discuss some of the key outstanding questions in the field.

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Figure 1. Domain structure of TET proteins. The C-terminal core catalytic domain shared by all TET enzymes consists of the DSBH domain, a cysteine-rich (Cys) domain, and binding sites for the Fe(II) and 2-OG cofactors. The DSBH domain contains a large low-complexity region of unknown function. TET1 and TET3 have an N-terminal CXXC domain that can bind directly to DNA and facilitate recruitment to genomic target sites.CC BY-NC · PubMed Central

Figure 2. Pathways of DNA demethylation mediated by TET enzymes. (A) Model of passive replication-dependent DNA demethylation. The diagrams illustrate the two opposite fates of a hemihydroxymethylated CpG dinucleotide through two rounds of DNA replication. The left panel shows the replication-dependent DNA demethylation, in which DNA methylation is lost on the DNA strand opposite to 5hmC. The right panel shows the reverse outcome, in which maintenance of DNA methylation is achieved by DNMT1 in complex with UHRF1/2 or DNMT3A/B. The relative extent of these two opposing outcomes of 5hmC deposition in vivo remains to be determined and is likely influenced by global as well as locus-specific factors. In both cases, newly replicated DNA dilutes 5hmC during cell division. (B) Model of active DNA demethylation by a TET/TDG (thymine–DNA–glycosylase)/BER (base excision repair)-dependent pathway. A cytosine base can be methylated by the DNA methylation machinery (DNMT1 or DNMT3A/B) to form 5mC, which in turn can be iteratively oxidized by TET enzymes to produce 5hmC, 5fC, and 5caC. TDG then recognizes 5fC and 5caC, and the oxidized cytosine base is excised. This yields an abasic site that is repaired by BER and results in restoration of the unmodified cytosine state. Additional pathways of active DNA demethylation have been suggested (for review, see Wu and Zhang 2014). (SAH) S-adenosyl-homocysteine; (SAM) S-adenosyl-methionine.CC BY-NC · PubMed Central

Figure 3. The dynamics of TET-mediated cytosine oxidation and its impact on DNA methylation patterns on regulatory elements in vivo. (A) Diagram illustrating the relative abundance of cytosines in the genome with “stable” levels of modifications as well as the small “transient” fractions that undergo rapid turnover and removal by active DNA demethylation processes. The stable levels of genomic 5caC have not been experimentally determined, as they are often under the detection limit. (B) Model illustrating the dual role of TET enzymes. The rate constant of TET enzymes to produce 5hmC from 5mC is fast, whereas the rate constants for further oxidation to 5fC and 5caC are considerably slower. On a majority of TET target sites, 5mC is oxidized and persists as “stable” 5hmC, likely due to low TET residence time (“stalling TET modification”). On a minority of sites, preferably located in open chromatin associated with regulatory elements, 5mC is oxidized iteratively to 5fC and 5caC and results in net DNA demethylation by the TET/TDG/BER pathway (“processive TET modification”). (C) Model illustrating the impact of loss of TET protein function on different regulatory elements. The protection of active and inactive CpG island promoters by the TET proteins is only one of several mechanisms by which they are protected against ectopic DNA methylation. In contrast, distal regulatory elements such as active enhancers are vulnerable to aberrant DNMT activity and become DNA hypermethylated upon loss of TET activity. (PcG) Polycomb group.CC BY-NC · PubMed Central

Figure 4. Illustration of the mutational landscape of TET2 in hematological diseases. A somatic mutation in TET2 results in premalignant hematopoiesis and clonal expansion. Additional oncogenic events cooperate with the initial TET2 mutation to drive the onset of a wide variety of hematopoietic malignancies. The frequencies of TET2 mutations in the different patient groups are indicated (for review, see Scourzic et al. 2015).CC BY-NC · PubMed Central

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“Thus, it was remarkable when ten eleven translocation protein 1 (TET1) was discovered and shown to be able to modify methylcytosine and potentially erase DNAmethylation (Tahiliani et al. 2009).”
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“Second, TET2 mutations are frequently observed in aged healthy individuals with clonal hematopoiesis and increase the propensity to develop hematopoieticmalignancies (Busque et al. 2012; Genovese et al. 2014; Jaiswal et al. 2014; Xie et al. 2014).”
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“Second, TET2 mutations are frequently observed in aged healthy individuals with clonal hematopoiesis and increase the propensity to develop hematopoieticmalignancies (Busque et al. 2012; Genovese et al. 2014; Jaiswal et al. 2014; Xie et al. 2014).”
Background
Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine
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“6-fold) substrates compared with the initial oxidation reaction of 5mC (Ito et al. 2011; Hu et al. 2015).”
Background
Oncometabolite 2-Hydroxyglutarate Is a Competitive Inhibitor of α-Ketoglutarate-Dependent Dioxygenases
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“Subsequent to the discovery of oxidized 5mC bases, it was demonstrated that TDG has no effect on 5hmC but shows robust recruitment and in vitro catalytic activity toward 5fC and 5caC (He et al. 2011; Maiti and Drohat 2011; Spruijt et al. 2013).”
BackgroundInfluential
Leukemic IDH1 and IDH2 Mutations Result in a Hypermethylation Phenotype, Disrupt TET2 Function, and Impair Hematopoietic Differentiation
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“By comparison, the products of further TET-mediated oxidation, 5fC and 5caC, are observed at ∼10-fold to 100-fold lower levels than 5hmC and often close to or under the detection limit (Kriaucionis and Heintz 2009; Globisch et al. 2010; Szwagierczak et al. 2010; He et al. 2011; Ito et al. 2011; Pfaffeneder et al. 2011…”
Background

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“In promoters, CpG islands may be protected against ectopic DNA methylation by additional mechanisms, including exclusion of de novo DNMTs and polycomb-associated proteins (Boulard et al., 2015; Noh et al., 2015; Ooi et al., 2007; Rasmussen and Helin, 2016).”
Background
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Background
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“In summary, the role of TET enzymes in the development of cancer has been examined and extensively proven (16, 66, 79) (Figure 3).”
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BackgroundMethod
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BackgroundMethod
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“Despite similar enzymatic activity, TET enzymes exhibit unique regulatory functions (Rasmussen and Helin, 2016).”
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“Ten-eleven translocation methylcytosine dioxygenase 1 (TET1) catalyzes the conversion of the modified DNA base 5-methylcytosine (5-mC) to 5-hydroxymethylcytosine (5-hmC) and initiates the first step of active DNA demethylation in mammals (62, 63).”
Background
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Background
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“IDH mutants have severely altered methylomes, [259_TD$DIFF]which is likely [260_TD$DIFF]to be due to [261_TD$DIFF] -hydroxyglutarate-mediated inhibition of TET family 50-methylcytosine hydroxylases [263_TD$DIFF], which catalyze a key step in the removal of DNA methylation [57,61,62].”
Background
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BackgroundResultInfluential
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Background
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Background
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“While Zheng et al. reported that HBx did not alter HDAC1 expression, HDAC catalytic activity, total histone acetylation patterns, and acetylated H3 or H4 distribution patterns in deﬁned gene promoters, including IGFBP3, CDH6, MT1F and IL4R in Huh7-based models [52], other studies using Hep3B-and…”
Result
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“DNA demethylation can be carried out passively, when a newly synthesized strand in proliferating cells is not methylated by Dnmt1 after DNA replication, or actively via the DNA demethylation pathway, which requires functioning members of the TET family (Dominguez and Shaknovich, 2014; Li et al., 2015b; Rasmussen and H…”
Background
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“In mammals, DNA methylation patterns are routinely established and maintained by three DNA methyltransferases (DNMT) [70,71] including DNMT1, DNMT3a, and DNMT3b, while in contrast, DNA demethylation can be achieved by the ten-eleven translocation (TET) enzymes through converting 5mC to 5-hydroxymethylcytosine (5hmC) […”
Background
The interactions between DNA methylation machinery and long non-coding RNAs in tumor progression and drug resistance
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Rocca, S., Carrà, G., Poggio, P., Morotti, A., & Brancaccio, M. (2018) · Molecular Cancer · doi:10.1186/s12943-018-0774-4 · Cited by 28
“This modification, in turn, promotes locus-specific reversal of DNA methylation, impacting on DNA methylation landscape [138].”
Hallmarks of aging: A user’s guide for comparative biologists
Biga, P. R., Duan, J. E., Young, T. E., Marks, J. R., Bronikowski, A. M., Decena-Segarra, L. P., Randolph, E. C., Pavuluri, A., Li, G., Fang, Y., et al. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102616 · Cited by 33
“Cytosine methylation resulting in 5-methylcytosine (5mC) is controlled by the combined action of DNA methyltransferases and ten eleven translocation (TET) enzymes (Rasmussen and Helin, 2016).”
Epithelial-mesenchymal transition promotes metabolic reprogramming to suppress ferroptosis
Guo, W., Duan, Z., Wu, J., & Zhou, B. P. (2025) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2025.02.013 · Cited by 33
Regulation of DNA methylation signatures on NF-κB and STAT3 pathway genes and TET activity in cigarette smoke extract–challenged cells/COPD exacerbation model in vitro
Kaur, G., & Batra, S. (2020) · Cell Biology and Toxicology · doi:10.1007/s10565-020-09522-8 · Cited by 27
Decoding DNA methylation in epigenetics of multiple myeloma
Yang, T., Liu, X., Kumar, S. K., Jin, F., & Dai, Y. (2021) · Blood Reviews · doi:10.1016/j.blre.2021.100872 · Cited by 28
Epigenetic modification and BRAF gene mutation in thyroid carcinoma
Huang, G. C., Chen, J., Zhou, J., Xiao, S., Zeng, W.-H., Xia, J., & Zeng, X. (2021) · Cancer Cell International · doi:10.1186/s12935-021-02405-w · Cited by 28
“The ten-eleven translocation (TET) protein DNA demethylase has been identified, and the TET protein family comprises three members: TET1, TET2, and TET3 [96].”
Background
Expression and prognosis analysis of TET family in acute myeloid leukemia
Zhang, T., Zhao, Y., Zhao, Y., & Zhou, J. (2020) · Aging · doi:10.18632/aging.102928 · Cited by 28
“The process of DNA methylation controlled by several molecules such as DNA methyltransferases (DNMTs) has been well characterized [3, 4], but the underlying mechanism of demethylation remains to be elucidated.”
BackgroundInfluential
An active glutamine/α-ketoglutarate/HIF-1α axis prevents pregnancy loss by triggering decidual IGF1+GDF15+NK cell differentiation
Yang, S., Tan, H.-X., Lai, Z., Peng, H., Yang, H., Fu, Q., Wang, H., Li, D., & Li, M. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04639-x · Cited by 33
“DNA methylation and transcription mediated by ten-eleven translocation(TET) methylcytosine dioxygenase is an important way for α-KG to participate in epigenetic regulation of genes [39].”
Background
CTCF and Its Multi-Partner Network for Chromatin Regulation
Moral‐Morales, A. D., Salgado-Albarrán, M., Sánchez-Pérez, Y., Wenke, N. K., Baumbach, J., & Soto‐Reyes, E. (2023) · Cells · doi:10.3390/cells12101357 · Cited by 30
The Ageing Brain: Effects on DNA Repair and DNA Methylation in Mice
Langie, S. A. S., Cameron, K., Ficz, G., Oxley, D., Tomaszewski, B., Gorniak, J., Maas, L. M., Godschalk, R., van Schooten, F., Reik, W., et al. (2017) · Genes · doi:10.3390/genes8020075 · Cited by 30
Primer in Genetics and Genomics, Article 6: Basics of Epigenetic Control
Fessele, K. L., & Wright, F. (2017) · Biological Research For Nursing · doi:10.1177/1099800417742967 · Cited by 32
Biomolecular and cellular effects in skin wound healing: the association between ascorbic acid and hypoxia-induced factor
Ghahremani‐Nasab, M., Bakhshayesh, A. R. D., Akbari‐Gharalari, N., & Mehdipour, A. (2023) · Journal of Biological Engineering · doi:10.1186/s13036-023-00380-6 · Cited by 34
Targeting latent viral infection in EBV-associated lymphomas
Kong, I. Y., & Giulino-Roth, L. G. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1342455 · Cited by 27
“This process can be reversed by the ten-eleven translocation (TET) enzyme, which converts the 5mC to cytosines by oxidizing the 5mC to form 5-hydroxymethylcytosine (5hmC) (28).”
Background
Gene body DNA hydroxymethylation restricts the magnitude of transcriptional changes during aging
Occean, J. R., Yang, N., Sun, Y., Dawkins, M. S., Munk, R. B., Belair, C., Dar, S. A., Anerillas, C., Wang, L., Shi, C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50725-y · Cited by 30
“Suggestively, transcriptional dysregulation is a hallmark of cancer, an age-related disease with extensively documented TET mutations as well as loss of 5hmC 80 – 82 .”
Background
Epigenome editing by CRISPR/Cas9 in clinical settings: possibilities and challenges
Pei, W., Zhang, Y., Yin, T., & Yu, Y. (2019) · Briefings in Functional Genomics · doi:10.1093/bfgp/elz035 · Cited by 28
Flavonoids Overcome Drug Resistance to Cancer Chemotherapy by Epigenetically Modulating Multiple Mechanisms
To, K. K. W., & Cho, W. C. S. (2021) · Current Cancer Drug Targets · doi:10.2174/1568009621666210203111220 · Cited by 27
5-methylcytosine turnover: Mechanisms and therapeutic implications in cancer
Turpin, M., & Salbert, G. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.976862 · Cited by 31
“DNMTs and TET-mediated demethylation can be promoted by TF binding to unmethylated and methylated regions of the genome respectively (Rasmussen and Helin, 2016).”
Background
Lineage tracing reveals B cell antibody class switching is stochastic, cell-autonomous, and tuneable
Horton, M. B., Cheon, H., Duffy, K. R., Brown, D. V., Naik, S. H., Alvarado, C., Groom, J. R., Heinzel, S., & Hodgkin, P. D. (2022) · Immunity · doi:10.1016/j.immuni.2022.08.004 · Cited by 25
Genetic and Epigenetic Mechanisms Regulating Blood Pressure and Kidney Dysfunction
Pandey, K. N. (2024) · Hypertension · doi:10.1161/hypertensionaha.124.22072 · Cited by 28
“113 TET enzymes are considered a significant target of future therapies for hypertension and kidney diseases by reversing the nature of gene repression.”
Background
TET2 expression is a potential prognostic and predictive biomarker in cytogenetically normal acute myeloid leukemia
Zhang, T., Zhou, J., Yang, D., Wang, Y., Wen, X., Guo, H. Y., Yang, L., Lian, X., Lin, J., & Qian, J. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.26373 · Cited by 27
“It is seen as a putative tumor suppressor gene during cancer initiation and development (Rasmussen & Helin, 2016).”
Background
5-Hydroxymethylcytosine and ten-eleven translocation dioxygenases in head and neck carcinoma
Misawa, K., Yamada, S., Mima, M., Nakagawa, T., Kurokawa, T., Imai, A., Mochizuki, D., Morita, K., Ishikawa, R., Endo, S., et al. (2019) · Journal of Cancer · doi:10.7150/jca.34806 · Cited by 26
“Missense and truncating mutations in TET genes are present in nearly all solid tumor types at a relatively low frequency [16].”
Background
MicroRNA-191 regulates endometrial cancer cell growth via TET1-mediated epigenetic modulation of APC
Yang, C., Ota-Kurogi, N., Ikeda, K., Okumura, T., Horie‐Inoue, K., Takeda, S., & Inoue, S. (2020) · The Journal of Biochemistry · doi:10.1093/jb/mvaa014 · Cited by 26
Cell plasticity in cancer: A complex interplay of genetic, epigenetic mechanisms and tumor micro-environment
Shenoy, S. (2020) · Surgical Oncology · doi:10.1016/j.suronc.2020.04.017 · Cited by 29
Epigenetic Regulatory Enzymes: mutation Prevalence and Coexistence in Cancers
Sharma, A., Liu, H., Herwig‐Carl, M. C., Dakal, T. C., & Schmidt‐Wolf, I. G. H. (2021) · Cancer Investigation · doi:10.1080/07357907.2021.1872593 · Cited by 26
Epigenetic Regulation of Cell-Fate Changes That Determine Adult Liver Regeneration After Injury
Aloia, L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.643055 · Cited by 25
Regulation of TET2 gene expression and 5mC oxidation in breast cancer cells by estrogen signaling
Zhu, X., Xiong, L., Lyu, R., Shen, Y., Liu, L., Li, S., Argueta, C. E., & Tan, L. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.12.042 · Cited by 26
Sirolimus increases the anti-cancer effect of Huai Er by regulating hypoxia inducible factor-1α-mediated glycolysis in hepatocellular carcinoma
Zhou, L., Zhao, Y., Pan, L.-C., Wang, J., Shi, X., Du, G., & He, Q. (2022) · World Journal of Gastroenterology · doi:10.3748/wjg.v28.i32.4600 · Cited by 27
AHR/TET2/NT5E axis downregulation is associated with the risk of systemic lupus erythematosus and its progression
Cheng, H., Hung‐Ke, L., Sheu, M., Lee, C., Tsai, Y., & Lai, D. (2022) · Immunology · doi:10.1111/imm.13600 · Cited by 26
“Ten-eleven translocation (TET) family proteins are Fe(II) and 2-oxoglutarate-dependent dioxygenases that catalyse the sequential oxidation of 5-methylcytosine (5mC) in DNA to 5-hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC) or 5-carboxylcytosine (5caC) [27].”
Background
Dynamic antagonism between key repressive pathways maintains the placental epigenome
Weigert, R., Hetzel, S., Bailly, N., Haggerty, C., Ilik, İ., Yung, P. Y. K., Navarro, C., Bolondi, A., Kumar, A. S., Anania, C., et al. (2023) · Nature Cell Biology · doi:10.1038/s41556-023-01114-y · Cited by 27
DNA methylation in the mouse cochlea promotes maturation of supporting cells and contributes to the failure of hair cell regeneration
Nguyen, J. D., Llamas, J., Shi, T., Crump, J. G., Groves, A. K., & Segil, N. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2300839120 · Cited by 26
“The action of thymine- DNA-glycosylase (TDG) and base excision repair (BER) ultimately restores the unmethylated cytosine (51).”
Background
Emerging epigenetic therapeutics for myeloid leukemia: modulating demethylase activity with ascorbate
Das, A. B., Smith-Díaz, C. C., & Vissers, M. C. M. (2020) · Haematologica · doi:10.3324/haematol.2020.259283 · Cited by 25
Hypoxia switches TET1 from being tumor-suppressive to oncogenic
Yang, Q., Dang, H., Liu, J., Wang, X., Wang, J., Lan, X., Ji, M., Xing, M., & Hou, P. (2023) · Oncogene · doi:10.1038/s41388-023-02659-w · Cited by 24
“As a member of the DNA dioxygenase family, TET1 is often thought to regulate gene expression via DNA demethylation [57].”
Background
OGT prevents DNA demethylation and suppresses the expression of transposable elements in heterochromatin by restraining TET activity genome-wide
Sepúlveda, H., Li, X., Arteaga-Vazquez, L. J., López-Moyado, I. F., Brunelli, M., Hernández-Espinosa, L., Yue, X., Angel, J. C., Brown, C., Dong, Z., et al. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01505-9 · Cited by 28
Structural analyses reveal that MBD 3 is a methylated CG binder
Liu, K., Lei, M., Wu, Z., Gan, B. S., Cheng, H., Li, Y., & Min, J. (2019) · FEBS Journal · doi:10.1111/febs.14850 · Cited by 26
Dynamic changes in DNA methylation during postnatal development in zebra finches Taeniopygia guttata exposed to different temperatures
Sheldon, E. L., Schrey, A. W., Hurley, L. L., & Griffith, S. C. (2020) · Journal of Avian Biology · doi:10.1111/jav.02294 · Cited by 28
Synthesis of 2-oxoglutarate derivatives and their evaluation as cosubstrates and inhibitors of human aspartate/asparagine-β-hydroxylase
Brewitz, L., Nakashima, Y., & Schofield, C. J. (2020) · Chemical Science · doi:10.1039/d0sc04301j · Cited by 25
Inhibition of TET‐mediated DNA demethylation suppresses osteoblast differentiation
Dusadeemeelap, C., Rojasawasthien, T., Matsubara, T., Kokabu, S., & Addison, W. N. (2022) · The FASEB Journal · doi:10.1096/fj.202101402r · Cited by 25
FGFR3△7–9 promotes tumor progression via the phosphorylation and destabilization of ten-eleven translocation-2 in human hepatocellular carcinoma
Jin, Z., Feng, H., Liang, J., Jing, X., Zhao, Q., Zhan, L., Shen, B., Cheng, X., Su, L., & Qiu, W. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-03089-2 · Cited by 25
Pan-cancer predictions of transcription factors mediating aberrant DNA methylation
Detilleux, D., Spill, Y. G., Balaramane, D., Weber, M., & Bardet, A. F. (2022) · Epigenetics & Chromatin · doi:10.1186/s13072-022-00443-w · Cited by 29
“We did not investigate here the mechanisms by which FOXA1 and GATA3 lead to demethylation and whether this occurs via a passive and/or an active demethylation through the recruitment of Ten-Eleven Translocation (TET) enzymes [50].”
Background
The yin and yang of itaconate metabolism and its impact on the tumor microenvironment
Chen, F., Dowerg, B., & Cordes, T. (2023) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2023.102996 · Cited by 22
TET Upregulation Leads to 5-Hydroxymethylation Enrichment in Hepatoblastoma
Rivas, M. P., Aguiar, T. F. M., Fernandes, G. R., de Caires-Junior, L. C., Goulart, E., Telles-Silva, K. A., Cypriano, M., de Toledo, S. R. C., Rosenberg, C., Carraro, D. M., et al. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00553 · Cited by 25
“Studies with animal models described TET overexpression in embryonic development stages repressing differentiation (Ito et al., 2010; RawłuszkoWieczorek et al., 2015; Rasmussen and Helin, 2016), as well as in cellular reprogramming of IPS cells (Bagci and Fisher, 2013).”
Background
Treatment-resistant schizophrenia: focus on the transsulfuration pathway
Berry, T. M., Hamza, E. A., & Moustafa, A. A. (2019) · Reviews in the Neurosciences · doi:10.1515/revneuro-2019-0057 · Cited by 25
“Fe(II) and α-ketoglutarate-dependent ten-eleven translocation (TET) enzymes demethylate DNA (Rasmussen and Helin, 2016), whereas Fe(II) and α-ketoglutaratedependent JumonjiC-domain-containing enzymes demethylate lysine residues of histones (Tsukada et al.”
BackgroundInfluential
Endogenous Retrovirus Transcript Levels Are Associated with Immunogenic Signatures in Multiple Metastatic Cancer Types
Topham, J. T., Titmuss, E., Pleasance, E., Williamson, L. M., Karasinska, J. M., Culibrk, L., Lee, M. K. C., Mendis, S. R., Denroche, R. E., Jang, G.-H., et al. (2020) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-20-0094 · Cited by 27
“3B and include TET2, which encodes the primary DNA demethylating enzyme in mammalian adult tissues (41).”
Background
Epigenetic targeting of cancer stem cells by polyphenols (cancer stem cells targeting)
Ghasemi, S., Xu, S., Nabavi, S. M., Amirkhani, M. A., Sureda, A., Tejada, S., & Lorigooini, Z. (2021) · Phytotherapy Research · doi:10.1002/ptr.7059 · Cited by 28
“In addition, ten-eleven translocation (TET) enzymes constitute another category of enzymes affecting DNA hypermethylation (Rasmussen & Helin, 2016).”
Background
A novel class of selective non-nucleoside inhibitors of human DNA methyltransferase 3A
Huang, S., Stillson, N. J., Sandoval, J. E., Yung, C., & Reich, N. O. (2021) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2021.127908 · Cited by 24
The role of diet in renal cell carcinoma incidence: an umbrella review of meta-analyses of observational studies
Liao, Z., Fang, Z., Gou, S., Luo, Y., Liu, Y., He, Z., Li, X., Peng, Y., Fu, Z., Li, D., et al. (2022) · BMC Medicine · doi:10.1186/s12916-021-02229-5 · Cited by 27
“However, TET enzymes are frequently mutated [167].”
Targeting epigenetic alterations in cancer stem cells
Verona, F., Pantina, V. D., Modica, C., Lo Iacono, M., D’Accardo, C., Porcelli, G., Cricchio, D., Turdo, A., Gaggianesi, M., Franco, S. D., et al. (2022) · Frontiers in Molecular Medicine · doi:10.3389/fmmed.2022.1011882 · Cited by 27
“, 2009), although until recently it was considered an irreversible process (Rasmussen and Helin, 2016).”
Distinct dynamics of parental 5-hydroxymethylcytosine during human preimplantation development regulate early lineage gene expression
Liang, D., Yan, R., Long, X., Ji, D., Song, B., Wang, M., Zhang, F., Cheng, X., Sun, F., Zhu, R., et al. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01475-y · Cited by 25
“This comparatively static landscape is perturbed locally by the TET (ten-eleven-translocation) family of dioxygenases, by which 5mC is converted into sequential oxidative derivates such as 5-hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC) and 5-carboxylcytosine (5caC) 4–6 .”
Background
A role for TET2 in parathyroid carcinoma
Barazeghi, E., Gill, A. J., Sidhu, S. B., Norlén, O., Dina, R. E., Palazzo, F. F., Hellman, P., Stalberg, P. L. H., & Westin, G. (2017) · Endocrine Related Cancer · doi:10.1530/erc-17-0009 · Cited by 24
“2016, Rasmussen & Helin 2016).”
Epigenetic modifications by polyphenolic compounds alter gene expression in the hippocampus
Frolinger, T., Herman, F. J., Sharma, A., Sims, S. L., Wang, J., & Pasinetti, G. M. (2018) · Biology Open · doi:10.1242/bio.035196 · Cited by 23
“In a first set of studies using real-time PCR, we quantified the expression of the epigenetics modifiersDNMTs and TETs, enzymes that are important for adding or removing methyl-groups to or from the DNA, respectively (Rasmussen and Helin, 2016; Robert et al., 2003; Robertson et al., 1999).”
Background
Restoration of TET2 deficiency inhibits tumor growth in head neck squamous cell carcinoma
Huang, R., Wang, Y., Ge, H., Wang, D., Wang, Y., Zhang, W., Yang, J., & Cheng, J. (2020) · Annals of Translational Medicine · doi:10.21037/atm.2020.02.145 · Cited by 23
“In addition, these TET enzymes play vital functions in cell fate determination, cell differentiation, development and various diseases including cancer (9).”
Background
Base-excision repair pathway shapes 5-methylcytosine deamination signatures in pan-cancer genomes
Silveira, A. B., Houy, A., Ganier, O., Özemek, B., Vanhuele, S., Vincent‐Salomon, A., Cassoux, N., Mariani, P., Pierron, G., Leyvraz, S., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54223-z · Cited by 22
Methylation in Syn and Psd95 genes underlie the inhibitory effect of oxytocin on oxycodone-induced conditioned place preference
Fan, X., Shi, G., & Zhao, P. (2019) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2019.10.010 · Cited by 23
Chemical and Light Inducible Epigenome Editing
Zhao, W., Wang, Y., & Liang, F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030998 · Cited by 23

Authors: Rasmussen, K. D., & Helin, K.
Affiliations: University of Copenhagen (DK)
Corresponding author: Helin, Kristian
ORCID: Rasmussen, Kasper Dindler
Helin, Kristian
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 2016-04-01
Volume: 30
Issue: 7
Pages: 733-750
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.276568.115
PMC: PMC4826392
OpenAlex: W2325267338
Cited by: 1,040
References: 162
Citations by year: 2026: 56 · 2025: 87 · 2024: 116 · 2023: 100 · 2022: 135 · 2021: 141 · 2020: 131 · 2019: 97 · 2018: 83 · 2017: 60 · 2016: 30
Type: posted content
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
Locations: Genes & Development (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by-nc)
HighWire Press Open Archive (submittedVersion)
Funders: Danish Medical Research Council (1333-00120B)
European Research Council (294666_DNAMET)
Danish Cancer Society
Danish National Research Foundation (DNRF 82)
Danish Council for Strategic Research
Novo Nordisk Foundation
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cancer-related gene regulation
Keywords: TET enzymes, DNA methylation, 5-methylcytosine oxidation, TET2, demethylation, cancer, developmental regulation, transcriptional regulation, gene expression
MeSH terms: Animals, Cytosine, DNA-Binding Proteins, Humans, Neoplasms, Oxidation-Reduction, Proto-Oncogene Proteins, Gene Expression Regulation, Neoplastic, DNA Methylation, Epigenesis, Genetic, Dioxygenases

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Role of TET enzymes in DNA methylation, development, and cancer

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