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The Dual Characteristics of Ten-eleven Translocation 1 in Cancer

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Chen Ge, Haiyang Wang, Haixu Chen, Wen Yue, Xinlong Yan

Abstract


DNA methylation abnormalities in tumors often manifest as an increase or decrease of 5-methylcytosine at the genomic level or individual promoter sites. The mechanism of DNA demethylation by ten-eleven translocation proteins (TET) in maintaining the stability of global genome methylation level has attracted extensive attention. The biological functions of TET1-mediated hydroxymethylation differ among cancers due to tumor heterogeneity. Herein, recent updates on the effects of TET1 on tumor proliferation, migration, and invasion by altering DNA methylation levels are reviewed, and the direct and indirect roles of TET1 in activating or suppressing tumor progression are also discussed. Besides, the potential uses of DNA methylation analysis in clinical diagnosis and research of tumor microenvironment in relation to epigenetics are prospected. In conclusion, further studies about the dual characteristics of TET1 in cancer diseases are warranted to expand our understanding of the effects of DNA methylation in tumor which could be instrumental in the development of tumor treatment.

Keywords


DNA methylation, Ten-eleven translocation proteins, Tumor

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References


Dawson MA, Kouzarides T, 2012, Cancer Epigenetics: From Mechanism to Therapy. Cell, 150:12–27. DOI: 10.1016/j.cell.2012.06.013.

Yu T, Liu D, Zhang T, et al., 2019, Inhibition of Tet1- and Tet2-mediated DNA Demethylation Promotes Immunomodulation of Periodontal Ligament Stem Cells. Cell Death Dis, 10:780. DOI: 10.1038/s41419-019-2025-z.

Mongelli A, Atlante S, Bachetti T, et al., 2020, Epigenetic Signaling and RNA Regulation in Cardiovascular Diseases. Int J Mol Sci, 21:509. DOI: 10.3390/ijms21020509.

Zhao R, Liu Z, Xu W, et al., 2020, Helicobacter pylori Infection Leads to KLF4 Inactivation in Gastric Cancer through a TET1-mediated DNA Methylation Mechanism. Cancer Med, 9:2551–63. DOI: 10.1002/cam4.2892.

Thiagalingam S, 2020, Epigenetic Memory in Development and Disease: Unraveling the Mechanism. Biochim Biophys Acta, 1873:188349. DOI: 10.1016/j.bbcan.2020.188349.

Hamidi T, Singh AK, Chen T, 2015, Genetic Alterations of DNA methylation machinery in human diseases. Epigenomics, 7:247–65. DOI: 10.2217/epi.14.80.

Wrangle J, Machida EO, Danilova L, et al., 2014, Functional Identification of Cancer-Specific Methylation of CDO1, HOXA9, and TAC1 for the Diagnosis of Lung Cancer. Clin Cancer Res, 20:1856–64. DOI: 10.1158/1078-0432.CCR- 13-2109.

Choo KB, 2011, Epigenetics in Disease and Cancer. Malays J Pathol, 33:61–70.

Li H, Zhou ZQ, Yang ZR, et al., 2017, MicroRNA-191 Acts as a Tumor Promoter by Modulating the TET1-p53 Pathway in Intrahepatic Cholangiocarcinoma. Hepatology, 66:136– 51. DOI: 10.1002/hep.29116.

Li L, Li C, Mao H, et al., 2016, Epigenetic Inactivation of the CpG Demethylase TET1 as a DNA Methylation Feedback Loop in Human Cancers. Sci Rep, 6:26591. DOI: 10.1038/srep26591.

Huang H, Jiang X, Li Z, et al., 2013, TET1 Plays an Essential Oncogenic Role in MLL-rearranged Leukemia. Proc Natl Acad Sci, 110:11994–9. DOI: 10.1073/pnas.1310656110.

Good CR, Panjarian S, Kelly AD, et al., 2018, TET1- Mediated Hypomethylation Activates Oncogenic Signaling in Triple-Negative Breast Cancer. Cancer Res, 78:4126–37. DOI: 10.1158/0008-5472.CAN-17-2082.

Oswald J, Engemann S, Lane N, et al., 2000, Active Demethylation of the Paternal Genome in the Mouse Zygote. Curr Biol, 10:475–8. DOI: 10.1016/S0960-9822(00)00448-6.

Mahadevan L, Ryu WS, Samuel AD, 1998, Demethylation of the Zygotic Paternal Genome. Nature, 392:140. DOI: 10.1038/32321.

Lorsbach RB, Moore J, Mathew S, et al., 2003, TET1, a Member of a Novel Protein Family, is Fused to MLL in Acute Myeloid Leukemia Containing the t(10;11)(q22;q23). Leukemia, 17:637–41. DOI: 10.1038/sj.leu.2402834.

Hu L, Li Z, Cheng J, et al., 2013, Crystal Structure of TET2- DNA Complex: Insight into TET-Mediated 5mC Oxidation. Cell, 155:1545–55. DOI: 10.1016/j.cell.2013.11.020.

Iyer LM, Tahiliani M, Rao A, et al., 2009, Prediction of Novel Families of Enzymes Involved in Oxidative and Other Complex Modifications of Bases in Nucleic Acids. Cell Cycle, 8:1698–710. DOI: 10.4161/cc.8.11.8580.

Iyer LM, Abhiman S, Aravind L, 2011, Natural History of Eukaryotic DNA Methylation Systems. Prog Mol Biol Transl Sci, 101:25–104. DOI: 10.1016/B978-0-12-387685-0.00002-0.

Pastor WA, Aravind L, Rao A, 2013, TETonic Shift: Biological Roles of TET Proteins in DNA Demethylation and Transcription. Nat Rev Mol Cell Biol, 14:341–56. DOI: 10.1038/nrm3589.

Frauer C, Rottach A, Meilinger D, et al., 2011, Different Binding Properties and Function of CXXC Zinc Finger Domains in Dnmt1 and Tet1. PLoS One, 6:e16627. DOI: 10.1371/journal.pone.0016627.

Xu Y, Wu F, Tan L, et al., 2011, Genome-wide Regulation of 5hmC, 5mC, and Gene Expression by Tet1 Hydroxylase in Mouse Embryonic Stem Cells. Mol Cell, 42:451–64. DOI: 10.1016/j.molcel.2011.04.005.

Ko M, An J, Bandukwala HS, et al., 2013, Modulation of TET2 Expression and 5-methylcytosine Oxidation by the CXXC Domain Protein IDAX. Nature, 497:122–6. DOI: 10.1038/nature12052.

Zhang W, Xia W, Wang Q, et al., 2016, Isoform Switch of TET1 Regulates DNA Demethylation and Mouse Development. Mol Cell, 64:1062–73. DOI: 10.1016/j. molcel.2016.10.030.

Good CR, Madzo J, Patel B, et al., 2017, A Novel Isoform of TET1 that Lacks a CXXC Domain is Overexpressed in Cancer. Nucleic Acids Res, 45:8269–81. DOI: 10.1093/nar/gkx435.

Jin SG, Zhang ZM, Dunwell TL, et al., 2016, Tet3 Reads 5-Carboxylcytosine through Its CXXC Domain and Is a Potential Guardian against Neurodegeneration. Cell Rep, 14:493–505. DOI: 10.1016/j.celrep.2015.12.044.

Kriaucionis S, Heintz N, 2009, The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain. Science, 324:929–30. DOI: 10.1126/science.1169786.

Tahiliani M, Koh KP, Shen Y, et al., 2009, Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1. Science, 324:930–5. DOI: 10.1126/science.1170116.

Ito S, Shen L, Dai Q, et al., 2011, Tet Proteins Can Convert 5-Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine. Science, 333:1300–3. DOI: 10.1126/ science.1210597.

He YF, Li BZ, Li Z, et al., 2011, Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision by TDG in Mammalian DNA. Science, 333:1303–7. DOI: 10.1126/ science.1210944.

Liu MY, Torabifard H, Crawford DJ, et al., 2017, Mutations along a TET2 Active Site Scaffold Stall Oxidation at 5-hydroxymethylcytosine. Nat Chem Biol, 13:181–7. DOI: 10.1038/nchembio.2250.

Yang H, Liu Y, Bai F, et al., 2013, Tumor Development is Associated with Decrease of TET Gene Expression and 5-methylcytosine Hydroxylation. Oncogene, 32:663–9. DOI: 10.1038/onc.2012.67.

Fu L, Guerrero CR, Zhong N, et al., 2014, Tet-Mediated Formation of 5-Hydroxymethylcytosine in RNA. J Am Chem Soc, 136:11582–5. DOI: 10.1021/ja505305z.

Basanta-Sanchez M, Wang R, Liu Z, et al., 2017, TET1- Mediated Oxidation of 5-Formylcytosine (5fC) to 5-Carboxycytosine (5caC) in RNA. Chembiochem, 18:72– 6. DOI: 10.1002/cbic.201600328.

Burleson JD, Siniard D, Yadagiri VK, et al., 2019, TET1 Contributes to Allergic Airway Inflammation and Regulates Interferon and Aryl Hydrocarbon Receptor Signaling Pathways in Bronchial Epithelial Cells. Sci Rep, 9:7361. DOI: 10.1038/s41598-019-43767-6.

Yamaguchi S, Shen L, Liu Y, et al., 2013, Role of Tet1 in Erasure of Genomic Imprinting. Nature, 504:460–4. DOI: 10.1038/nature12805.

Wu X, Zhang Y, 2017, TET-mediated Active DNA Demethylation: Mechanism, Function and Beyond. Nat Rev Genet, 18:517–34. DOI: 10.1038/nrg.2017.33.

Williams K, Christensen J, Pedersen MT, et al., 2011. TET1 and Hydroxymethylcytosine in Transcription and DNA Methylation Fidelity. Nature, 473:343–8. DOI: 10.1038/ nature10066.

Tsai YP, Chen HF, Chen SY, et al., 2014, TET1 Regulates Hypoxia-induced Epithelial-mesenchymal Transition by Acting as a Co-activator. Genome Biol, 15:513. DOI: 10.1186/s13059-014-0513-0.

Kao SH, Wu KJ, Lee WH, 2016, Hypoxia, Epithelial- Mesenchymal Transition, and TET-Mediated Epigenetic Changes. J Clin Med, 5:24. DOI: 10.3390/jcm5020024.

Gong F, Guo Y, Niu Y, et al., 2017, Epigenetic Silencing of TET2 and TET3 Induces an EMT-like Process in Melanoma. Oncotarget, 8:315–28. DOI: 10.18632/oncotarget.13324.

Chen HF, Wu, KJ, 2016, Epigenetics, TET Proteins, and Hypoxia in Epithelial-mesenchymal Transition and Tumorigenesis. Biomedicine, 6:1. DOI: 10.7603/s40681- 016-0001-9.

Lu F, Liu Y, Jiang L, et al., 2014, Role of Tet Proteins in Enhancer Activity and Telomere Elongation. Genes Dev, 28:2103–19. DOI: 10.1101/gad.248005.114.

Lio CW, Yue X, López-Moyado IF, et al., 2020, TET Methylcytosine Oxidases: New Insights from a Decade of Research. J Biosci, 45:21. DOI: 10.1007/s12038-019-9973-4.

Scourzic L, Mouly E, Bernard OA, 2015, TET Proteins and the Control Of Cytosine Demethylation in Cancer. Genome Med, 7:9. DOI: 10.1186/s13073-015-0134-6.

Pei Y, Tao R, Li J, et al., 2016, TET1 Inhibits Gastric Cancer Growth and Metastasis by PTEN Demethylation and Re-expression. Oncotarget, 7:31322–35. DOI: 10.18632/ oncotarget.8900.

Park SJ, Lee BR, Kim HS, et al., 2016, Inhibition of Migration and Invasion by Tet-1 Overexpression in Human Lung Carcinoma H460 Cells. Oncol Res, 23:89–98. DOI: 10.3727/096504015X14496932933539.

Wu J, Li H, Shi M, et al., 2019, TET1-mediated DNA Hydroxymethylation Activates Inhibitors of the Wnt/β- catenin Signaling Pathway to Suppress EMT in Pancreatic Tumor Cells. J Exp Clin Cancer Res, 38:348. DOI: 10.1186/ s13046-019-1334-5.

Duan H, Yan Z, Chen W, et al., 2017, TET1 Inhibits EMT of Ovarian Cancer Cells Through Activating Wnt/β-Catenin Signaling Inhibitors DKK1 and SFRP2. Gynecol Oncol, 147:408–17. DOI: 10.1016/j.ygyno.2017.08.010.

Neri F, Dettori D, Incarnato D, et al., 2015, TET1 is a Tumour Suppressor that Inhibits Colon Cancer Growth by Derepressing Inhibitors of the WNT Pathway. Oncogene, 34:4168–76. DOI: 10.1038/onc.2014.356.

Tian Y, Pan F, Sun X, et al., 2017, Association of TET1 Expression with Colorectal Cancer Progression. Scand J Gastroenterol, 52:312–20. DOI: 10.1080/00365521.2016.1253767.

Hsu CH, Peng KL, Kang ML, et al., 2012, TET1 Suppresses Cancer Invasion by Activating the Tissue Inhibitors of Metalloproteinases. Cell Rep, 2:568–79. DOI: 10.1016/j. celrep.2012.08.030.

Fan J, Zhang Y, Mu J, et al., 2018, TET1 Exerts its Anti-tumor Functions via Demethylating DACT2 and SFRP2 to Antagonize Wnt/β-Catenin Signaling Pathway in Nasopharyngeal Carcinoma Cells. Clin Epigenetics, 10:103. DOI: 10.1186/s13148-018-0535-7.

Forloni M, Gupta R, Nagarajan A, et al., 2016, Oncogenic EGFR Represses the TET1 DNA Demethylase to Induce Silencing of Tumor Suppressors in Cancer Cells. Cell Rep, 16:457–71. DOI: 10.1016/j.celrep.2016.05.087.

Sun M, Song CX, Huang H, et al., 2013, HMGA2/TET1/ HOXA9 Signaling Pathway Regulates Breast Cancer Growth and Metastasis. Proc Natl Acad Sci, 110:9920–5. DOI: 10.1073/pnas.1305172110.

Wang C, Ye H, Zhang L, et al., 2019, Enhanced Expression of Ten-eleven Translocation 1 Reverses Gemcitabine Resistance in Cholangiocarcinoma Accompanied by a Reduction in P-Glycoprotein Expression. Cancer Med, 8:990–1003. DOI: 10.1002/cam4.1983.

Collignon E, Canale A, Wardi CA, et al., 2018, Immunity Drives TET1 Regulation in Cancer through NF-kB. Sci Adv, 4:eaap7309.

Seo JS, Choi YH, Moon JW, et al., 2017, Hinokitiol Induces DNA Demethylation via DNMT1 and UHRF1 Inhibition in Colon Cancer Cells. BMC Cell Biol, 18:14. DOI: 10.1186/ s12860-017-0130-3.

Hore TA, 2017, Modulating Epigenetic Memory through Vitamins and TET: Implications for Regenerative Medicine and Cancer Treatment. Epigenomics, 9:863–71. DOI: 10.2217/epi-2017-0021.

Gustafson CB, Yang C, Dickson KM, et al., 2015, Epigenetic Reprogramming of Melanoma Cells by Vitamin C Treatment. Clin Epigenetics, 7:51. DOI: 10.1186/s13148- 015-0087-z.

Camarena V, Wang G, 2016, The Epigenetic Role of Vitamin C in Health and Disease. Cell Mol Life Sci, 73:1645–58. DOI: 10.1007/s00018-016-2145-x.

Ceccarelli V, Ronchetti S, Marchetti MC, et al., 2020, Molecular Mechanisms Underlying Eicosapentaenoic Acid Inhibition of HDAC1 and DNMT Expression and Activity in Carcinoma Cells. Biochim Biophys Acta, 1863:194481. DOI: 10.1016/j.bbagrm.2020.194481.

Ceccarelli V, Valentini V, Ronchetti S, et al., 2018, Eicosapentaenoic Acid Induces DNA Demethylation in Carcinoma Cells through a TET1-Dependent Mechanism. FASEB J, 32:5990–6001. DOI: 10.1096/fj.201800245R.

Han X, Zhou Y, You Y, et al., 2017, TET1 Promotes Cisplatin-resistance Via Demethylating the Vimentin Promoter in Ovarian Cancer: TET1 in Ovarian Cancer. Cell Biol Int, 41:405–14. DOI:10.1002/cbin.10734.

Wang W, Li X, Wang F, et al., 2018, Effect of TET1 Regulating MGMT on Chemotherapy Resistance of Oral Squamous Cell Carcinoma Stem Cells. J Cell Biochem, 119:723–35. DOI: 10.1002/jcb.26236.

Melamed P, Yosefzon Y, David C, et al., 2018, Tet Enzymes, Variants, and Differential Effects on Function. Front Cell Dev Biol, 6:22. DOI: 10.3389/fcell.2018.00022.

Pei Y, Lei Y, Liu X, 2016, MiR-29a Promotes Cell Proliferation and EMT in Breast Cancer by Targeting Ten Eleven Translocation 1. Biochim Biophys Acta, 1862:2177– 85. DOI: 10.1016/j.bbadis.2016.08.014.

Morita S, Horii T, Kimura M, et al., 2013, miR-29 Represses the Activities of DNA Methyltransferases and DNA Demethylases. Int J Mol Sci, 14:14647–58. DOI: 10.3390/ijms140714647.

Chuang KH, Whitney-Miller CL, Chu CY, et al., 2015, MicroRNA-494 is a Master Epigenetic Regulator of Multiple Invasion-suppressor microRNAs by Targeting ten Eleven Translocation 1 in Invasive Human Hepatocellular Carcinoma Tumors. Hepatology, 62:466–80. DOI: 10.1002/hep.27816.

Chen N, Zhao G, Yan X, et al., 2018, A Novel FLI1 Exonic Circular RNA Promotes Metastasis in Breast Cancer by Coordinately Regulating TET1 and DNMT1. Genome Biol, 19:218. DOI: 10.1186/s13059-018-1594-y.

Wang P, Yan Y, Yu W, et al., 2019, Role of Ten‐eleven Translocation Proteins and 5-hydroxymethylcytosine in Hepatocellular Carcinoma. Cell Prolif, 52:e12626. DOI: 10.1111/cpr.12626.

Liu J, Jiang J, Mo J, et al., 2019, Global DNA 5-Hydroxymethylcytosine and 5-Formylcytosine Contents Are Decreased in the Early Stage of Hepatocellular Carcinoma. Hepatology, 69:196–208. DOI: 10.1002/ hep.30146.

Koch A, Joosten SC, Feng Z, et al., 2018, Analysis of DNA methylation in cancer: location revisited. Nat Rev Clin Oncol, 15:459–66. DOI: 10.1038/s41571-018-0004-4.

Heyn H, Esteller M, 2012, DNA Methylation Profiling in the Clinic: Applications and Challenges. Nat Rev Genet, 13:679–92. DOI: 10.1038/nrg3270.

Zhang M, Fujiwara K, Che X, et al., 2017, DNA Methylation in the Tumor Microenvironment. J Zhejiang Univ Sci B, 18:365–72. DOI: 10.1631/jzus.B1600579.

Zhang M, Yang H, Wan L, et al., 2020, Single-cell Transcriptomic Architecture and Intercellular Crosstalk of Human Intrahepatic Cholangiocarcinoma. J Hepatol, 1:39. DOI: 10.1016/j.jhep.2020.05.039.

Klymenko Y, Nephew KP, 2018, Epigenetic Crosstalk between the Tumor Microenvironment and Ovarian Cancer Cells: A Therapeutic Road Less Traveled. Cancers, 10:295. DOI: 10.3390/cancers10090295.




DOI: http://dx.doi.org/10.18063/c+.v2i2.287

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