Roles of ten‑eleven translocation family proteins and their O‑linked β‑N‑acetylglucosaminylated forms in cancer development (Review)
- Authors:
- Hong-Jiao Li
- Yi Wang
- Bing-Xin Li
- Yang Yang
- Feng Guan
- Xing-Chen Pang
- Xiang Li
-
Affiliations: Key Laboratory of Resource Biology and Biotechnology Western China, College of Life Sciences, Northwest University, Xi'an, Shaanxi 710069, P.R. China, Department of Hematology, Provincial People's Hospital, Xi'an, Shaanxi 710069, P.R. China - Published online on: November 3, 2020 https://doi.org/10.3892/ol.2020.12262
- Article Number: 1
-
Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Schubeler D: Function and information content of DNA methylation. Nature. 517:321–326. 2015. View Article : Google Scholar : PubMed/NCBI | |
Scott-Browne JP, Lio CJ and Rao A: TET proteins in natural and induced differentiation. Curr Opin Genet Dev. 46:202–208. 2017. View Article : Google Scholar : PubMed/NCBI | |
Yang X and Qian K: Protein O-GlcNAcylation: Emerging mechanisms and functions. Nat Rev Mol Cell Biol. 18:452–465. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wells L, Vosseller K and Hart GW: Glycosylation of nucleocytoplasmic proteins: Signal transduction and O-GlcNAc. Science. 291:2376–2378. 2001. View Article : Google Scholar : PubMed/NCBI | |
Hart GW, Housley MP and Slawson C: Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature. 446:1017–1022. 2007. View Article : Google Scholar : PubMed/NCBI | |
Vella P, Scelfo A, Jammula S, Chiacchiera F, Williams K, Cuomo A, Roberto A, Christensen J, Bonaldi T, Helin K and Pasini D: Tet proteins connect the O-linked N-acetylglucosamine transferase Ogt to chromatin in embryonic stem cells. Mol Cell. 49:645–656. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hrit J, Goodrich L, Li C, Wang BA, Nie J, Cui X, Martin EA, Simental E, Fernandez J, Liu MY, et al: OGT binds a conserved C-terminal domain of TET1 to regulate TET1 activity and function in development. Elife. 7:e348702018. View Article : Google Scholar : PubMed/NCBI | |
Baylin SB and Jones PA: A decade of exploring the cancer epigenome-biological and translational implications. Nat Rev Cancer. 11:726–734. 2011. View Article : Google Scholar : PubMed/NCBI | |
Darılmaz Yüce G and Ortaç Ersoy E: Lung cancer and epigenetic modifications. Tuberk Toraks. 64:163–170. 2016.(In Turkish). View Article : Google Scholar : PubMed/NCBI | |
Sasanakietkul T, Murtha TD, Javid M, Korah R and Carling T: Epigenetic modifications in poorly differentiated and anaplastic thyroid cancer. Mol Cell Endocrinol. 469:23–37. 2018. View Article : Google Scholar : PubMed/NCBI | |
Alam R, Abdolmaleky HM and Zhou JR: Microbiome, inflammation, epigenetic alterations, and mental diseases. Am J Med Genet B Neuropsychiatr Genet. 174:651–660. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ciesielski P, Jozwiak P and Krzeslak A: TET proteins and epigenetic modifications in cancers. Postepy Hig Med Dosw (Online). 69:1371–1383. 2015.(In Polish). View Article : Google Scholar : PubMed/NCBI | |
Li D and Zeng Z: Epigenetic regulation of histone H3 in the process of hepatocellular tumorigenesis. Biosci Rep. 39:BSR201918152019. View Article : Google Scholar : PubMed/NCBI | |
Losi L, Lauriola A, Tazzioli E, Gozzi G, Scurani L, D'Arca D and Benhattar J: Involvement of epigenetic modification of TERT promoter in response to all-trans retinoic acid in ovarian cancer cell lines. J Ovarian Res. 12:622019. View Article : Google Scholar : PubMed/NCBI | |
Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L and Rao A: Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 324:930–935. 2009. View Article : Google Scholar : PubMed/NCBI | |
Song J, Moscinski L, Zhang H, Zhang X and Hussaini M: Does SF3B1/TET2 double mutation portend better or worse prognosis Than Isolated SF3B1 or TET2 Mutation? Cancer Genomics Proteomics. 16:91–98. 2019. View Article : Google Scholar : PubMed/NCBI | |
Shen L, Wu H, Diep D, Yamaguchi S, D'Alessio AC, Fung HL, Zhang K and Zhang Y: Genome-wide analysis reveals TET- and TDG-dependent 5-methylcytosine oxidation dynamics. Cell. 153:692–706. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ko M, An J, Bandukwala HS, Chavez L, Aijö T, Pastor WA, Segal MF, Li H, Koh KP, Lähdesmäki H, et al: Modulation of TET2 expression and 5-methylcytosine oxidation by the CXXC domain protein IDAX. Nature. 497:122–126. 2013. View Article : Google Scholar : PubMed/NCBI | |
Good CR, Madzo J, Patel B, Maegawa S, Engel N, Jelinek J and Issa JJ: A novel isoform of TET1 that lacks a CXXC domain is overexpressed in cancer. Nucleic Acids Res. 45:8269–8281. 2017. View Article : Google Scholar : PubMed/NCBI | |
Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, Laiho A, Tahiliani M, Sommer CA, Mostoslavsky G, et al: Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell. 8:200–213. 2011. View Article : Google Scholar : PubMed/NCBI | |
Dawlaty MM, Breiling A, Le T, Barrasa MI, Raddatz G, Gao Q, Powell BE, Cheng AW, Faull KF, Lyko F and Jaenisch R: Loss of Tet enzymes compromises proper differentiation of embryonic stem cells. Dev Cell. 29:102–111. 2014. View Article : Google Scholar : PubMed/NCBI | |
Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L, He X, Jin SG, et al: The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature. 477:606–610. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C and Zhang Y: Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science. 333:1300–1303. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cheng J, Guo S, Chen S, Mastriano SJ, Liu C, D'Alessio AC, Hysolli E, Guo Y, Yao H, Megyola CM, et al: An extensive network of TET2-targeting microRNAs regulates malignant hematopoiesis. Cell Rep. 5:471–481. 2013. View Article : Google Scholar : PubMed/NCBI | |
Yang H, Liu Y, Bai F, Zhang JY, Ma SH, Liu J, Xu ZD, Zhu HG, Ling ZQ, Ye D, et al: Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene. 32:663–669. 2013. View Article : Google Scholar : PubMed/NCBI | |
Haferlach T, Nagata Y, Grossmann V, Okuno Y, Bacher U, Nagae G, Schnittger S, Sanada M, Kon A, Alpermann T, et al: Landscape of genetic lesions in 944 patients with myelodysplastic syndromes. Leukemia. 28:241–247. 2014. View Article : Google Scholar : PubMed/NCBI | |
Fernandez-Mercado M, Yip BH, Pellagatti A, Davies C, Larrayoz MJ, Kondo T, Pérez C, Killick S, McDonald EJ, Odero MD, et al: Mutation patterns of 16 genes in primary and secondary acute myeloid leukemia (AML) with normal cytogenetics. PLoS One. 7:e423342012. View Article : Google Scholar : PubMed/NCBI | |
Shih AH, Abdel-Wahab O, Patel JP and Levine RL: The role of mutations in epigenetic regulators in myeloid malignancies. Nat Rev Cancer. 12:599–612. 2012. View Article : Google Scholar : PubMed/NCBI | |
Li R, Zhou Y, Cao Z, Liu L, Wang J, Chen Z, Xing W, Chen S, Bai J, Yuan W, et al: TET2 loss dysregulates the behavior of bone marrow mesenchymal stromal cells and accelerates Tet2−/−Driven myeloid malignancy progression. Stem Cell Reports. 10:166–179. 2018. View Article : Google Scholar : PubMed/NCBI | |
Li Z, Cai X, Cai CL, Wang J, Zhang W, Petersen BE, Yang FC and Xu M: Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood. 118:4509–4518. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wang L, Ozark PA, Smith ER, Zhao Z, Marshall SA, Rendleman EJ, Piunti A, Ryan C, Whelan AL, Helmin KA, et al: TET2 coactivates gene expression through demethylation of enhancers. Sci Adv. 4:eaau69862018. View Article : Google Scholar : PubMed/NCBI | |
Pan W, Zhu S, Qu K, Meeth K, Cheng J, He K, Ma H, Liao Y, Wen X, Roden C, et al: The DNA Methylcytosine Dioxygenase Tet2 sustains immunosuppressive function of Tumor-infiltrating myeloid cells to promote melanoma progression. Immunity. 47:284–297.e5. 2017. View Article : Google Scholar : PubMed/NCBI | |
Itoh H, Kadomatsu T, Tanoue H, Yugami M, Miyata K, Endo M, Morinaga J, Kobayashi E, Miyamoto T, Kurahashi R, et al: TET2-dependent IL-6 induction mediated by the tumor microenvironment promotes tumor metastasis in osteosarcoma. Oncogene. 37:2903–2920. 2018. View Article : Google Scholar : PubMed/NCBI | |
Levine ZG and Walker S: The Biochemistry of O-GlcNAc Transferase: Which functions make it essential in mammalian cells? Annu Rev Biochem. 85:631–657. 2016. View Article : Google Scholar : PubMed/NCBI | |
Ma J, Banerjee P, Whelan SA, Liu T, Wei AC, Ramirez-Correa G, McComb ME, Costello CE, O'Rourke B, Murphy A and Hart GW: Comparative proteomics reveals dysregulated mitochondrial O-GlcNAcylation in diabetic hearts. J Proteome Res. 15:2254–2264. 2016. View Article : Google Scholar : PubMed/NCBI | |
Hart GW, Slawson C, Ramirez-Correa G and Lagerlof O: Cross talk between O-GlcNAcylation and phosphorylation: Roles in signaling, transcription, and chronic disease. Annu Rev Biochem. 80:825–858. 2011. View Article : Google Scholar : PubMed/NCBI | |
Love DC and Hanover JA: The hexosamine signaling pathway: Deciphering the ‘O-GlcNAc code’. Sci STKE. 2005:re132005.PubMed/NCBI | |
Gambetta MC and Muller J: A critical perspective of the diverse roles of O-GlcNAc transferase in chromatin. Chromosoma. 124:429–442. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bond MR and Hanover JA: O-GlcNAc cycling: A link between metabolism and chronic disease. Annu Rev Nutr. 33:205–229. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hanover JA, Krause MW and Love DC: Bittersweet memories: Linking metabolism to epigenetics through O-GlcNAcylation. Nat Rev Mol Cell Biol. 13:312–321. 2012. View Article : Google Scholar : PubMed/NCBI | |
Mulloy B, Dell A, Stanley P and James HP: Structural analysis of glycans. In: Essentials of Glycobiology 3rd. Varki A, Cummings RD, Esko JD, Stanley P, Hart GW, et al: Cold Spring Harbor; NY: pp. 639–652. 2015, PubMed/NCBI | |
Maynard JC, Burlingame AL and Medzihradszky KF: Cysteine S-linked N-acetylglucosamine (S-GlcNAcylation), A new post-translational modification in mammals. Mol Cell Proteomics. 15:3405–3411. 2016. View Article : Google Scholar : PubMed/NCBI | |
Berthier A, Vinod M, Porez G, Steenackers A, Alexandre J, Yamakawa N, Gheeraert C, Ploton M, Maréchal X, Dubois-Chevalier J, et al: Combinatorial regulation of hepatic cytoplasmic signaling and nuclear transcriptional events by the OGT/REV-ERBα complex. Proc Natl Acad Sci USA. 115:E11033–E11042. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gao J, Yang Y, Qiu R, Zhang K, Teng X, Liu R and Wang Y: Proteomic analysis of the OGT interactome: Novel links to epithelial-mesenchymal transition and metastasis of cervical cancer. Carcinogenesis. 39:1222–1234. 2018. View Article : Google Scholar : PubMed/NCBI | |
Biwi J, Clarisse C, Biot C, Kozak RP, Madunic K, Mortuaire M, Wuhrer M, Spencer DIR, Schulz C, Guerardel Y, et al: OGT Controls the expression and the glycosylation of E-cadherin, and affects glycosphingolipid structures in human colon cell lines. Proteomics. 19:e18004522019. View Article : Google Scholar : PubMed/NCBI | |
Shi Y, Tomic J, Wen F, Shaha S, Bahlo A, Harrison R, Dennis JW, Williams R, Gross BJ, Walker S, et al: Aberrant O-GlcNAcylation characterizes chronic lymphocytic leukemia. Leukemia. 24:1588–1598. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hayakawa K, Hirosawa M, Tabei Y, Arai D, Tanaka S, Murakami N, Yagi S and Shiota K: Epigenetic switching by the metabolism- sensing factors in the generation of orexin neurons from mouse embryonic stem cells. J Biol Chem. 288:17099–17110. 2013. View Article : Google Scholar : PubMed/NCBI | |
Toleman C, Paterson AJ, Whisenhunt TR and Kudlow JE: Characterization of the histone acetyltransferase (HAT) domain of a bifunctional protein with activable O-GlcNAcase and HAT activities. J Biol Chem. 279:53665–53673. 2004. View Article : Google Scholar : PubMed/NCBI | |
Singh JP, Qian K, Lee JS, Zhou J, Han X, Zhang B, Ong Q, Ni W, Jiang M, Ruan HB, et al: O-GlcNAcase targets pyruvate kinase M2 to regulate tumor growth. Oncogene. 39:560–573. 2020. View Article : Google Scholar : PubMed/NCBI | |
Macauley MS, Shan X, Yuzwa SA, Gloster TM and Vocadlo DJ: Elevation of Global O-GlcNAc in rodents using a selective O-GlcNAcase inhibitor does not cause insulin resistance or perturb glucohomeostasis. Chem Biol. 17:949–958. 2010. View Article : Google Scholar : PubMed/NCBI | |
Fuentes-García G, Castañeda-Patlan MC, Vercoutter-Edouart AS, Lefebvre T and Robles-Flores M: O-GlcNAcylation Is Involved in the regulation of stem cell markers expression in colon cancer cells. Front Endocrinol (Lausanne). 10:2892019. View Article : Google Scholar : PubMed/NCBI | |
Jang H, Kim TW, Yoon S, Choi SY, Kang TW, Kim SY, Kwon YW, Cho EJ and Youn HD: O-GlcNAc regulates pluripotency and reprogramming by directly acting on core components of the pluripotency network. Cell Stem Cell. 11:62–74. 2012. View Article : Google Scholar : PubMed/NCBI | |
Olivier-Van Stichelen S, Wang P, Comly M, Love DC and Hanover JA: Nutrient-driven O-linked N-acetylglucosamine (O-GlcNAc) cycling impacts neurodevelopmental timing and metabolism. J Biol Chem. 292:6076–6085. 2017. View Article : Google Scholar : PubMed/NCBI | |
Abramowitz LK, Harly C, Das A, Bhandoola A and Hanover JA: Blocked O-GlcNAc cycling disrupts mouse hematopoeitic stem cell maintenance and early T cell development. Sci Rep. 9:125692019. View Article : Google Scholar : PubMed/NCBI | |
Delatte B and Fuks F: TET proteins: On the frenetic hunt for new cytosine modifications. Brief Funct Genomics. 12:191–204. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ito R, Katsura S, Shimada H, Tsuchiya H, Hada M, Okumura T, Sugawara A and Yokoyama A: TET3-OGT interaction increases the stability and the presence of OGT in chromatin. Genes Cells. 19:52–65. 2014. View Article : Google Scholar : PubMed/NCBI | |
Shi FT, Kim H, Lu W, He Q, Liu D, Goodell MA, Wan M and Songyang Z: Ten-eleven translocation 1 (Tet1) is regulated by O-linked N-acetylglucosamine transferase (Ogt) for target gene repression in mouse embryonic stem cells. J Biol Chem. 288:20776–20784. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q, Liu X, Gao W, Li P, Hou J, Li J and Wong J: Differential regulation of the ten-eleven translocation (TET) family of dioxygenases by O-linked β-N-acetylglucosamine transferase (OGT). J Biol Chem. 289:5986–5996. 2014. View Article : Google Scholar : PubMed/NCBI | |
Bauer C, Gobel K, Nagaraj N, Colantuoni C, Wang M, Müller U, Kremmer E, Rottach A and Leonhardt H: Phosphorylation of TET proteins is regulated via O-GlcNAcylation by the O-linked N-acetylglucosamine transferase (OGT). J Biol Chem. 290:4801–4812. 2015. View Article : Google Scholar : PubMed/NCBI | |
Singh JP, Zhang K, Wu J and Yang X: O-GlcNAc signaling in cancer metabolism and epigenetics. Cancer Lett. 356:244–250. 2015. View Article : Google Scholar : PubMed/NCBI | |
Fujiki R, Hashiba W, Sekine H, Yokoyama A, Chikanishi T, Ito S, Imai Y, Kim J, He HH, Igarashi K, et al: GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature. 480:557–560. 2011. View Article : Google Scholar : PubMed/NCBI | |
Chen Q, Chen Y, Bian C, Fujiki R and Yu X: TET2 promotes histone O-GlcNAcylation during gene transcription. Nature. 493:561–564. 2013. View Article : Google Scholar : PubMed/NCBI | |
Deplus R, Delatte B, Schwinn MK, Defrance M, Mendez J, Murphy N, Dawson MA, Volkmar M, Putmans P, Calonne E, et al: TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J. 32:645–655. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hsu CH, Peng KL, Kang ML, Chen YR, Yang YC, Tsai CH, Chu CS, Jeng YM, Chen YT, Lin FM, et al: TET1 suppresses cancer invasion by activating the tissue inhibitors of metalloproteinases. Cell Rep. 2:568–579. 2012. View Article : Google Scholar : PubMed/NCBI | |
Guan W, Guyot R, Samarut J, Flamant F, Wong J and Gauthier KC: Methylcytosine dioxygenase TET3 interacts with thyroid hormone nuclear receptors and stabilizes their association to chromatin. Proc Natl Acad Sci USA. 114:8229–8234. 2017. View Article : Google Scholar : PubMed/NCBI | |
Phoomak C, Silsirivanit A, Park D, Sawanyawisuth K, Vaeteewoottacharn K, Wongkham C, Lam EW, Pairojkul C, Lebrilla CB and Wongkham S: O-GlcNAcylation mediates metastasis of cholangiocarcinoma through FOXO3 and MAN1A1. Oncogene. 37:5648–565. 2018. View Article : Google Scholar : PubMed/NCBI | |
Liberti MV and Locasale JW: The warburg effect: How does it benefit cancer cells? Trends Biochem Sci. 41:211–228. 2016. View Article : Google Scholar : PubMed/NCBI | |
Ma Z and Vosseller K: Cancer metabolism and elevated O-GlcNAc in oncogenic signaling. J Biol Chem. 289:34457–34465. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yang WH, Kim JE, Nam HW, Ju JW, Kim HS, Kim YS and Cho JW: Modification of p53 with O-linked N-acetylglucosamine regulates p53 activity and stability. Nat Cell Biol. 8:1074–1083. 2026. View Article : Google Scholar | |
Itkonen HM, Minner S, Guldvik IJ, Sandmann MJ, Tsourlakis MC, Berge V, Svindland A, Schlomm T and Mills IG: O-GlcNAc transferase integrates metabolic pathways to regulate the stability of c-MYC in human prostate cancer cells. Cancer Res. 73:5277–5287. 2013. View Article : Google Scholar : PubMed/NCBI | |
Olivier-Van Stichelen S, Guinez C, Mir AM, Perez-Cervera Y, Liu C, Michalski JC and Lefebvre T: The hexosamine biosynthetic pathway and O-GlcNAcylation drive the expression of β-catenin and cell proliferation. Am J Physiol Endocrinol Metab. 302:E417–E424. 2012. View Article : Google Scholar : PubMed/NCBI | |
Thomson JP, Ottaviano R, Unterberger EB, Lempiäinen H, Muller A, Terranova R, Illingworth RS, Webb S, Kerr AR, Lyall MJ, et al: Loss of Tet1-Associated 5-hydroxymethylcytosine is concomitant with aberrant promoter hypermethylation in liver cancer. Cancer Res. 76:3097–3108. 2016. View Article : Google Scholar : PubMed/NCBI | |
Delhommeau F, Dupont S, Della Valle V, James C, Trannoy S, Massé A, Kosmider O, Le Couedic JP, Robert F, Alberdi A, et al: Mutation in TET2 in myeloid cancers. N Engl J Med. 360:2289–2301. 2029. View Article : Google Scholar | |
Itzykson R, Kosmider O, Renneville A, Gelsi-Boyer V, Meggendorfer M, Morabito M, Berthon C, Adès L, Fenaux P, Beyne-Rauzy O, et al: Prognostic score including gene mutations in chronic myelomonocytic leukemia. J Clin Oncol. 31:2428–2436. 2013. View Article : Google Scholar : PubMed/NCBI | |
Nibourel O, Kosmider O, Cheok M, Boissel N, Renneville A, Philippe N, Dombret H, Dreyfus F, Quesnel B, Geffroy S, et al: Incidence and prognostic value of TET2 alterations in de novo acute myeloid leukemia achieving complete remission. Blood. 116:1132–1135. 2010. View Article : Google Scholar : PubMed/NCBI | |
Dominguez PM, Ghamlouch H, Rosikiewicz W, Kumar P, Béguelin W, Fontán L, Rivas MA, Pawlikowska P, Armand M, Mouly E, et al: TET2 deficiency causes germinal center hyperplasia, impairs plasma cell differentiation, and promotes B-cell lymphomagenesis. Cancer Discov. 8:1632–1653. 2018.PubMed/NCBI | |
Cao T, Pan W, Sun X and Shen H: Increased expression of TET3 predicts unfavorable prognosis in patients with ovarian cancer-a bioinformatics integrative analysis. J Ovarian Res. 12:1012019. View Article : Google Scholar : PubMed/NCBI | |
Carella A, Tejedor JR, García MG, Urdinguio RG, Bayón GF, Sierra M, López V, García-Toraño E, Santamarina-Ojeda P, Pérez RF, et al: Epigenetic downregulation of TET3 reduces genome-wide 5hmC levels and promotes glioblastoma tumorigenesis. Int J Cancer. 146:373–387. 2020. View Article : Google Scholar : PubMed/NCBI |