Scientific Papers

Vitamin C activates young LINE-1 elements in mouse embryonic stem cells via H3K9me3 demethylation | Epigenetics & Chromatin


  • Gut P, Verdin E. The nexus of chromatin regulation and intermediary metabolism. Nature. 2013;502(7472):489–98.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dai Z, Ramesh V, Locasale JW. The evolving metabolic landscape of chromatin biology and epigenetics. Nat Rev Genet. 2020;21(12):737–53.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carey BW, Finley LWS, Cross JR, Allis CD, Thompson CB. Intracellular α-ketoglutarate maintains the pluripotency of embryonic stem cells. Nature. 2015;518(7539):413–6.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Thienpont B, Steinbacher J, Zhao H, D’Anna F, Kuchnio A, Ploumakis A, et al. Tumour hypoxia causes DNA hypermethylation by reducing TET activity. Nature. 2016;537(7618):63–8.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Blaschke K, Ebata KT, Karimi MM, Zepeda-Martínez JA, Goyal P, Mahapatra S, et al. Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells. Nature. 2013;500(7461):222–6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Young JI, Züchner S, Wang G. Regulation of the epigenome by vitamin C. Annu Rev Nutr. 2015;6(35):545–64.

    Article 

    Google Scholar
     

  • Minor EA, Court BL, Young JI, Wang G. Ascorbate induces ten-eleven translocation (Tet) methylcytosine dioxygenase-mediated generation of 5-hydroxymethylcytosine. J Biol Chem. 2013;288(19):13669–74.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Monfort A, Wutz A. Breathing-in epigenetic change with vitamin C. EMBO Rep. 2013;14(4):337–46.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chung T-L, Brena RM, Kolle G, Grimmond SM, Berman BP, Laird PW, et al. Vitamin C promotes widespread yet specific DNA demethylation of the epigenome in human embryonic stem cells. Stem Cells. 2010;28(10):1848–55.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Stadtfeld M, Apostolou E, Ferrari F, Choi J, Walsh RM, Chen T, et al. Ascorbic acid prevents loss of Dlk1-Dio3 imprinting and facilitates generation of all-iPS cell mice from terminally differentiated B cells. Nat Genet. 2012;44(4):398–405.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Esteban MA, Wang T, Qin B, Yang J, Qin D, Cai J, et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell. 2010;6(1):71–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen J, Guo L, Zhang L, Wu H, Yang J, Liu H, et al. Vitamin C modulates TET1 function during somatic cell reprogramming. Nat Genet. 2013;45(12):1504–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Doege CA, Inoue K, Yamashita T, Rhee DB, Travis S, Fujita R, et al. Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature. 2012;488(7413):652–5.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Costa Y, Ding J, Theunissen TW, Faiola F, Hore TA, Shliaha PV, et al. NANOG-dependent function of TET1 and TET2 in establishment of pluripotency. Nature. 2013;495(7441):370–4.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gao Y, Chen J, Li K, Wu T, Huang B, Liu W, et al. Replacement of Oct4 by Tet1 during iPSC induction reveals an important role of DNA methylation and hydroxymethylation in reprogramming. Cell Stem Cell. 2013;12(4):453–69.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen J, Liu H, Liu J, Qi J, Wei B, Yang J, et al. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat Genet. 2013;45(1):34–42.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang T, Chen K, Zeng X, Yang J, Wu Y, Shi X, et al. The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell. 2011;9(6):575–87.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dickson KM, Gustafson CB, Young JI, Züchner S, Wang G. Ascorbate-induced generation of 5-hydroxymethylcytosine is unaffected by varying levels of iron and 2-oxoglutarate. Biochem Biophys Res Commun. 2013;439(4):522–7.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yin R, Mao S-Q, Zhao B, Chong Z, Yang Y, Zhao C, et al. Ascorbic acid enhances Tet-mediated 5-methylcytosine oxidation and promotes DNA demethylation in mammals. J Am Chem Soc. 2013;135(28):10396–403.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ebata KT, Mesh K, Liu S, Bilenky M, Fekete A, Acker MG, et al. Vitamin C induces specific demethylation of H3K9me2 in mouse embryonic stem cells via Kdm3a/b. Epigenet Chromatin. 2017;12(10):36.

    Article 

    Google Scholar
     

  • DiTroia SP, Percharde M, Guerquin M-J, Wall E, Collignon E, Ebata KT, et al. Maternal vitamin C regulates reprogramming of DNA methylation and germline development. Nature. 2019;573(7773):271–5.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yue X, Rao A. TET family dioxygenases and the TET activator vitamin C in immune responses and cancer. Blood. 2020;136(12):1394–401.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gustafson CB, Yang C, Dickson KM, Shao H, Van Booven D, Harbour JW, et al. Epigenetic reprogramming of melanoma cells by vitamin C treatment. Clin Epigenet. 2015;7(1):51.

    Article 

    Google Scholar
     

  • Agathocleous M, Meacham CE, Burgess RJ, Piskounova E, Zhao Z, Crane GM, et al. Ascorbate regulates haematopoietic stem cell function and leukaemogenesis. Nature. 2017;549(7673):476–81.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A, Hammell M, et al. Ten things you should know about transposable elements. Genome Biol. 2018;19(1):199.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Klawitter S, Fuchs NV, Upton KR, Muñoz-Lopez M, Shukla R, Wang J, et al. Reprogramming triggers endogenous L1 and Alu retrotransposition in human induced pluripotent stem cells. Nat Commun. 2016;8(7):10286.

    Article 

    Google Scholar
     

  • Gerdes P, Lim SM, Ewing AD, Larcombe MR, Chan D, Sanchez-Luque FJ, et al. Retrotransposon instability dominates the acquired mutation landscape of mouse induced pluripotent stem cells. Nat Commun. 2022;13(1):7470.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wissing S, Muñoz-Lopez M, Macia A, Yang Z, Montano M, Collins W, et al. Reprogramming somatic cells into iPS cells activates LINE-1 retroelement mobility. Hum Mol Genet. 2012;21(1):208–18.

    Article 
    PubMed 

    Google Scholar
     

  • Fueyo R, Judd J, Feschotte C, Wysocka J. Roles of transposable elements in the regulation of mammalian transcription. Nat Rev Mol Cell Biol. 2022;23(7):481–97.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lawson HA, Liang Y, Wang T. Transposable elements in mammalian chromatin organization. Nat Rev Genet. 2023;24:712.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gazquez-Gutierrez A, Witteveldt J, Heras SR, Macias S. Sensing of transposable elements by the antiviral innate immune system. RNA. 2021;27(7):735–52.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • de la Rica L, Deniz Ö, Cheng KCL, Todd CD, Cruz C, Houseley J, et al. TET-dependent regulation of retrotransposable elements in mouse embryonic stem cells. Genome Biol. 2016;17(1):234.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Deniz Ö, de la Rica L, Cheng KCL, Spensberger D, Branco MR. SETDB1 prevents TET2-dependent activation of IAP retroelements in naïve embryonic stem cells. Genome Biol. 2018;19(1):6.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Walter M, Teissandier A, Pérez-Palacios R, Bourc’his D. An epigenetic switch ensures transposon repression upon dynamic loss of DNA methylation in embryonic stem cells. Elife. 2016;27(5): e11418.

    Article 

    Google Scholar
     

  • Liu M, Ohtani H, Zhou W, Ørskov AD, Charlet J, Zhang YW, et al. Vitamin C increases viral mimicry induced by 5-aza-2’-deoxycytidine. Proc Natl Acad Sci USA. 2016;113(37):10238–44.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Silva J, Barrandon O, Nichols J, Kawaguchi J, Theunissen TW, Smith A. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol. 2008;6(10): e253.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carey TS, Cao Z, Choi I, Ganguly A, Wilson CA, Paul S, et al. BRG1 governs nanog transcription in early mouse embryos and embryonic stem cells via antagonism of histone H3 lysine 9/14 acetylation. Mol Cell Biol. 2015;35(24):4158–69.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yang WR, Ardeljan D, Pacyna CN, Payer LM, Burns KH. SQuIRE reveals locus-specific regulation of interspersed repeat expression. Nucleic Acids Res. 2019;47(5): e27.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gagnier L, Belancio VP, Mager DL. Mouse germ line mutations due to retrotransposon insertions. Mob DNA. 2019;13(10):15.

    Article 

    Google Scholar
     

  • de la Rica L, Stanley JS, Branco MR. Profiling DNA methylation and hydroxymethylation at retrotransposable elements. Methods Mol Biol. 2016;1400:387–401.

    Article 
    PubMed 

    Google Scholar
     

  • Hu X, Zhang L, Mao S-Q, Li Z, Chen J, Zhang R-R, et al. Tet and TDG mediate DNA demethylation essential for mesenchymal-to-epithelial transition in somatic cell reprogramming. Cell Stem Cell. 2014;14(4):512–22.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, Matsuoka C, et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells. 2006;11(7):805–14.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Robbez-Masson L, Tie CHC, Conde L, Tunbak H, Husovsky C, Tchasovnikarova IA, et al. The HUSH complex cooperates with TRIM28 to repress young retrotransposons and new genes. Genome Res. 2018;28(6):836–45.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, et al. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature. 2010;463(7278):237–40.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tomaz RA, Harman JL, Karimlou D, Weavers L, Fritsch L, Bou-Kheir T, et al. Jmjd2c facilitates the assembly of essential enhancer-protein complexes at the onset of embryonic stem cell differentiation. Development. 2017;144(4):567–79.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pedersen MT, Kooistra SM, Radzisheuskaya A, Laugesen A, Johansen JV, Hayward DG, et al. Continual removal of H3K9 promoter methylation by Jmjd2 demethylases is vital for ESC self-renewal and early development. EMBO J. 2016;35(14):1550–64.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Iwamori N, Zhao M, Meistrich ML, Matzuk MM. The testis-enriched histone demethylase, KDM4D, regulates methylation of histone H3 lysine 9 during spermatogenesis in the mouse but is dispensable for fertility. Biol Reprod. 2011;84(6):1225–34.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu S, Brind’Amour J, Karimi MM, Shirane K, Bogutz A, Lefebvre L, et al. Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells. Genes Dev. 2014;28(18):2041–55.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, et al. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature. 2010;464(7290):927–31.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Karimi MM, Goyal P, Maksakova IA, Bilenky M, Leung D, Tang JX, et al. DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell. 2011;8(6):676–87.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Streva VA, Jordan VE, Linker S, Hedges DJ, Batzer MA, Deininger PL. Sequencing, identification and mapping of primed L1 elements (SIMPLE) reveals significant variation in full length L1 elements between individuals. BMC Genomics. 2015;16(1):220.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Witherspoon DJ, Xing J, Zhang Y, Watkins WS, Batzer MA, Jorde LB. Mobile element scanning (ME-Scan) by targeted high-throughput sequencing. BMC Genomics. 2010;30(11):410.

    Article 

    Google Scholar
     

  • Macia A, Widmann TJ, Heras SR, Ayllon V, Sanchez L, Benkaddour-Boumzaouad M, et al. Engineered LINE-1 retrotransposition in nondividing human neurons. Genome Res. 2017;27(3):335–48.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Navarro FC, Hoops J, Bellfy L, Cerveira E, Zhu Q, Zhang C, et al. TeXP: Deconvolving the effects of pervasive and autonomous transcription of transposable elements. PLoS Comput Biol. 2019;15(8): e1007293.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hajkova P. Epigenetic reprogramming–taking a lesson from the embryo. Curr Opin Cell Biol. 2010;22(3):342–50.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131(5):861–72.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–76.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ying Q-L, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, et al. The ground state of embryonic stem cell self-renewal. Nature. 2008;453(7194):519–23.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Castro-Diaz N, Ecco G, Coluccio A, Kapopoulou A, Yazdanpanah B, Friedli M, et al. Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev. 2014;28(13):1397–409.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sookdeo A, Hepp CM, McClure MA, Boissinot S. Revisiting the evolution of mouse LINE-1 in the genomic era. Mob DNA. 2013;4(1):3.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Naas TP, DeBerardinis RJ, Moran JV, Ostertag EM, Kingsmore SF, Seldin MF, et al. An actively retrotransposing, novel subfamily of mouse L1 elements. EMBO J. 1998;17(2):590–7.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bulut-Karslioglu A, De La Rosa-Velázquez IA, Ramirez F, Barenboim M, Onishi-Seebacher M, Arand J, et al. Suv39h-dependent H3K9me3 marks intact retrotransposons and silences LINE elements in mouse embryonic stem cells. Mol Cell. 2014;55(2):277–90.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Percharde M, Lin C-J, Yin Y, Guan J, Peixoto GA, Bulut-Karslioglu A, et al. A LINE1-nucleolin partnership regulates early development and ESC identity. Cell. 2018;174(2):391-405.e19.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jin Y, Tam OH, Paniagua E, Hammell M. TEtranscripts: a package for including transposable elements in differential expression analysis of RNA-seq datasets. Bioinformatics. 2015;31(22):3593–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9(9):R137.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27(11):1571–2.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     



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