The H19 Imprinting Control Region Mediates Preimplantation Imprinted Methylation of Nearby Sequences in Yeast Artificial Chromosome Transgenic Mice

REFERENCES

• Kaffer CR, Srivastava M, Park KY, Ives E, Hsieh S, Batlle J, Grinberg A, Huang SP, Pfeifer K. 2000. A transcriptional insulator at the imprinted H19/Igf2 locus. Genes Dev. 14:1908–1919.
   PubMed Web of Science ®Google Scholar
• Thorvaldsen JL, Duran KL, Bartolomei MS. 1998. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 12:3693–3702.
   PubMed Web of Science ®Google Scholar
• Tremblay KD, Duran KL, Bartolomei MS. 1997. A 5′ 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol. Cell. Biol. 17:4322–4329.
   PubMed Web of Science ®Google Scholar
• Bell AC, Felsenfeld G. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482–485.
   PubMed Web of Science ®Google Scholar
• Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. 2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486–489.
   PubMed Web of Science ®Google Scholar
• Bourc'his D, Bestor TH. 2004. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431:96–99.
   PubMed Web of Science ®Google Scholar
• Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. 2004. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900–903.
   PubMed Web of Science ®Google Scholar
• Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M, Kohara Y, Okano M, Li E, Nozaki M, Sasaki H. 2007. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet. 16:2272–2280.
   PubMed Web of Science ®Google Scholar
• Henckel A, Chebli K, Kota SK, Arnaud P, Feil R. 2012. Transcription and histone methylation changes correlate with imprint acquisition in male germ cells. EMBO J. 31:606–615.
   PubMed Web of Science ®Google Scholar
• Hata K, Okano M, Lei H, Li E. 2002. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129:1983–1993.
   PubMed Web of Science ®Google Scholar
• Bowman AB, Levorse JM, Ingram RS, Tilghman SM. 2003. Functional characterization of a testis-specific DNA binding activity at the H19/Igf2 imprinting control region. Mol. Cell. Biol. 23:8345–8351.
   PubMedGoogle Scholar
• Drewell RA, Brenton JD, Ainscough JF, Barton SC, Hilton KJ, Arney KL, Dandolo L, Surani MA. 2000. Deletion of a silencer element disrupts H19 imprinting independently of a DNA methylation epigenetic switch. Development 127:3419–3428.
   PubMedGoogle Scholar
• Ideraabdullah FY, Abramowitz LK, Thorvaldsen JL, Krapp C, Wen SC, Engel N, Bartolomei MS. 2011. Novel cis-regulatory function in ICR-mediated imprinted repression of H19. Dev. Biol. 355:349–357.
   PubMedGoogle Scholar
• Katz DJ, Beer MA, Levorse JM, Tilghman SM. 2005. Functional characterization of a novel Ku70/80 pause site at the H19/Igf2 imprinting control region. Mol. Cell. Biol. 25:3855–3863.
   PubMedGoogle Scholar
• Reed MR, Riggs AD, Mann JR. 2001. Deletion of a direct repeat element has no effect on Igf2 and H19 imprinting. Mamm. Genome 12:873–876.
   PubMedGoogle Scholar
• Szabo PE, Han L, Hyo-Jung J, Mann JR. 2006. Mutagenesis in mice of nuclear hormone receptor binding sites in the Igf2/H19 imprinting control region. Cytogenet. Genome Res. 113:238–246.
   PubMedGoogle Scholar
• Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. 2000. Demethylation of the zygotic paternal genome. Nature 403:501–502.
   PubMed Web of Science ®Google Scholar
• Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, Dean W, Reik W, Walter J. 2000. Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10:475–478.
   PubMed Web of Science ®Google Scholar
• Tomizawa S, Kobayashi H, Watanabe T, Andrews S, Hata K, Kelsey G, Sasaki H. 2011. Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development 138:811–820.
   PubMed Web of Science ®Google Scholar
• Hemberger M, Dean W, Reik W. 2009. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat. Rev. Mol. Cell Biol. 10:526–537.
   PubMed Web of Science ®Google Scholar
• Engel N, West AG, Felsenfeld G, Bartolomei MS. 2004. Antagonism between DNA hypermethylation and enhancer-blocking activity at the H19 DMD is uncovered by CpG mutations. Nat. Genet. 36:883–888.
   PubMedGoogle Scholar
• Schoenherr CJ, Levorse JM, Tilghman SM. 2003. CTCF maintains differential methylation at the Igf2/H19 locus. Nat. Genet. 33:66–69.
   PubMed Web of Science ®Google Scholar
• Tanimoto K, Shimotsuma M, Matsuzaki H, Omori A, Bungert J, Engel JD, Fukamizu A. 2005. Genomic imprinting recapitulated in the human beta-globin locus. Proc. Natl. Acad. Sci. U. S. A. 102:10250–10255.
   PubMedGoogle Scholar
• Matsuzaki H, Okamura E, Shimotsuma M, Fukamizu A, Tanimoto K. 2009. A randomly integrated transgenic H19 imprinting control region acquires methylation imprinting independently of its establishment in germ cells. Mol. Cell. Biol. 29:4595–4603.
   PubMedGoogle Scholar
• Gebert C, Kunkel D, Grinberg A, Pfeifer K. 2010. H19 imprinting control region methylation requires an imprinted environment only in the male germ line. Mol. Cell. Biol. 30:1108–1115.
   PubMedGoogle Scholar
• Park KY, Sellars EA, Grinberg A, Huang SP, Pfeifer K. 2004. The H19 differentially methylated region marks the parental origin of a heterologous locus without gametic DNA methylation. Mol. Cell. Biol. 24:3588–3595.
   PubMedGoogle Scholar
• Tanimoto K, Sugiura A, Omori A, Felsenfeld G, Engel JD, Fukamizu A. 2003. Human beta-globin locus control region HS5 contains CTCF- and developmental stage-dependent enhancer-blocking activity in erythroid cells. Mol. Cell. Biol. 23:8946–8952.
   PubMedGoogle Scholar
• Tanimoto K, Liu Q, Grosveld F, Bungert J, Engel JD. 2000. Context-dependent EKLF responsiveness defines the developmental specificity of the human epsilon-globin gene in erythroid cells of YAC transgenic mice. Genes Dev. 14:2778–2794.
   PubMedGoogle Scholar
• Yu RN, Ito M, Saunders TL, Camper SA, Jameson JL. 1998. Role of Ahch in gonadal development and gametogenesis. Nat. Genet. 20:353–357.
   PubMed Web of Science ®Google Scholar
• Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S. 2011. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479:74–79.
   PubMed Web of Science ®Google Scholar
• Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, Galjart N, de Laat W. 2006. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev. 20:2349–2354.
   PubMed Web of Science ®Google Scholar
• Shimotsuma M, Matsuzaki H, Tanabe O, Campbell AD, Engel JD, Fukamizu A, Tanimoto K. 2007. Linear distance from the locus control region determines epsilon-globin transcriptional activity. Mol. Cell. Biol. 27:5664–5672.
   PubMedGoogle Scholar
• Lee G, Saito I. 1998. Role of nucleotide sequences of loxP spacer region in Cre-mediated recombination. Gene 216:55–65.
   PubMed Web of Science ®Google Scholar
• Matsuzaki H, Okamura E, Fukamizu A, Tanimoto K. 2010. CTCF binding is not the epigenetic mark that establishes post-fertilization methylation imprinting in the transgenic H19 ICR. Hum. Mol. Genet. 19:1190–1198.
   PubMedGoogle Scholar
• Shimizu T, Oishi T, Omori A, Sugiura A, Hirota K, Aoyama H, Saito T, Sugaya T, Kon Y, Engel JD, Fukamizu A, Tanimoto K. 2005. Identification of cis-regulatory sequences in the human angiotensinogen gene by transgene coplacement and site-specific recombination. Mol. Cell. Biol. 25:2938–2945.
   PubMed Web of Science ®Google Scholar
• Tanimoto K, Sugiura A, Kanafusa S, Saito T, Masui N, Yanai K, Fukamizu A. 2008. A single nucleotide mutation in the mouse renin promoter disrupts blood pressure regulation. J. Clin. Invest. 118:1006–1016.
   PubMed Web of Science ®Google Scholar
• Chotalia M, Smallwood SA, Ruf N, Dawson C, Lucifero D, Frontera M, James K, Dean W, Kelsey G. 2009. Transcription is required for establishment of germline methylation marks at imprinted genes. Genes Dev. 23:105–117.
   PubMedGoogle Scholar
• Ciccone DN, Su H, Hevi S, Gay F, Lei H, Bajko J, Xu G, Li E, Chen T. 2009. KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461:415–418.
   PubMed Web of Science ®Google Scholar
• Henckel A, Nakabayashi K, Sanz LA, Feil R, Hata K, Arnaud P. 2009. Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum. Mol. Genet. 18:3375–3383.
   PubMedGoogle Scholar
• Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X. 2007. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449:248–251.
   PubMed Web of Science ®Google Scholar
• Watanabe T, Tomizawa S, Mitsuya K, Totoki Y, Yamamoto Y, Kuramochi-Miyagawa S, Iida N, Hoki Y, Murphy PJ, Toyoda A, Gotoh K, Hiura H, Arima T, Fujiyama A, Sado T, Shibata T, Nakano T, Lin H, Ichiyanagi K, Soloway PD, Sasaki H. 2011. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332:848–852.
   PubMed Web of Science ®Google Scholar
• You JS, Kelly TK, De Carvalho DD, Taberlay PC, Liang G, Jones PA. 2011. OCT4 establishes and maintains nucleosome-depleted regions that provide additional layers of epigenetic regulation of its target genes. Proc. Natl. Acad. Sci. U. S. A. 108:14497–14502.
   PubMedGoogle Scholar
• Han L, Lin IG, Hsieh CL. 2001. Protein binding protects sites on stable episomes and in the chromosome from de novo methylation. Mol. Cell. Biol. 21:3416–3424.
   PubMed Web of Science ®Google Scholar
• Hori N, Nakano H, Takeuchi T, Kato H, Hamaguchi S, Oshimura M, Sato K. 2002. A dyad oct-binding sequence functions as a maintenance sequence for the unmethylated state within the H19/Igf2-imprinted control region. J. Biol. Chem. 277:27960–27967.
   PubMedGoogle Scholar
• Hori N, Yamane M, Kouno K, Sato K. 31 October 2012. Induction of DNA demethylation depending on two sets of Sox2 and adjacent Oct3/4 binding sites (Sox-Oct motifs) within the mouse H19/insulin-like growth factor 2 (Igf2) imprinted control region. J. Biol. Chem. [Epub ahead of print.] doi:10.1074/jbc.M112.424580.
   Google Scholar
• Demars J, Shmela ME, Rossignol S, Okabe J, Netchine I, Azzi S, Cabrol S, Le Caignec C, David A, Le Bouc Y, El-Osta A, Gicquel C. 2010. Analysis of the IGF2/H19 imprinting control region uncovers new genetic defects, including mutations of OCT-binding sequences, in patients with 11p15 fetal growth disorders. Hum. Mol. Genet. 19:803–814.
   PubMedGoogle Scholar
• Poole RL, Leith DJ, Docherty LE, Shmela ME, Gicquel C, Splitt M, Temple IK, Mackay DJ. 2012. Beckwith-Wiedemann syndrome caused by maternally inherited mutation of an OCT-binding motif in the IGF2/H19-imprinting control region, ICR1. Eur. J. Hum. Genet. 20:240–243.
   PubMedGoogle Scholar
• Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, Cheng X, Bestor TH. 2007. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448:714–717.
   PubMed Web of Science ®Google Scholar
• Otani J, Nankumo T, Arita K, Inamoto S, Ariyoshi M, Shirakawa M. 2009. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep. 10:1235–1241.
   PubMed Web of Science ®Google Scholar
• Jackson JP, Lindroth AM, Cao X, Jacobsen SE. 2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560.
   PubMed Web of Science ®Google Scholar
• Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH. 2003. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13:1192–1200.
   PubMed Web of Science ®Google Scholar
• Tamaru H, Selker EU. 2001. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277–283.
   PubMed Web of Science ®Google Scholar
• Arpanahi A, Brinkworth M, Iles D, Krawetz SA, Paradowska A, Platts AE, Saida M, Steger K, Tedder P, Miller D. 2009. Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res. 19:1338–1349.
   PubMed Web of Science ®Google Scholar
• Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009. Distinctive chromatin in human sperm packages genes for embryo development. Nature 460:473–478.
   PubMed Web of Science ®Google Scholar
• Delaval K, Govin J, Cerqueira F, Rousseaux S, Khochbin S, Feil R. 2007. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J. 26:720–729.
   PubMedGoogle Scholar
• Choufani S, Shuman C, Weksberg R. 2010. Beckwith-Wiedemann syndrome. Am. J. Med. Genet. C Semin. Med. Genet. 154C:343–354.
   PubMed Web of Science ®Google Scholar
• Eggermann T. 2010. Russell-Silver syndrome. Am. J. Med. Genet. C Semin. Med. Genet. 154C:355–364.
   PubMed Web of Science ®Google Scholar
• Leighton PA, Saam JR, Ingram RS, Stewart CL, Tilghman SM. 1995. An enhancer deletion affects both H19 and Igf2 expression. Genes Dev. 9:2079–2089.
   PubMed Web of Science ®Google Scholar