Sox-Oct motifs contribute to maintenance of the unmethylated H19 ICR in YAC transgenic mice

Human Molecular Genetics

Volumn 22, Issue 22, 2013, Pages 4627-4637

  Sakaguchi, Ryuuta ^a   Okamura, Eiichi ^a   Matsuzaki, Hitomi ^a   Fukamizu, Akiyoshi ^a   Tanimoto, Keiji ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; HEMOGLOBIN BETA CHAIN; TRANSCRIPTION FACTOR CTCF;

ANIMAL EXPERIMENT; ARTICLE; BACTERIOPHAGE LAMBDA; BECKWITH WIEDEMANN SYNDROME; BINDING SITE; BLASTOCYST; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; FERTILIZATION; GENE; GENE MUTATION; H19 GENE; LOXP SITE; MOUSE; NONHUMAN; NUCLEIC ACID STRUCTURE; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; SOMATIC CELL; SOUTHERN BLOTTING; SOX OCT MOTIF; TRANSGENIC MOUSE; WILD TYPE; YEAST ARTIFICIAL CHROMOSOME;

ALLELES; AMINO ACID MOTIFS; ANIMALS; BECKWITH-WIEDEMANN SYNDROME; BETA-GLOBINS; CHROMOSOMES, ARTIFICIAL, YEAST; DNA METHYLATION; FEMALE; GENOMIC IMPRINTING; HUMANS; INSULIN-LIKE GROWTH FACTOR II; LOCUS CONTROL REGION; MALE; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; PEDIGREE; REPRESSOR PROTEINS;

EID: 84887001456     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt311     Document Type: Article

References (34)

1. Holmgren, C., Kanduri, C., Dell, G., Ward, A., Mukhopadhya, R., Kanduri, M., Lobanenkov, V. and Ohlsson, R. (2001) Cpg methylation regulates the Igf2/H19 insulator. Curr. Biol., 11, 1128-1130.
2. Bell, A.C. and Felsenfeld, G. (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature, 405, 482-485.
3. Hark, A.T., Schoenherr, C.J., Katz, D.J., Ingram, R.S., Levorse, J.M. and Tilghman, S.M. (2000) CTCF Mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature, 405, 486-489.
4. Tanimoto, K., Shimotsuma, M., Matsuzaki, H., Omori, A., Bungert, J., Engel, J.D. and Fukamizu, A. (2005) Genomic imprinting recapitulated in the humanbeta-globin locus. Proc. Natl Acad. Sci.USA, 102, 10250-10255.
5. Matsuzaki, H., Okamura, E., Fukamizu, A. and 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.
6. Iqbal, K., Jin, S.G., Pfeifer, G.P. and Szabo, P.E. (2011) Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc. Natl Acad. Sci. USA, 108, 3642-3647.
7. Wossidlo, M., Nakamura, T., Lepikhov, K., Marques, C.J., Zakhartchenko, V., Boiani, M., Arand, J., Nakano, T., Reik, W. and Walter, J. (2011) 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun., 2, 241.
8. Schoenherr, C.J., Levorse, J.M. and Tilghman, S.M. (2003)CTCFmaintains differential methylation at the Igf2/H19 locus. Nat. Genet., 33, 66-69.
9. Pant, V., Mariano, P., Kanduri, C., Mattsson, A., Lobanenkov, V., Heuchel, R. and Ohlsson, R. (2003) The nucleotides responsible for the direct physical contact between the chromatin insulator protein CTCF and the H19 imprinting control region manifest parent of origin-specific long-distance insulation and methylation-free domains. Genes Dev., 17, 586-590.
10. Szabo, P.E., Tang, S.H., Silva, F.J., Tsark, W.M. and Mann, J.R. (2004) Role of CTCF binding sites in the Igf2/H19 imprinting control region. Mol. Cell. Biol., 24, 4791-4800.
11. Engel, N., Thorvaldsen, J.L. and Bartolomei, M.S. (2006) CTCF binding sites promote transcription initiation and prevent DNA methylation on the maternal allele at the imprinted H19/Igf2 locus. Hum. Mol. Genet., 15, 2945-2954.
12. Okamura, E., Matsuzaki, H., Sakaguchi, R., Takahashi, T., Fukamizu, A. and Tanimoto, K. (2013) The H19 imprinting control region mediates preimplantation imprinted methylation of nearby sequences in yeast artificial chromosome transgenic mice. Mol. Cell. Biol., 33, 858-871.
13. Sparago, A., Cerrato, F., Vernucci, M., Ferrero, G.B., Silengo, M.C. and Riccio, A. (2004) Microdeletions in the human H19 DMR result in loss of IGF2 imprinting and Beckwith-Wiedemann syndrome. Nat. Genet., 36, 958-960.
14. Prawitt, D., Enklaar, T., Gartner-rupprecht, B., Spangenberg, C., Oswald, M., Lausch, E., Schmidtke, P., Reutzel, D., Fees, S., Lucito, R. et al. (2005) Microdeletion of target sites for insulator protein CTCF in a chromosome 11p15 imprinting center in Beckwith-Wiedemann syndrome and Wilms' tumor. Proc. Natl Acad. Sci. USA, 102, 4085-4090.
15. Cerrato, F., Sparago, A., Verde, G., De Crescenzo, A., Citro, V., Cubellis, M.V., Rinaldi, M.M., Boccuto, L., Neri, G., Magnani, C. et al. (2008) Different mechanisms cause imprinting defects at the IGF2/H19 locus in Beckwith-Wiedemann syndromeand Wilms' tumour.Hum.Mol. Genet., 17, 1427-1435.
16. Demars, J., Shmela, M.E., Rossignol, S., Okabe, J., Netchine, I., Azzi, S., Cabrol, S., Le Caignec, C., David, A., Le Bouc, Y. et al. (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.
17. Poole, R.L., Leith, D.J., Docherty, L.E., Shmela, M.E., Gicquel, C., Splitt, M., Temple, I.K. and Mackay, D.J. (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.
18. Berland, S., Appelback, M., Bruland, O., Beygo, J., Buiting, K., Mackay, D.J., Karen Temple, I. and Houge, G. (2013) Evidence for anticipation in Beckwith-Wiedemann syndrome. Eur. J. Hum. Genet. doi: 10.1038/ ejhg.2013.71. [Epub ahead of print].
19. Hori, N., Nakano, H., Takeuchi, T., Kato, H., Hamaguchi, S., Oshimura, M. and Sato, K. (2002)Adyad 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.
20. Hori, N., Yamane, M., Kouno, K. and Sato, K. (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., 287, 44006-44016.
21. Lee, G. and Saito, I. (1998) Role of nucleotide sequences of loxP spacer region in Cre-mediated recombination. Gene, 216, 55-65.
22. Shimizu, T., Oishi, T., Omori, A., Sugiura, A., Hirota, K., Aoyama, H., Saito, T., Sugaya, T., Kon, Y., Engel, J.D. et al. (2005) Identification of cis-regulatory sequences in the human angiotensinogen gene by transgene coplacement and site-specific recombination. Mol. Cell. Biol., 25, 2938-2945.
23. Shimotsuma, M., Matsuzaki, H., Tanabe, O., Campbell, A.D., Engel, J.D., Fukamizu, A. and Tanimoto, K. (2007) Linear distance from the locus control region determines epsilon-globin transcriptional activity. Mol. Cell. Biol., 27, 5664-5672.
24. Donohoe, M.E., Silva, S.S., Pinter, S.F., Xu, N. and Lee, J.T. (2009) The pluripotency factor Oct4 interactswith Ctcf and also controls X-chromosome pairing and counting. Nature, 460, 128-132.
25. You, J.S., Kelly, T.K., De Carvalho, D.D., Taberlay, P.C., Liang, G. and Jones, P.A. (2011) OCT4 establishes and maintains nucleosome-depleted regions that provide additional layers of epigenetic regulation of its target genes. Proc. Natl Acad. Sci. USA, 108, 14497-14502.
26. Weth, O. and Renkawitz, R. (2011) CTCF function is modulated by neighboring DNA binding factors. Biochem. Cell Biol., 89, 459-468.
27. Ideraabdullah, F.Y., Abramowitz, L.K., Thorvaldsen, J.L., Krapp, C., Wen, S.C., Engel, N. and Bartolomei, M.S. (2011) Novel cis-regulatory function in ICR-mediated imprinted repression of H19. Dev. Biol., 355, 349-357.
28. Bungert, J., Tanimoto, K., Patel, S., Liu, Q., Fear, M. and Engel, J.D. (1999) Hypersensitive site 2 specifies a unique function within the human beta-globin locus control region to stimulate globin gene transcription. Mol. Cell. Biol., 19, 3062-3072.
29. Beygo, J., Citro, V., Sparago, A., De Crescenzo, A., Cerrato, F., Heitmann, M., Rademacher, K., Guala, A., Enklaar, T., Anichini, C. et al. (2013) The molecular function and clinical phenotype of partial deletions of the IGF2/ H19 imprinting control region depends on the spatial arrangement of the remaining CTCF-binding sites. Hum. Mol. Genet., 22, 544-557.
30. Pant, V., Kurukuti, S., Pugacheva, E., Shamsuddin, S., Mariano, P., Renkawitz, R., Klenova, E., Lobanenkov, V. and Ohlsson, R. (2004) Mutation of a single CTCF target site within the H19 imprinting control region leads to loss of Igf2 imprinting and complex patterns of de novo methylation upon maternal inheritance. Mol. Cell. Biol., 24, 3497-3504.
31. Park, K.Y., Sellars, E.A., Grinberg, A., Huang, S.P. and 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.
32. Gebert, C., Kunkel, D., Grinberg, A. and Pfeifer, K. (2010) H19 imprinting control region methylation requires an imprinted environment only in the male germ line. Mol. Cell. Biol., 30, 1108-1115.
33. Tanimoto, K., Sugiura, A., Omori, A., Felsenfeld, G., Engel, J.D. and 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.
34. Tanimoto, K., Liu, Q., Bungert, J. and Engel, J.D. (1999) The polyoma virus enhancer cannot substitute for DNase I core hypersensitive sites 2-4 in the human beta-globin LCR. Nucleic Acids Res., 27, 3130-3137.