H19 Imprinting Control Region Methylation Requires an Imprinted Environment Only in the Male Germ Line

REFERENCES

• Bartolomei, M. S., A. L. Webber, M. E. Brunkow, and S. M. Tilghman. 1993. Epigenetic mechanisms underlying the imprinting of the mouse H19-gene. Genes Dev. 7:1663–1673.
   PubMed Web of Science ®Google Scholar
• Bartolomei, M. S., S. Zemel, and S. M. Tilghman. 1991. Parental imprinting of the mouse H19 gene. Nature 351:153–155.
   PubMed Web of Science ®Google Scholar
• Bell, A. C., and G. Felsenfeld. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482–485.
   PubMed Web of Science ®Google Scholar
• Cerrato, F., A. Sparago, G. Verde, A. De Crescenzo, V. Citro, M. V. Cubellis, M. M. Rinaldi, L. Boccuto, G. Neri, C. Magnani, P. D'Angelo, P. Collini, D. Perotti, G. Sebastio, E. R. Maher, and A. Riccio. 2008. Different mechanisms cause imprinting defects at the IGF2/H19 locus in Beckwith-Wiedemann syndrome and Wilms' tumour. Hum. Mol. Genet. 17:1427–1435.
   PubMed Web of Science ®Google Scholar
• Ciccone, D. N., H. Su, S. Hevi, F. Gay, H. Lei, J. Bajko, G. L. Xu, E. Li, and T. P. Chen. 2009. KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461:415–418.
   PubMed Web of Science ®Google Scholar
• Cranston, M. J., T. L. Spinka, D. A. Elson, and M. S. Bartolomei. 2001. Elucidation of the minimal sequence required to imprint H19 transgenes. Genomics 73:98–107.
   PubMedGoogle Scholar
• Cui, H. M., E. L. Niemitz, J. D. Ravenel, P. Onyango, S. A. Brandenburg, V. V. Lobanenkov, and A. P. Feinberg. 2001. Loss of imprinting of insulin-like growth factor-II in Wilms' tumor commonly involves altered methylation but not mutations of CTCF or its binding site. Cancer Res. 61:4947–4950.
   PubMed Web of Science ®Google Scholar
• Davis, T. L., J. M. Trasler, S. B. Moss, G. J. Yang, and M. S. Bartolomei. 1999. Acquisition of the H19 methylation imprint occurs differentially on the parental alleles during spermatogenesis. Genomics 58:18–28.
   PubMed Web of Science ®Google Scholar
• Davis, T. L., G. J. Yang, J. R. McCarrey, and M. S. Bartolomei. 2000. The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum. Mol. Genet. 9:2885–2894.
   PubMedGoogle Scholar
• DeBaun, M. R., E. L. Niemitz, D. E. McNeil, S. A. Brandenburg, M. P. Lee, and A. P. Feinberg. 2002. Epigenetic alterations of H19 and LIT1 distinguish patients with Beckwith-Wiedemann syndrome with cancer and birth defects. Am. J. Hum. Genet. 70:604–611.
   PubMedGoogle Scholar
• Dechiara, T. M., E. J. Robertson, and A. Efstratiadis. 1991. Parental imprinting of the mouse insulin-like growth factor-Ii. Gene Cell 64:849–859.
   Google Scholar
• de la Puente, A., J. Hall, Y. Z. Wu, G. Leone, J. Peters, B. J. Yoon, P. Soloway, and C. Plass. 2002. Structural characterization of Rasgrf1 and a novel linked imprinted locus. Gene 291:287–297.
   PubMedGoogle Scholar
• Delaval, K., A. Wagschal, and R. Feil. 2006. Epigenetic deregulation of imprinting in congenital diseases of aberrant growth. Bioessays 28:453–459.
   PubMed Web of Science ®Google Scholar
• El-Maarri, O., K. Buiting, E. G. Peery, P. M. Kroisel, B. Balaban, K. Wagner, B. Urman, J. Heyd, C. Lich, C. I. Brannan, J. Walter, and B. Horsthemke. 2001. Maternal methylation imprints on human chromosome 15 are established during or after fertilization. Nat. Genet. 27:341–344.
   PubMed Web of Science ®Google Scholar
• Engel, N., A. G. West, G. Felsenfeld, and M. S. Bartolomei. 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
• Feil, R., J. Walter, N. D. Allen, and W. Reik. 1994. Developmental control of allelic methylation in the imprinted mouse Igf2 and H19 genes. Development 120:2933–2943.
   PubMed Web of Science ®Google Scholar
• Ferguson-Smith, A. C., H. Sasaki, B. M. Cattanach, and M. A. Surani. 1993. Parental-origin-specific epigenetic modification of the mouse H19 gene. Nature 362:751–755.
   PubMed Web of Science ®Google Scholar
• Geuns, E., M. De Rycke, A. Van Steirteghem, and I. Liebaers. 2003. Methylation imprints of the imprint control region of the SNRPN-gene in human gametes and preimplantation embryos. Hum. Mol. Genet. 12:2873–2879.
   PubMed Web of Science ®Google Scholar
• Gould, T. D., and K. Pfeifer. 1998. Imprinting of mouse Kvlqt1 is developmentally regulated. Hum. Mol. Genet. 7:483–487.
   PubMedGoogle Scholar
• Hajkova, P., K. Ancelin, T. Waldmann, N. Lacoste, U. C. Lange, F. Cesari, C. Lee, G. Almouzni, R. Schneider, and M. A. Surani. 2008. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452:877–881.
   PubMed Web of Science ®Google Scholar
• Hajkova, P., O. El-Maarri, S. Engemann, J. Oswald, A. Olek, J. Walter, and K. I. Mills. 2002. DNA-methylation analysis by the bisulfite-assisted genomic sequencing method. DNA Methylation Protoc. 2002:143–154.
   Google Scholar
• Hajkova, P., S. Erhardt, N. Lane, T. Haaf, O. El-Maarri, W. Reik, J. Walter, and M. A. Surani. 2002. Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 117:15–23.
   PubMed Web of Science ®Google Scholar
• Han, L., D. H. Lee, and P. E. Szabo. 2008. CTCF is the master organizer of domain-wide allele-specific chromatin at the H19/Igf2 imprinted region. Mol. Cell. Biol. 28:1124–1135.
   PubMed Web of Science ®Google Scholar
• Hark, A. T., C. J. Schoenherr, D. J. Katz, R. S. Ingram, J. M. Levorse, and S. M. Tilghman. 2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486–489.
   PubMed Web of Science ®Google Scholar
• Kaffer, C. R., A. Grinberg, and K. Pfeifer. 2001. Regulatory mechanisms at the mouse Igf2/H19 locus. Mol. Cell. Biol. 21:8189–8196.
   PubMedGoogle Scholar
• Kaffer, C. R., M. Srivastava, K. Y. Park, E. Ives, S. Hsieh, J. Batlle, A. Grinberg, S. P. Huang, and K. Pfeifer. 2000. A transcriptional insulator at the imprinted H19/Igf2 locus. Genes Dev. 14:1908–1919.
   PubMed Web of Science ®Google Scholar
• Kanduri, C., V. Pant, D. Loukinov, E. Pugacheva, C. F. Qi, A. Wolffe, R. Ohlsson, and V. V. Lobanenkov. 2000. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr. Biol. 10:853–856.
   PubMed Web of Science ®Google Scholar
• Kanduri, M., C. Kanduri, P. Mariano, A. A. Vostrov, W. Quitschke, V. Lobanenkov, and R. Ohlsson. 2002. Multiple nucleosome positioning sites regulate the CTCF-mediated insulator function of the H19 imprinting control region. Mol. Cell. Biol. 22:3339–3344.
   PubMedGoogle Scholar
• Kurukuti, S., V. K. Tiwari, G. Tavoosidana, E. Pugacheva, A. Murrell, Z. H. Zhao, V. Lobanenkov, W. Reik, and R. Ohlsson. 2006. CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc. Natl. Acad. Sci. USA 103:10684–10689.
   PubMed Web of Science ®Google Scholar
• Lakso, M., J. G. Pichel, J. R. Gorman, B. Sauer, Y. Okamoto, E. Lee, F. W. Alt, and H. Westphal. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. USA 93:5860–5865.
   PubMed Web of Science ®Google Scholar
• Leighton, P. A., R. S. Ingram, J. Eggenschwiler, A. Efstratiadis, and S. M. Tilghman. 1995. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature 375:34–39.
   PubMed Web of Science ®Google Scholar
• Leighton, P. A., J. R. Saam, R. S. Ingram, C. L. Stewart, and S. M. Tilghman. 1995. An enhancer deletion affects both H19 and Igf2 expression. Genes Dev. 9:2079–2089.
   PubMed Web of Science ®Google Scholar
• Li, J. Y., D. J. Lees-Murdock, G. L. Xu, and C. P. Walsh. 2004. Timing of establishment of paternal methylation imprints in the mouse. Genomics 84:952–960.
   PubMed Web of Science ®Google Scholar
• Li, T., J. F. Hu, X. W. Qiu, J. Q. Ling, H. L. Chen, S. K. Wang, A. J. Hou, T. H. Vu, and A. R. Hoffman. 2008. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop. Mol. Cell. Biol. 28:6473–6482.
   PubMed Web of Science ®Google Scholar
• Lopes, S., A. Lewis, R. Hajkova, W. Dean, J. Oswald, T. Forne, A. Murrell, M. Constancia, M. Bartolomei, J. Walter, and W. Reik. 2003. Epigenetic modifications in an imprinting cluster are controlled by a hierarchy of DMRs suggesting long-range chromatin interactions. Hum. Mol. Genet. 12:295–305.
   PubMed Web of Science ®Google Scholar
• Lucifero, D., C. Mertineit, H. J. Clarke, T. H. Bestor, and J. M. Trasler. 2002. Methylation dynamics of imprinted genes in mouse germ cells. Genomics 79:530–538.
   PubMed Web of Science ®Google Scholar
• Matsuzaki, H., E. Okamura, M. Shimotsuma, A. Fukamizu, and K. Tanimoto. 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
• Mayer, W., A. Niveleau, J. Walter, R. Fundele, and T. Haaf. 2000. Embryogenesis—demethylation of the zygotic paternal genome. Nature 403:501–502.
   PubMed Web of Science ®Google Scholar
• McGrath, J., and D. Solter. 1984. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179–183.
   PubMed Web of Science ®Google Scholar
• Monk, M., M. Boubelik, and S. Lehnert. 1987. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ-cell lineages during mouse embryo development. Development 99:371–382.
   PubMed Web of Science ®Google Scholar
• Murrell, A. 2006. Genomic imprinting and cancer: from primordial germ cells to somatic cells. Sci. World J. 6:1888–1910.
   Google Scholar
• Murrell, A., S. Heeson, and W. Reik. 2004. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat. Genet. 36:889–893.
   PubMed Web of Science ®Google Scholar
• Nagy, A., M. Gertsenstein, K. Vintersten, and R. Behringer. 2003. Manipulating the mouse embryo, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Oswald, J., S. Engemann, N. Lane, W. Mayer, A. Olek, R. Fundele, W. Dean, W. Reik, and J. Walter. 2000. Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10:475–478.
   PubMed Web of Science ®Google Scholar
• Park, K. Y., E. A. Sellars, A. Grinberg, S. P. Huang, and K. Pfeifer. 2004. The H19 differentially methylated region marks the parental origin of a heterologous locus without gametic DNA methylation. Mol. Cell. Biol. 24:3588–3595.
   PubMed Web of Science ®Google Scholar
• Prawitt, D., T. Enklaar, B. Gartner-Rupprecht, C. Spangenberg, E. Lausch, D. Reutzel, S. Fees, M. Korzon, I. Brozek, J. Limon, D. E. Housman, J. Pelletier, and B. Zabel. 2005. Microdeletion and IGF2 loss of imprinting in a cascade causing Beckwith-Wiedemann syndrome with Wilms' tumor. Nat. Genet. 37:785–786.
   PubMedGoogle Scholar
• Schofield, P. N., J. A. Joyce, W. K. Lam, V. Grandjean, A. Ferguson-Smith, W. Reik, and E. R. Maher. 2001. Genomic imprinting and cancer; new paradigms in the genetics of neoplasia. Toxicol. Lett. 120:151–160.
   PubMed Web of Science ®Google Scholar
• Singh, V., and M. Srivastava. 2008. Enhancer blocking activity of the insulator at H19-ICR is independent of chromatin barrier establishment. Mol. Cell. Biol. 28:3767–3775.
   PubMedGoogle Scholar
• Spear, B. T. 1999. Alpha-fetoprotein gene regulation: lessons from transgenic mice. Semin. Cancer Biol. 9:109–116.
   PubMed Web of Science ®Google Scholar
• Srivastava, M., S. Hsieh, A. Grinberg, L. Williams-Simons, S. P. Huang, and K. Pfeifer. 2000. H19 and Igf2 monoallelic expression is regulated in two distinct ways by a shared cis acting regulatory region upstream of H19. Genes Dev. 14:1186–1195.
   PubMedGoogle Scholar
• Surani, M. A. H., S. C. Barton, and M. L. Norris. 1984. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548–550.
   PubMed Web of Science ®Google Scholar
• Szabo, P. E., G. P. Pfeifer, and J. R. Mann. 1998. Characterization of novel parent-specific epigenetic modifications upstream of the imprinted mouse H19 gene. Mol. Cell. Biol. 18:6767–6776.
   PubMedGoogle Scholar
• Takai, D., and P. A. Jones. 2003. The CpG island searcher: a new WWW resource. In Silico Biol. 3:235–240.
   PubMedGoogle Scholar
• Tanimoto, K., M. Shimotsuma, H. Matsuzaki, A. Omori, J. Bungert, J. D. Engel, and A. Fukamizu. 2005. Genomic imprinting recapitulated in the human beta-globin locus. Proc. Natl. Acad. Sci. USA 102:10250–10255.
   PubMedGoogle Scholar
• Thorvaldsen, J. L., K. L. Duran, and M. S. Bartolomei. 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
• Thorvaldsen, J. L., M. R. W. Mann, O. Nwoko, K. L. Duran, and M. S. Bartolomei. 2002. Analysis of sequence upstream of the endogenous H19 gene reveals elements both essential and dispensable for imprinting. Mol. Cell. Biol. 22:2450–2462.
   PubMedGoogle Scholar
• Tremblay, K. D., K. L. Duran, and M. S. Bartolomei. 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
• Tremblay, K. D., J. R. Saam, R. S. Ingram, S. M. Tilghman, and M. S. Bartolomei. 1995. A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat. Genet. 9:407–413.
   PubMed Web of Science ®Google Scholar
• Yoon, Y. S., S. Jeong, Q. Rong, K. Y. Park, J. H. Chung, and K. Pfeifer. 2007. Analysis of the H19ICR insulator. Mol. Cell. Biol. 27:3499–3510.
   PubMed Web of Science ®Google Scholar