CTCF Is the Master Organizer of Domain-Wide Allele-Specific Chromatin at the H19/Igf2 Imprinted Region

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
• 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
• Bell, A. C., A. G. West, and G. Felsenfeld. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98:387–396.
   PubMed Web of Science ®Google Scholar
• Brannan, C. I., and M. S. Bartolomei. 1999. Mechanisms of genomic imprinting. Curr. Opin. Genet. Dev. 9:164–170.
   PubMed Web of Science ®Google Scholar
• Choo, J. H., J. D. Kim, J. H. Chung, L. Stubbs, and J. Kim. 2006. Allele-specific deposition of macroH2A1 in imprinting control regions. Hum. Mol. Genet. 15:717–724.
   PubMedGoogle Scholar
• Constância, M., W. Dean, S. Lopes, T. Moore, G. Kelsey, and W. Reik. 2000. Deletion of a silencer element in Igf2 results in loss of imprinting independent of H19. Nat. Genet. 26:203–206.
   PubMedGoogle Scholar
• Delaval, K., J. Govin, F. Cerqueira, S. Rousseaux, S. Khochbin, and R. Feil. 2007. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J. 26:720–729.
   PubMed Web of Science ®Google Scholar
• Doyen, C. M., W. An, D. Angelov, V. Bondarenko, F. Mietton, V. M. Studitsky, A. Hamiche, R. G. Roeder, P. Bouvet, and S. Dimitrov. 2006. Mechanism of polymerase II transcription repression by the histone variant macroH2A. Mol. Cell. Biol. 26:1156–1164.
   PubMedGoogle Scholar
• Eden, S., M. Constancia, T. Hashimshony, W. Dean, B. Goldstein, A. C. Johnson, I. Keshet, W. Reik, and H. Cedar. 2001. An upstream repressor element plays a role in Igf2 imprinting. EMBO J. 20:3518–3525.
   PubMedGoogle Scholar
• Engel, N., J. L. Thorvaldsen, and M. S. Bartolomei. 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.
   PubMed Web of Science ®Google Scholar
• Feil, R., M. A. Handel, N. D. Allen, and W. Reik. 1995. Chromatin structure and imprinting: developmental control of DNase-I sensitivity in the mouse insulin-like growth factor 2 gene. Dev. Genet. 17:240–252.
   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
• Filippova, G. N., S. Fagerlie, E. M. Klenova, C. Myers, Y. Dehner, G. Goodwin, P. E. Neiman, S. J. Collins, and V. V. Lobanenkov. 1996. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell. Biol. 16:2802–2813.
   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
• Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293:1074–1080.
   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
• Kim, T. H., Z. K. Abdullaev, A. D. Smith, K. A. Ching, D. I. Loukinov, R. D. Green, M. Q. Zhang, V. V. Lobanenkov, and B. Ren. 2007. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128:1231–1245.
   PubMed Web of Science ®Google Scholar
• Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128:693–705.
   PubMed Web of Science ®Google Scholar
• Kurukuti, S., V. K. Tiwari, G. Tavoosidana, E. Pugacheva, A. Murrell, Z. 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
• 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
• Lewis, A., K. Mitsuya, D. Umlauf, P. Smith, W. Dean, J. Walter, M. Higgins, R. Feil, and W. Reik. 2004. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat. Genet. 36:1291–1295.
   PubMed Web of Science ®Google Scholar
• Li, B., M. Carey, and J. L. Workman. 2007. The role of chromatin during transcription. Cell 128:707–719.
   PubMed Web of Science ®Google Scholar
• Mikkelsen, T. S., M. Ku, D. B. Jaffe, B. Issac, E. Lieberman, G. Giannoukos, P. Alvarez, W. Brockman, T. K. Kim, R. P. Koche, W. Lee, E. Mendenhall, A. O'Donovan, A. Presser, C. Russ, X. Xie, A. Meissner, M. Wernig, R. Jaenisch, C. Nusbaum, E. S. Lander, and B. E. Bernstein. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560.
   PubMed Web of Science ®Google Scholar
• Moon, H., G. Filippova, D. Loukinov, E. Pugacheva, Q. Chen, S. T. Smith, A. Munhall, B. Grewe, M. Bartkuhn, R. Arnold, L. J. Burke, R. Renkawitz-Pohl, R. Ohlsson, J. Zhou, R. Renkawitz, and V. Lobanenkov. 2005. CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep. 6:165–170.
   PubMedGoogle Scholar
• Murrell, A., S. Heeson, L. Bowden, M. Constancia, W. Dean, G. Kelsey, and W. Reik. 2001. An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO Rep. 2:1101–1106.
   PubMed Web of Science ®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
• Pant, V., P. Mariano, C. Kanduri, A. Mattsson, V. Lobanenkov, R. Heuchel, and R. Ohlsson. 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.
   PubMed Web of Science ®Google Scholar
• Ripoche, M. A., C. Kress, F. Poirier, and L. Dandolo. 1997. Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev. 11:1596–1604.
   PubMed Web of Science ®Google Scholar
• Rotwein, P., and L. J. Hall. 1990. Evolution of insulin-like growth factor II: characterization of the mouse IGF-II gene and identification of two pseudo-exons. DNA Cell Biol. 9:725–735.
   PubMedGoogle Scholar
• Schoenherr, C. J., J. M. Levorse, and S. M. Tilghman. 2003. CTCF maintains differential methylation at the Igf2/H19 locus. Nat. Genet. 33:66–69.
   PubMed Web of Science ®Google Scholar
• Splinter, E., H. Heath, J. Kooren, R. J. Palstra, P. Klous, F. Grosveld, N. Galjart, and W. de Laat. 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
• Szabó, P., and J. R. Mann. 1994. Expression and methylation of imprinted genes during in vitro differentiation of mouse parthenogenetic and androgenetic embryonic stem cell lines. Development 120:1651–1660.
   PubMed Web of Science ®Google Scholar
• Szabó, P., S. H. Tang, A. Rentsendorj, G. P. Pfeifer, and J. R. Mann. 2000. Maternal-specific footprints at putative CTCF sites in the H19 imprinting control region give evidence for insulator function. Curr. Biol. 10:607–610.
   PubMed Web of Science ®Google Scholar
• Szabó, P. E., and J. R. Mann. 1995. Biallelic expression of imprinted genes in the mouse germ line: implications for erasure, establishment, and mechanisms of genomic imprinting. Genes Dev. 9:1857–1868.
   PubMed Web of Science ®Google Scholar
• Szabó, P. E., S. H. Tang, M. R. Reed, F. J. Silva, W. M. Tsark, and J. R. Mann. 2002. The chicken beta-globin insulator element conveys chromatin boundary activity but not imprinting at the mouse Igf2/H19 domain. Development 129:897–904.
   PubMed Web of Science ®Google Scholar
• Szabó, P. E., S. H. Tang, F. J. Silva, W. M. Tsark, and J. R. Mann. 2004. Role of CTCF binding sites in the Igf2/H19 imprinting control region. Mol. Cell. Biol. 24:4791–4800.
   PubMed Web of Science ®Google 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
• 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
• Yang, Y., J. F. Hu, G. A. Ulaner, T. Li, X. Yao, T. H. Vu, and A. R. Hoffman. 2003. Epigenetic regulation of Igf2/H19 imprinting at CTCF insulator binding sites. J. Cell Biochem. 90:1038–1055.
   PubMedGoogle Scholar