Interruption of intrachromosomal looping by CCCTC binding factor decoy proteins abrogates genomic imprinting of human insulin-like growth factor II

Journal of Cell Biology

Volumn 193, Issue 3, 2011, Pages 475-487

  Zhang, He ^a,b   Niu, Beibei ^b   Hu, Ji Fan ^b   Ge, Shengfang ^a   Wang, Haibo ^a,b   Li, Tao ^b   Ling, Jianqun ^b   Steelman, Brandon N ^b   Qian, Guanxiang ^a   Hoffman, Andrew R ^b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; HISTONE H3; METHYL CPG BINDING PROTEIN; METHYLTRANSFERASE; METHYLTRANSFERASE SSS1; POLYCOMB GROUP PROTEIN; POLYCOMB GROUP PROTEIN EZH2; POLYCOMB GROUP PROTEIN SUZ12; SOMATOMEDIN B; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ALLELE; AMINO TERMINAL SEQUENCE; ARTICLE; CANCER CELL; CHROMOSOME; CONTROLLED STUDY; FIBROBLAST; GENE OVEREXPRESSION; GENETIC CONSERVATION; GENOME IMPRINTING; HISTONE METHYLATION; HUMAN; HUMAN CELL; INTRACHROMOSOMAL LOOP; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; REGULATORY MECHANISM;

ALLELES; CARRIER PROTEINS; CHROMATIN; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FIBROBLASTS; GENE SILENCING; GENOMIC IMPRINTING; HUMANS; INSULIN-LIKE GROWTH FACTOR II; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; ZINC FINGERS;

EID: 79956219904     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201101021     Document Type: Article

References (47)

1. Arney, K.L. 2003. H19 and Igf2-enhancing the confusion? Trends Genet. 19:17-23.
2. Bartolomei, M.S. 2003. Epigenetics: role of germ cell imprinting. Adv. Exp. Med. Biol. 518:239-245.
3. 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.
4. Bell, A.C., and G. Felsenfeld. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature. 405:482-485.
5. 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.
6. Bell, A.C., A.G. West, and G. Felsenfeld. 2001. Insulators and boundaries: versatile regulatory elements in the eukaryotic genome. Science. 291:447-450.
7. Chen, H.L., T. Li, X.W. Qiu, J. Wu, J.Q. Ling, Z.H. Sun, W. Wang, W. Chen, A. Hou, T.H. Vu, et al. 2006. Correction of aberrant imprinting of IGF2 in human tumors by nuclear transfer-induced epigenetic reprogramming. EMBO J. 25:5329-5338.
8. Cui, H., P. Onyango, S. Brandenburg, Y. Wu, C.L. Hsieh, and A.P. Feinberg. 2002. Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2. Cancer Res. 62:6442-6446.
9. Dekker, J., K. Rippe, M. Dekker, and N. Kleckner. 2002. Capturing chromosome conformation. Science. 295:1306-1311.
10. Donohoe, M.E., S.S. Silva, S.F. Pinter, N. Xu, and J.T. Lee. 2009. The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature. 460:128-132.
11. Dunn, K.L., and J.R. Davie. 2003. The many roles of the transcriptional regulator CTCF. Biochem. Cell Biol. 81:161-167.
12. Engel, N., and M.S. Bartolomei. 2003. Mechanisms of insulator function in gene regulation and genomic imprinting. Int. Rev. Cytol. 232:89-127.
13. Feinberg, A.P. 1993. Genomic imprinting and gene activation in cancer. Nat. Genet. 4:110-113.
14. Filippova, G.N. 2008. Genetics and epigenetics of the multifunctional protein CTCF. Curr. Top. Dev. Biol. 80:337-360.
15. Fitzpatrick, G.V., E.M. Pugacheva, J.Y. Shin, Z. Abdullaev, Y. Yang, K. Khatod, V.V. Lobanenkov, and M.J. Higgins. 2007. Allele-specific binding of CTCF to the multipartite imprinting control region KvDMR1. Mol. Cell. Biol. 27:2636-2647.
16. Hark, A.T., C.J. Schoenherr, D.J. Katz, R.S. Ingram, J.M. Levorse, and S.M. Tilghman. 2000. CTCF mediates methylation-sensitive enhancerblocking activity at the H19/Igf2 locus. Nature. 405:486-489.
17. Hu, J.F., T.H. Vu, and A.R. Hoffman. 1996. Promoter-specific modulation of insulin-like growth factor II genomic imprinting by inhibitors of DNA methylation. J. Biol. Chem. 271:18253-18262.
18. Hu, J.F., T.H. Vu, and A.R. Hoffman. 1997. Genomic deletion of an imprint maintenance element abolishes imprinting of both insulin-like growth factor II and H19. J. Biol. Chem. 272:20715-20720.
19. 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.
20. 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.
21. 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.
22. Li, T., J.F. Hu, X. Qiu, J. Ling, H. Chen, S. Wang, A. 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.
23. Ling, J.Q., T. Li, J.F. Hu, T.H. Vu, H.L. Chen, X.W. Qiu, A.M. Cherry, and A.R. Hoffman. 2006. CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science. 312:269-272.
24. Mann, J.R., P.E. Szabó, M.R. Reed, and J. Singer-Sam. 2000. Methylated DNA sequences in genomic imprinting. Crit. Rev. Eukaryot. Gene Expr. 10:241-257.
25. Moore, T., M. Constancia, M. Zubair, B. Bailleul, R. Feil, H. Sasaki, and W. Reik. 1997. Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2. Proc. Natl. Acad. Sci. USA. 94:12509-12514.
26. Mukhopadhyay, R., W. Yu, J. Whitehead, J. Xu, M. Lezcano, S. Pack, C. Kanduri, M. Kanduri, V. Ginjala, A. Vostrov, et al. 2004. The binding sites for the chromatin insulator protein CTCF map to DNA methylation-free domains genome-wide. Genome Res. 14:1594-1602.
27. Murrell, A., S. Heeson, and W. Reik. 2004. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parentspecific chromatin loops. Nat. Genet. 36:889-893.
28. Ohlsson, R., R. Renkawitz, and V. Lobanenkov. 2001. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet. 17:520-527.
29. Ohlsson, R., V. Lobanenkov, and E. Klenova. 2010. Does CTCF mediate between nuclear organization and gene expression? Bioessays. 32:37-50.
30. Pant, V., S. Kurukuti, E. Pugacheva, S. Shamsuddin, P. Mariano, R. Renkawitz, E. Klenova, V. Lobanenkov, and R. Ohlsson. 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. Phillips, J.E., and V.G. Corces. 2009. CTCF: master weaver of the genome. Cell. 137:1194-1211.
32. Recillas-Targa, F., I.A. De La Rosa-Velázquez, E. Soto-Reyes, and L. Benítez-Bribiesca. 2006. Epigenetic boundaries of tumour suppressor gene promoters: the CTCF connection and its role in carcinogenesis. J. Cell. Mol. Med. 10:554-568.
33. Reik, W., M. Constancia, W. Dean, K. Davies, L. Bowden, A. Murrell, R. Feil, J. Walter, and G. Kelsey. 2000. Igf2 imprinting in development and disease. Int. J. Dev. Biol. 44:145-150.
34. Renbaum, P., D. Abrahamove, A. Fainsod, G.G. Wilson, S. Rottem, and A. Razin. 1990. Cloning, characterization, and expression in Escherichia coli of the gene coding for the CpG DNA methylase from Spiroplasma sp. strain MQ1(M.SssI). Nucleic Acids Res. 18:1145-1152.
35. Sasaki, H., K. Ishihara, and R. Kato. 2000. Mechanisms of Igf2/H19 imprinting: DNA methylation, chromatin and long-distance gene regulation. J. Biochem. 127:711-715.
36. 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.
37. Sparago, A., F. Cerrato, M. Vernucci, G.B. Ferrero, M.C. Silengo, and A. Riccio. 2004. Microdeletions in the human H19 DMR result in loss of IGF2 imprinting and Beckwith-Wiedemann syndrome. Nat. Genet. 36:958-960.
38. 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.
39. Sullivan, M.J., T. Taniguchi, A. Jhee, N. Kerr, and A.E. Reeve. 1999. Relaxation of IGF2 imprinting in Wilms tumours associated with specific changes in IGF2 methylation. Oncogene. 18:7527-7534.
40. 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.
41. 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.
42. Ulaner, G.A., T.H. Vu, T. Li, J.F. Hu, X.M. Yao, Y. Yang, R. Gorlick, P. Meyers, J. Healey, M. Ladanyi, and A.R. Hoffman. 2003. Loss of imprinting of IGF2 and H19 in osteosarcoma is accompanied by reciprocal methylation changes of a CTCF-binding site. Hum. Mol. Genet. 12:535-549.
43. Vu, T.H., A.H. Nguyen, and A.R. Hoffman. 2010. Loss of IGF2 imprinting is associated with abrogation of long-range intrachromosomal interactions in human cancer cells. Hum. Mol. Genet. 19:901-919.
44. West, A.G., M. Gaszner, and G. Felsenfeld. 2002. Insulators: many functions, many mechanisms. Genes Dev. 16:271-288.
45. Wolffe, A.P. 2000. Transcriptional control: imprinting insulation. Curr. Biol. 10:R463-R465.
46. Xu, G.L., and T.H. Bestor. 1997. Cytosine methylation targetted to predetermined sequences. Nat. Genet. 17:376-378.
47. Yusufzai, T.M., H. Tagami, Y. Nakatani, and G. Felsenfeld. 2004. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell. 13:291-298.