Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes

Genes and Development

Volumn 20, Issue 10, 2006, Pages 1268-1282

  Mancini DiNardo, Debora ^a   Steele, Scott J S ^a   Levorse, John M ^a   Ingram, Robert S ^a   Tilghman, Shirley M ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

DNA methylation; Genomic imprinting; Kcnq1ot1; Noncoding RNA; RNA dependent silencing

Indexed keywords

POTASSIUM CHANNEL KCNQ1;

ANIMAL CELL; ARTICLE; CHROMOSOME 7; CONTROLLED STUDY; DNA METHYLATION; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE SEQUENCE; GENE SILENCING; GENOME IMPRINTING; GENOTYPE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SILENT GENE;

ANIMALS; CPG ISLANDS; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DNA METHYLATION; GENOMIC IMPRINTING; METHYLTRANSFERASES; MICE; PROMOTER REGIONS (GENETICS); RNA, ANTISENSE; RNA, MESSENGER, STORED; RNA, UNTRANSLATED; SEQUENCE DELETION; TERMINATOR REGIONS (GENETICS); TRANSCRIPTION, GENETIC;

EID: 33646598385     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1416906     Document Type: Article

References (60)

1. Andrews, J.D., Mancini, D.N., Singh, S.M., and Rodenhiser, D.I. 1996. Site and sequence specific DNA methylation in the neurofibromatosis (NF1) gene includes C5839T: The site of the recurrent substitution mutation in exon 31. Hum. Mol. Genet. 5: 503-507.
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. Bhogal, B., Arnaudo, A., Dymkowski, A., Best, A., and Davis, T.L. 2004. Methylation at mouse Cdkn1c is acquired during postimplantation development and functions to maintain imprinted expression. Genomics 84: 961-970.
4. Bielinska, B., Blaydes, S.M., Buiting, K., Yang, T., Krajewska-Walasek, M., Horsthemke, B., and Brannan, C.I. 2000. De novo deletions of SNRPN exon 1 in early human and mouse embryos result in a paternal to maternal imprint switch. Nat. Genet. 25: 74-78.
5. Bourc'his, D., Xu, G.L., Lin, C.S., Bollman, B., and Bestor, T.H. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science 294: 2536-2539.
6. Brown, C.J., Hendrich, B.D., Rupert, J.L., Lafreniere, R.G., Xing, Y., Lawrence, J., and Willard, H.F. 1992. The human XIST gene: Analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71: 527-542.
7. Cao, R. and Zhang, Y. 2004. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 14: 155-164.
8. Carrel, L. and Willard, H.F. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404.
9. Caspary, T., Cleary, M.A., Baker, C.C., Guan, X.-J., and Tilghman, S.M. 1998. Multiple mechanisms regulate imprinting of the mouse distal chromosome 7 gene cluster. Mol. Cell. Biol. 18: 3466-3474.
10. Davis, T.L., Yang, G.J., McCarrey, J.R., and Bartolomei, M.S. 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.
11. Dykxhoorn, D.M., Novina, C.D., and Sharp, P.A. 2003. Killing the messenger: Short RNAs that silence gene expresssion. Nat. Rev. Mol. Cell Biol. 4: 457-467.
12. Engemann, S., Strodicke, M., Paulsen, M., Franck, O., Reinhardt, R., Lane, N., Reik, W., and Walter, J. 2000. Sequence and functional comparison in the Beckwith-Wiedemann region: Implications for a novel imprinting centre and extended imprinting. Hum. Mol. Genet. 9: 2691-2706.
13. Enklaar, T., Esswein, M., Oswald, M., Hilbert, K., Winterpacht, A., Higgins, M., Zabel, B., and Prawitt, D. 2000. Mtr1, a novel biallelically expressed gene in the center of the mouse distal chromosome 7 imprinting cluster, is a member of the Trp gene family. Genomics 67: 179-187.
14. Fitzpatrick, G.V., Soloway, P.D., and Higgins, M.J. 2002. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat. Genet. 9: 426-431.
15. Gould, T.D. and Pfeifer, K. 1998. Imprinting of Kvlqt1 is developmentally regulated. Hum. Mol. Genet. 7: 483-487.
16. Guillemot, F., Caspary, T., Tilghman, S.M., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Anderson, D.J., Joyner, A.L., Rossant, J., and Nagy, A. 1995. Genomic imprinting of Mash-2, a mouse gene required for trophoblast development. Nat. Genet. 9: 235-241.
17. 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.
18. Hata, K., Okano, M., Lei, H., and Li, E. 2002. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129: 1983-1993.
19. Hatada, I. and Mukai, T. 1995. Genomic imprinting of p57/KIP2, a cyclin-dependent kinase inhibitor, in mouse. Nat. Genet. 11: 204-206.
20. Hatada, I., Ohashi, H., Fukushima, Y., Kanetko, Y., Inoue, M., Komoto, Y., Okada, A., Ohishi, S., Nabetani, A., Morisaki, H., et al. 1996. An imprinted gene p57KIP2 is mutated in Beckwith-Wiedemann syndrome. Nat. Genet. 14: 171-173.
21. Hendrich, B.D., Brown, C.J., and Willard, H.F. 1993. Evolutionary conservation of possible functional domains of the human and murine XIST genes. Hum. Mol. Genet. 2: 663-672.
22. Hoskins, R.A., Smith, C.D., Carlson, J.W., Carvalho, A.B., Halpern, A., Kaminker, J.S., Kennedy, C., Mungall, C.J., Sullivan, B.A., Sutton, G.G., et al. 2002. Heterochromatic sequences in a Drosophila whole-genome shotgun assembly. Genome Biol. 3: RESEARCH0085.
23. Kaffer, C.R., Srivastava, M., Park, K.Y., Ives, E., Hsieh, S., Batlle, J., Grinberg, A., Huang, S.P., and Pfeifer, K. 2000. A transcriptional insulator at the imprinted H19/Igf2 locus. Genes & Dev. 14: 1908-1919.
24. Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Urven, L., McCarrey, J., Cedar, H., and Razin, A. 1992. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes & Dev. 6: 705-714.
25. Kanduri, C., Pant, V., Loukinov, D., Pugacheva, E., Qi, C.F., Wolffe, A., Ohlsson, R., and Lobanenkov, V.V. 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.
26. Kaneda, M., Okano, M., Hata, K., Sado, T., Tsujimoto, N., Li, E., and Sasaki, H. 2004. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429: 900-903.
27. Lam, W.W., Hatada, I., Ohishi, S., Mukai, T., Joyce, J.A., Cole, T.R., Donnai, D., Reik, W., Schofield, P.N., and Maher, E.R. 1999. Analysis of germline CDKN1C (p57KIP2) mutations in familial and sporadic Beckwith-Wiedemann syndrome (BWS) provides a novel genotype-phenotype correlation. J. Med. Genet. 36: 518-523.
28. Leighton, P.A., Ingram, R.S., Eggenschwiler, J., Efstratiadis, A., and Tilghman, S.M. 1995. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature 375: 34-39.
29. Lewis, A., Mitsuya, K., Umlauf, D., Smith, P., Dean, W., Walter, J., Higgins, M., Feil, R., and Reik, W. 2004. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat. Genet. 36: 1291-1295.
30. Li, E., Beard, C., and Jaenisch, R. 1993. The role of DNA methylation in genomic imprinting. Nature 366: 362-365.
31. Lin, S.P., Youngson, N., Takada, S., Seitz, H., Reik, W., Paulsen, M., Cavaille, J., and Ferguson-Smith, A.C. 2003. Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat. Genet. 35: 97-102.
32. Mager, J., Montgomery, N.D., de Villena, F.P., and Magnuson, T. 2003. Genome imprinting regulated by the mouse Polycomb group protein Eed. Nat. Genet. 33: 502-507.
33. Maher, E.R. and Reik, W. 2000. Beckwith-Wiedemann syndrome: Imprinting in clusters revisited. J. Clin. Invest. 105: 247-252.
34. Mancini, D.N., Rodenhiser, D.I., Ainsworth, P.J., O'Malley, F.P., Singh, S.M., Xing, W., and Archer, T.K. 1998. CpG methylation within the 5′ regulatory region of the BRCA1 gene is tumor specific and includes a putative CREB binding site. Oncogene 16: 1161-1169.
35. Mancini-DiNardo, D., Steele, S.J.S., Ingram, R.S., and Tilghman, S.M. 2003. A differentially methylated region within the gene Kcnq1 functions as an imprinted promoter and silencer. Hum. Mol. Genet. 12: 283-294.
36. Matzke, M.A. and Birchler, J.A. 2005. RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6: 24-35.
37. McGrath, J. and Solter, D. 1984. Inability of mouse blastomere nuclei transferred to enucleated zygotes to support development in vitro. Science 226: 1317-1319.
38. Nielsen, S.J., Schneider, R., Bauer, U.M., Bannister, A.J., Morrison, A., O'Carroll, D., Firestein, R., Cleary, M., Jenuwein, T., Herrera, R.E., et al. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412: 561-565.
39. Ogawa, Y. and Lee, J.T. 2002. Antisense regulation in X inactivation and autosomal imprinting. Cytogenet. Genome Res. 99: 59-65.
40. O'Keefe, D., Dao, D., Zhao, L., Sanderson, R., Warburton, D., Weiss, L., Anyane-Yeboa, K., and Tycko, B. 1997. Coding mutations in p57KIP2 are present in some cases of Beckwith-Wiedemann syndrome but are rare or absent in Wilms tumors. Am. J. Hum. Genet. 61: 295-303.
41. Paulsen, M., Khare, T., Burgard, C., Tierling, S., and Walter, J. 2005. Evolution of the Beckwith-Wiedemann syndrome region in vertebrates. Genome Res. 15: 146-153.
42. Reinhart, B., Elijanne, M., and Chaillet, J.R. 2002. Shared role for differentially methylated domains of imprinted genes. Mol. Cell. Biol. 22: 2089-2098.
43. Schoenherr, C.J., Levorse, J.M., and Tilghman, S.M. 2003. CTCF maintains differential methylation at the Igf2/H19 locus. Nat. Genet. 33: 66-69.
44. Sleutels, F., Zwart, R., and Barlow, D.P. 2002. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415: 810-813.
45. Smilinich, N.J., Day, C.D., Fitzpatrick, G.V., Caldwell, G.M., Lossie, A.C., Cooper, P.R., Smallwood, A.C., Joyce, J.A., Schofield, P.N., Reik, W., et al. 1999. A maternally methylated CpG island in KvLQT1 is associated with an antisense paternal transcript and loss of imprinting in Beckwith-Wiedemann syndrome. Proc. Natl. Acad. Sci. 96: 8064-8069.
46. Stoger, R., Kubicka, P., Liu, C.-G., Kafri, T., Razin, A., Cedar, H., and Barlow, D.P. 1993. Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell 73: 61-71.
47. Surani, M.A.H., Barton, S.C., and Norris, M.L. 1984. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308: 548-550.
48. Tanaka, M., Puchyr, M., Gertsenstein, M., Harpal, K., Jaenisch, R., Rossant, J., and Nagy, A. 1999. Parental origin-specific expression of Mash2 is established at the time of implantation with its imprinting mechanism highly resistant to genome-wide demethylation. Mech. Dev. 87: 129-142.
49. Thakur, N., Kanduri, M., Holmgren, C., Mukhopadhyay, R., and Kanduri, C. 2003. Bidirectional silencing and DNA methylation-sensitive methylation- spreading properties of the Kcnq1 imprinting control region map to the same regions. J. Biol. Chem. 278: 9514-9519.
50. Thakur, N., Tiwari, V.K., Thomassin, H., Pandey, R.R., Kanduri, M., Gondor, A., Grange, T., Ohlsson, R., and Kanduri, C. 2004. An antisense RNA regulates the bidirectional silencing property of the Kcnq1 imprinting control region. Mol. Cell. Biol. 24: 7855-7862.
51. Thorvaldson, J.L., Duran, K.L., and Bartolomei, M.S. 1998. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes & Dev. 12: 3693-3702.
52. Tremblay, K.D., Saam, J.R., Ingram, R.S., Tilghman, S.M., and Bartolomei, M.S. 1995. A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat. Genet. 9: 407-413.
53. Umlauf, D., Goto, Y., Cao, R., Cerqueira, F., Wagschal, A., Zhang, Y., and Feil, R. 2004. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat. Genet. 36: 1296-1300.
54. Wang, L., Brown, J.L., Cao, R., Zhang, Y., Kassis, J.A., and Jones, R.S. 2004. Hierarchical recruitment of polycomb group silencing complexes. Mol. Cell 14: 637-646.
55. Wutz, A., Smrzka, O.W., Schweifer, N., Schellander, K., Wagner, E.F., and Barlow, D.P. 1997. Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature 389: 745-749.
56. Wutz, A., Rasmussen, T.P., and Jaenisch, R. 2002. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat. Genet. 30: 167-174.
57. Yan, Y., Frisén, J., Lee, M.-H., Massagué, J., and Barbacid, M. 1997. Ablation of the CDK inhibitor p57KIP2 results in increased apoptosis and delayed differentiation during mouse development. Genes & Dev. 11: 973-983.
58. Yatsuki, H., Joh, K., Higashimoto, K., Soejima, H., Arai, Y., Wang, Y., Hatada, I., Obata, Y., Morisaki, H., Zhang, Z., et al. 2002. Domain regulation of imprinting cluster in Kip2/Lit1 subdomain on mouse chromosome 7F4/F5: Large-scale DNA methylation analysis reveals that DMR-Lit1 is a putative imprinting control region. Genome Res. 12: 1860-1870.
59. Yoon, B.J., Herman, H., Sikora, A., Smith, L.T., Plass, C., and Soloway, P.D. 2002. Regulation of DNA methylation of Rasgrf1. Nat. Genet. 30: 92-96.
60. Zhang, P., Liégeois, N.J., Wong, C., Finegold, M., Hou, H., Thompson, J.C., Silverman, A., Harper, J.W., DePinho, R.A., and Elledge, S.J. 1997. Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann sydrome. Nature 387: 151-158.