The Igf2/H19 imprinting control region exhibits sequence-specific and cell-type-dependent DNA methylation-mediated repression

Nucleic Acids Research

Volumn 37, Issue 3, 2009, Pages 793-803

  Chen, Yinming ^a   Dhupelia, Amrita ^a   Schoenherr, Christopher J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; PHENYLALANINE; SOMATOMEDIN B; THREONINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR H19; UNCLASSIFIED DRUG; CCCTC BINDING FACTOR; CCCTC-BINDING FACTOR; DNA BINDING PROTEIN; IGF2 PROTEIN, MOUSE; REPRESSOR PROTEIN; RNA H19; UNTRANSLATED RNA;

ANIMAL CELL; ARTICLE; BACTERIOPHAGE LAMBDA; CELL DENSITY; CELL STRAIN COS7; CELL TYPE; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; GENE DELETION; GENE NUMBER; GENE REPRESSION; GENETIC TRANSFECTION; GENOME IMPRINTING; HELA CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPORTER GENE; ANIMAL; CELL LINE; CPG ISLAND; GENE SILENCING; GENETICS; METABOLISM; MOLECULAR GENETICS; PROMOTER REGION;

BACTERIA (MICROORGANISMS); ENTEROBACTERIA PHAGE LAMBDA;

ANIMALS; BASE SEQUENCE; CELL LINE; CPG ISLANDS; DNA METHYLATION; DNA-BINDING PROTEINS; GENE SILENCING; GENOMIC IMPRINTING; HUMANS; INSULIN-LIKE GROWTH FACTOR II; MICE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; RNA, UNTRANSLATED;

EID: 63349112163     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn985     Document Type: Article

References (49)

1. Rollins,R.A., Haghighi,F., Edwards,J.R., Das,R., Zhang,M.Q., Ju,J. and Bestor,T.H. (2006) Large-scale structure of genomic methylation patterns. Genome Res., 16, 157-163.
2. Walsh,C.P., Chaillet,J.R. and Bestor,T.H. (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet., 20, 116-117.
3. Hansen,R.S., Wijmenga,C., Luo,P., Stanek,A.M., Canfield,T.K., Weemaes,C.M. and Gartler,S.M. (1999) The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc. Natl Acad. Sci. USA, 96, 14412-14417.
4. Gonzalo,S., Jaco,I., Fraga,M.F., Chen,T., Li,E., Esteller,M. and Blasco,M.A. (2006) DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat. Cell Biol., 8 416-424.
5. Mohandas,T., Sparkes,R.S. and Shapiro,L.J. (1981) Reactivation of an inactive human X chromosome: Evidence for X inactivation by DNA methylation. Science, 211, 393-396.
6. Jones,P.A., Taylor,S.M., Mohandas,T. and Shapiro,L.J. (1982) Cell cycle-specific reactivation of an inactive X-chromosome locus by 5-azadeoxycytidine. Proc. Natl Acad. Sci. USA, 79, 1215-1219.
7. Wolf,S.F. and Migeon,B.R. (1982) Studies of X chromosome DNA methylation in normal human cells. Nature, 295, 667-671.
8. Li,E., Beard,C. and Jaenisch,R. (1993) Role for DNA methylation in genomic imprinting. Nature, 366, 362-365.
9. Bird,A.P. and Wolffe,A.P. (1999) Methylation-induced repression-belts, braces, and chromatin. Cell, 99, 451-454.
10. Ehrlich,M. (2003) Expression of various genes is controlled by DNA methylation during mammalian development. J. Cell Biochem., 88 899-910.
11. Migeon,B.R. (1994) X-chromosome inactivation: Molecular mechanisms and genetic consequences. Trends Genet., 10, 230-235.
12. Jones,P.A. and Baylin,S.B. (2002) The fundamental role of epigenetic events in cancer. Nat. Rev. Genet., 3, 415-428.
13. Ehrlich,M. (2006) Cancer-linked DNA hypomethylation and its relationship to hypermethylation. Curr. Top. Microbiol. Immunol., 310, 251-274.
14. Illingworth,R., Kerr,A., Desousa,D., Jorgensen,H., Ellis,P., Stalker,J., Jackson,D., Clee,C., Plumb,R. et al. (2008) A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol., 6, e22.
15. Mohn,F., Weber,M., Rebhan,M., Roloff,T.C., Richter,J., Stadler,M.B., Bibel,M. and Schubeler,D. (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell, 30, 755-766.
16. Momparler,R.L. and Bovenzi,V. (2000) DNA methylation and cancer. J. Cell Physiol., 183, 145-154.
17. Grewal,S.I. and Jia,S. (2007) Heterochromatin revisited. Nat. Rev. Genet., 8, 35-46.
18. Buschhausen,G., Wittig,B., Graessmann,M. and Graessmann,A. (1987) Chromatin structure is required to block transcription of the methylated herpes simplex virus thymidine kinase gene. Proc. Natl Acad. Sci. USA 84, 1177-1181.
19. Kass,S.U., Landsberger,N. and Wolffe,A.P. (1997) DNA methylation directs a time-dependent repression of transcription initiation. Curr. Biol. 7, 157-165.
20. Iguchi-Ariga,S.M. and Schaffner,W. (1989) CpG methylation of the cAMP-responsive enhancer/promoter sequence TGACGTCA abolishes specific factor binding as well as transcriptional activation. Genes Dev., 3, 612-619.
21. Comb,M. and Goodman,H.M. (1990) CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2. Nucleic Acids Res., 18, 3975-3982.
22. Jones,P.L., Veenstra,G.J., Wade,P.A., Vermaak,D., Kass,S.U., Landsberger,N., Strouboulis,J. and Wolffe,A.P. (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet., 19, 187-191.
23. Nan,X., Ng,H.H., Johnson,C.A., Laherty,C.D., Turner,B.M., Eisenman,R.N. and Bird,A. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature, 393, 386-389.
24. Ng,H.H., Zhang,Y., Hendrich,B., Johnson,C.A., Turner,B.M., Erdjument-Bromage,H., Tempst,P., Reinberg,D. and Bird,A. (1999) MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet., 23, 58-61.
25. Nuber,U.A., Kriaucionis,S., Roloff,T.C., Guy,J., Selfridge,J., Steinhoff,C., Schulz,R., Lipkowitz,B., Ropers,H.H., Holmes,M.C. et al. (2005) Up-regulation of glucocorticoid-regulated genes in a mouse model of rett syndrome. Hum. Mol. Genet., 14, 2247-2256.
26. Chahrour,M., Jung,S.Y., Shaw,C., Zhou,X., Wong,S.T., Qin,J. and Zoghbi,H.Y. (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science, 320, 1224-1229.
27. Unoki,M., Nishidate,T. and Nakamura,Y. (2004) ICBP90, an E2F-1 target, recruits HDAC1 and binds to methyl-CpG through its SRA domain. Oncogene, 23, 7601-7610.
28. Johnson,L.M., Bostick,M., Zhang,X., Kraft,E., Henderson,I., Callis,J. and Jacobsen,S.E. (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr. Biol., 17, 379-384.
29. Damelin,M. and Bestor,T.H. (2007) Biological functions of DNA methyltransferase 1 require its methyltransferase activity. Mol. Cell Biol., 27, 3891-3899.
30. Klose,R.J., Sarraf,S.A., Schmiedeberg,L., McDermott,S.M., Stancheva,I. and Bird,A.P. (2005) DNA binding selectivity of MeCP2 due to a requirement for A/T sequences adjacent to methyl-CpG. Mol. Cell, 19, 667-678.
31. Prokhortchouk,A., Hendrich,B., Jorgensen,H., Ruzov,A., Wilm,M., Georgiev,G., Bird,A. and Prokhortchouk,E. (2001) The p120 catenin partner kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev., 15, 1613-1618.
32. Zhang,X.Y., Jabrane-Ferrat,N., Asiedu,C.K., Samac,S., Peterlin,B.M. and Ehrlich,M. (1993) The major histocompatibility complex class II promoter-binding protein RFX (NF-X) is a methylated DNA-binding protein. Mol. Cell Biol., 13, 6810-6818.
33. Sengupta,P.K., Ehrlich,M. and Smith,B.D. (1999) A methylation-responsive MDBP/RFX site is in the first exon of the collagen alpha2(I) promoter. J. Biol. Chem., 274, 36649-36655.
34. Thorvaldsen,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.
35. Yates,P.A., Burman,R.W., Mummaneni,P., Krussel,S. and Turker,M.S. (1999) Tandem B1 elements located in a mouse methylation center provide a target for de novo DNA methylation. J. Biol. Chem., 274, 36357-36361.
36. Klose,R.J. and Bird,A.P. (2006) Genomic DNA methylation: The mark and its mediators. Trends Biochem. Sci., 31, 89-97.
37. Drewell,R.A., Brenton,J.D., Ainscough,J.F., Barton,S.C., Hilton,K.J., Arney,K.L., Dandolo,L. and Surani,M.A. (2000) Deletion of a silencer element disrupts H19 imprinting independently of a DNA methylation epigenetic switch. Development, 127, 3419-3428.
38. 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.
39. 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.
40. 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.
41. Engel,N., West,A.G., Felsenfeld,G. and Bartolomei,M.S. (2004) Antagonism between DNA hypermethylation and enhancer-blocking activity at the H19 DMD is uncovered by CpG mutations. Nat. Genet., 36, 883-888.
42. Hsieh,C.L. (1997) Stability of patch methylation and its impact in regions of transcriptional initiation and elongation. Mol. Cell Biol. 17, 5897-5904.
43. 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.
44. Reese,K.J., Lin,S., Verona,R.I., Schultz,R.M. and Bartolomei,M.S. (2007) Maintenance of paternal methylation and repression of the imprinted H19 gene requires MBD3. PLoS Genet., 3, e137.
45. Graessmann,A., Sandberg,G., Guhl,E. and Graessmann,M. (1994) Methylation of single sites within the herpes simplex virus tk coding region and the simian virus 40 T-antigen intron causes gene inactivation. Mol. Cell Biol., 14, 2004-2010.
46. Santoro,R. and Grummt,I. (2001) Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol. Cell, 8, 719-725.
47. Hsieh,C.L. (1994) Dependence of transcriptional repression on CpG methylation density. Mol. Cell. Biol., 14, 5487-5494.
48. Lorincz,M.C., Dickerson,D.R., Schmitt,M. and Groudine,M. (2004) Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat. Struct. Mol Biol., 11, 1068-1075.
49. Stirzaker,C., Song,J.Z., Davidson,B. and Clark,S.J. (2004) Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res., 64, 3871-3877.