DNA methylation, chromatin boundaries, and mechanisms of genomic imprinting

Archives of Medical Research

Volumn 33, Issue 5, 2002, Pages 428-438

  Recillas Targa, Félix ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Cancer; Chromatin; CTCF; Genomic imprinting; Insulator

Indexed keywords

DEOXYRIBONUCLEASE I; DNA FRAGMENT; GENE PRODUCT; HISTONE H3; METHYL CPG BINDING PROTEIN; NUCLEAR FACTOR; SOMATOMEDIN B; UNTRANSLATED RNA; ZINC FINGER PROTEIN;

ALLELE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL DIVISION; CHROMATIN STRUCTURE; DNA FLANKING REGION; DNA METHYLATION; DNA SEQUENCE; EMBRYO DEVELOPMENT; GAMETOGENESIS; GENE ACTIVATION; GENE CLUSTER; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE LOCATION; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENE REPLICATION; GENE SILENCING; GENETIC ANALYSIS; GENETIC ORGANIZATION; GENETIC TRANSCRIPTION; GENOME IMPRINTING; HUMAN; MOLECULAR MECHANICS; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTO ONCOGENE; REVIEW; TRANSGENE; TUMOR SUPPRESSOR GENE;

ALLELES; ANIMALS; CHROMATIN; DNA METHYLATION; GENE EXPRESSION REGULATION; GENOMIC IMPRINTING; HUMANS; INSULIN-LIKE GROWTH FACTOR II; MODELS, BIOLOGICAL; MODELS, GENETIC; PROTEIN STRUCTURE, TERTIARY; RNA, UNTRANSLATED;

EID: 0036760218     PISSN: 01884409     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0188-4409(02)00366-1     Document Type: Review

References (102)

1. Tilghman S.M. The sins of the fathers and mothers. genomic imprinting in mammalian development Cell. 96:1999;185-193.
2. Bulger M., Groudine M. Looping versus linking. toward a model for long-distance gene activation Genes Dev. 13:1999;2465-2477.
3. Wolffe A.P. Transcriptional control. imprinting insulation Curr Biol. 10:2000;R463-R465.
4. Brandeis M., Kafri T., Ariel M., Chaillet J.R., McCarrey J., Razin A., Cedar H. The ontogeny of allelic-specific methylation associated with imprinted genes in the mouse. EMBO J. 12:1993;3669-3677.
5. Szabo P.E., Mann J.R. Biallelic expression of imprinted genes in the mouse germ line. implications of erasure, establishment and mechanisms of genomic imprinting Genes Dev. 9:1995;1857-1868.
6. Shemer R., Briger Y., Riggs A.D., Razin A. Structure of the imprinted mouse Snrpn gene and establishment of its parental-specific methylation pattern. Proc Natl Acad Sci USA. 94:1997;10267-10272.
7. Tada M., Tada T., Lefebre L., Barton S.C., Surani M.A. Embryonic germ cells induce epigenetic reprogramming of somatic nucleus in hybrid cells. EMBO J. 16:1997;6510-6520.
8. Wolffe A.P., Matzke M.A. Epigenetics. regulation through repression Science. 286:1999;481-486.
9. Li E., Bestor T.H., Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell. 69:1992;915-926.
10. Li E., Beard C., Jaenisch R. The role of DNA methylation in genomic imprinting. Nature. 366:1993;362-365.
11. Lei H., Oh S.P., Okano M., Juttermann R., Goss K.A., Jaenisch R., Li E. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development. 122:1996;3195-3205.
12. Okano M., Bell D.W., Haber D.A., Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for the novo methylation and mammalian development. Cell. 99:1999;247-257.
13. Jackson-Grusby L., Beard C., Possemato R., Tudor M., Fambrough D., Csankowszki G., Dausman J., Lee P., Wilson C.H., Lander E., Jaenisch R. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet. 27:2001;31-39.
14. Caspary T., Clearly M.A., Baker C.C., Guan X.-J., Tilghman S.M. Multiple mechanisms regulate imprinting of the mouse distal chromosome 7 gene cluster. Mol Cell Biol. 18:1998;3466-3474.
15. Brannan C.I., Bartolomei M.S. Mechanisms of genomic imprinting. Curr Opin Genet Dev. 9:1999;164-170.
16. Sleutels F., Barlow D.P., Lyle R. The uniqueness of the imprinting mechanism. Curr Opin Genet Dev. 10:2000;229-233.
17. Bartolomei M.S., Zemel S., Tilghman S.M. Parental imprinting of the mouse H19 gene. Nature. 351:1991;153-155.
18. DeChiara T.M., Robertson E.J., Esftratiadis A. Parental imprinting of the mouse insulin-like growth factor II gene. Cell. 74:1991;505-514.
19. Kaffer C.R., Srivastava M., Park K.-Y., Ives E., Hsieh S., Batlle J., Grinberg A., Huang S.-P., Pfeifer K. A transcriptional insulator at the imprinted H19/Igf2 locus. Genes Dev. 14:2000;1908-1919.
20. Ashe H.L., Monks J., Wijgerde M., Fraser P., Proudfoot N.J. Intergenic transcription and trans-induction of the human β-globin locus. Genes Dev. 11:1997;2494-2509.
21. Gribnau J., Diderich K., Pruzina S., Calozolari R., Fraser P. Intergenic transcription and developmental remodeling of chromatin sub-domains in the human β-globin locus. Mol Cell. 5:2000;377-386.
22. Leighton P.A., Saam J.R., Ingram R.S., Stewart C.L., Tilghman S.M. An enhancer deletion affects both H19 and Igf2 expression. Genes Dev. 9:1995;2079-2089.
23. Lalande M. Parental imprinting and human disease. Annu Rev Genet. 30:1997;173-195.
24. Laird P.W., Jaenisch R. The role of DNA methylation in cancer genetics and epigenetics. Annu Rev Genet. 30:1996;441-464.
25. Thorvaldsen J.L., Duran K.L., Bartolomei M.S. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 12:1998;3693-3702.
26. Kaffer C.R., Srivastava M., Park K.-Y., Ives E., Hsieh S., Batlle J., Grinberg A., Huang S.-P., Pfeifer K. A transcriptional insulator at the imprinted H19/Igf2 locus. Genes Dev. 14:2000;1908-1919.
27. Webber A.L., Ingram R.S., Levorse J.M., Tilghman S.M. Location of enhancers is essential for the imprinting of H19 and Igf2 genes. Nature. 391:1998;711-715.
28. Schmidt J.V., Levorse J.M., Tilghman S.M. Enhancer competition between H19 and Igf2 does not mediate their imprinting. Proc Natl Acad Sci USA. 96:1999;9733-9738.
29. Hark A.T., Tilghman S.M. Chromatin conformation of the H19 epigenetic mark. Hum Mol Genet. 7:1998;1979-1985.
30. Szabo P.E., Pfeifer G.P., Mann J.R. Characterization of novel parent-specific epigenetic modifications upstream of the imprinted mouse H19 gene. Mol Cell Biol. 18:1998;6767-6778.
31. Khosla S., Aitchison A., Gregory R., Allen N.D., Feil R. Parental allele-specific chromatin configuration in a boundary-imprinting-control element upstream of the mouse H19 gene. Mol Cell Biol. 19:1999;2556-2566.
32. Boyes J., Felsenfeld G. Tissue-specific factors additively increase the probability of the all-or-none formation of a hypersensitive site. EMBO J. 15:1996;2496-2507.
33. Shibata H., Yoshino K., Sunahara S., Gondo Y., Katsuki M., Ueda T., Kamiya M., Muramatsu M., Kalcheva I., Plass C., Chapman V.M., Hayashizakim Y. Inactive allele-specific methylation and chromatin structure of the imprinting gene U2af1-rs1 on mouse chromosome 11. Genomics. 35:1996;248-252.
34. Feil R., Boyano M.D., Allen N.D., Kelsey G. Parental chromosome-specific chromatin conformation in the imprinted U2af1-rs1 gene in the mouse. J Biol Chem. 272:1997;20893-20900.
35. Schweizer J., Zynger D., Francke U. In vivo nuclease hypersensitivity studies reveal multiple sites of parental origin-dependent differential chromatin conformation in the 150 kb SNRPN transcription unit. Hum Mol Genet. 8:1999;555-566.
36. Pedone P.V., Pikaart M.J., Cerrato F., Vernucci M., Ungaro P., Bruni C.B., Riccio A. Role of histone acetylation and DNA methylation in the maintenance of the imprinted expression of the H19 and Igf2 genes. FEBS Lett. 458:1999;45-50.
37. Svensson K., Mattsson R., James T., Wentzel P., Pilartz M., MacLaughlin J., Miller S.J., Olsson T., Eriksson U.J., Ohlsson R. The paternal allele of the H19 gene is progressively silenced during early mouse development. the acetylation status of histones may be involved in the generation of variegated expression patterns Development. 125:1998;61-69.
38. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature. 410:2001;120-124.
39. Nakayama J., Rice J.C., Strahl B.D., Allis C.D., Grewal S.I. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science. 292:2001;110-113.
40. Nielsen S.J., Schneider R., Bauer U.-M., Bannister A.J., Morrison A., O'Carroll D., Firestein R., Clearly M., Jenuwein T., Herrera R.E., Kouzarides T. Rb targets histone H3 methylation and HP1 to promoters. Nature. 412:2001;561-565.
41. Srivastava M., Hsiek S., Grinberg A., Williams-Simons L., Huang S.-P., Pfeifer K. H19 and Igf2 monoallelic expression is regulated in two distinct ways by a shared cis acting regulatory region upstream of H19. Genes Dev. 14:2000;1186-1195.
42. Drewell R.A., Brenton J.D., Ainscough J.F.-X., Barton S.C., Hilton K.J., Arney K.L., Dandolo L., Surani M.A. Deletion of a silencer element disrupts H19 imprinting independently of a DNA methylation epigenetic switch. Development. 127:2000;3419-3428.
43. Constancia M., Dean W., Lopes S., Moore T., Kelsey G., Reik W. Deletion of a silencer element in Igf2 results in loss of imprinting independent of H19. Nature Genet. 26:2000;203-206.
44. Hark A.T., Schoenherr C.J., Katz D.J., Ingram R.S., Levorse J.M., Tilghman S.M. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature. 405:2000;486-489.
45. Bell A.C., Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature. 405:2000;482-485.
46. Szabo P.E., Tang S.-H.E., Rentsendorj A., Pfeifer G.P., Mann J.R. Maternal-specific footprints at putative CTCF sites in the H19 imprinting control region give evidence for insulator function. Curr Biol. 10:2000;607-610.
47. Kanduri C., Pant V., Loukinov D., Pugacheva E., Qui C.F., Wolffe A., Ohlsson R., Lobanenkov V.V. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr Biol. 10:2000;853-856.
48. Bell A.C., Felsenfeld G. Stopped at the border. boundaries and insulators Curr Opin Genet Dev. 9:1999;191-198.
49. Bell A.C., West A.G., Felsenfeld G. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell. 98:1999;387-396.
50. Recillas-Targa F., Bell A.C., Felsenfeld G. Positional enhancer-blocking activity of the chicken β-globin insulator in transiently transfected cells. Proc Natl Acad Sci USA. 96:1999;14354-14359.
51. Bell A.C., West A.G., Felsenfeld G. Insulators and boundaries. versatile regulatory elements in the eukaryotic genome Science. 291:2001;447-450.
52. Chung J.H., Whiteley M., Felsenfeld G. A 5′ element of the chicken β-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell. 74:1993;505-514.
53. Pikaart M.J., Recillas-Targa F., Felsenfeld G. Loss of transcriptional activity of a transgene is accompanied by DNA methylation and histone deacetylation and is prevented by insulators. Genes Dev. 12:1998;2852-2862.
54. Recillas-Targa F. The chicken α- and β-globin gene domains and their chromatin organization. Cell Mol Biol Lett. 5:2000;451-467.
55. Klenova E.M., Nicolas R.H., Paterson H.F., Carne A.F., Heath C.M., Goodwin G.H., Neiman P.E., Lobenenkov V.V. CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms. Mol Cell Biol. 13:1993;7612-7624.
56. Filippova G.N., Fagerlie S., Klenova E.M., Myers C., Dehner Y., Goodwin G., Neiman P.E., Collins S.J., Lobenenkov V.V. 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. 16:1996;2802-2813.
57. Burcin M., Arnold R., Luts M., Kaiser B., Runge D., Lottspeich F., Filippova G.N., Lobanenkov V.V., Reinkawitz R. Negative protein 1, which is required for function of the chicken lysozyme gene silencer in conjunction with hormone receptors, is identical to the multivalent zinc finger repressor CTCF. Mol Cell Biol. 17:1997;1281-1288.
58. Saitoh N., Bell A.C., Recillas-Targa F., West A.G., Simpson M., Pikaart M., Felsenfeld G. Structural and functional conservation at the boundaries of the chicken β-globin domain. EMBO J. 19:2000;2315-2322.
59. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature. 393:1998;386-389.
60. Jones P.L., Veenstra G.J., Wade P.A., Vermaak D., Kass S.U., Landsberger N., Strouboulis J., Wolffe A.P. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet. 19:1998;187-191.
61. Wade P.A., Gegonne A., Jones P.L., Ballestar E., Aubry F., Wolffe A.P. Mi-2 complex couples DNA methylation to chromatin remodeling and histone deacetylation. Nat Genet. 23:1999;62-66.
62. Dorsett D. Distant liaisons. long-range enhancer-promoter interactions in Drosophila Curr Opin Genet Dev. 9:1999;505-514.
63. Sun F.-L., Elgin S.C.R. Putting boundaries on silence. Cell. 99:1999;459-462.
64. Donze D., Adams C.R., Rine J., Kamakaka R. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev. 13:1999;698-708.
65. Litt M.D., Simpson M., Recillas-Targa F., Prioleau M.N., Felsenfeld G. Transition in histone acetylation reveals boundaries of three separately neighboring loci. EMBO J. 20:2001;2224-2235.
66. Litt M.D., Simpson M., Gaszner M., Allis C.D., Felsenfeld G. Correlation between histone lysine methylation and developmental changes at the chicken β-globin locus. Science. 293:2001;2453-2455.
67. Gerasimova T.I., Corces V.G. Polycomb and trithorax group proteins mediate the function of a chromatin insulator. Cell. 92:1998;511-521.
68. Falls J.G., Puford D.J., Wylie A.A., Jirtle R.L. Genomic imprinting. implications of human disease Am J Pathol. 154:1999;635-647.
69. Bartolomei M.S., Tilghman S.M. Genomic imprinting in mammals. Annu Rev Genet. 31:1997;493-525.
70. Nicholls R.D., Saitoh S., Horsthemke B. Imprinting in Prader-Willi and Angelman syndromes. Trends Genet. 14:1998;194-200.
71. Rougeulle C., Glatt H., Lalande M. The Angelman syndrome candidate gene, UBE3A/E6-AP, is imprinted in brains. Nat Genet. 17:1997;14-15.
72. Vu T.H., Hoffman A.R. Imprinting of the Angelman syndrome gene, UBE3A, is restricted to brain. Nat Genet. 17:1997;12-13.
73. Glenn C.C., Nicholls R.D., Robinson W.P., Saitoh S., Niikawa N., Schinzel A., Horsthemke B., Driscoll D.J. Modification of 15q11-q13 DNA methylation imprints in unique Angelman and Prader-Willi patients. Hum Mol Genet. 2:1993;1377-1382.
74. Reed M.L., Leff S.E. Maternal imprinting of human SNRPN, a gene deleted in Prader-Willi syndrome. Nat Genet. 6:1994;163-167.
75. Sutcliffe J.S., Han M., Christian S.L., Ledbetter D.H. Neuronally-expressed mecdin gene. an imprinted candidate gene in Prader-Willi syndrome Lancet. 350:1997;1520-1521.
76. Ogawa O., Eccles M.R., Szeto J., McNoe L.A., Yun K., Maw M.A., Smith P.J., Reeve A.E. Relaxation of insulin-like growth factor II gene imprinting implicated in Wilm's tumor. Nature. 362:1993;749-751.
77. Steenman M.J., Rainier S., Dorby C.J., Grundy P., Horon I.L., Feinberg A.P. Loss of imprinting of IGF2 is linked to reduced expression and abnormal methylation of H19 in Wilm's tumor. Nat Genet. 7:1994;433-439.
78. Squire J., Weksberg R. Genomic imprinting in tumors. Semin Cancer Biol. 7:1996;41-47.
79. Feinberg A.P. Multiple genetic abnormalities of 11p15 in Wilm's tumor. Med Pediat Oncol. 27:1996;484-489.
80. Li M., Squire J.A., Weksberg R. Molecular genetics of Beckwith-Wiedemann syndrome. Curr Opin Pediat. 9:1997;623-629.
81. Reeve A.E., Housiaux P.J., Gardner R.J., Chewings W.E., Grindley R.M., Millow L.J. Loss of a Harvey ras allele in sporadic Wilms' tumor. Nature. 309:1984;174-176.
82. Weksberg R., Teshima I., Williams B.R., Greenberg C.R., Pueschel S.M., Chernos J.E., Fowlow S.B., Hoyme E., Anderson I.J., Whiteman D.A. Molecular characterization of cytogenetic alterations associated with the Beckwith-Wiedemann syndrome (BWS) phenotype refines the localization and suggests the gene for BWS is imprinted. Hum Mol Genet. 2:1993;549-556.
83. Hoovers J.M., Kalikin L.M., Johnson L.A., Alders M., Redeker B., Law D.J., Bliek J., Steenman M., Benedict M., Wiegant J. Multiple genetic loci within 11p15 defined by Beckwith-Wiedemann syndrome rearrangement breakpoints and subchromosomal transferable fragments. Proc Natl Acad Sci USA. 92:1995;12456-12460.
84. KIP on chromosome 11p15. Proc Natl Acad Sci USA. 93:1996;3026-3030.
85. KIP2 is mutated in Beckwith-Wiedemann syndrome. Nat Genet. 14:1996;171-173.
86. Kornfeld S. Structure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu Rev Biochem. 61:1992;307-330.
87. De Souza A.T., Hankins G.R., Washington M.K., Fine R.L., Orton T.C., Jirtle R.L. Frequent loss of heterozygosity on 6q at the mannose 6-phosphate/insulin-like growth factor II receptor locus in human hepatocellular tumors. Oncogene. 10:1995;1725-1729.
88. De Souza A.T., Hankins G.R., Washington M.K., Orton T.C., Jirtle R.L. M6P/IGF2R gene is mutated in human hepatocellular carcinomas with loss of heterozygosity. Nat Genet. 11:1995;447-449.
89. Hankins G.R., De Souza A.T., Bentley R.C., Patel M.R., Marks J.R., Iglehart J.D., Jirtle R.L. M6P/IGF2 receptor. a candidate breast tumor suppressor gene Oncogene. 12:1996;2003-2009.
90. Yamada T., De Souza A.T., Finkelstein S., Jirtle R.L. Loss of the gene encoding mannose 6-phosphate/insulin-like growth factor II receptor is an early event in liver carcinogenesis. Proc Natl Acad Sci USA. 94:1997;10351-10355.
91. Xu Y.Q., Grundy P., Polychronakos C. Aberrant imprinting of the insulin-like growth factor II receptor gene in Wilms' tumor. Oncogene. 14:1997;1041-1046.
92. Smrzka O.W., Fae I., Stöger R., Kruzbauer R., Fischer G.F., Henn T., Weith A., Barlow D.P. Conservation of a maternal-specific methylation signal at the human Igf2R locus. Hum Mol Genet. 4:1995;1945-1952.
93. Wutz A., Smrzka O.W., Schweifer N., Schellander K., Wagner E.F., Barlow D.P. Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature. 389:1997;745-749.
94. Birger Y., Shemer R., Perk J., Razin A. The imprinting box of the mouse Igf2r gene. Nature. 397:1999;84-88.
95. Feinberg A.P. Cancer epigenetics takes center stage. Proc Natl Acad Sci USA. 98:2001;392-394.
96. Cui H., Horon I.L., Ohlsson R., Hamilton S.R., Feinberg A.P. Loss of imprinting in normal tissue of colorectal cancer patients with microsatellite instability. Nat Med. 4:1998;1276-1280.
97. Nakagawa H., Chadwick R.B., Peltomäki P., Plass C., Nakamura Y., de la Chapelle A. Loss of imprinting of the insulin-like growth factor II gene occurs by allelic methylation in a core region of H19-associated CTCF-binding sites in colorectal cancer. Proc Natl Acad Sci USA. 98:2001;591-596.
98. Cui H., Niemitz E.L., Ravenel J.D., Onyango P., Brandenburg S.A., Lobanenkov V.V., Feinberg A.P. Loss of imprinting of insulin-like growth factor-II in Wilms' tumor commonly involves altered methylation but not mutations of CTCF or its binding sites. Cancer Res. 61:2001;4947-4950.
99. Filippova G.N., Thienes C.P., Penn B.H., Cho D.H., Hu Y.J., Moore J.M., Klesert T.R., Lobanenkov V.V., Tapscott S.J. CTCF-binding sites flank CTG/CAG repeats and form a methylation-sensitive insulator at the DM1 locus. Nat Genet. 28:2001;335-343.
100. Ohlsson R., Renkawitz R., Lobanenkov V. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet. 17:2001;520-527.
101. Joyce J.A., Lam W.K., Catchpoole D.J., Jenks P., Reik W., Maher E.R., Schofield P.N. Imprinting of IGF2 and H19. lack of reciprocity in sporadic Beckwith-Wiedemann syndrome Hum Mol Genet. 6:1997;1543-1548.
102. Vassetzky Y.S., Hair A., Razin S.V. Rearrangement of chromatin domains in cancer and development. J Cell Biochem Suppl. 35:2000;54-60.