Altered intra-nuclear organisation of heterochromatin and genes in ICF syndrome

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Jefferson, Andrew ^a,c   Colella, Stefano ^a,d   Moralli, Daniela ^a   Wilson, Natalie ^a   Yusuf, Mohammed ^a   Gimelli, Giorgio ^b   Ragoussis, Jiannis ^a   Volpi, Emanuela V ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b G GASLINI INSTITUTE   (Italy)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CELL TRANSLOCATION GENE 2 PROTEIN; BLOOD CLOTTING FACTOR 13; BLOOD CLOTTING FACTOR 13 A1; CALPONIN; CALPONIN 3; CARRIER PROTEIN; INHIBITOR OF DIFFERENTIATION 3; RGS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CELL NUCLEUS; CHROMOSOME 1; CHROMOSOME 16; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DISEASE CLASSIFICATION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE LOCATION; GENE SEQUENCE; GENETIC ORGANIZATION; HETEROCHROMATIN; HUMAN; HUMAN CELL; IMMUNODEFICIENCY CENTROMERIC REGION INSTABILITY AND FACIAL ANOMALY SYNDROME; INTERPHASE; METAPHASE;

ABNORMALITIES, MULTIPLE; CELL NUCLEUS; CHROMOSOMES, HUMAN, PAIR 1; DNA METHYLATION; HETEROCHROMATIN; HUMANS; SYNDROME;

EID: 77955331986     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011364     Document Type: Article

References (65)

1. Tiepolo L, Maraschio P, Gimelli G, Cuoco C, Gargani GF, et al. (1979) Multibranched chromosomes 1, 9, and 16 in a patient with combined IgA and IgE deficiency. Hum Genet 51: 127-137.
2. Ehrlich M (2003) The ICF syndrome, a DNA methyltransferase 3B deficiency and immunodeficiency disease. Clin Immunol 109: 17-28.
3. Schuffenhauer S, Bartsch O, Stumm M, Buchholz T, Petropoulou T, et al. (1995) DNA, FISH and complementation studies in ICF syndrome: DNA hypomethylation of repetitive and single copy loci and evidence for a trans acting factor. Hum Genet 96: 562-571.
4. Sumner AT, Mitchell AR, Ellis PM (1998) A FISH study of chromosome fusion in the ICF syndrome: involvement of paracentric heterochromatin but not of the centromeres themselves. J Med Genet 35: 833-835.
5. Stacey M, Bennett MS, Hulten M (1995) FISH analysis on spontaneously arising micronuclei in the ICF syndrome. J Med Genet 32: 502-508.
6. Tuck-Muller CM, Narayan A, Tsien F, Smeets DF, Sawyer J, et al. (2000) DNA hypomethylation and unusual chromosome instability in cell lines from ICF syndrome patients. Cytogenet Cell Genet 89: 121-128.
7. Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, et al. (1999) Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402: 187-191.
8. Hassan KM, Norwood T, Gimelli G, Gartler SM, Hansen RS (2001) Satellite 2 methylation patterns in normal and ICF syndrome cells and association of hypomethylation with advanced replication. Hum Genet 109: 452-462.
9. Jeanpierre M, Turleau C, Aurias A, Prieur M, Ledeist F, et al. (1993) An embryonic-like methylation pattern of classical satellite DNA is observed in ICF syndrome. Hum Mol Genet 2: 731-735.
10. Kondo T, Bobek MP, Kuick R, Lamb B, Zhu X, et al. (2000) Whole-genome methylation scan in ICF syndrome: hypomethylation of non-satellite DNA repeats D4Z4 and NBL2. Hum Mol Genet 9: 597-604.
11. Maraschio P, Zuffardi O, Dalla Fior T, Tiepolo L (1988) Immunodeficiency, centromeric heterochromatin instability of chromosomes 1, 9, and 16, and facial anomalies: the ICF syndrome. J Med Genet 25: 173-180.
12. Tao Q, Huang H, Geiman TM, Lim CY, Fu L, et al. (2002) Defective de novo methylation of viral and cellular DNA sequences in ICF syndrome cells. Hum Mol Genet 11: 2091-2102.
13. Hansen RS, Stoger R, Wijmenga C, Stanek AM, Canfield TK, et al. (2000) Escape from gene silencing in ICF syndrome: evidence for advanced replication time as a major determinant. Hum Mol Genet 9: 2575-2587.
14. Jin B, Tao Q, Peng J, Soo HM, Wu W, et al. (2008) DNA methyltransferase 3B (DNMT3B) mutations in ICF syndrome lead to altered epigenetic modifications and aberrant expression of genes regulating development, neurogenesis and immune function. Hum Mol Genet 17: 690-709.
15. Wijmenga C, van den Heuvel LP, Strengman E, Luyten JA, van der Burgt IJ, et al. (1998) Localization of the ICF syndrome to chromosome 20 by homozygosity mapping. Am J Hum Genet 63: 803-809.
16. Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257.
17. Wijmenga C, Hansen RS, Gimelli G, Bjorck EJ, Davies EG, et al. (2000) Genetic variation in ICF syndrome: evidence for genetic heterogeneity. Hum Mutat 16: 509-517.
18. Ueda Y, Okano M, Williams C, Chen T, Georgopoulos K, et al. (2006) Roles for Dnmt3b in mammalian development: a mouse model for the ICF syndrome. Development 133: 1183-1192.
19. Jiang YL, Rigolet M, Bourc'his D, Nigon F, Bokesoy I, et al. (2005) DNMT3B mutations and DNA methylation defect define two types of ICF syndrome. Hum Mutat 25: 56-63.
20. Kubota T, Furuumi H, Kamoda T, Iwasaki N, Tobita N, et al. (2004) ICF syndrome in a girl with DNA hypomethylation but without detectable DNMT3B mutation. Am J Med Genet A 129: 290-293.
21. Ehrlich M, Buchanan KL, Tsien F, Jiang G, Sun B, et al. (2001) DNA methyltransferase 3B mutations linked to the ICF syndrome cause dysregulation of lymphogenesis genes. Hum Mol Genet 10: 2917-2931.
22. Bickmore WA, van der Maarel SM (2003) Perturbations of chromatin structure in human genetic disease: recent advances. Hum Mol Genet 12 Spec No 2: R207-213.
23. O'Keefe RT, Henderson SC, Spector DL (1992) Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences. J Cell Biol 116: 1095-1110.
24. Hernandez R, Frady A, Zhang XY, Varela M, Ehrlich M (1997) Preferential induction of chromosome 1 multibranched figures and whole-arm deletions in a human pro-B cell line treated with 5-azacytidine or 5-azadeoxycytidine. Cytogenet Cell Genet 76: 196-201.
25. Ji W, Hernandez R, Zhang XY, Qu GZ, Frady A, et al. (1997) DNA demethylation and pericentromeric rearrangements of chromosome 1. Mutat Res 379: 33-41.
26. Kokalj-Vokac N, Almeida A, Viegas-Pequignot E, Jeanpierre M, Malfoy B, et al. (1993) Specific induction of uncoiling and recombination by azacytidine in classical satellite-containing constitutive heterochromatin. Cytogenet Cell Genet 63: 11-15.
27. Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, et al. (2005) Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci U S A 102: 15785-15790.
28. Blanco-Betancourt CE, Moncla A, Milili M, Jiang YL, Viegas-Pequignot EM, et al. (2004) Defective B-cell-negative selection and terminal differentiation in the ICF syndrome. Blood 103: 2683-2690.
29. Gisselsson D, Shao C, Tuck-Muller CM, Sogorovic S, Palsson E, et al. (2005) Interphase chromosomal abnormalities and mitotic missegregation of hypomethylated sequences in ICF syndrome cells. Chromosoma 114: 118-126.
30. Luciani JJ, Depetris D, Missirian C, Mignon-Ravix C, Metzler-Guillemain C, et al. (2005) Subcellular distribution of HP1 proteins is altered in ICF syndrome. Eur J Hum Genet 13: 41-51.
31. Luciani JJ, Depetris D, Usson Y, Metzler-Guillemain C, Mignon-Ravix C, et al. (2006) PML nuclear bodies are highly organised DNA-protein structures with a function in heterochromatin remodelling at the G2 phase. J Cell Sci 119: 2518-2531.
32. Maraschio P, Cortinovis M, Dainotti E, Tupler R, Tiepolo L (1992) Interphase cytogenetics of the ICF syndrome. Ann Hum Genet 56: 273-278.
33. Matarazzo MR, Boyle S, D'Esposito M, Bickmore WA (2007) Chromosome territory reorganization in a human disease with altered DNA methylation. Proc Natl Acad Sci U S A 104: 16546-16551.
34. Miniou P, Jeanpierre M, Blanquet V, Sibella V, Bonneau D, et al. (1994) Abnormal methylation pattern in constitutive and facultative (X inactive chromosome) heterochromatin of ICF patients. Hum Mol Genet 3: 2093-2102.
35. Sawyer JR, Swanson CM, Wheeler G, Cunniff C (1995) Chromosome instability in ICF syndrome: formation of micronuclei from multibranched chromosomes 1 demonstrated by fluorescence in situ hybridization. Am J Med Genet 56: 203-209.
36. Grewal SI, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8: 35-46.
37. Richards EJ, Elgin SC (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108: 489-500.
38. Gilbert N, Thomson I, Boyle S, Allan J, Ramsahoye B, et al. (2007) DNA methylation affects nuclear organization, histone modifications, and linker histone binding but not chromatin compaction. J Cell Biol 177: 401-411.
39. Hepperger C, Otten S, von Hase J, Dietzel S (2007) Preservation of large-scale chromatin structure in FISH experiments. Chromosoma 116: 117-133.
40. Jaco I, Canela A, Vera E, Blasco MA (2008) Centromere mitotic recombination in mammalian cells. J Cell Biol 181: 885-892.
41. Cockell M, Gasser SM (1999) Nuclear compartments and gene regulation. Curr Opin Genet Dev 9: 199-205.
42. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, et al. (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145: 1119-1131.
43. Shopland LS, Lynch CR, Peterson KA, Thornton K, Kepper N, et al. (2006) Folding and organization of a contiguous chromosome region according to the gene distribution pattern in primary genomic sequence. J Cell Biol 174: 27-38.
44. Tanabe H, Muller S, Neusser M, von Hase J, Calcagno E, et al. (2002) Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates. Proc Natl Acad Sci U S A 99: 4424-4429.
45. Scheuermann MO, Tajbakhsh J, Kurz A, Saracoglu K, Eils R, et al. (2004) Topology of genes and nontranscribed sequences in human interphase nuclei. Exp Cell Res 301: 266-279.
46. Dietzel S, Zolghadr K, Hepperger C, Belmont AS (2004) Differential large-scale chromatin compaction and intranuclear positioning of transcribed versus non-transcribed transgene arrays containing beta-globin regulatory sequences. J Cell Sci 117: 4603-4614.
47. Hewitt SL, High FA, Reiner SL, Fisher AG, Merkenschlager M (2004) Nuclear repositioning marks the selective exclusion of lineage-inappropriate transcription factor loci during T helper cell differentiation. Eur J Immunol 34: 3604-3613.
48. Kosak ST, Skok JA, Medina KL, Riblet R, Le Beau MM, et al. (2002) Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296: 158-162.
49. Williams RR, Azuara V, Perry P, Sauer S, Dvorkina M, et al. (2006) Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J Cell Sci 119: 132-140.
50. Ferreira J, Paolella G, Ramos C, Lamond AI (1997) Spatial organization of large-scale chromatin domains in the nucleus: a magnified view of single chromosome territories. J Cell Biol 139: 1597-1610.
51. Sadoni N, Langer S, Fauth C, Bernardi G, Cremer T, et al. (1999) Nuclear organization of mammalian genomes. Polar chromosome territories build up functionally distinct higher order compartments. J Cell Biol 146: 1211-1226.
52. Barki-Celli L, Lefebvre C, Le Baccon P, Nadeau G, Bonnefoix T, et al. (2005) Differences in nuclear positioning of 1q12 pericentric heterochromatin in normal and tumor B lymphocytes with 1q rearrangements. Genes Chromosomes Cancer 43: 339-349.
53. Saurin AJ, Shiels C, Williamson J, Satijn DP, Otte AP, et al. (1998) The human polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J Cell Biol 142: 887-898.
54. Heidari M, Rice KL, Phillips JK, Kees UR, Greene WK (2006) The nuclear oncoprotein TLX1/HOX11 associates with pericentromeric satellite 2 DNA in leukemic T-cells. Leukemia 20: 304-312.
55. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG (1999) Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3: 207-217.
56. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, et al. (1997) Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91: 845-854.
57. Grogan JL, Mohrs M, Harmon B, Lacy DA, Sedat JW, et al. (2001) Early transcription and silencing of cytokine genes underlie polarization of T helper cell subsets. Immunity 14: 205-215.
58. Francastel C, Magis W, Groudine M (2001) Nuclear relocation of a transactivator subunit precedes target gene activation. Proc Natl Acad Sci U S A 98: 12120-12125.
59. Francastel C, Walters MC, Groudine M, Martin DI (1999) A functional enhancer suppresses silencing of a transgene and prevents its localization close to centrometric heterochromatin. Cell 99: 259-269.
60. Schubeler D, Francastel C, Cimbora DM, Reik A, Martin DI, et al. (2000) Nuclear localization and histone acetylation: a pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Genes Dev 14: 940-950.
61. Bartova E, Kozubek S, Jirsova P, Kozubek M, Gajova H, et al. (2002) Nuclear structure and gene activity in human differentiated cells. J Struct Biol 139: 76-89.
62. Roldan E, Fuxa M, Chong W, Martinez D, Novatchkova M, et al. (2005) Locus 'decontraction' and centromeric recruitment contribute to allelic exclusion of the immunoglobulin heavy-chain gene. Nat Immunol 6: 31-41.
63. Pezzolo A, Prigione I, Chiesa S, Castellano E, Gimelli G, et al. (2002) A novel case of immunodeficiency, centromeric instability, and facial anomalies (the ICF syndrome): immunologic and cytogenetic studies. Haematologica 87: 329-331.
64. Enukashvily NI, Donev R, Waisertreiger IS, Podgornaya OI (2007) Human chromosome 1 satellite 3 DNA is decondensed, demethylated and transcribed in senescent cells and in A431 epithelial carcinoma cells. Cytogenet Genome Res 118: 42-54.
65. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.