Methylation profiling in individuals with uniparental disomy identifies novel differentially methylated regions on chromosome 15

Genome Research

Volumn 20, Issue 9, 2010, Pages 1271-1278

  Sharp, Andrew J ^a,h   Migliavacca, Eugenia ^a,b   Dupre, Yann ^a   Stathaki, Elisavet ^a   Sailani, Mohammad Reza ^a   Baumer, Alessandra ^c   Schinzel, Albert ^c   Mackay, Deborah J ^d,e   Robinson, David O ^d,e   Cobellis, Gilda ^f   Cobellis, Luigi ^f   Brunner, Han G ^g   Steiner, Bernhard ^c   Antonarakis, Stylianos E ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d WESSEX REGIONAL GENETICS LABORATORY   (United Kingdom)

^e UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^f SECOND UNIVERSITY OF NAPLES   (Italy)

^g RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^h MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHROMOSOME 15Q; CLINICAL ARTICLE; DNA METHYLATION; GENE FUNCTION; GENE LOCATION; GENOME IMPRINTING; HUMAN; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRADER WILLI SYNDROME; PRIORITY JOURNAL; UNIPARENTAL DISOMY;

ANGELMAN SYNDROME; CHROMOSOMES, HUMAN, PAIR 15; DNA; DNA METHYLATION; GENE EXPRESSION PROFILING; HUMANS; PRADER-WILLI SYNDROME; PROTEINS; SNRNP CORE PROTEINS; UNIPARENTAL DISOMY;

EID: 77956282732     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.108597.110     Document Type: Article

References (70)

1. Abu-Amero S, Price S, Wakeling E, Stanier P, Trembath R, Preece MA, Moore GE. 1997. Lack of hemizygosity for the insulin-like growth factor I receptor gene in a quantitative study of 33 Silver Russell syndrome probands and their families. Eur J Hum Genet 5: 235-241. (Pubitemid 27453905)
2. Barlow DP, Stöger R, Herrmann BG, Saito K, Schweifer N. 1991. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature 349: 84-87. (Pubitemid 21912022)
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57: 289-300.
4. Bittel DC, Kibiryeva N, Talebizadeh Z, Driscoll DJ, Butler MG. 2005. Microarray analysis of gene/transcript expression in Angelman syndrome: Deletion versus UPD. Genomics 85: 85-91. (Pubitemid 39655693)
5. Bock C, Walter J, Paulsen M, Lengauer T. 2007. CpG island mapping by epigenome prediction. PLoS Comput Biol 3: e110. doi: 10.1371/journal.pcbi. 0030110.
6. Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics 19: 185-193. (Pubitemid 36181903)
7. Buiting K, Saitoh S, Gross S, Dittrich B, Schwartz S, Nicholls RD, Horsthemke B. 1995. Inherited microdeletions in the Angelman and Prader-Willi syndromes define an imprinting centre on human chromosome 15. Nat Genet 9: 395-400.
8. Cheverud JM, Hager R, Roseman C, Fawcett G, Wang B, Wolf JB. 2008. Genomic imprinting effects on adult body composition in mice. Proc Natl Acad Sci 105: 4253-4258. (Pubitemid 351754367)
9. Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, Aerts J, Andrews TD, Barnes C, Campbell P, et al. 2010. Origins and functional impact of copy number variation in the human genome. Nature 464: 704-712.
10. Cook EH Jr, Lindgren V, Leventhal BL, Courchesne R, Lincoln A, Shulman C, Lord C, Courchesne E. 1997. Autism or atypical autismin maternally but not paternally derived proximal 15q duplication. Am J Hum Genet 60: 928-934. (Pubitemid 27146502)
11. Daelemans C, Ritchie ME, Smits G, Abu-Amero S, Sudbery IM, Forrest MS, Campino S, Clark TG, Stanier P, Kwiatkowski D, et al. 2010. High-throughput analysis of candidate imprinted genes and allele-specific gene expression in the human term placenta. BMC Genet 11: 25. doi:10.1186/1471-2156-11-25.
12. Deltour L, Montagutelli X, Guenet JL, Jami J, Páldi A. 1995. Tissue- and developmental stage-specific imprinting of the mouse proinsulin gene, Ins2. Dev Biol 168: 686-688.
13. Dindot SV, Person R, Strivens M, Garcia R, Beaudet AL. 2009. Epigenetic profiling at mouse imprinted gene clusters reveals novel epigenetic and genetic features at differentially methylated regions. Genome Res 19: 1374-1383.
14. Dittrich B, Robinson WP, Knoblauch H, Buiting K, Schmidt K, Gillessen-Kaesbach G, Horsthemke B. 1992. Molecular diagnosis of the Prader- Willi and Angelman syndromes by detection of parent-of-origin specific DNA methylation in 15q11-13. Hum Genet 90: 313-315.
15. Dockery L, Gerfen J, Harview C, Rahn-Lee C, Horton R, Park Y, Davis TL. 2009. Differential methylation persists at the mouse Rasgrf1 DMR in tissues displaying monoallelic and biallelic expression. Epigenetics 4: 241-247.
16. Ferguson-Smith AC, Greally JM. 2007. Epigenetics: Perceptive enzymes. Nature 449: 148-149.
17. Gabriel JM, Higgins MJ, Gebuhr TC, Shows TB, Saitoh S, Nicholls RD. 1998. A model system to study genomic imprinting of human genes. Proc Natl Acad Sci 95: 14857-14862. (Pubitemid 29003721)
18. Gardiner-Garden M, FrommerM. 1987. CpG islands in vertebrate genomes. J Mol Biol 196: 261-282.
19. Gentleman RC, Carey VJ, Bates DM, Bolstad B, DettlingM, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. 2004. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5: R80. doi: 10.1186/gb-2004-5-10-r80.
20. Giannoukakis N, Deal C, Paquette J, Goodyer CG, Polychronakos C. 1993. Parental genomic imprinting of the human IGF2 gene. Nat Genet 4: 98-101. (Pubitemid 23165922)
21. Hayashizaki Y, Shibata H, Hirotsune S, Sugino H, Okazaki Y, Sasaki N, Hirose K, Imoto H, Okuizumi H, Muramatsu M. 1994. Identification of an imprinted U2af binding protein related sequence on mouse chromosome 11 using the RLGS method. Nat Genet 6: 33-40. (Pubitemid 24191910)
22. Hogart A, Nagarajan RP, Patzel KA, Yasui DH, Lasalle JM. 2007. 15q11-13 GABAA receptor genes are normally biallelically expressed in brain yet are subject to epigenetic dysregulation in autism-spectrum disorders. Hum Mol Genet 16: 691-703. (Pubitemid 46585668)
23. Howard TK, Algar EM, Glatz JA, Reeve AE, Smith PJ. 1993. The insulin-like growth factor 1 receptor gene is normally biallelically expressed in human juvenile tissue and tumours. Hum Mol Genet 2: 2089-2092.
24. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X. 2007. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449: 248-251. (Pubitemid 47402375)
25. Jong MT, Gray TA, Ji Y, Glenn CC, Saitoh S, Driscoll DJ, Nicholls RD. 1999. A novel imprinted gene, encoding a RING zinc-finger protein, and overlapping antisense transcript in the Prader-Willi syndrome critical region. Hum Mol Genet 8: 783-793. (Pubitemid 29189045)
26. Kaneko-Ishino T, Kuroiwa Y, Miyoshi N, Kohda T, Suzuki R, Yokoyama M, Viville S, Barton SC, Ishino F, Surani MA. 1995. Peg1/Mest imprinted gene on chromosome 6 identified by cDNA subtraction hybridization. Nat Genet 11: 52-59.
27. Kelsey G, Bodle D, Miller HJ, Beechey CV, Coombes C, Peters J, Williamson CM. 1999. Identification of imprinted loci by methylation-sensitive representational difference analysis: Application to mouse distal chromosome 2. Genomics 62: 129-138. (Pubitemid 30053926)
28. Kim J, Kollhoff A, Bergmann A, Stubbs L. 2003. Methylation-sensitive binding of transcription factor YY1 to an insulator sequence within the paternally expressed imprinted gene, Peg3. Hum Mol Genet 12: 233-245. (Pubitemid 36204421)
29. Klinakis A, Szabolcs M, Chen G, Xuan S, Hibshoosh H, Efstratiadis A. 2009. Igf1r as a therapeutic target in a mouse model of basal-like breast cancer. Proc Natl Acad Sci 106: 2359-2364.
30. Kobayashi H, Suda C, Abe T, Kohara Y, Ikemura T, Sasaki H. 2006. Bisulfite sequencing and dinucleotide content analysis of 15 imprinted mouse differentially methylated regions (DMRs): Paternally methylated DMRs contain less CpGs than maternally methylated DMRs. Cytogenet Genome Res 113: 130-137.
31. Kong A, Steinthorsdottir V, Masson G, Thorleifsson G, Sulem P, Besenbacher S, Jonasdottir A, Sigurdsson A, Kristinsson KT, Jonasdottir A, et al. 2009. Parental origin of sequence variants associated with complex diseases. Nature 462: 868-874.
32. Kosaki K, Kosaki R, Craigen WJ, Matsuo N. 2000. Isoform-specific imprinting of the human PEG1/MEST gene. Am J Hum Genet 66: 309-312. (Pubitemid 30481491)
33. Kotzot D, Utermann G. 2005. Uniparental disomy (UPD) other than 15: Phenotypes and bibliography updated. Am J Med Genet A 136: 287-305. (Pubitemid 40973797)
34. Lau JC, Hanel ML, Wevrick R. 2004. Tissue-specific and imprinted epigenetic modifications of the human NDN gene. Nucleic Acids Res 32: 3376-3382. (Pubitemid 39117453)
35. Luedi PP, Dietrich FS, Weidman JR, Bosko JM, Jirtle RL, Hartemink AJ. 2007. Computational and experimental identification of novel human imprinted genes. Genome Res 17: 1723-1730.
36. Ma DQ, Whitehead PL, Menold MM, Martin ER, Ashley-Koch AE, Mei H, Ritchie MD, Delong GR, Abramson RK, Wright HH, et al. 2005. Identification of significant association and gene-gene interaction of GABA receptor subunit genes in autism. Am J Hum Genet 77: 377-388. (Pubitemid 41192645)
37. Meguro M, Mitsuya K, Sui H, Shigenami K, Kugoh H, Nakao M, Oshimura M. 1997. Evidence for uniparental, paternal expression of the human GABAA receptor subunit genes, using microcell-mediated chromosome transfer. Hum Mol Genet 6: 2127-2133. (Pubitemid 27477955)
38. Monk D, Arnaud P, Apostolidou S, Hills FA, Kelsey G, Stanier P, Feil R, Moore GE. 2006. Limited evolutionary conservation of imprinting in the human placenta. Proc Natl Acad Sci 103: 6623-6628.
39. Neuhausen SL, Brummel S, Ding YC, Singer CF, Pfeiler G, Lynch HT, Nathanson KL, Rebbeck TR, Garber JE, Couch F, et al. 2009. Genetic variation in insulin-like growth factor signaling genes and breast cancer risk among BRCA1 and BRCA2 carriers. Breast Cancer Res 11: R76. doi:10.1188/bcr2414.
40. Nicholls RD, Knoll JH, Butler MG, Karam S, Lalande M. 1989. Genetic imprinting suggested bymaternal heterodisomy in nondeletion Prader- Willi syndrome. Nature 342: 281-285. (Pubitemid 19283323)
41. Ogawa O, McNoe LA, Eccles MR, Morison IM, Reeve AE. 1993. Human insulin-like growth factor type I and type II receptors are not imprinted. Hum Mol Genet 2: 2163-2165. (Pubitemid 24003417)
42. Ohta T, Buiting K, Kokkonen H, McCandless S, Heeger S, Leisti H, Driscoll DJ, Cassidy SB, Horsthemke B, Nicholls RD. 1999. Molecular mechanism of angelman syndrome in two large families involves an imprinting mutation. Am J Hum Genet 64: 385-396. (Pubitemid 129500522)
43. 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. (Pubitemid 29519904)
44. Pelizzola M, Koga Y, Urban AE, Krauthammer M, Weissman S, Halaban R, Molinaro AM. 2008. MEDME: An experimental and analytical methodology for the estimation of DNA methylation levels based on microarray derived MeDIP-enrichment. Genome Res 18: 1652-1659.
45. Prendergast GC, Lawe D, Ziff EB. 1991. Association of Myn, the murine homolog of Max, with c-Myc stimulates methylation-sensitive DNA binding and ras cotransformation. Cell 65: 395-407. (Pubitemid 121002049)
46. Reik W, Walter J. 2001. Genomic imprinting: Parental influence on the genome. Nat Rev Genet 2: 21-32. (Pubitemid 33674766)
47. Reinhart B, Eljanne M, Chaillet JR. 2002. Shared role for differentially methylated domains of imprinted genes. Mol Cell Biol 22: 2089-2098. (Pubitemid 34224617)
48. Reinhart B, Paoloni-Giacobino A, Chaillet JR. 2006. Specific differentially methylated domain sequences direct the maintenance of methylation at imprinted genes. Mol Cell Biol 26: 8347-8356. (Pubitemid 44748569)
49. Rougeulle C, Glatt H, Lalande M. 1997. The Angelman syndrome candidate gene, UBE3A/E6-AP, is imprinted in brain. Nat Genet 17: 14-15.
50. Sachdev D, Zhang X, Matise I, Gaillard-Kelly M, Yee D. 2009. The type I insulin-like growth factor receptor regulates cancer metastasis independently of primary tumor growth by promoting invasion and survival. Oncogene 29: 251-262.
51. Schroer RJ, Phelan MC, Michaelis RC, Crawford EC, Skinner SA, Cuccaro M, Simensen RJ, Bishop J, Skinner C, Fender D, et al. 1998. Autism and maternally derived aberrations of chromosome 15q. Am J Med Genet 76: 327-336. (Pubitemid 28136106)
52. Sharp AJ, Locke DP, McGrath SD, Cheng Z, Bailey JA, Samonte RV, Pertz LM, Clark RA, Schwartz S, Segraves R, et al. 2005. Segmental duplications and copy number variation in the human genome. Am J Hum Genet 77: 78-88. (Pubitemid 40848038)
53. Sharp AJ, Itsara A, Cheng Z, Alkan C, Schwartz S, Eichler EE. 2007. Optimal design of oligonucleotide microarrays for measurement of DNA copy number. Hum Mol Genet 16: 2770-2779. (Pubitemid 350018519)
54. Smith RJ, Dean W, Konfortova G, Kelsey G. 2003. Identification of novel imprinted genes in a genome-wide screen for maternal methylation. Genome Res 13: 558-569. (Pubitemid 36511915)
55. Smyth GK. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: doi: 10.2202/1544-6115.1027.
56. Smyth GK, Michaud J, Scott HS. 2005. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075. (Pubitemid 40668046)
57. Solomon DL, Amati B, Land H. 1993. Distinct DNA binding preferences for the c-Myc/Max and Max/Max dimers. Nucleic Acids Res 21: 5372-5376. (Pubitemid 23348600)
58. Suh Y, Atzmon G, Cho MO, Hwang D, Liu B, Leahy DJ, Barzilai N, Cohen P. 2008. Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc Natl Acad Sci 105: 3438-3442. (Pubitemid 351723571)
59. Sutcliffe JS, NakaoM, Christian S, Orstavik KH, Tommerup N, Ledbetter DH, Beaudet AL. 1994. Deletions of a differentially methylated CpG island at the SNRPN gene define a putative imprinting control region. Nat Genet 8: 52-58. (Pubitemid 24274060)
60. Tatton-Brown K, Pilz DT, Orstavik KH, Patton M, Barber JC, Collinson MN, Maloney VK, Huang S, Crolla JA, Marks K, et al. 2009. 15q overgrowth syndrome: A newly recognized phenotype associated with overgrowth, learning difficulties, characteristic facial appearance, renal anomalies and increased dosage of distal chromosome 15q. Am J Med Genet A 149A: 147-154.
61. Vega VB, Cheung E, Palanisamy N, Sung WK. 2009. Inherent signals in sequencing-based Chromatin-ImmunoPrecipitation control libraries. PLoS ONE 4: e5241. doi: 10.1371/journal.pone.0005241.
62. Walenkamp MJ, van der Kamp HJ, Pereira AM, Kant SG, van Duyvenvoorde HA, Kruithof MF, Breuning MH, Romijn JA, Karperien M, Wit JM. 2006. A variable degree of intrauterine and postnatal growth retardation in a family with a missense mutation in the insulin-like growth factor I receptor. J Clin Endocrinol Metab 91: 3062-3070. (Pubitemid 44271756)
63. Wang X, Sun Q, McGrath SD, Mardis ER, Soloway PD, Clark AG. 2008. Transcriptome-wide identification of novel imprinted genes in neonatal mouse brain. PLoS ONE 3: e3839. doi: 10.1371/journal.pone.0003839.
64. Webb T, Maina EN, Soni S, Whittington J, Boer H, Clarke D, Holland A. 2008. In search of the psychosis gene in people with Prader-Willi syndrome. Am J Med Genet A 146: 843-853.
65. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schübeler D. 2005. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 37: 853-862. (Pubitemid 41077111)
66. Wen B, Wu H, Bjornsson H, Green RD, Irizarry R, Feinberg AP. 2008. Overlapping euchromatin/heterochromatin-associated marks are enriched in imprinted gene regions and predict allele-specific modification. Genome Res 18: 1806-1813.
67. Williamson CM, Blake A, Thomas S, Beechey CV, Hancock J, Cattanach BM, Peters J. 2009. World Wide Web site - mouse imprinting data and references. MRC Harwell, Oxfordshire, UK.
68. Wood AJ, Schulz R, Woodfine K, Koltowska K, Beechey CV, Peters J, Bourc'his D, Oakey RJ. 2008. Regulation of alternative polyadenylation by genomic imprinting. Genes Dev 22: 1141-1146.
69. Yoon BJ, Herman H, Sikora A, Smith LT, Plass C, Soloway PD. 2002. Regulation of DNA methylation of Rasgrf1. Nat Genet 30: 92-96.
70. Zhou H, Brockington M, Jungbluth H, Monk D, Stanier P, Sewry CA, Moore GE, Muntoni F. 2006. Epigenetic allele silencing unveils recessive RYR1 mutations in core myopathies. Am J Hum Genet 79: 859-868. (Pubitemid 44763400)