The PEG13-DMR and brain-specific enhancers dictate imprinted expression within the 8q24 intellectual disability risk locus

Epigenetics and Chromatin

Volumn 7, Issue 1, 2014, Pages

  Court, Franck ^a   Camprubi, Cristina ^a,g   Garcia, Cristina Vicente ^b,c   Guillaumet Adkins, Amy ^a   Sparago, Angela ^d   Seruggia, Davide ^b,c   Sandoval, Juan ^a   Esteller, Manel ^a,e,f   Martin Trujillo, Alex ^a   Riccio, Andrea ^d   Montoliu, Lluis ^b,c   Monk, David ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^e UNIVERSITY OF BARCELONA   (Spain)

^f INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^g Sistemas Genomicos SL   (Spain)

Author keywords

Chromatin looping; DNA methylation; Imprinting

Indexed keywords

COHESIN; HISTONE H3; PEPTIDES AND PROTEINS; PROTEIN KCNK9; PROTEIN PEG13; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ADULT; ALLELE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME 8Q; CONTROLLED STUDY; CPG ISLAND; DNA CONFORMATION; DNA METHYLATED REGION; DNA METHYLATION; ENHANCER REGION; EXPRESSED SEQUENCE TAG; FRONTAL CORTEX; GENE EXPRESSION; GENE LOCUS; GENE MAPPING; GENETIC TRANSCRIPTION; GENOME IMPRINTING; HISTONE MODIFICATION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; INTELLECTUAL IMPAIRMENT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TANDEM REPEAT;

EID: 84899104949     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-7-5     Document Type: Article

References (39)

1. Mechanisms of long range silencing by imprinted macro non-coding RNAs. Pauler FM, Barlow DP, Hudson QJ, Curr Opin Genet Dev 2012 22 283 289 10.1016/j.gde.2012.02.005 22386265
2. Dnmt3L and the establishment of maternal genomic imprints. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH, Science 2003 21 2536 2539
3. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Hata K, Okano M, Lei H, Li E, Development 2003 129 1983 1993
4. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, Tajima S, Mitsuya K, Okano M, Koseki H, Nature 2007 450 908 912 10.1038/nature06397 17994007
5. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Segonds-Pichon A, Sato S, Hata K, Andrews SR, Kelsey G, Nat Genet 2011 43 811 814 10.1038/ng.864 21706000
6. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C, Mol Cell 2008 2008 32 232 246
7. The Airn noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, Fraser P, Science 2008 322 1717 1720 10.1126/science.1163802 18988810
8. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. Nativio R, Wendt KS, Ito Y, Huddleston JE, Uribe-Lewis S, Woodfine K, Krueger C, Reik W, Peters JM, Murrell A, PLoS Genet 2009 5 1000739 10.1371/journal.pgen.1000739 19956766
9. Epigenetics of autism spectrum disorders. Schanen NC, Hum Mol Genet 2006 15 Spec No 2 138 R150 16987877
10. Prader-Willi syndrome and Angelman syndrome. Buiting K, Am J Med Genet C: Semin Med Genet 2010 154C 365 376 10.1002/ajmg.c.30273 20803659
11. Maternally inherited Birk-Barel mental retardation dysmorphism syndrome caused by a mutation in the genomically imprinted potassium channel KCNK9. Barel O, Shalev SA, Ofir R, Cohen A, Zlotogora J, Shorer Z, Mazor G, Finer G, Khateeb S, Zilberberg N, Birk OS, Am J Hum Genet 2008 83 193 199 10.1016/j.ajhg.2008. 07.010 18678320
12. A truncating mutation of TRAPPC9 is associated with autosomal-recessive intellectual disability and postnatal microcephaly. Mochida GH, Mahajnah M, Hill AD, Basel-Vanagaite L, Gleason D, Hill RS, Bodell A, Crosier M, Straussberg R, Walsh CA, Am J Hum Genet 2009 85 897 902 10.1016/j.ajhg.2009.10.027 20004763
13. Identification of mutations in TRAPPC9, which encodes the NIK- and IKK-beta-binding protein, in nonsyndromic autosomal-recessive mental retardation. Mir A, Kaufman L, Noor A, Motazacker MM, Jamil T, Azam M, Kahrizi K, Rafiq MA, Weksberg R, Nasr T, Naeem F, Tzschach A, Kuss AW, Ishak GE, Doherty D, Ropers HH, Barkovich AJ, Najmabadi H, Ayub M, Vincent JB, Am J Hum Genet 2009 85 909 915 10.1016/j.ajhg.2009.11.009 20004765
14. A homozygous splice site mutation in TRAPPC9 causes intellectual disability and microcephaly. Kakar N, Goebel I, Daud S, Nürnberg G, Agha N, Ahmad A, Nürnberg P, Kubisch C, Ahmad J, Borck G, Eur J Med Genet 2012 55 727 731 10.1016/j.ejmg.2012.08.010 22989526
15. TRAPPC9-related autosomal recessive intellectual disability: report of a new mutation and clinical phenotype. Marangi G, Leuzzi V, Manti F, Lattante S, Orteschi D, Pecile V, Neri G, Zollino M, Eur J Hum Genet 2013 21 229 232 10.1038/ejhg.2012.79 22549410
16. Sequence-based bioinformatic prediction and QUASEP identify genomic imprinting of the KCNK9 potassium channel gene in mouse and human. Ruf N, Bahring S, Galetzka D, Pliushch G, Luft FC, Nürnberg P, Haaf T, Kelsey G, Zechner U, Hum Mol Genet 2007 16 2591 2599 10.1093/hmg/ddm216 17704508
17. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Gregg C, Zhang J, Weissbourd B, Luo S, Schroth GP, Haig D, Dulac C, Science 2010 329 643 648 10.1126/science.1190830 20616232
18. Chromosome-wide analysis of parental allele-specific chromatin and DNA methylation. Singh P, Wu X, Lee DH, Li AX, Rauch TA, Pfeifer GP, Mann JR, Szabó PE, Mol Cell Biol 2011 31 1757 1770 10.1128/MCB.00961-10 21321082
19. Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Xie W, Barr CL, Kim A, Yue F, Lee AY, Eubanks J, Dempster EL, Ren B, Cell 2012 148 816 831 10.1016/j.cell.2011.12.035 22341451
20. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM, Nature 2000 405 486 489 10.1038/35013106 10839547
21. High-resolution profiling of histone methylations in the human genome. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K, Cell 2007 129 823 837 10.1016/j.cell.2007.05.009 17512414
22. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, MacIsaac KD, Rolfe PA, Conboy CM, Gifford DK, Fraenkel E, Nat Genet 2007 39 730 732 10.1038/ng2047 17529977
23. Imprinting at the PLAGL1 domain is contained within a 70-kb CTCF/cohesin-mediated non-allelic chromatin loop. Iglesias-Platas I, Court F, Camprubi C, Sparago A, Guillaumet-Adkins A, Martin-Trujillo A, Riccio A, Moore GE, Monk D, Nucleic Acids Res 2013 41 2171 2179 10.1093/nar/gks1355 23295672
24. Disruption of genomic neighbourhood at the imprinted IGF2-H19 locus in Beckwith-Wiedemann syndrome and Silver-Russell syndrome. Nativio R, Sparago A, Ito Y, Weksberg R, Riccio A, Murrell A, Hum Mol Genet 2011 20 1363 1374 10.1093/hmg/ddr018 21282187
25. Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Lunyak VV, Prefontaine GG, Núñez E, Cramer T, Ju BG, Ohgi KA, Hutt K, Roy R, García-Díaz A, Zhu X, Yung Y, Montoliu L, Glass CK, Rosenfeld MG, Science 2007 317 248 251 10.1126/science.1140871 17626886
26. Dioxin receptor and SLUG transcription factors regulate the insulator activity of B1 SINE retrotransposons via an RNA polymerase switch. Román AC, González-Rico FJ, Moltó E, Hernando H, Neto A, Vicente-Garcia C, Ballestar E, Gómez-Skarmeta JL, Vavrova-Anderson J, White RJ, Montoliu L, Fernández-Salguero PM, Genome Res 2011 21 422 432 10.1101/gr.111203.110 21324874
27. CTCF: master weaver of the genome. Phillips JE, Corces VG, Cell 2009 137 1194 1211 10.1016/j.cell.2009.06.001 19563753
28. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B, Nature 2009 459 108 112 10.1038/nature07829 19295514
29. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Welstead GG, Creyghton MP, Bilodeau S, Cheng AW, Markoulaki S, Young RA, Jaenisch R, Proc Natl Acad Sci USA 2010 107 21931 21936 10.1073/pnas.1016071107 21106759
30. Genomic occupancy of the transcriptional co-activators p300 and CBP. Holmqvist PH, Mannervik M, Transcription 2013 4 18 23 10.4161/trns.22601 23131664
31. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Kriaucionis S, Heintz N, Science 2009 324 929 930 10.1126/science.1169786 19372393
32. Global epigenomic reconfiguration during mammalian brain development. Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, Lucero J, Huang Y, Dwork AJ, Schultz MD, Yu M, Tonti-Filippini J, Heyn H, Hu S, Wu JC, Rao A, Esteller M, He C, Haghighi FG, Sejnowski TJ, Behrens MM, Ecker JR, Science 2013 341 [Epub]
33. MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Mellén P, Ayata S, Dewell S, Kriaucionis S, Heintz N, Cell 2012 151 1417 1430 10.1016/j.cell.2012.11.022 23260135
34. 5-hmC in the brain is abundant in synaptic genes and shows differences at the exon-intron boundary. Khare T, Pai S, Koncevicius K, Pal M, Kriukiene E, Liutkeviciute Z, Irimia M, Jia P, Ptak C, Xia M, Tice R, Tochigi M, Moréra S, Nazarians A, Belsham D, Wong AH, Blencowe BJ, Wang SC, Kapranov P, Kustra R, Labrie V, Klimasauskas S, Petronis A, Nat Struct Mol Biol 2012 19 1037 1043 10.1038/nsmb.2372 22961382
35. Covalent modification of DNA regulates memory formation. Miller CA, Sweatt JD, Neuron 2007 53 857 69 10.1016/j.neuron.2007.02.022 17359920
36. Neuron-specific impairment of inter-chromosomal pairing and transcription in a novel model of human 15q-duplication syndrome. Meguro-Horike M, Yasui DH, Powell W, Schroeder DI, Oshimura M, Lasalle JM, Horike S, Hum Mol Genet 2011 20 3798 37810 10.1093/hmg/ddr298 21725066
37. 15q11.2-13.3 chromatin analysis reveals epigenetic regulation of CHRNA7 with deficiencies in Rett and autism brain. Yasui DH, Scoles HA, Horike S, Meguro-Horike M, Dunaway KW, Schroeder DI, Dunaway KW, Schroeder DI, Lasalle JM, Hum Mol Genet 2011 20 4311 4323 10.1093/hmg/ddr357 21840925
38. Stability of genomic imprinting and gestational-age dynamic methylation in complicated pregnancies conceived following assisted reproductive technologies. Camprubí C, Iglesias-Platas I, Martin-Trujillo A, Salvador-Alarcon C, Angeles Rodriguez M, Rodriguez Barredo D, Court F, Monk D, Biol Reprod 2013 89 1 9 10.1095/biolreprod.113.110478
39. Genomic matrix attachment region and chromosome conformation capture quantitative real time PCR assays identify novel putative regulatory elements at the imprinted Dlk1/Gtl2 locus. Braem C, Recolin B, Rancourt RC, Angiolini C, Barthès P, Branchu P, Court F, Cathala G, Ferguson-Smith AC, Forné T, J Biol Chem 2008 283 18612 18620 10.1074/jbc.M801883200 18458080