Smchd1 regulates a subset of autosomal genes subject to monoallelic expression in addition to being critical for X inactivation

Epigenetics and Chromatin

Volumn 6, Issue 1, 2013, Pages

  Mould, Arne W ^a,b   Pang, Zhenyi ^a   Pakusch, Miha ^c   Tonks, Ian D ^a   Stark, Mitchell ^a   Carrie, Dianne ^a   Mukhopadhyay, Pamela ^a   Seidel, Annica ^a   Ellis, Jonathan J ^a   Deakin, Janine ^d   Wakefield, Matthew J ^c,e   Krause, Lutz ^a   Blewitt, Marnie E ^c,e   Kay, Graham F ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Clustered protocadherins; Genomic imprinting; Monoallelic expression; Smchd1; X inactivation

Indexed keywords

CADHERIN; CELL PROTEIN; PROTOCADHERIN ALPHA; PROTOCADHERIN BETA; PROTOCADHERIN GAMMA; SMCHD1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOSOMAL DISORDER; BIALLELIC EXPRESSION; CHROMOSOME; CPG ISLAND; EMBRYO DEVELOPMENT; EPIGENETICS; GENE CLUSTER; GENE DISRUPTION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC ANALYSIS; GENOME IMPRINTING; GENOTYPE; HUMAN; MICROARRAY ANALYSIS; MONOALLELIC EXPRESSION; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACENTA; PRIORITY JOURNAL; RNA EXTRACTION; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; X CHROMOSOME INACTIVATION;

MUS;

EID: 84879817115     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-6-19     Document Type: Article

References (91)

1. Gene action in the X-chromosome of the mouse (Mus musculus L.). Lyon M, Nature 1961 190 372 373 10.1038/190372a0 13764598
2. Differential activity of maternally and paternally derived chromosome regions in mice. Cattanach BM, Kirk M, Nature 1985 315 496 498 10.1038/315496a0 4000278
3. Allelic inactivation regulates olfactory receptor gene expression. Chess A, Simon I, Cedar H, Axel R, Cell 1994 78 823 834 10.1016/S0092-8674(94)90562-2 8087849
4. A map of pheromone receptor activation in the mammalian brain. Belluscio L, Koentges G, Axel R, Dulac C, Cell 1999 97 209 220 10.1016/S0092-8674(00) 80731-X 10219242
5. Regulation of IL-4 expression by activation of individual alleles. Riviere I, Sunshine MJ, Littman DR, Immunity 1998 9 217 228 10.1016/S1074- 7613(00)80604-4 9729042
6. The RAG proteins and V(D)J recombination: complexes, ends, and transposition. Fugmann SD, Lee AI, Shockett PE, Villey IJ, Schatz DG, Annu Rev Immunol 2000 18 495 527 10.1146/annurev.immunol.18.1.495 10837067
7. The mechanism and regulation of chromosomal V(D)J recombination. Bassing CH, Swat W, Alt FW, Cell 2002 109 Suppl 45 55 11983152
8. Allelic exclusion of Ly49-family genes encoding class I MHC-specific receptors on NK cells. Held W, Roland J, Raulet DH, Nature 1995 376 355 358 10.1038/376355a0 7630404
9. Monoallelic yet combinatorial expression of variable exons of the protocadherin-α gene cluster in single neurons. Esumi S, Kakazu N, Taguchi Y, Hirayama T, Sasaki A, Hirabayashi T, Koide T, Kitsukawa T, Hamada S, Yagi T, Nat Genet 2005 37 171 176 10.1038/ng1500 15640798
10. Allelic gene regulation of Pcdh-α and Pcdh-γ clusters involving both monoallelic and biallelic expression in single Purkinje cells. Kaneko R, Kato H, Kawamura Y, Esumi S, Hirayama T, Hirabayashi T, Yagi T, J Biol Chem 2006 281 30551 30560 10.1074/jbc.M605677200 16893882
11. Identification of the cluster control region for the protocadherin-β genes located beyond the protocadherin-γ cluster. Yokota S, Hirayama T, Hirano K, Kaneko R, Toyoda S, Kawamura Y, Hirabayashi M, Hirabayashi T, Yagi T, J Biol Chem 2011 286 31885 31895 10.1074/jbc.M111.245605 21771796
12. Widespread monoallelic expression on human autosomes. Gimelbrant A, Hutchinson JN, Thompson BR, Chess A, Science 2007 318 1136 1140 10.1126/science.1148910 18006746
13. Autosomal monoallelic expression in the mouse. Zwemer L, Zak A, Thompson B, Kirby A, Daly M, Chess A, Gimelbrant A, Genome Biol 2012 13 10 10.1186/gb-2012-13-2-r10 22348269
14. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HF, Nature 1991 349 38 44 10.1038/349038a0 1985261
15. Investigation of elements sufficient to imprint the mouse Air promoter. Sleutels F, Barlow DP, Mol Cell Biol 2001 21 5008 5017 10.1128/MCB.21.15.5008- 5017.2001 11438657
16. Antisense intergenic transcription in V(D)J recombination. Bolland DJ, Wood AL, Johnston CM, Bunting SF, Morgan G, Chakalova L, Fraser PJ, Corcoran AE, Nat Immunol 2004 5 630 637 10.1038/ni1068 15107847
17. X inactivation, differentiation, and DNA methylation. Riggs AD, Cytogenet Cell Genet 1975 14 9 25 10.1159/000130315 1093816
18. 5-azacytidine-induced re-expression of alleles on the inactive X chromosome in a hybrid mouse cell line. Graves JA, Exp Cell Res 1982 141 99 105 10.1016/0014-4827(82)90072-6 6180921
19. Differential methylation of hypoxanthine phosphoribosyltransferase genes on active and inactive human X chromosomes. Yen PH, Patel P, Chinault AC, Mohandas T, Shapiro LJ, Proc Natl Acad Sci U S A 1984 81 1759 1763 10.1073/pnas.81.6.1759 6324214
20. Genomic imprinting determines methylation of parental alleles in transgenic mice. Reik W, Collick A, Norris ML, Barton SC, Surani MA, Nature 1987 328 248 251 10.1038/328248a0 3600805
21. Transient homologous chromosome pairing marks the onset of X inactivation. Xu N, Tsai CL, Lee JT, Science 2006 311 1149 1152 10.1126/science.1122984 16424298
22. Imprinting at the mouse Ins2 locus: evidence for cis- and trans-allelic interactions. Duvillie B, Bucchini D, Tang T, Jami J, Paldi A, Genomics 1998 47 52 57 10.1006/geno.1997.5070 9465295
23. Homologous association of oppositely imprinted chromosomal domains. LaSalle JM, Lalande M, Science 1996 272 725 728 10.1126/science.272.5262.725 8614834
24. A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Barr ML, Bertram EG, Nature 1949 163 676 10.1038/163676a0 18120749
25. Asynchronous replication timing of imprinted loci is independent of DNA methylation, but consistent with differential subnuclear localization. Gribnau J, Hochedlinger K, Hata K, Li E, Jaenisch R, Genes Dev 2003 17 759 773 10.1101/gad.1059603 12651894
26. Differences between homologous alleles of olfactory receptor genes require the Polycomb Group protein Eed. Alexander MK, Mlynarczyk-Evans S, Royce-Tolland M, Plocik A, Kalantry S, Magnuson T, Panning B, J Cell Biol 2007 179 269 276 10.1083/jcb.200706053 17954609
27. Cell cycle analysis and X-chromosome inactivation in the developing mouse. Mukherjee AB, Proc Natl Acad Sci U S A 1976 73 1608 1611 10.1073/pnas.73.5.1608 1064031
28. Replication asynchrony between homologs 15q11.2: cytogenetic evidence for genomic imprinting. Izumikawa Y, Naritomi K, Hirayama K, Hum Genet 1991 87 1 5 10.1007/BF01213082 2037275
29. Asynchronous replication and allelic exclusion in the immune system. Mostoslavsky R, Singh N, Tenzen T, Goldmit M, Gabay C, Elizur S, Qi P, Reubinoff BE, Chess A, Cedar H, Bergman Y, Nature 2001 414 221 225 10.1038/35102606 11700561
30. An N-ethyl-N-nitrosourea screen for genes involved in variegation in the mouse. Blewitt ME, Vickaryous NK, Hemley SJ, Ashe A, Bruxner TJ, Preis JI, Arkell R, Whitelaw E, Proc Natl Acad Sci U S A 2005 102 7629 7634 10.1073/pnas.0409375102 15890782
31. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Blewitt ME, Gendrel AV, Pang Z, Sparrow DB, Whitelaw N, Craig JM, Apedaile A, Hilton DJ, Dunwoodie SL, Brockdorff N, Kay GF, Whitelaw E, Nat Genet 2008 40 663 669 10.1038/ng.142 18425126
32. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Gendrel AV, Apedaile A, Coker H, Termanis A, Zvetkova I, Godwin J, Tang YA, Huntley D, Montana G, Taylor S, Giannoulatou E, Heard E, Stancheva I, Brockdorff N, Dev Cell 2012 23 265 279 10.1016/j.devcel.2012.06.011 22841499
33. Sensitive flow cytometric analysis reveals a novel type of parent-of-origin effect in the mouse genome. Preis JI, Downes M, Oates NA, Rasko JE, Whitelaw E, Curr Biol 2003 13 955 959 10.1016/S0960-9822(03)00335-X 12781134
34. Epigenetic regulator Smchd1 functions as a tumor suppressor. Leong HS, Chen K, Hu Y, Lee S, Corbin J, Pakusch M, Murphy JM, Majewski IJ, Smyth GK, Alexander WS, Hilton DJ, Blewitt ME, Cancer Res 2012 73 1591 1599 23269277
35. A re-annotation pipeline for Illumina BeadArrays: improving the interpretation of gene expression data. Barbosa-Morais NL, Dunning MJ, Samarajiwa SA, Darot JF, Ritchie ME, Lynch AG, Tavare S, Nucleic Acids Res 2010 38 17 10.1093/nar/gkp866 19850720
36. The necdin gene is deleted in Prader-Willi syndrome and is imprinted in human and mouse. MacDonald HR, Wevrick R, Hum Mol Genet 1997 6 1873 1878 10.1093/hmg/6.11.1873 9302265
37. A novel imprinted gene, encoding a RING zinc-finger protein, and overlapping antisense transcript in the Prader-Willi syndrome critical region. Jong MT, Gray TA, Ji Y, Glenn CC, Saitoh S, Driscoll DJ, Nicholls RD, Hum Mol Genet 1999 8 783 793 10.1093/hmg/8.5.783 10196367
38. Comparative DNA sequence analysis of mouse and human protocadherin gene clusters. Wu Q, Zhang T, Cheng JF, Kim Y, Grimwood J, Schmutz J, Dickson M, Noonan JP, Zhang MQ, Myers RM, Maniatis T, Genome Res 2001 11 389 404 10.1101/gr.167301 11230163
39. Single-neuron diversity generated by Protocadherin-β cluster in mouse central and peripheral nervous systems. Hirano K, Kaneko R, Izawa T, Kawaguchi M, Kitsukawa T, Yagi T, Front Mol Neurosci 2012 5 90 22969705
40. Ubiquitous expression and imprinting of Snrpn in the mouse. Barr JA, Jones J, Glenister PH, Cattanach BM, Mamm Genome 1995 6 405 407 10.1007/BF00355641 7647462
41. The Angelman syndrome candidate gene, UBE3A/E6-AP, is imprinted in brain. Rougeulle C, Glatt H, Lalande M, Nat Genet 1997 17 14 15 10.1038/ng0997-14 9288088
42. Imprinting of the Angelman syndrome gene, UBE3A, is restricted to brain. Vu TH, Hoffman AR, Nat Genet 1997 17 12 13 10.1038/ng0997-12 9288087
43. Imprinted expression of the murine Angelman syndrome gene, Ube3a, in hippocampal and Purkinje neurons. Albrecht U, Sutcliffe JS, Cattanach BM, Beechey CV, Armstrong D, Eichele G, Beaudet AL, Nat Genet 1997 17 75 78 10.1038/ng0997-75 9288101
44. A novel maternally expressed gene, ATP10C, encodes a putative aminophospholipid translocase associated with Angelman syndrome. Meguro M, Kashiwagi A, Mitsuya K, Nakao M, Kondo I, Saitoh S, Oshimura M, Nat Genet 2001 28 19 20 11326269
45. The human aminophospholipid-transporting ATPase gene ATP10C maps adjacent to UBE3A and exhibits similar imprinted expression. Herzing LB, Kim SJ, Cook EH Jr, Ledbetter DH, Am J Hum Genet 2001 68 1501 1505 10.1086/320616 11353404
46. Gender influences monoallelic expression of ATP10A in human brain. Hogart A, Patzel KA, LaSalle JM, Hum Genet 2008 124 235 242 10.1007/s00439-008-0546-0 18726118
47. Atp10a, a gene adjacent to the PWS/AS gene cluster, is not imprinted in mouse and is insensitive to the PWS-IC. DuBose AJ, Johnstone KA, Smith EY, Hallett RA, Resnick JL, Neurogenetics 2010 11 145 151 10.1007/s10048-009-0226-9 19894069
48. On the conflicting reports of imprinting status of mouse ATP10a in the adult brain: strain-background-dependent imprinting? Kayashima T, Ohta T, Niikawa N, Kishino T, J Hum Genet 2003 48 492 493 10.1007/s10038-003-0061-z 12955587
49. Atp10a, the mouse ortholog of the human imprinted ATP10A gene, escapes genomic imprinting. Kayashima T, Yamasaki K, Joh K, Yamada T, Ohta T, Yoshiura K, Matsumoto N, Nakane Y, Mukai T, Niikawa N, Kishino T, Genomics 2003 81 644 647 10.1016/S0888-7543(03)00077-6 12782135
50. Paternal expression of a novel imprinted gene, Peg12/Frat3, in the mouse 7C region homologous to the Prader-Willi syndrome region. Kobayashi S, Kohda T, Ichikawa H, Ogura A, Ohki M, Kaneko-Ishino T, Ishino F, Biochem Biophys Res Commun 2002 290 403 408 10.1006/bbrc.2001.6160 11779183
51. Retrotransposed genes such as Frat3 in the mouse Chromosome 7C Prader-Willi syndrome region acquire the imprinted status of their insertion site. Chai JH, Locke DP, Ohta T, Greally JM, Nicholls RD, Mamm Genome 2001 12 813 821 10.1007/s00335-001-2083-1 11845283
52. Small evolutionarily conserved RNA, resembling C/D box small nucleolar RNA, is transcribed from PWCR1, a novel imprinted gene in the Prader-Willi deletion region, which is highly expressed in brain. Schweizer J, Rees CA, Francke U, de los Santos T, Am J Hum Genet 2000 67 1067 1082 10.1086/303106 11007541
53. Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. Cavaille J, Buiting K, Kiefmann M, Lalande M, Brannan CI, Horsthemke B, Bachellerie JP, Brosius J, Huttenhofer A, Proc Natl Acad Sci U S A 2000 97 14311 14316 10.1073/pnas.250426397 11106375
54. 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
55. Overlapping euchromatin/heterochromatin-associated marks are enriched in imprinted gene regions and predict allele-specific modification. Wen B, Wu H, Bjornsson H, Green RD, Irizarry R, Feinberg AP, Genome Res 2008 18 1806 1813 10.1101/gr.067587.108 18849526
56. Successful computational prediction of novel imprinted genes from epigenomic features. Brideau CM, Eilertson KE, Hagarman JA, Bustamante CD, Soloway PD, Mol Cell Biol 2010 30 3357 3370 10.1128/MCB.01355-09 20421412
57. Structure of the imprinted mouse Snrpn gene and establishment of its parental-specific methylation pattern. Shemer R, Birger Y, Riggs AD, Razin A, Proc Natl Acad Sci U S A 1997 94 10267 10272 10.1073/pnas.94.19.10267 9294199
58. Methylation dynamics of imprinted genes in mouse germ cells. Lucifero D, Mertineit C, Clarke HJ, Bestor TH, Trasler JM, Genomics 2002 79 530 538 10.1006/geno.2002.6732 11944985
59. A mouse model for Prader-Willi syndrome imprinting-centre mutations. Yang T, Adamson TE, Resnick JL, Leff S, Wevrick R, Francke U, Jenkins NA, Copeland NG, Brannan CI, Nat Genet 1998 19 25 31 10.1038/ng0598-25 9590284
60. De novo deletions of SNRPN exon 1 in early human and mouse embryos result in a paternal to maternal imprint switch. Bielinska B, Blaydes SM, Buiting K, Yang T, Krajewska-Walasek M, Horsthemke B, Brannan CI, Nat Genet 2000 25 74 78 10.1038/75629 10802660
61. Establishment and maintenance of DNA methylation patterns in mouse Ndn: implications for maintenance of imprinting in target genes of the imprinting center. Hanel ML, Wevrick R, Mol Cell Biol 2001 21 2384 2392 10.1128/MCB.21.7.2384-2392.2001 11259587
62. Imprinted methylation and its effect on expression of the mouse Zfp127 gene. Hershko A, Razin A, Shemer R, Gene 1999 234 323 327 10.1016/S0378-1119(99) 00192-4 10395905
63. MeCP2 deficiency in Rett syndrome causes epigenetic aberrations at the PWS/AS imprinting center that affects UBE3A expression. Makedonski K, Abuhatzira L, Kaufman Y, Razin A, Shemer R, Hum Mol Genet 2005 14 1049 1058 10.1093/hmg/ddi097 15757975
64. Tissue-specific and imprinted epigenetic modifications of the human NDN gene. Lau JC, Hanel ML, Wevrick R, Nucleic Acids Res 2004 32 3376 3382 10.1093/nar/gkh671 15247330
65. Parent-specific complementary patterns of histone H3 lysine 9 and H3 lysine 4 methylation at the Prader-Willi syndrome imprinting center. Xin Z, Allis CD, Wagstaff J, Am J Hum Genet 2001 69 1389 1394 10.1086/324469 11592036
66. Observation of antigen-dependent CD8+ T-cell/ dendritic cell interactions in vivo. Schaefer BC, Schaefer ML, Kappler JW, Marrack P, Kedl RM, Cell Immunol 2001 214 110 122 10.1006/cimm.2001.1895 12088410
67. Bidirectional action of the Igf2r imprint control element on upstream and downstream imprinted genes. Zwart R, Sleutels F, Wutz A, Schinkel AH, Barlow DP, Genes Dev 2001 15 2361 2366 10.1101/gad.206201 11562346
68. The IC-SNURF-SNRPN transcript serves as a host for multiple small nucleolar RNA species and as an antisense RNA for UBE3A. Runte M, Huttenhofer A, Gross S, Kiefmann M, Horsthemke B, Buiting K, Hum Mol Genet 2001 10 2687 2700 10.1093/hmg/10.23.2687 11726556
69. Ube3a-ATS is an atypical RNA polymerase II transcript that represses the paternal expression of Ube3a. Meng L, Person RE, Beaudet AL, Hum Mol Genet 2012 21 3001 3012 10.1093/hmg/dds130 22493002
70. Transcription is required to establish maternal imprinting at the Prader-Willi syndrome and Angelman syndrome locus. Smith EY, Futtner CR, Chamberlain SJ, Johnstone KA, Resnick JL, PLoS Genet 2011 7 1002422 10.1371/journal.pgen.1002422 22242001
71. An unexpected function of the Prader-Willi syndrome imprinting center in maternal imprinting in mice. Wu MY, Jiang M, Zhai X, Beaudet AL, Wu RC, PLoS One 2012 7 34348 10.1371/journal.pone.0034348 22496793
72. Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing. Latos PA, Pauler FM, Koerner MV, Şenergin HB, Hudson QJ, Stocsits RR, Allhoff W, Stricker SH, Klement RM, Warczok KE, Aumayr K, Pasierbek P, Barlow DP, Science 2012 338 1469 1472 10.1126/science.1228110 23239737
73. The Air 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
74. Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Zipursky SL, Sanes JR, Cell 2010 143 343 353 10.1016/j.cell.2010.10. 009 21029858
75. Regulatory elements required for the activation and repression of the protocadherin-α gene cluster. Kehayova P, Monahan K, Chen W, Maniatis T, Proc Natl Acad Sci U S A 2011 108 17195 17200 10.1073/pnas.1114357108 21949399
76. Identification of long-range regulatory elements in the protocadherin-α gene cluster. Ribich S, Tasic B, Maniatis T, Proc Natl Acad Sci USA 2006 103 19719 19724 10.1073/pnas.0609445104 17172445
77. SMC proteins and chromosome mechanics: from bacteria to humans. Hirano T, Philos Trans R Soc Lond B Biol Sci 2005 360 507 514 10.1098/rstb.2004.1606 15897176
78. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases. Iyer LM, Abhiman S, Aravind L, Biol Direct 2008 3 8 10.1186/1745-6150-3-8 18346280
79. Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Lemmers RJ, Tawil R, Petek LM, Balog J, Block GJ, Santen GW, Amell AM, van der Vliet PJ, Almomani R, Straasheijm KR, Krom YD, Klooster R, Sun Y, den Dunnen JT, Helmer Q, Donlin-Smith CM, Padberg GW, van Engelen BG, de Greef JC, Aartsma-Rus AM, Frants RR, de Visser M, Desnuelle C, Sacconi S, Filippova GN, Bakker B, Bamshad MJ, Tapscott SJ, Miller DG, van der Maarel SM, Nat Genet 2012 44 1370 1374 10.1038/ng.2454 23143600
80. GMI1, a structural-maintenance-of-chromosomes-hinge domain-containing protein, is involved in somatic homologous recombination in Arabidopsis. Bohmdorfer G, Schleiffer A, Brunmeir R, Ferscha S, Nizhynska V, Kozak J, Angelis KJ, Kreil DP, Schweizer D, Plant J 2011 67 420 433 10.1111/j.1365-313X.2011. 04604.x 21481027
81. Nagy A, Gertsenstein M, Vintersten K, Behringer R, Manipulating the Mouse Embryo-A Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press 3 2003
82. Towards standardization of RNA quality assessment using user-independent classifiers of microcapillary electrophoresis traces. Imbeaud S, Graudens E, Boulanger V, Barlet X, Zaborski P, Eveno E, Mueller O, Schroeder A, Auffray C, Nucleic Acids Res 2005 33 56 10.1093/nar/gni054 15800207
83. Beadarray: R classes and methods for Illumina bead-based data. Dunning MJ, Smith ML, Ritchie ME, Tavare S, Bioinformatics 2007 23 2183 2184 10.1093/bioinformatics/btm311 17586828
84. Limma: linear models for microarray data. Smyth GK, Bioinformatics and Computational Biology Solutions using R and Bioconductor New York: Springer, Gentleman R, Carey V, Dudoit S, Irizarry WH R, 2005 397 420
85. Bioconductor: open software development for computational biology and bioinformatics. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J, Genome Biol 2004 5 80 10.1186/gb-2004-5-10-r80 15461798
86. DAVID: database for annotation, visualization, and integrated discovery. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA, Genome Biol 2003 4 3 10.1186/gb-2003-4-5-p3 12734009
87. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schubeler D, Nat Genet 2005 37 853 862 10.1038/ng1598 16007088
88. Genome-scale ChIP-chip analysis using 10,000 human cells. Acevedo LG, Iniguez AL, Holster HL, Zhang X, Green R, Farnham PJ, Biotechniques 2007 43 791 797 10.2144/000112625 18251256
89. MethPrimer: designing primers for methylation PCRs. Li LC, Dahiya R, Bioinformatics 2002 18 1427 1431 10.1093/bioinformatics/18.11.1427 12424112
90. BiQ analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bock C, Reither S, Mikeska T, Paulsen M, Walter J, Lengauer T, Bioinformatics 2005 21 4067 4068 10.1093/bioinformatics/bti652 16141249
91. Activity map of the tammar X chromosome shows that marsupial X inactivation is incomplete and escape is stochastic. Al Nadaf S, Waters PD, Koina E, Deakin JE, Jordan KS, Graves JA, Genome Biol 2010 11 122 10.1186/gb-2010-11-12-r122 21182760