Epigenetic Functions of Smchd1 Repress Gene Clusters on the Inactive X Chromosome and on Autosomes

REFERENCES

• Hirano T. 2006. At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell Biol. 7:311–322.
   PubMed Web of Science ®Google Scholar
• Blewitt ME, Gendrel AV, Pang Z, Sparrow DB, Whitelaw N, Craig JM, Apedaile A, Hilton DJ, Dunwoodie SL, Brockdorff N, Kay GF, Whitelaw E. 2008. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat. Genet. 40:663–669.
   PubMed Web of Science ®Google Scholar
• Blewitt ME, Vickaryous NK, Hemley SJ, Ashe A, Bruxner TJ, Preis JI, Arkell R, Whitelaw E. 2005. An N-ethyl-N-nitrosourea screen for genes involved in variegation in the mouse. Proc. Natl. Acad. Sci. U. S. A. 102:7629–7634.
   PubMed Web of Science ®Google Scholar
• 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. 2012. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev. Cell 23:265–279.
   PubMed Web of Science ®Google Scholar
• Kanno T, Bucher E, Daxinger L, Huettel B, Bohmdorfer G, Gregor W, Kreil DP, Matzke M, Matzke AJ. 2008. A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat. Genet. 40:670–675.
   PubMed Web of Science ®Google Scholar
• Lorkovic ZJ, Naumann U, Matzke AJ, Matzke M. 2012. Involvement of a GHKL ATPase in RNA-directed DNA methylation in Arabidopsis thaliana. Curr. Biol. 22:933–938.
   PubMedGoogle Scholar
• Moissiard G, Cokus SJ, Cary J, Feng S, Billi AC, Stroud H, Husmann D, Zhan Y, Lajoie BR, McCord RP, Hale CJ, Feng W, Michaels SD, Frand AR, Pellegrini M, Dekker J, Kim JK, Jacobsen SE. 2012. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336:1448–1451.
   PubMed Web of Science ®Google Scholar
• Bohmdorfer G, Schleiffer A, Brunmeir R, Ferscha S, Nizhynska V, Kozak J, Angelis KJ, Kreil DP, Schweizer D. 2011. GMI1, a structural-maintenance-of-chromosomes-hinge domain-containing protein, is involved in somatic homologous recombination in Arabidopsis. Plant J. 67:420–433.
   PubMedGoogle Scholar
• Dejardin J, Kingston RE. 2009. Purification of proteins associated with specific genomic loci. Cell 136:175–186.
   PubMed Web of Science ®Google Scholar
• Horsthemke B, Wagstaff J. 2008. Mechanisms of imprinting of the Prader-Willi/Angelman region. Am. J. Med. Genet. A 146A:2041–2052.
   PubMed Web of Science ®Google Scholar
• Esumi S, Kakazu N, Taguchi Y, Hirayama T, Sasaki A, Hirabayashi T, Koide T, Kitsukawa T, Hamada S, Yagi T. 2005. Monoallelic yet combinatorial expression of variable exons of the protocadherin-alpha gene cluster in single neurons. Nat. Genet. 37:171–176.
   PubMed Web of Science ®Google Scholar
• Lewandoski M, Wassarman KM, Martin GR. 1997. Zp3-cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line. Curr. Biol. 7:148–151.
   PubMed Web of Science ®Google Scholar
• Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. 2004. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900–903.
   PubMed Web of Science ®Google Scholar
• Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31:e15.
   PubMed Web of Science ®Google Scholar
• Smyth GK. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:Article3.
   PubMedGoogle Scholar
• Borgel J, Guibert S, Li Y, Chiba H, Schubeler D, Sasaki H, Forne T, Weber M. 2010. Targets and dynamics of promoter DNA methylation during early mouse development. Nat. Genet. 42:1093–1100.
   PubMed Web of Science ®Google Scholar
• Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G, Cantor CR, Field JK, van den Boom D. 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.
   PubMed Web of Science ®Google Scholar
• Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, Gribnau J, Barillot E, Bluthgen N, Dekker J, Heard E. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–385.
   PubMed Web of Science ®Google Scholar
• Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–380.
   PubMed Web of Science ®Google Scholar
• Yang T, Adamson TE, Resnick JL, Leff S, Wevrick R, Francke U, Jenkins NA, Copeland NG, Brannan CI. 1998. A mouse model for Prader-Willi syndrome imprinting-centre mutations. Nat. Genet. 19:25–31.
   PubMed Web of Science ®Google Scholar
• Bielinska B, Blaydes SM, Buiting K, Yang T, Krajewska-Walasek M, Horsthemke B, Brannan CI. 2000. De novo deletions of SNRPN exon 1 in early human and mouse embryos result in a paternal to maternal imprint switch. Nat. Genet. 25:74–78.
   PubMed Web of Science ®Google Scholar
• Chamberlain SJ, Brannan CI. 2001. The Prader-Willi syndrome imprinting center activates the paternally expressed murine Ube3a antisense transcript but represses paternal Ube3a. Genomics 73:316–322.
   PubMed Web of Science ®Google Scholar
• Abramowitz LK, Bartolomei MS. 2012. Genomic imprinting: recognition and marking of imprinted loci. Curr. Opin. Genet. Dev. 22:72–78.
   PubMed Web of Science ®Google Scholar
• Hershko A, Razin A, Shemer R. 1999. Imprinted methylation and its effect on expression of the mouse Zfp127 gene. Gene 234:323–327.
   PubMedGoogle Scholar
• Hanel ML, Wevrick R. 2001. Establishment and maintenance of DNA methylation patterns in mouse Ndn: implications for maintenance of imprinting in target genes of the imprinting center. Mol. Cell. Biol. 21:2384–2392.
   PubMed Web of Science ®Google Scholar
• Ferguson-Smith AC. 2011. Genomic imprinting: the emergence of an epigenetic paradigm. Nat. Rev. Genet. 12:565–575.
   PubMed Web of Science ®Google Scholar
• Morishita H, Yagi T. 2007. Protocadherin family: diversity, structure, and function. Curr. Opin. Cell Biol. 19:584–592.
   PubMed Web of Science ®Google Scholar
• Kaneko R, Kato H, Kawamura Y, Esumi S, Hirayama T, Hirabayashi T, Yagi T. 2006. Allelic gene regulation of Pcdh-alpha and Pcdh-gamma clusters involving both monoallelic and biallelic expression in single Purkinje cells. J. Biol. Chem. 281:30551–30560.
   PubMed Web of Science ®Google Scholar
• Wu Q, Zhang T, Cheng JF, Kim Y, Grimwood J, Schmutz J, Dickson M, Noonan JP, Zhang MQ, Myers RM, Maniatis T. 2001. Comparative DNA sequence analysis of mouse and human protocadherin gene clusters. Genome Res. 11:389–404.
   PubMed Web of Science ®Google Scholar
• Harris RA, Wang T, Coarfa C, Nagarajan RP, Hong C, Downey SL, Johnson BE, Fouse SD, Delaney A, Zhao Y, Olshen A, Ballinger T, Zhou X, Forsberg KJ, Gu J, Echipare L, O'Geen H, Lister R, Pelizzola M, Xi Y, Epstein CB, Bernstein BE, Hawkins RD, Ren B, Chung WY, Gu H, Bock C, Gnirke A, Zhang MQ, Haussler D, Ecker JR, Li W, Farnham PJ, Waterland RA, Meissner A, Marra MA, Hirst M, Milosavljevic A, Costello JF. 2010. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol. 28:1097–1105.
   PubMed Web of Science ®Google Scholar
• Hansen RS, Canfield TK, Fjeld AD, Gartler SM. 1996. Role of late replication timing in the silencing of X-linked genes. Hum. Mol. Genet. 5:1345–1353.
   PubMedGoogle Scholar
• Hansen RS, Stoger R, Wijmenga C, Stanek AM, Canfield TK, Luo P, Matarazzo MR, D'Esposito M, Feil R, Gimelli G, Weemaes CM, Laird CD, Gartler SM. 2000. Escape from gene silencing in ICF syndrome: evidence for advanced replication time as a major determinant. Hum. Mol. Genet. 9:2575–2587.
   PubMed Web of Science ®Google Scholar
• Nozawa RS, Nagao K, Igami KT, Shibata S, Shirai N, Nozaki N, Sado T, Kimura H, Obuse C. 2013. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat. Struct. Mol. Biol. 20:566–573.
   PubMed Web of Science ®Google Scholar
• Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, Cobb BS, Yokomori K, Dillon N, Aragon L, Fisher AG, Merkenschlager M. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422–433.
   PubMed Web of Science ®Google Scholar
• Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796–801.
   PubMed Web of Science ®Google Scholar
• Sado T, Fenner MH, Tan SS, Tam P, Shioda T, Li E. 2000. X inactivation in the mouse embryo deficient for Dnmt1: distinct effect of hypomethylation on imprinted and random X inactivation. Dev. Biol. 225:294–303.
   PubMed Web of Science ®Google Scholar
• Bressler J, Tsai TF, Wu MY, Tsai SF, Ramirez MA, Armstrong D, Beaudet AL. 2001. The SNRPN promoter is not required for genomic imprinting of the Prader-Willi/Angelman domain in mice. Nat. Genet. 28:232–240.
   PubMedGoogle Scholar
• Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536–2539.
   PubMed Web of Science ®Google Scholar
• Fan T, Hagan JP, Kozlov SV, Stewart CL, Muegge K. 2005. Lsh controls silencing of the imprinted Cdkn1c gene. Development 132:635–644.
   PubMedGoogle Scholar
• Myant K, Termanis A, Sundaram AY, Boe T, Li C, Merusi C, Burrage J, de Las Heras JI, Stancheva I. 2011. LSH and G9a/GLP complex are required for developmentally programmed DNA methylation. Genome Res. 21:83–94.
   PubMed Web of Science ®Google Scholar
• Yagi T. 2008. Clustered protocadherin family. Dev. Growth Differ. 50(Suppl 1):S131–S140.
   PubMedGoogle Scholar
• Esumi S, Kaneko R, Kawamura Y, Yagi T. 2006. Split single-cell RT-PCR analysis of Purkinje cells. Nat. Protoc. 1:2143–2151.
   PubMedGoogle Scholar
• Tang F, Lao K, Surani MA. 2011. Development and applications of single-cell transcriptome analysis. Nat. Methods 8:S6–S11.
   PubMed Web of Science ®Google Scholar
• Kawaguchi M, Toyama T, Kaneko R, Hirayama T, Kawamura Y, Yagi T. 2008. Relationship between DNA methylation states and transcription of individual isoforms encoded by the protocadherin-alpha gene cluster. J. Biol. Chem. 283:12064–12075.
   PubMed Web of Science ®Google Scholar
• Guo Y, Monahan K, Wu H, Gertz J, Varley KE, Li W, Myers RM, Maniatis T, Wu Q. 2012. CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice. Proc. Natl. Acad. Sci. U. S. A. 109:21081–21086.
   PubMed Web of Science ®Google Scholar
• Golan-Mashiach M, Grunspan M, Emmanuel R, Gibbs-Bar L, Dikstein R, Shapiro E. 2012. Identification of CTCF as a master regulator of the clustered protocadherin genes. Nucleic Acids Res. 40:3378–3391.
   PubMed Web of Science ®Google Scholar
• Hirayama T, Tarusawa E, Yoshimura Y, Galjart N, Yagi T. 2012. CTCF is required for neural development and stochastic expression of clustered Pcdh genes in neurons. Cell Rep 2:345–357.
   PubMedGoogle Scholar
• Monahan K, Rudnick ND, Kehayova PD, Pauli F, Newberry KM, Myers RM, Maniatis T. 2012. Role of CCCTC binding factor (CTCF) and cohesin in the generation of single-cell diversity of protocadherin-alpha gene expression. Proc. Natl. Acad. Sci. U. S. A. 109:9125–9130.
   PubMed Web of Science ®Google Scholar
• Gerard M, Hernandez L, Wevrick R, Stewart CL. 1999. Disruption of the mouse necdin gene results in early post-natal lethality. Nat. Genet. 23:199–202.
   PubMed Web of Science ®Google Scholar
• Muscatelli F, Abrous DN, Massacrier A, Boccaccio I, Le Moal M, Cau P, Cremer H. 2000. Disruption of the mouse Necdin gene results in hypothalamic and behavioral alterations reminiscent of the human Prader-Willi syndrome. Hum. Mol. Genet. 9:3101–3110.
   PubMedGoogle Scholar
• Hasegawa S, Hamada S, Kumode Y, Esumi S, Katori S, Fukuda E, Uchiyama Y, Hirabayashi T, Mombaerts P, Yagi T. 2008. The protocadherin-alpha family is involved in axonal coalescence of olfactory sensory neurons into glomeruli of the olfactory bulb in mouse. Mol. Cell Neurosci. 38:66–79.
   PubMedGoogle Scholar
• Wang X, Weiner JA, Levi S, Craig AM, Bradley A, Sanes JR. 2002. Gamma protocadherins are required for survival of spinal interneurons. Neuron 36:843–854.
   PubMed Web of Science ®Google Scholar
• Weiner JA, Wang X, Tapia JC, Sanes JR. 2005. Gamma protocadherins are required for synaptic development in the spinal cord. Proc. Natl. Acad. Sci. U. S. A. 102:8–14.
   PubMed Web of Science ®Google Scholar
• Boyle AL, Ballard SG, Ward DC. 1990. Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization. Proc. Natl. Acad. Sci. U. S. A. 87:7757–7761.
   PubMed Web of Science ®Google Scholar
• Bailey JA, Carrel L, Chakravarti A, Eichler EE. 2000. Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc. Natl. Acad. Sci. U. S. A. 97:6634–6639.
   PubMed Web of Science ®Google Scholar
• Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N, Glass JL, Attreed M, Avner P, Wutz A, Barillot E, Greally JM, Voinnet O, Heard E. 2010. LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141:956–969.
   PubMed Web of Science ®Google Scholar
• Tang YA, Huntley D, Montana G, Cerase A, Nesterova TB, Brockdorff N. 2010. Efficiency of Xist-mediated silencing on autosomes is linked to chromosomal domain organisation. Epigenet Chromatin 3:10.
   PubMed Web of Science ®Google Scholar
• 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. 2012. Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Nat. Genet. 44:1370–1374.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57:289–300.
   Web of Science ®Google Scholar