, Volume 118, Issue 3, pp 279–290 | Cite as

Monoallelic gene expression in mammals

  • Irina S. Zakharova
  • Alexander I. Shevchenko
  • Suren M. ZakianEmail author


Three systems of monoallelic gene expression in mammals are known, namely, X-chromosome inactivation, imprinting, and allelic exclusion. In all three systems, monoallelic expression is regulated epigenetically and is frequently directed by long non-coding RNAs (ncRNAs). This review briefs all three systems of monoallelic gene expression in mammals focusing on chromatin modifications, spatial chromosome organization in the nucleus, and the functioning of ncRNAs.


Imprint Gene H3K27 Trimethylation Monoallelic Expression Xist Gene Inactive Chromatin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Prof. L.V. Vysotskaya (Novosibirsk State University, Russia) and Prof. E.S. Belyaeva (Institute of Cytology and Genetics, Russian Academy of Sciences, Siberian Department, Novosibirsk, Russia) for helpful comments and discussion. We are grateful to Claire Senner for valuable comments and suggestions. The work was funded by grant no. 08-04-00346 from the Russian Foundation for Basic Research.


  1. Afshar R, Pierce S, Bolland DJ, Corcoran A, Oltz EM (2006) Regulation of IgH gene assembly: role of the intronic enhancer and 50DQ52 region in targeting DHJH recombination. J Immunol 176:2439–2447PubMedGoogle Scholar
  2. Alexander MK, Mlynarczyk-Evans S, Royce-Tolland M, Plocik A, Kalantry S, Magnuson T, Panning B (2007) Differences between homologous alleles of olfactory receptor genes require the Polycomb Group protein Eed. J Cell Biol 179:269–276PubMedCrossRefGoogle Scholar
  3. Augui S, Filion GJ, Huar S, Nora E, Guggiari M, Maresca M, Stewart AF, Heard E (2007) Sensing X chromosome pairs before X inactivation via a novel X-pairing region of the Xic. Science 318:1632–1636PubMedCrossRefGoogle Scholar
  4. Bacher CP, Guggiari M, Brors B, Augui S, Clerc P, Avner P, Eils R, Heard E (2006) Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation. Nat Cell Biol 8:293–299PubMedCrossRefGoogle Scholar
  5. Barlow DP (1997) Competition—a common motif for the imprinting mechanism? EMBO J 16:6899–6905PubMedCrossRefGoogle Scholar
  6. Bartova E, Kozubek S (2006) Nuclear architecture in the light of gene expression and cell differentiation studies. Biol Cell 98:323–336PubMedCrossRefGoogle Scholar
  7. Bassing CH, Swat W, Alt FW (2002) The mechanism and regulation of chromosomal V(D)J recombination. Cell 109:S45–S55PubMedCrossRefGoogle Scholar
  8. Beechey CV, Cattanach BM, Blake A, Peters J (2008) MRC Harwell, Oxfordshire. Mouse imprinting data and references.
  9. Blank RD, Campbell GR, Calabro A, D’Eustachio P (1988) A linkage map of mouse chromosome 12: localization of IgH and effects of sex and interference on recombination. Genetics 120:1073–1083PubMedGoogle Scholar
  10. Bolland DJ, Wood AL, Johnston CM, Bunting SF, Morgan G, Chakalova L, Fraser PJ, Corcoran AE (2004) Antisense intergenic transcription in V(D)J recombination. Nat Immunol 5:630–637PubMedCrossRefGoogle Scholar
  11. Bolland DJ, Wood AL, Afshar R, Featherstone K, Oltz EM, Corcoran AE (2007) Antisense intergenic transcription precedes Igh D-to-J recombination and is controlled by the intronic enhancer Emu. Mol Cell Biol 27:5523–5533PubMedCrossRefGoogle Scholar
  12. Cedar H, Bergman Y (2008) Choreography of Ig allelic exclusion. Curr Opin Immunol 20:1–10CrossRefGoogle Scholar
  13. Chaumeil J, Le Baccon P, Wutz A, Heard E (2006) A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev 20:2223–2237PubMedCrossRefGoogle Scholar
  14. Chess A, Simon I, Cedar H, Alex R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823–834PubMedCrossRefGoogle Scholar
  15. Chow JC, Hall LL, Clemson CM, Lawrence JB, Brown CJ (2003) Characterization of expression at the human XIST locus in somatic, embryonal carcinoma, and transgenic cell lines. Genomics 82:309–322PubMedCrossRefGoogle Scholar
  16. Clemson CM, Hall LL, Byron M, McNeil J, Lawrence JB (2006) The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced non-genic sequences. Proc Natl Acad Sci USA 103:7688–7693PubMedCrossRefGoogle Scholar
  17. Delaval K, Feil R (2004) Epigenetic regulation of mammalian genomic imprinting. Curr Opin Genet Dev 14:188–195PubMedCrossRefGoogle Scholar
  18. Engemann S, Strodicke M, Paulsen M, Franck O, Reinhardt R, Lane N, Reik W, Walter J (2000) Sequence and functional comparison in the Beckwith–Wiedemann region: implications for a novel imprinting centre and extended imprinting. Hum Mol Genet 9:2691–2706PubMedCrossRefGoogle Scholar
  19. Fitzpatrick GV, Pugacheva EM, Shin JY, Abdullaev Z, Yang Y, Khatod K, Lobanenkov VV, Higgins MJ (2007) Allele-specific binding of CTCF to the multipartite imprinting control region KvDMR1. Mol Cell Biol 27:2636–2647PubMedCrossRefGoogle Scholar
  20. Foster H, Bridger J (2005) The genome and the nucleus: a marriage made by evolution. Genome organization and nuclear architecture. Chromosoma 114:212–229PubMedCrossRefGoogle Scholar
  21. Fugmann SD, Lee AI, Shockett PE, Villey IJ, Schatz DG (2000) The RAG proteins and V(D)J recombination: complexes ends and transcription. Annu Rev Immunology 18:495–537CrossRefGoogle Scholar
  22. Fuss SH, Omura M, Mombaerts P (2007) Local and cis effects of the H element on expression of odorant receptor genes in mouse. Cell 130:373–384PubMedCrossRefGoogle Scholar
  23. Gimelbrant A, Hutchinson JN, Thompson BR, Chess A (2007) Widespread monoallelic expression on human autosomes. Science 318:1136–1140PubMedCrossRefGoogle Scholar
  24. Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–702PubMedCrossRefGoogle Scholar
  25. Godfrey PA, Malnic B, Buck LB (2004) The mouse olfactory receptor gene family. Proc Natl Acad Sci USA 101:2156–2161PubMedCrossRefGoogle Scholar
  26. Goldmit M, Bergman Y (2004) Monoallelic gene expression: a repertoire of recurrent themes. Immunol Rev 200:197–214PubMedCrossRefGoogle Scholar
  27. Goldmit M, Yanhong J, Skok J, Roldan E, Jung S, Cedar H, Bergman Y (2005) Epigenetic ontogeny of the ҝ-locus during B-cell development. Nat Immunol 6:198–203PubMedCrossRefGoogle Scholar
  28. Goren A, Cedar H (2003) Replicating by the clock. Nat Rev Mol Cell Biol 4:25–32PubMedCrossRefGoogle Scholar
  29. Gribnau J, Hochedlinger K, Hata K, Li E, Jaenisch R (2003) Asynchronous replication timing of imprinted loci is independent of DNA methylation, but consistent with differential subnuclear localization. Genes Dev 17:759–773PubMedCrossRefGoogle Scholar
  30. Heard E (2005) Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr Opin Genet Dev 15:482–489PubMedCrossRefGoogle Scholar
  31. Heard E, Disteche CM (2006) Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 20:1848–1867PubMedCrossRefGoogle Scholar
  32. Hemberger M, Redies C, Krause R, Oswald J, Walter J, Fundele RH (1998) H19 and Igf2 are expressed and differentially imprinted in neuroectoderm-derived cells in the mouse brain. Dev Genes Evol 208:393–402PubMedCrossRefGoogle Scholar
  33. Hesslein DG, Schatz DG (2001) Factors and forces controlling V(D)J recombination. Adv Immunol 78:169–232PubMedCrossRefGoogle Scholar
  34. Kambere MB, Lane RP (2007) Co-regulation of a large and rapidly evolving repertoire of odorant receptor genes. BMC Neurosci 8:S2PubMedCrossRefGoogle Scholar
  35. Kanduri C, Thakur N, Pandey R (2006) The length of the transcript encoded from the Kcnq1ot1 antisense promoter determines the degree of silencing. EMBO J 25:2096–2106PubMedCrossRefGoogle Scholar
  36. Khor B, Sleckman BP (2002) Allelic exclusion at the TCRbeta locus. Curr Opin Immunol 14:230–234PubMedCrossRefGoogle Scholar
  37. Kohlmaier A, Savarese F, Lachner M, Martens J, Jenuwein T, Wutz A (2004) A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol 2:E171PubMedCrossRefGoogle Scholar
  38. Krangel MS (2003) Gene segment selection in V(D)J recombination: accessibility and beyond. Nat Immunol 4:624–630PubMedCrossRefGoogle Scholar
  39. Lee JT, Lu N (1999) Targeted mutagenesis of Tsix leads to non-random X inactivation. Cell 99:47–57PubMedCrossRefGoogle Scholar
  40. Lee JT, Davidow LS, Warshawsky D (1999) Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet 21:400–404PubMedCrossRefGoogle Scholar
  41. Lefranc MP, Clement O, Kaas Q, Duprat E, Chastellan P, Coelho I, Combres K, Ginestoux C, Giudicelli V, Chaume D, Lefranc G (2005) IMGT-Choreography for immunogenetics and immunoinformatics. In Silico Biol 5:45–60PubMedGoogle Scholar
  42. Lewis A, Mitsuya K, Umlauf D, Smith P, Dean W (2004) Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat Genet 36:1291–1295PubMedCrossRefGoogle Scholar
  43. Lin H, Gupta V, VerMilyea MD, Falciani F, Lee JT (2007) Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biol 5:e326PubMedCrossRefGoogle Scholar
  44. Liu Z, Widlak P, Zou Y, Xiao F, Oh M, Li S, Chang MY, Shay JW, Garrard WT (2006) A recombination silencer that specifies heterochromatin positioning and ikaros association in the immunoglobulin kappa locus. Immunity 24:405–415PubMedCrossRefGoogle Scholar
  45. Liu Y, Subrahmanyam R, Chakrabborty T, Sen R, Desiderio S (2007) A plant homeodomain in RAG2 that binds hypermethylated lysine 4 of histone H3 is necessary for efficient antigen-receptor-gene rearrangement. Immunity 27:561–571PubMedCrossRefGoogle Scholar
  46. Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R (2006) Interchromosomal interactions and olfactory receptor choice. Cell 126:403–413PubMedCrossRefGoogle Scholar
  47. Luikenhuis S, Wutz A, Jaenisch R (2001) Antisense transcription through the Xist locus mediates Tsix function in embryonic stem cells. Mol Cell Biol 21:8512–8520PubMedCrossRefGoogle Scholar
  48. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723PubMedCrossRefGoogle Scholar
  49. Malnic B, Godfrey PA, Buck L (2004) The human olfactory receptor gene family. Proc Natl Acad Sci USA 101:2584–2589PubMedCrossRefGoogle Scholar
  50. Mancini-Dinardo D, Steele SJ, Levorse JM, Ingram RS, Tilghman SM (2006) Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev 20:1268–1282PubMedCrossRefGoogle Scholar
  51. Matthews AG, Kuo AJ, Ramón-Maiques S, Han S, Champagne KS, Ivanov D, Gallardo M, Carney D, Cheung P, Ciccone DN, Walter KL, Utz PJ, Shi Y, Kutateladze TG, Yang W, Gozani O, Oettinger MA (2007) RAG2 PDH finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 450:1106–1110PubMedCrossRefGoogle Scholar
  52. Migeon BR, Lee CH, Chowdhury AK, Carpenter H (2002) Species differences in TSIX/Tsix reveal the roles of these genes in X-chromosome inactivation. Am J Hum Genet 71:286–293PubMedCrossRefGoogle Scholar
  53. Mohammad F, Pandey RR, Nagano T, Chakalova L, Mondal T, Fraser P, Kanduri C (2008) Kcnq1ot1/Lit1 noncoding RNA mediates transcriptional silencing by targeting to the perinucleolar region. Mol Cell Biol 28:3713–3728PubMedCrossRefGoogle Scholar
  54. Mostoslavsky R, Singh N, Tenzen T, Goldmit M, Gabay C, Elizur S, Qi P, Reubinoff BE, Chess A, Cedar H, Bergman Y (2001) Asynchronous replication and allelic exclusion in the immune system. Nature 414:221–225PubMedCrossRefGoogle Scholar
  55. Murakami K, Oshimura M, Kugoh H (2007) Suggestive evidence for chromosomal localization of non-coding RNA from imprinted LIT1. J Hum Genet 52:926–933PubMedCrossRefGoogle Scholar
  56. Murphy SK, Jirtle RL (2003) Imprinting evolution and the price of silence. Bioessays 25:577–588PubMedCrossRefGoogle Scholar
  57. Navarro P, Pichard S, Ciaudo C, Avner P, Rougeulle C (2005) Tsix transcription across the Xist gene alters chromatin conformation without affecting Xist transcription: implications for X-chromosome inactivation. Genes Dev 19:1474–1484PubMedCrossRefGoogle Scholar
  58. Navarro P, Page DR, Avner P, Rougeulle C (2006) Tsix mediated epigenetic switch of a CTCF-flanked region of the Xist promoter determines the Xist transcription program. Genes Dev 20:2787–2792PubMedCrossRefGoogle Scholar
  59. Nesterova TB, Popova BC, Cobb BS, Norton S, Senner CE, Tang YA, Spruce T, Rodriguez TA, Sado T, Merkenschlager M, Brockdorff N (2008) Dicer regulates Xist promoter methylation in ES cells indirectly through transcriptional control of Dnmt3a. Epigenetics Chromatin 1:2PubMedCrossRefGoogle Scholar
  60. Ogawa Y, Sun BK, Lee JT (2008) Intersection of the RNA interference and X-inactivation pathways. Science 320:1336–1341PubMedCrossRefGoogle Scholar
  61. Ohlsson R, Hedborg F, Holmgren L, Walsh C, Ekstrom TJ (1994) Overlapping patterns of IGF2 and H19 expression during human development: biallelic IGF2 expression correlates with a lack of H19 expression. Development 120:361–368PubMedGoogle Scholar
  62. O’Neill MJ (2005) The influence of non-coding RNAs on allele-specific gene expression in mammals. Hum Mol Genet 14:113–120CrossRefGoogle Scholar
  63. Oudejans CB, Westerman B, Wouters D, Gooyer S, Leegwater PA, van Wijk IJ, Sleutels F (2001) Allelic IGF2R repression does not correlate with expression of antisence RNA in human extraembrionic tissue. Genomics 73:331–337PubMedCrossRefGoogle Scholar
  64. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C (2008) Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 32(2):232–246PubMedCrossRefGoogle Scholar
  65. Parada LA, Sotiriou S, Misteli T (2004) Spatial genome organization. Exp Cell Res 296:64–70PubMedCrossRefGoogle Scholar
  66. Pauler FM, Koerner MV, Barlow DP (2007) Silencing by imprinted non-coding RNAs: is transcription the answer? Trends Genet 23:284–292PubMedCrossRefGoogle Scholar
  67. Perlot T, Alt FW, Bassing CH, Suh H, Pinaud E (2005) Elucidation of IgH intronic enhancer functions via germ-line deletion. Proc Natl Acad Sci USA 102:14362–14367PubMedCrossRefGoogle Scholar
  68. Ramon-Maiques S, Kuo AJ, Carney D, Matthews AG, Oettinger MA, Gozani O, Yang W (2007) The plant homeodomain finger of RAG2 recognises histone H3 methylated at both lysine-4 and argentine-2. Proc Natl Acad Sci USA 104:18993–18998PubMedCrossRefGoogle Scholar
  69. Reik W, Maher ER (1997) Imprinting in clusters: lessons from Beckwith–Wiedemann syndrome. Trends Genet 13:330–334PubMedCrossRefGoogle Scholar
  70. Riesewijk AM, Schepens MT, Welch TR, van den Berg-Loonen EM, Mariman EM, Ropers HH, Kalscheuer VM (1996) Maternal-specific methylation of the human IGF2R gene is not accompanied by allele-specific transcription. Genomics 31:158–166PubMedCrossRefGoogle Scholar
  71. Rougeulle C, Heard E (2002) Antisense RNA in imprinting: spreading silence through Air. Trends Genet 18:434–437PubMedCrossRefGoogle Scholar
  72. Sado T, Wang Z, Sasaki H, Li E (2001) Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development 128:1275–1286PubMedGoogle Scholar
  73. Sado T, Hoki Y, Sasaki H (2005) Tsix silences Xist through modification of chromatin structure. Dev Cell 9:159–165PubMedCrossRefGoogle Scholar
  74. Schmidt JV, Levorse JM, Tilghman SM (1999) Enhancer competition between H19 and Igf2 does not mediate their imprinting. Proc Natl Acad Sci USA 96:9733–9738PubMedCrossRefGoogle Scholar
  75. Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M, Yoshihara Y, Sakano H (2003) Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302:2088–2094PubMedCrossRefGoogle Scholar
  76. Shearwin KE, Callen BP, Egan JB (2005) Transcriptional interference—a crash course. Trends Genet 21:339–345PubMedCrossRefGoogle Scholar
  77. Shibata S, Wutz A (2008) Transcript versus transcription? Epigenetics 3:246–249PubMedGoogle Scholar
  78. Shin JY, Fitzpatrick GV, Higgins MJ (2008) Two distinct mechanisms of silencing by the KvDMR1 imprinting control region. EMBO J 27:168–178PubMedCrossRefGoogle Scholar
  79. Simon I, Tenzen T, Reubinoff BE, Hillman D, McCarrey JR, Cedar H (1999) Asynchronous replication of imprinted genes is established in the gametes maintained during development. Nature 401:929–932PubMedCrossRefGoogle Scholar
  80. Singh N, Ebrahimi FAW, Gimelbrant AA, Ensminger AW, Tackett MR, Qi P, Gribnau J, Chess A (2003) Coordination of the random asynchronous replication of autosomal loci. Nat Genet 33:1–3CrossRefGoogle Scholar
  81. Sleutels F, Zwart R, Barlow DP (2002) The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415:810–813PubMedGoogle Scholar
  82. Sleutels F, Tjon G, Ludwig T, Barlow DP (2003) Imprinted silencing of Slc22a2 and Slc22a3 does not need transcriptional overlap between Igf2r and Air. EMBO J 22:3696–3704PubMedCrossRefGoogle Scholar
  83. Smrzka OW, Fae I, Stoger R, Kurzbauer R, Fischer GF, Henn T, Weith A, Barlow DP (1995) Conservation of a maternal-specific methylation signal at the human IGF2R locus. Hum Mol Genet 4:1945–1952PubMedCrossRefGoogle Scholar
  84. Stavropoulos N, Lu N, Lee JT (2001) A functional role for Tsix transcription in blocking Xist RNA accumulation but not in X-chromosome choice. Proc Natl Acad Sci USA 98:10232–10237PubMedCrossRefGoogle Scholar
  85. Stoger R, Kubicka P, Liu CG, Kafri T, Razin A, Cedar H, Barlow DP (1993) Maternal specific methylation of imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell 73:61–71PubMedCrossRefGoogle Scholar
  86. Sun BK, Deaton AM, Lee JT (2006) A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol Cell 21:617–628PubMedCrossRefGoogle Scholar
  87. Terranova R, Yokobayashi S, Stadler MB, Otte AP, van Lohuizen M, Orkin SH, Peters AH (2008) Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev Cell 15:668–679PubMedCrossRefGoogle Scholar
  88. Thakur N, Tiwari VK, Thomassin H, Pandey RR, Kanduri M, Göndör A, Grange T, Ohlsson R, Kanduri C (2004) An antisense RNA regulates the bidirectional silencing property of the Kcnq1 imprinting control region. Mol Cell Biol 24:7855–7862PubMedCrossRefGoogle Scholar
  89. Tsai CL, Rowntree RK, Cohen DE, Lee JT (2008) Higher order chromatin structure at the X-inactivation center via looping DNA. Dev Biol 319:416–425PubMedCrossRefGoogle Scholar
  90. Umlauf D, Goto Y, Cao R, Cerqueira F, Wagschal A, Zhang Y, Feil R (2004) Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat Genet 36:1296–1300PubMedCrossRefGoogle Scholar
  91. Verdel A, Moazed D (2005) RNAi-directed assembly of heterochromatin in fission yeast. FEBS Lett 579:5872–5878PubMedCrossRefGoogle Scholar
  92. Vu TH, Li T, Hoffman AR (2004) Promoter-restricted histone code, not the differentially methylated DNA regions or antisense transcripts, marks the imprinting status of IGF2R in human and mouse. Hum Mol Genet 13:2233–2245PubMedCrossRefGoogle Scholar
  93. Wassenegger M (2005) The role of the RNAi machinery in heterochromatin formation. Cell 122:13–16PubMedCrossRefGoogle Scholar
  94. Weksberg R, Shen DR, Fei YL, Song QL, Squire J (1993) Disruption of insulin-like growth factor 2 imprinting in Beckwith–Wiedemann syndrome. Nat Genet 5:143–150PubMedCrossRefGoogle Scholar
  95. Wutz A, Jaenisch R (2000) A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol Cell 5:695–705PubMedCrossRefGoogle Scholar
  96. Wutz A, Rasmussen TP, Jaenisch R (2002) Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 30:167–174PubMedCrossRefGoogle Scholar
  97. Xu N, Tsai CL, Lee JT (2006) Transient homologous chromosome pairing marks the onset of X inactivation. Science 311:1149–1152PubMedCrossRefGoogle Scholar
  98. Xu N, Donohoe ME, Silva SS, Lee JT (2007) Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein. Nat Genet 39:1390–1396PubMedCrossRefGoogle Scholar
  99. Yamasaki Y, Kayashima T, Soejima H, Kinoshita A, Yoshiura K, Matsumoto N, Ohta T, Urano T, Masuzaki H, Ishimaru T, Mukai T, Niikawa N, Kishino T (2005) Neuron-specific relaxation of Igf2r imprinting is associated with neuron-specific histone modifications and lack of its antisense transcript Air. Hum Mol Genet 14:2511–2520PubMedCrossRefGoogle Scholar
  100. Zhang LF, Huynh KD, Lee JT (2007) Perinucleolar targeting of the inactive X during S phase: evidence for a role in the maintenance of silencing. Cell 129:693–706PubMedCrossRefGoogle Scholar
  101. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322:750–756PubMedCrossRefGoogle Scholar

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© Springer-Verlag 2009

Authors and Affiliations

  • Irina S. Zakharova
    • 1
  • Alexander I. Shevchenko
    • 1
  • Suren M. Zakian
    • 1
    • 2
    Email author
  1. 1.Siberian Department, Institute of Cytology and GeneticsRussian Academy of SciencesNovosibirskRussia
  2. 2.Institute of Cytology and GeneticsNovosibirskRussia

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