Skip to main content
SpringerLink
Log in

How Many Non-coding RNAs Does It Take to Compensate Male/Female Genetic Imbalance?

  • Chapter
  • First Online:
Non-coding RNA and the Reproductive System

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 886))

Abstract

Genetic sex determination in mammals relies on dimorphic sex chromosomes that confer phenotypic/physiologic differences between males and females. In this heterogametic system, X and Y chromosomes diverged from an ancestral pair of autosomes, creating a genetic disequilibrium between XX females and XY males. Dosage compensation mechanisms alleviate intrinsic gene dosage imbalance, leading to equal expression levels of most X-linked genes in the two sexes. In therian mammals, this is achieved through inactivation of one of the two X chromosomes in females. Failure to undergo X-chromosome inactivation (XCI) results in developmental arrest and death. Although fundamental for survival, a surprising loose conservation in the mechanisms to achieve XCI during development in therian lineage has been, and continues, to be uncovered. XCI involves the concerted action of non-coding RNAs (ncRNAs), including the well-known Xist RNA, and has thus become a classical paradigm to study the mode of action of this particular class of transcripts. In this chapter, we will describe the processes coping with sex chromosome genetic imbalance and how ncRNAs underlie dosage compensation mechanisms and influence male-female differences in mammals. Moreover, we will discuss how ncRNAs have been tinkered with during therian evolution to adapt XCI mechanistic to species-specific constraints.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agrelo R, Souabni A, Novatchkova M, Haslinger C, Leeb M, Komnenovic V, Kishimoto H, Gresh L, Kohwi-Shigematsu T, Kenner L, Wutz A (2009) SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev Cell 16(4):507–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al Nadaf S, Waters PD, Koina E, Deakin JE, Jordan KS, Graves JA (2010) Activity map of the tammar X chromosome shows that marsupial X inactivation is incomplete and escape is stochastic. Genome Biol 11(12):R122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anguera MC, Ma W, Clift D, Namekawa S, Kelleher RJ 3rd, Lee JT (2011) Tsx produces a long noncoding RNA and has general functions in the germline, stem cells, and brain. PLoS Genet 7(9):e1002248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Augui S, Filion GJ, Huart 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(5856):1632–1636

    Article  CAS  PubMed  Google Scholar 

  • Augui S, Nora EP, Heard E (2011) Regulation of X-chromosome inactivation by the X-inactivation centre. Nat Rev Genet 12(6):429–442

    Article  CAS  PubMed  Google Scholar 

  • Barakat TS, Gunhanlar N, Pardo CG, Achame EM, Ghazvini M, Boers R, Kenter A, Rentmeester E, Grootegoed JA, Gribnau J (2011) RNF12 activates Xist and is essential for X chromosome inactivation. PLoS Genet 7(1):e1002001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barr ML, Bertram EG (1949) A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 163(4148):676

    Article  CAS  PubMed  Google Scholar 

  • Barr H, Hermann A, Berger J, Tsai HH, Adie K, Prokhortchouk A, Hendrich B, Bird A (2007) Mbd2 contributes to DNA methylation-directed repression of the Xist gene. Mol Cell Biol 27(10):3750–3757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barton SC, Surani MA, Norris ML (1984) Role of paternal and maternal genomes in mouse development. Nature 311(5984):374–376

    Article  CAS  PubMed  Google Scholar 

  • Beard C, Li E, Jaenisch R (1995) Loss of methylation activates Xist in somatic but not in embryonic cells. Genes Dev 9(19):2325–2334

    Article  CAS  PubMed  Google Scholar 

  • Beletskii A, Hong YK, Pehrson J, Egholm M, Strauss WM (2001) PNA interference mapping demonstrates functional domains in the noncoding RNA Xist. Proc Natl Acad Sci U S A 98(16):9215–9220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berletch JB, Yang F, Disteche CM (2010) Escape from X inactivation in mice and humans. Genome Biol 11(6):213

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Borsani G, Tonlorenzi R, Simmler MC, Dandolo L, Arnaud D, Capra V, Grompe M, Pizzuti A, Muzny D, Lawrence C, Willard HF, Avner P, Ballabio A (1991) Characterization of a murine gene expressed from the inactive X chromosome. Nature 351(6324):325–329

    Article  CAS  PubMed  Google Scholar 

  • Brockdorff N, Ashworth A, Kay GF, Cooper P, Smith S, McCabe VM, Norris DP, Penny GD, Patel D, Rastan S (1991) Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 351(6324):329–331

    Article  CAS  PubMed  Google Scholar 

  • Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, Swift S, Rastan S (1992) The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 71(3):515–526

    Article  CAS  PubMed  Google Scholar 

  • Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448(7150):191–195

    Article  CAS  PubMed  Google Scholar 

  • Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HF (1991a) A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349(6304):38–44

    Article  CAS  PubMed  Google Scholar 

  • Brown CJ, Lafreniere RG, Powers VE, Sebastio G, Ballabio A, Pettigrew AL, Ledbetter DH, Levy E, Craig IW, Willard HF (1991b) Localization of the X inactivation centre on the human X chromosome in Xq13. Nature 349(6304):82–84

    Article  CAS  PubMed  Google Scholar 

  • Brown CJ, Hendrich BD, Rupert JL, Lafreniere RG, Xing Y, Lawrence J, Willard HF (1992) The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71(3):527–542

    Article  CAS  PubMed  Google Scholar 

  • Burgoyne PS, Thornhill AR, Boudrean SK, Darling SM, Bishop CE, Evans EP (1995) The genetic basis of XX-XY differences present before gonadal sex differentiation in the mouse. Philos Trans R Soc Lond B Biol Sci 350(1333):253–260, discussion 260–251

    Article  CAS  PubMed  Google Scholar 

  • Calabrese JM, Sun W, Song L, Mugford JW, Williams L, Yee D, Starmer J, Mieczkowski P, Crawford GE, Magnuson T (2012) Site-specific silencing of regulatory elements as a mechanism of X inactivation. Cell 151(5):951–963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(16):2223–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, McClusky R, Itoh Y, Reue K, Arnold AP (2013) X and Y chromosome complement influence adiposity and metabolism in mice. Endocrinology 154(3):1092–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chureau C, Prissette M, Bourdet A, Barbe V, Cattolico L, Jones L, Eggen A, Avner P, Duret L (2002) Comparative sequence analysis of the X-inactivation center region in mouse, human, and bovine. Genome Res 12(6):894–908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chureau C, Chantalat S, Romito A, Galvani A, Duret L, Avner P, Rougeulle C (2010) Ftx is a non-coding RNA which affects Xist expression and chromatin structure within the X-inactivation center region. Hum Mol Genet 20(4):705–718

    Article  PubMed  CAS  Google Scholar 

  • Chuva de Sousa Lopes SM, Hayashi K, Shovlin TC, Mifsud W, Surani MA, McLaren A (2008) X chromosome activity in mouse XX primordial germ cells. PLoS Genet 4(2):e30

    Article  PubMed  PubMed Central  Google Scholar 

  • Clemson CM, McNeil JA, Willard HF, Lawrence JB (1996) XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol 132(3):259–275

    Article  CAS  PubMed  Google Scholar 

  • Cohen DE, Davidow LS, Erwin JA, Xu N, Warshawsky D, Lee JT (2007) The DXPas34 repeat regulates random and imprinted X inactivation. Dev Cell 12(1):57–71

    Article  CAS  PubMed  Google Scholar 

  • de Napoles M, Mermoud JE, Wakao R, Tang YA, Endoh M, Appanah R, Nesterova TB, Silva J, Otte AP, Vidal M, Koseki H, Brockdorff N (2004) Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell 7(5):663–676

    Article  PubMed  Google Scholar 

  • De Vries GJ, Rissman EF, Simerly RB, Yang LY, Scordalakes EM, Auger CJ, Swain A, Lovell-Badge R, Burgoyne PS, Arnold AP (2002) A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J Neurosci 22(20):9005–9014

    PubMed  Google Scholar 

  • Deng X, Hiatt JB, Nguyen DK, Ercan S, Sturgill D, Hillier LW, Schlesinger F, Davis CA, Reinke VJ, Gingeras TR, Shendure J, Waterston RH, Oliver B, Lieb JD, Disteche CM (2011) Evidence for compensatory upregulation of expressed X-linked genes in mammals, caenorhabditis elegans and drosophila melanogaster. Nat Genet 43(12):1179–1185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dewing P, Shi T, Horvath S, Vilain E (2003) Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Brain Res Mol Brain Res 118(1–2):82–90

    Article  CAS  PubMed  Google Scholar 

  • Dindot SV, Kent KC, Evers B, Loskutoff N, Womack J, Piedrahita JA (2004) Conservation of genomic imprinting at the XIST, IGF2, and GTL2 loci in the bovine. Mamm Genome 15(12):966–974

    Article  CAS  PubMed  Google Scholar 

  • Dupont C, Gribnau J (2013) Different flavors of X-chromosome inactivation in mammals. Curr Opin Cell Biol 25(3):314–321

    Article  CAS  PubMed  Google Scholar 

  • Duret L, Chureau C, Samain S, Weissenbach J, Avner P (2006) The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312(5780):1653–1655

    Article  CAS  PubMed  Google Scholar 

  • Elisaphenko EA, Kolesnikov NN, Shevchenko AI, Rogozin IB, Nesterova TB, Brockdorff N, Zakian SM (2008) A dual origin of the Xist gene from a protein-coding gene and a set of transposable elements. PLoS One 3(6):e2521

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K, Surka C, Kadri S, Xing J, Goren A, Lander ES, Plath K, Guttman M (2013) The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341(6147):1237973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gontan C, Achame EM, Demmers J, Barakat TS, Rentmeester E, van IW, Grootegoed JA, Gribnau J (2012) RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nature 485(7398):386–390

    Article  CAS  PubMed  Google Scholar 

  • Grant J, Mahadevaiah SK, Khil P, Sangrithi MN, Royo H, Duckworth J, McCarrey JR, VandeBerg JL, Renfree MB, Taylor W, Elgar G, Camerini-Otero RD, Gilchrist MJ, Turner JM (2012) Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation. Nature 487(7406):254–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graves JA (2010) Review: sex chromosome evolution and the expression of sex-specific genes in the placenta. Placenta 31(Suppl):S27–S32

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Nakagawa S (2010) The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev Cell 19(3):469–476

    Article  CAS  PubMed  Google Scholar 

  • Heard E, Rougeulle C, Arnaud D, Avner P, Allis CD, Spector DL (2001) Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell 107(6):727–738

    Article  CAS  PubMed  Google Scholar 

  • Hendriksen PJ, Hoogerbrugge JW, Themmen AP, Koken MH, Hoeijmakers JH, Oostra BA, van der Lende T, Grootegoed JA (1995) Postmeiotic transcription of X and Y chromosomal genes during spermatogenesis in the mouse. Dev Biol 170(2):730–733

    Article  CAS  PubMed  Google Scholar 

  • Hosler BA, LaRosa GJ, Grippo JF, Gudas LJ (1989) Expression of REX-1, a gene containing zinc finger motifs, is rapidly reduced by retinoic acid in F9 teratocarcinoma cells. Mol Cell Biol 9(12):5623–5629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon Y, Lee JT (2011) YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146(1):119–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston CM, Newall AE, Brockdorff N, Nesterova TB (2002) Enox, a novel gene that maps 10 kb upstream of Xist and partially escapes X inactivation. Genomics 80(2):236–244

    Article  CAS  PubMed  Google Scholar 

  • Jonkers I, Barakat TS, Achame EM, Monkhorst K, Kenter A, Rentmeester E, Grosveld F, Grootegoed JA, Gribnau J (2009) RNF12 is an X-Encoded dose-dependent activator of X chromosome inactivation. Cell 139(5):999–1011

    Article  CAS  PubMed  Google Scholar 

  • Koina E, Chaumeil J, Greaves IK, Tremethick DJ, Graves JA (2009) Specific patterns of histone marks accompany X chromosome inactivation in a marsupial. Chromosome Res 17(1):115–126

    Article  CAS  PubMed  Google Scholar 

  • Lee JT (2000) Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell 103(1):17–27

    Article  CAS  PubMed  Google Scholar 

  • Lee JT, Lu N (1999) Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99(1):47–57

    Article  CAS  PubMed  Google Scholar 

  • Lee JT, Davidow LS, Warshawsky D (1999) Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet 21(4):400–404

    Article  CAS  PubMed  Google Scholar 

  • Luikenhuis S, Wutz A, Jaenisch R (2001) Antisense transcription through the Xist locus mediates Tsix function in embryonic stem cells. Mol Cell Biol 21(24):8512–8520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372–373

    Article  CAS  PubMed  Google Scholar 

  • Mahadevaiah SK, Royo H, VandeBerg JL, McCarrey JR, Mackay S, Turner JM (2009) Key features of the X inactivation process are conserved between marsupials and eutherians. Curr Biol 19(17):1478–1484

    Article  CAS  PubMed  Google Scholar 

  • Mak W, Nesterova TB, de Napoles M, Appanah R, Yamanaka S, Otte AP, Brockdorff N (2004) Reactivation of the paternal X chromosome in early mouse embryos. Science 303(5658):666–669

    Article  CAS  PubMed  Google Scholar 

  • Makhlouf M, Rougeulle C (2011) Linking X chromosome inactivation to pluripotency: necessity or fate? Trends Mol Med 17(6):329–336

    Article  PubMed  Google Scholar 

  • Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R (1997) Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev 11(2):156–166

    Article  CAS  PubMed  Google Scholar 

  • Masui O, Bonnet I, Le Baccon P, Brito I, Pollex T, Murphy N, Hupe P, Barillot E, Belmont AS, Heard E (2011) Live-cell chromosome dynamics and outcome of X chromosome pairing events during ES cell differentiation. Cell 145(3):447–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGrath J, Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37(1):179–183

    Article  CAS  PubMed  Google Scholar 

  • Migeon BR, Chowdhury AK, Dunston JA, McIntosh I (2001) Identification of TSIX, encoding an RNA antisense to human XIST, reveals differences from its murine counterpart: implications for X inactivation. Am J Hum Genet 69(5):951–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minkovsky A, Barakat TS, Sellami N, Chin MH, Gunhanlar N, Gribnau J, Plath K (2013) The pluripotency factor-bound intron 1 of Xist is dispensable for X chromosome inactivation and reactivation in vitro and in vivo. Cell Rep 3(3):905–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monk M, Harper MI (1979) Sequential X chromosome inactivation coupled with cellular differentiation in early mouse embryos. Nature 281(5729):311–313

    Article  CAS  PubMed  Google Scholar 

  • Moreira de Mello JC, de Araujo ES, Stabellini R, Fraga AM, de Souza JE, Sumita DR, Camargo AA, Pereira LV (2010) Random X inactivation and extensive mosaicism in human placenta revealed by analysis of allele-specific gene expression along the X chromosome. PLoS One 5(6):e10947

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mueller JL, Mahadevaiah SK, Park PJ, Warburton PE, Page DC, Turner JM (2008) The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 40(6):794–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(12):1474–1484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(20):2787–2792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navarro P, Chambers I, Karwacki-Neisius V, Chureau C, Morey C, Rougeulle C, Avner P (2008) Molecular coupling of Xist regulation and pluripotency. Science 321(5896):1693–1695

    Article  CAS  PubMed  Google Scholar 

  • Navarro P, Oldfield A, Legoupi J, Festuccia N, Dubois A, Attia M, Schoorlemmer J, Rougeulle C, Chambers I, Avner P (2010) Molecular coupling of Tsix regulation and pluripotency. Nature 468(7322):457–460

    Article  CAS  PubMed  Google Scholar 

  • Nechanitzky R, Davila A, Savarese F, Fietze S, Grosschedl R (2012) Satb1 and Satb2 are dispensable for X chromosome inactivation in mice. Dev Cell 23(4):866–871

    Article  CAS  PubMed  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(7398):381–385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohhata T, Hoki Y, Sasaki H, Sado T (2006) Tsix-deficient X chromosome does not undergo inactivation in the embryonic lineage in males: implications for Tsix-independent silencing of Xist. Cytogenet Genome Res 113(1–4):345–349

    Article  CAS  PubMed  Google Scholar 

  • Ohhata T, Hoki Y, Sasaki H, Sado T (2008) Crucial role of antisense transcription across the Xist promoter in Tsix-mediated Xist chromatin modification. Development 135(2):227–235

    Article  CAS  PubMed  Google Scholar 

  • Ohno S, Kaplan WD, Kinosita R (1959) Formation of the sex chromatin by a single X-chromosome in liver cells of rattus norvegicus. Exp Cell Res 18:415–418

    Article  CAS  PubMed  Google Scholar 

  • Okamoto I, Otte AP, Allis CD, Reinberg D, Heard E (2004) Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303(5658):644–649

    Article  CAS  PubMed  Google Scholar 

  • Okamoto I, Patrat C, Thepot D, Peynot N, Fauque P, Daniel N, Diabangouaya P, Wolf JP, Renard JP, Duranthon V, Heard E (2011) Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 472(7343):370–374

    Article  CAS  PubMed  Google Scholar 

  • Panning B, Jaenisch R (1996) DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes Dev 10(16):1991–2002

    Article  CAS  PubMed  Google Scholar 

  • Pelton TA, Sharma S, Schulz TC, Rathjen J, Rathjen PD (2002) Transient pluripotent cell populations during primitive ectoderm formation: correlation of in vivo and in vitro pluripotent cell development. J Cell Sci 115(Pt 2):329–339

    CAS  PubMed  Google Scholar 

  • Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N (1996) Requirement for Xist in X chromosome inactivation. Nature 379(6561):131–137

    Article  CAS  PubMed  Google Scholar 

  • Peters AH, Mermoud JE, O’Carroll D, Pagani M, Schweizer D, Brockdorff N, Jenuwein T (2002) Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat Genet 30(1):77–80

    Article  CAS  PubMed  Google Scholar 

  • Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300(5616):131–135

    Article  CAS  PubMed  Google Scholar 

  • Pullirsch D, Hartel R, Kishimoto H, Leeb M, Steiner G, Wutz A (2010) The trithorax group protein Ash2l and Saf-A are recruited to the inactive X chromosome at the onset of stable X inactivation. Development 137(6):935–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasmussen TP, Mastrangelo MA, Eden A, Pehrson JR, Jaenisch R (2000) Dynamic relocalization of histone MacroH2A1 from centrosomes to inactive X chromosomes during X inactivation. J Cell Biol 150(5):1189–1198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rastan S (1982) Timing of X-chromosome inactivation in post-implantation mouse embryos. J Embryol Exp Morphol 71:11–24

    CAS  PubMed  Google Scholar 

  • Rastan S (1983) Non-random X-chromosome inactivation in mouse X-autosome translocation embryos – location of the inactivation centre. J Embryol Exp Morphol 78:1–22

    CAS  PubMed  Google Scholar 

  • Rastan S, Brown SD (1990) The search for the mouse X-chromosome inactivation centre. Genet Res 56(2–3):99–106

    Article  CAS  PubMed  Google Scholar 

  • Ray PF, Winston RM, Handyside AH (1997) XIST expression from the maternal X chromosome in human male preimplantation embryos at the blastocyst stage. Hum Mol Genet 6(8):1323–1327

    Article  CAS  PubMed  Google Scholar 

  • Rogers MB, Hosler BA, Gudas LJ (1991) Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development 113(3):815–824

    CAS  PubMed  Google Scholar 

  • Rougeulle C, Chaumeil J, Sarma K, Allis CD, Reinberg D, Avner P, Heard E (2004) Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol Cell Biol 24(12):5475–5484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sado T, Wang Z, Sasaki H, Li E (2001) Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development 128(8):1275–1286

    CAS  PubMed  Google Scholar 

  • Sado T, Li E, Sasaki H (2002) Effect of Tsix disruption on Xist expression in male ES cells. Cytogenet Genome Res 99(1–4):115–118

    CAS  PubMed  Google Scholar 

  • Sado T, Okano M, Li E, Sasaki H (2004) De novo DNA methylation is dispensable for the initiation and propagation of X chromosome inactivation. Development 131(5):975–982

    Article  CAS  PubMed  Google Scholar 

  • Sarma K, Levasseur P, Aristarkhov A, Lee JT (2010) Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proc Natl Acad Sci U S A 107(51):22196–22201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savarese F, Flahndorfer K, Jaenisch R, Busslinger M, Wutz A (2006) Hematopoietic precursor cells transiently reestablish permissiveness for X inactivation. Mol Cell Biol 26(19):7167–7177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao C, Takagi N (1990) An extra maternally derived X chromosome is deleterious to early mouse development. Development 110(3):969–975

    CAS  PubMed  Google Scholar 

  • Shibata S, Lee JT (2004) Tsix transcription- versus RNA-based mechanisms in Xist repression and epigenetic choice. Curr Biol 14(19):1747–1754

    Article  CAS  PubMed  Google Scholar 

  • Shin J, Bossenz M, Chung Y, Ma H, Byron M, Taniguchi-Ishigaki N, Zhu X, Jiao B, Hall LL, Green MR, Jones SN, Hermans-Borgmeyer I, Lawrence JB, Bach I (2010) Maternal Rnf12/RLIM is required for imprinted X-chromosome inactivation in mice. Nature 467(7318):977–981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simmler MC, Cunningham DB, Clerc P, Vermat T, Caudron B, Cruaud C, Pawlak A, Szpirer C, Weissenbach J, Claverie JM, Avner P (1996) A 94 kb genomic sequence 3′ to the murine Xist gene reveals an AT rich region containing a new testis specific gene Tsx. Hum Mol Genet 5(11):1713–1726

    Article  CAS  PubMed  Google Scholar 

  • Solari AJ (1974) The behavior of the XY pair in mammals. Int Rev Cytol 38:273–317

    Article  CAS  PubMed  Google Scholar 

  • Spencer RJ, del Rosario BC, Pinter SF, Lessing D, Sadreyev RI, Lee JT (2011) A boundary element between Tsix and Xist binds the chromatin insulator Ctcf and contributes to initiation of X-chromosome inactivation. Genetics 189(2):441–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stavropoulos N, Rowntree RK, Lee JT (2005) Identification of developmentally specific enhancers for Tsix in the regulation of X chromosome inactivation. Mol Cell Biol 25(7):2757–2769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugimoto M, Abe K (2007) X chromosome reactivation initiates in nascent primordial germ cells in mice. PLoS Genet 3(7):e116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun BK, Deaton AM, Lee JT (2006) A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol Cell 21(5):617–628

    Article  CAS  PubMed  Google Scholar 

  • Sun S, Fukue Y, Nolen L, Sadreyev R, Lee JT (2011) Characterization of Xpr (Xpct) reveals instability but no effects on X-chromosome pairing or Xist expression. Transcription 1(1):46–56

    Article  CAS  Google Scholar 

  • Sun S, Del Rosario BC, Szanto A, Ogawa Y, Jeon Y, Lee JT (2013) Jpx RNA activates Xist by evicting CTCF. Cell 153(7):1537–1551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi N, Sasaki M (1975) Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256(5519):640–642

    Article  CAS  PubMed  Google Scholar 

  • Takagi N, Sugawara O, Sasaki M (1982) Regional and temporal changes in the pattern of X-chromosome replication during the early post-implantation development of the female mouse. Chromosoma 85(2):275–286

    Article  CAS  PubMed  Google Scholar 

  • Tam PP, Zhou SX, Tan SS (1994) X-chromosome activity of the mouse primordial germ cells revealed by the expression of an X-linked lacZ transgene. Development 120(10):2925–2932

    CAS  PubMed  Google Scholar 

  • Tan SS, Williams EA, Tam PP (1993) X-chromosome inactivation occurs at different times in different tissues of the post-implantation mouse embryo. Nat Genet 3(2):170–174

    Article  CAS  PubMed  Google Scholar 

  • Tian D, Sun S, Lee JT (2010) The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143(3):390–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner JM (2007) Meiotic sex chromosome inactivation. Development 134(10):1823–1831

    Article  CAS  PubMed  Google Scholar 

  • Turner JM, Mahadevaiah SK, Elliott DJ, Garchon HJ, Pehrson JR, Jaenisch R, Burgoyne PS (2002) Meiotic sex chromosome inactivation in male mice with targeted disruptions of Xist. J Cell Sci 115(Pt 21):4097–4105

    Article  CAS  PubMed  Google Scholar 

  • Vallot C, Huret C, Lesecque Y, Resch A, Oudrhiri N, Bennaceur-Griscelli A, Duret L, Rougeulle C (2013) XACT, a long noncoding transcript coating the active X chromosome in human pluripotent cells. Nat Genet 45(3):239–241

    Article  CAS  PubMed  Google Scholar 

  • Vigneau S, Augui S, Navarro P, Avner P, Clerc P (2006) An essential role for the DXPas34 tandem repeat and Tsix transcription in the counting process of X chromosome inactivation. Proc Natl Acad Sci U S A 103(19):7390–7395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wake N, Takagi N, Sasaki M (1976) Non-random inactivation of X chromosome in the rat yolk sac. Nature 262(5569):580–581

    Article  CAS  PubMed  Google Scholar 

  • Wutz A, Jaenisch R (2000) A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol Cell 5(4):695–705

    Article  CAS  PubMed  Google Scholar 

  • Wutz A, Rasmussen TP, Jaenisch R (2002) Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 30(2):167–174

    Article  CAS  PubMed  Google Scholar 

  • Yen ZC, Meyer IM, Karalic S, Brown CJ (2007) A cross-species comparison of X-chromosome inactivation in eutheria. Genomics 90(4):453–463

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. UMR7216 Epigenetics and Cell Fate, CNRS/Université Paris Diderot, 35 rue Hélène Brion, 75013, Paris, France

    Jean-François Ouimette & Claire Rougeulle

Authors
  1. Jean-François Ouimette
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claire Rougeulle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claire Rougeulle .

Editor information

Editors and Affiliations

  1. Department of Anatomy and Neuroscience, The University of Melbourne Department of Anatomy and Neuroscience, Parkville, Victoria, Australia

    Dagmar Wilhelm

  2. School of BioSciences, The University of Melbourne School of BioSciences, Melbourne, Victoria, Australia

    Pascal Bernard

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Ouimette, JF., Rougeulle, C. (2016). How Many Non-coding RNAs Does It Take to Compensate Male/Female Genetic Imbalance?. In: Wilhelm, D., Bernard, P. (eds) Non-coding RNA and the Reproductive System. Advances in Experimental Medicine and Biology, vol 886. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7417-8_3

Download citation

Publish with us

Policies and ethics

Search

Navigation