Skip to main content
Log in

Transcriptional modulation of entire chromosomes: dosage compensation

  • Review Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Dosage compensation is a regulatory system designed to equalize the transcription output of the genes of the sex chromosomes that are present in different doses in the sexes (X or Z chromosome, depending on the animal species involved). Different mechanisms of dosage compensation have evolved in different animal groups. In Drosophila males, a complex (male-specific lethal) associates with the X chromosome and enhances the activity of most X-linked genes by increasing the rate of RNAPII elongation. In Caenorhabditis, a complex (dosage compensation complex) that contains a number of proteins involved in condensing chromosomes decreases the level of transcription of both X chromosomes in the XX hermaphrodite. In mammals, dosage compensation is achieved by the inactivation, early during development, of most X-linked genes on one of the two X chromosomes in females. The mechanism involves the synthesis of an RNA (Tsix) that protects one of the two Xs from inactivation, and of another RNA (Xist) that coats the other X chromosome and recruits histone and DNA modifying enzymes. This review will focus on the current progress in understanding the dosage compensation mechanisms in the three taxa where it has been best studied at the molecular level: flies, round worms and mammals.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Albritton S. E., Kranz A. L., Rao P., Kramer M., Dieterich C. and Ercan S. 2014 Sex-biased gene expression and evolution of the X chromosome in nematodes. Genetics 197, 865–883.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Albritton S. E., Kranz A. L., Winterkorn L. H., Street L. A. and Ercan S. 2017 Cooperation between a hierarchical set of recruitment sites targets the X chromosome for dosage compensation. Elife. https://doi.org/10.7554/eLife.23645.

  • Alekseyenko A. A., Peng S., Larschan E., Gorchakov A. A., Lee O. K., Kharchenko P. et al. 2008 A sequence motif within chromatin entry sites directs MSL establishment on the Drosophila X chromosome. Cell 134, 599–609.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Almeida M., Pintacuda G., Masui O., Koseki Y., Gdula M., Cerase A. et al. 2017 PCGF3/5-PRC1 initiates Polycomb recruitment in X chromosome inactivation. Science 356, 1081–1084.

    Article  PubMed  CAS  Google Scholar 

  • Amrein H. and Axel R. 1997 Genes expressed in neurons of adult male Drosophila. Cell 88, 459–469.

    Article  PubMed  CAS  Google Scholar 

  • Bala Tannan N., Brahmachary M., Garg P., Alnefaie R., Watson C. T., Thomas N. S. and Sharp A. J. 2014 DNA methylation profiling in X;autosome translocations supports a role for L1 repeats in the spread of X chromosome inactivation. Hum. Mol. Genet. 23, 1224–1236.

    Article  CAS  Google Scholar 

  • Balaton B. P., Cotton A. M. and Brown C. J. 2015 Derivation of consensus inactivation status for X-linked genes from genome-wide studies. Biol. Sex Differ. https://doi.org/10.1186/s13293-015-0053-7.

  • Barr M. L. and Bertram E. G. 1949 A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 163, 676.

    Article  PubMed  CAS  Google Scholar 

  • Bell O., Schwaiger M., Oakeley E. J., Lienert F., Beisel C., Stadler M. B. et al. 2010 Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nat. Struct. Mol. Biol. 17, 894–900.

    Article  PubMed  CAS  Google Scholar 

  • Belote J. M. and Lucchesi J. C. 1980 Control of X chromosome transcription by the maleless gene in Drosophila. Nature 285, 573–575.

    Article  PubMed  CAS  Google Scholar 

  • Brejc K., Bian Q., Uzawa S., Wheeler B. S., Anderson E. C., King D. S. et al. 2017 Dynamic control of X chromosome conformation and repression by a histone H4K20 demethylase. Cell 171, 85–102.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Brown S. W. and Chandra H. S. 1973 Inactivation system of the mammalian X chromosome. Proc. Natl. Acad. Sci. USA 70, 195–199.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brown C. J. and Willard H. F. 1994 The human X-inactivation centre is not required for maintenance of X-chromosome inactivation. Nature 368, 154–156.

    Article  PubMed  CAS  Google Scholar 

  • Brown C. J., Ballabio A., Rupert J. L., Lafreniere R. G., Grompe M., Tonlorenzi R. et al. 1991 A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349, 38–44.

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee S. N. and Mukherjee A. S. 1971 Chromosomal basis of dosage compensation in Drosophila. Chromosoma 36, 46–59.

    Article  PubMed  CAS  Google Scholar 

  • Chen C. K., Blanco M., Jackson C., Aznauryan E., Ollikainen N., Surka C. et al. 2016 Xist recruits the X chromosome to the nuclear lamina to enable chromosome-wide silencing. Science 354, 468–472.

    Article  PubMed  CAS  Google Scholar 

  • Chu C., Zhang Q. C., da Rocha S. T., Flynn R. A., Bharadwaj M., Calabrese J. M. et al. 2015 Systematic discovery of Xist RNA binding proteins. Cell 161, 404–416.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Costanzi C. and Pehrson J. R. 1998 Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393, 599–601.

    Article  PubMed  CAS  Google Scholar 

  • Cotton A. M., Chen C. Y., Lam L. L., Wasserman W. W., Kobor M. S. and Brown C. 2014 Spread of X-chromosome inactivation into autosomal sequences: role for DNA elements, chromatin features and chromosomal domains. Hum. Mol. Genet. 23, 1211–1223.

    Article  PubMed  CAS  Google Scholar 

  • Crane E., Bian Q., McCord R. P., Lajoie B. R., Wheeler B. S., Ralston E. J. et al. 2015 Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523, 240–244.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Csankovszki G., McDonel P. and Meyer B. J. 2004 Recruitment and spreading of the C. elegans dosage compensation complex along X chromosomes. Science 303, 1182–1185.

    Article  PubMed  CAS  Google Scholar 

  • Cugusi S., Ramos E., Ling H., Yokoyama R., Luk K. M. and Lucchesi J. C. 2013 Topoisomerase II plays a role in dosage compensation in Drosophila. Transcription 4, 238–250.

    Article  PubMed  Google Scholar 

  • da Rocha S. T., Boeva V., Escamilla-Del-Arenal M., Ancelin K., Granier C., Matias N. R. et al. 2014 Jarid2 is implicated in the initial Xist-induced targeting of PRC2 to the inactive X Chromosome.Mol. Cell 53, 301–316.

    Article  PubMed  CAS  Google Scholar 

  • Davidson R. G., Nitowsky H. M. and Childs B. 1963 Demonstration of two populations of cells in the human female heterozygous for glucose-6-phosphate dehydrogenase variants. Proc. Natl. Acad. Sci. USA 50, 481–485.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dawes H. E., Berlin D. S., Lapidus D. M., Nusbaum C., Davis T. L. and Meyer B. J. 1999 Dosage compensation proteins targeted to X chromosomes by a determinant of hermaphrodite fate. Science 284, 1800–1804.

    Article  PubMed  CAS  Google Scholar 

  • Deng X., Berletch J. B., Ma W., Nguyen D. K., Hiatt J. B., Noble W. S. et al. 2013 Mammalian X upregulation is associated with enhanced ranscription initiation, RNA half-life, and MOF-mediated H4K16acetylation. Dev. Cell 25, 55–68.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • DiBartolomeis S. M., Tartof K. D. and Jackson F. R. 1992 A superfamily of Drosophila satellite related (SR) DNA repeats restricted to the X chromosome euchromatin. Nucleic Acids Res. 20, 1113–1116.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dunlap D., Yokoyama R., Ling H., Sun H. Y., McGill K., Cugusi S. et al. 2012 Distinct contributions of MSL complex subunits to the transcriptional enhancement responsible for dosage compensation in Drosophila. Nucleic Acids Res. 40, 11281–11291.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Engreitz J. M., Pandya-Jones A., McDonel P., Shishkin A., Sirokman K., Surka C. et al. 2013 The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341, 1237973.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ercan S., Giresi P. G., Whittle C. M., Zhang X., Green R. D. and Lieb J. D. 2007 X chromosome repression by localization of the C. elegans dosage compensation machinery to sites of transcription initiation. Nat. Genet. 39, 403–408.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ferrari F., Plachetka A., Alekseyenko A. A., Jung Y. L., Ozsolak F., Kharchenko P. V. et al. 2013 “Jump start and gain” model for dosage compensation in Drosophila based on direct sequencing of nascent transcripts. Cell Rep. 5, 629–636.

    Article  PubMed  CAS  Google Scholar 

  • Gendrel A. V. and Heard E. 2014 Noncoding RNAs and epigenetic mechanisms during X-chromosome inactivation. Annu. Rev. Cell. Dev. Biol. 30, 561–580.

    Article  PubMed  CAS  Google Scholar 

  • Grimaud C. and Becker P. B. 2009 The dosage compensation complex shapes the conformation of the X chromosome in Drosophila. Genes Dev. 23, 2490–2495.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gupta V., Parisi M., Sturgill D., Nuttall R., Doctolero M., Dudko O. K. et al. 2006 Global analysis of X-chromosome dosage compensation. J. Biol. 5, 3–25.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hilfiker A., Hilfiker-Kleiner D., Pannuti A. and Lucchesi J. C. 1997 Mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila. EMBO J. 16, 2054–2060.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hodgkin J. 1983 X chromosome dosage and gene expression in C. elegans: two unusual dumpy genes. Mol. Gen. Genet. 192, 452–458.

    Article  Google Scholar 

  • Ilik I. A., Quinn J. J., Georgiev P., Tavares-Cadete F., Maticzka D., Toscano S. et al. 2013 Tandem stem-loops in roX RNAs act together to mediate X chromosome dosage compensation in Drosophila. Mol. Cell 51, 156–173.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jeppesen P. and Turner B. M. 1993 The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74, 281–289.

    Article  PubMed  CAS  Google Scholar 

  • Jonkers I., Barakat T. S., Achame E. M., Monkhorst K., Kenter A., Rentmeester E. et al. 2009 RNF12 is an X-Encoded dose-dependent activator of X chromosome inactivation. Cell 139, 999–1011.

    Article  PubMed  CAS  Google Scholar 

  • Joshi S. S. and Meller V. H. 2017 Satellite repeats identify X chromatin for dosage compensation in Drosophila melanogaster males. Curr. Biol. 27, 1393–1402.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kennison J. A. 1981 The genetic and cytological organization of the Y chromosome of Drosophila melanogaster. Genetics 98, 529–548.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lakhotia S. C. and Mukherjee A. S. 1969 Chromosomal basis of dosage compensation in Drosophila: I. Cellular autonomy of hyperactivity of the male \(X\)-chromosome in salivary glands and sex differentiation. Genetics Res. 14, 137–150.

    Article  CAS  Google Scholar 

  • Lakhotia S. C. and Mukherjee A. S. 1970 Compensation in Drosophila. III. Early completion of replication by the male X –chromosome in male: further evidence and its implications. J. Cell Biol. 47, 18–33.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larschan E., Alekseyenko A. A., Gortchakov A. A., Peng S., Li B., Yang P. et al. 2007 MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism. Mol. Cell 28, 121–133.

    Article  PubMed  CAS  Google Scholar 

  • Larschan E., Bishop E. P., Kharchenko P. V., Core L. J., Lis J. T., Park P. J. et al. 2011 X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature 471, 115–118.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larschan E., Soruco M. M., Lee O. K., Peng S., Bishop E., Chery J. et al. 2012 Identification of chromatin-associated regulators of MSL complex targeting in Drosophila dosage compensation. PLoS Genet. 8, e1002830.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lau A. C., Nabeshima K. and Csankovszki G. 2014 The C. elegans dosage compensation complex mediates interphase X chromosome compaction. Epigenet. Chromatin 7, 31–46.

    Article  Google Scholar 

  • Lee J. T. and Lu N. 1999 Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99, 47–57.

    Article  PubMed  CAS  Google Scholar 

  • Lee C. G., Chang K. A., Kuroda M. I. and Hurwitz J. 1997 The NTPase/helicase activities of Drosophila maleless, an essential factor in dosage compensation. EMBO J. 16, 2671–2681.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li F., Schiemann A. H. and Scott M. J. 2008 Incorporation of the noncoding roX RNAs alters the chromatin-binding specificity of the Drosophila MSL1/MSL2 complex. Mol. Cell. Biol. 28, 1252–1264.

    Article  PubMed  CAS  Google Scholar 

  • Lucchesi J. C. 1978 Gene dosage compensation and the evolution of sex chromosomes. Science 202, 711–716.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Maenner S., Müller M., Fröhlich J., Langer D. and Becker P. B. 2013 ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Mol. Cell 51, 174–184.

    Article  PubMed  CAS  Google Scholar 

  • Marin R., Cortez D., Lamanna F., Pradeepal M. M., Leushkin E., Julien P. et al. 2017 Convergent origination of a Drosophila–like dosage compensation mechanism in a reptile lineage. Genome Res. 27, 1974–1987.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McDonel P., Jans J., Peterson B. K. and Meyer B. J. 2006 Clustered DNA motifs mark X chromosomes for repression by a dosage compensation complex. Nature 444, 614–618.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McHugh C. A., Chen C. K., Chow A., Surka C. F., Tran C, McDonel P. et al. 2015 The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521, 232–236.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meisel R. P., Malone J. H. and Clark A. G. 2012 Disentangling the relationship between sex-biased gene expression and X-linkage. Genome Res. 22, 1255–1265.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meller V. H., Wu K. H., Roman G., Kuroda M. I. and Davis R. L. 1997 roX1 RNA paints the X chromosome of male Drosophila and is regulated by the dosage compensation system. Cell 88, 445–457.

    Article  PubMed  CAS  Google Scholar 

  • Meneely P. M. and Wood W. B. 1984 An autosomal gene that affects X chromosome expression and sex determination in Caenorhabditis elegans. Genetics 106, 29–44.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Menon D. U., Coarfa C., Xiao W., Gunaratne P. H. and Meller V. H. 2014 siRNAs from an X-linked satellite repeat promote X-chromosome recognition in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 111, 16460–16465.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meyer B. J. and Casson L. P. 1986 Caenorhabditis elegans compensates for the difference in X chromosome dosage between the sexes by regulating transcript levels. Cell 47, 871–881.

    Article  PubMed  CAS  Google Scholar 

  • Migeon B. R., Beer M. A. and Bjornsson H. T. 2017 Embryonic loss of human females with partial trisomy 19 identifies region critical for the single active X. PLoS One 12, e0170403.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mukherjee A. S. and Beermann W. 1965 Synthesis of ribonucleic acid by the X-chromosome of Drosophila melnogaster and the problem of dosage compensation. Nature 207, 785–786.

    Article  PubMed  CAS  Google Scholar 

  • Muller H. J. 1932 Further studies on the nature and causes of gene mutations. Proc. 6th Int. Congr. Genet. 1, 213–255.

    Google Scholar 

  • Nesterova T. B., Johnston C. M., Appanah R., Newall A. E., Godwin J., Alexiou M. et al. 2003 Skewing X chromosome choice by modulating sense transcription across the Xist locus. Genes Dev. 17, 2177–2190.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nguyen D. K. and Disteche C. M. 2006 Dosage compensation of the active X chromosome in mammals. Nat. Genet. 38, 47–53.

    Article  PubMed  CAS  Google Scholar 

  • Norris D. P., Brockdorff N. and Rastan S. 1991 Methylation status of CpG-rich islands on active and inactive mouse X chromosomes. Mamm. Genome. 1, 78–83.

    Article  PubMed  CAS  Google Scholar 

  • Ogawa Y. and Lee J. T. 2003 Xite, X-inactivation intergenic transcription elements that regulate the probability of choice. Mol. Cell 11, 731–743.

    Article  PubMed  CAS  Google Scholar 

  • Ohno S. 1967 Sex chromosomes and sex-linked genes. Springer, Berlin.

    Book  Google Scholar 

  • Ohno S., Kaplan W. D. and 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  PubMed  CAS  Google Scholar 

  • Parisi M., Nuttall R., Naiman D., Bouffard G., Malley J., Andrews J. et al. 2003 Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299, 697–700.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Patil D. P., Chen C. K., Pickering B. F., Chow A., Jackson C., Guttman M. and Jaffrey S. R. 2016 m(6)A RNA methylation promotes XIST-mediated transcriptional repression. Nature 537, 369–373.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Prabhakaran M. and Kelley R. L. 2012 Mutations in the transcription elongation factor SPT5 disrupt a reporter for dosage compensation in Drosophila. PLoS Genet. 8, e1003073.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramírez F., Lingg T., Toscano S., Lam K. C., Georgiev P., Chung H. R. et al. 2015 High-affinity sites form an interaction network to facilitate spreading of the MSL complex across the X chromosome in Drosophila. Mol. Cell 60, 146–162.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rice W. R. 1984 Sex chromosomes and the evolution of sexual dimorphism. Evolution 38, 735–742.

    Article  PubMed  Google Scholar 

  • Rose G., Krzwinska E., Kim J., Revuelta L., Ferretti L. and Krizwiski J. 2016 Dosage compensation in the African malaria mosquito Anopheles gambiae. Genome Biol. Evol. 8, 411–425.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saifi G. M. and Chandra H. S. 1999 An apparent excess of sex- and reproduction-related genes on the human X chromosome. Proc. Biol. Sci. 266, 203–209.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sarma K., Cifuentes-Rojas C., Ergun A., Del Rosario A., Jeon Y., White F. et al. 2014 ATRX directs binding of PRC2 to Xist RNA and polycomb targets. Cell 159, 869–893.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sass G. L., Pannuti A. and Lucchesi J. C. 2003 Male-specific lethal complex of Drosophila targets activated regions of the X chromosome for chromatin remodeling. Proc. Natl. Acad. Sci. USA 100, 8287–8291.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schauer T., Ghavi-Helm Y., Sexton T., Albig C., Regnard C., Cavalli G. et al. 2017 Chromosome topology guides the Drosophila dosage compensation complex for target gene activation. EMBO Rep. e201744292.

  • Sharman G. B. 1971 Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 230, 231–232.

    Article  PubMed  CAS  Google Scholar 

  • Simon M. D., Pinter S. F., Fang R., Sarma K., Rutenberg-Schoenberg M., Bowman S. K. et al. 2013 High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature 504, 465–469.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith E. R., Pannuti A., Gu W., Steurnagel A., Cook R. G., Allis C. D. et al. 2000 The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol. Cell. Biol. 20, 312–318.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith E. R., Allis C. D. and Lucchesi J. C. 2001 Linking global histone acetylation to the transcription enhancement of X-chromosomal genes in Drosophila males. J. Biol. Chem. 276, 31483–31486.

    Article  PubMed  CAS  Google Scholar 

  • Soruco M. M., Chery J., Bishop E. P., Siggers T., Tolstorukov M. Y., Leydon A. R. et al. 2013 The CLAMP protein links the MSL complex to the X chromosome during Drosophila dosage compensation. Genes Dev. 27, 1551–1556.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Straub T., Grimaud C., Gilfillan G. D., Mitterweger A. and Becker P. B. 2008 The chromosomal high- affinity binding sites for the Drosophila dosage compensation complex. PLoS Genet. 4, e1000302.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Strukov Y. G., Sural T. H., Kuroda M. I. and Sedat J. W. 2011 Evidence of activity-specific, radial organization of mitotic chromosomes in Drosophila. PLoS Biol. 9, e1000574.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tian D., Sun S. and Lee J. T. 2010 The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143, 390–403.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ulianov S. V., Khrameeva E. E., Gavrilov A. A., Flyamer I. M., Kos P., Mikhaleva E. A. et al. 2016 Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains. Genome Res. 26, 70–84.

    Article  PubMed  PubMed Central  Google Scholar 

  • Urban J. A., Doherty C. A, Jordan W. T. 3rd, Bliss J. E., Feng J., Soruco M. M. et al. 2017 The essential Drosophila CLAMP protein differentially regulates non-coding roX RNAs in male and females. Chromosome Res. 25, 101–113.

    Article  PubMed  CAS  Google Scholar 

  • Villa R, Schauer T, Smialowski P, Straub T. and Becker P. B. 2016 PionX sites mark the X chromosome for dosage compensation.Nature 537, 244–248.

    Article  PubMed  CAS  Google Scholar 

  • Wang P. J., McCarrey J. R., Yang F. and Page D. C. 2001 An abundance of X-linked genes expressed in spermatogonia. Nat Genet. 27, 422–426.

    Article  PubMed  CAS  Google Scholar 

  • Waring G. L. and Pollack J. C. 1987 Cloning and characterization of a dispersed, multicopy, X chromosome sequence in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 84, 2843–2847.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu L., Zee B. M., Wang Y., Garcia B. A. and Dou Y. 2011 The RING finger protein MSL2 in the MOF complex is an E3 ubiquitin ligase for H2B K34 and is involved in crosstalk with H3 K4 and K79 methylation. Mol. Cell 43, 132–144.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang F., Deng X., Ma W., Berletch J. B., Rabaia N., Wei G. et al. 2015 The lncRNA Firre anchors the inactive X chromosome to the nucleolus by binding CTCF and maintains H3K27me3 methylation. Genome Biol. 16, 52–69.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng S., Villa R., Wang J., Feng Y., Wang J., Becker P. B. et al. 2014 Structural basis of X chromosome DNA recognition by the MSL2 CXC domain during Drosophila dosage compensation. Genes Dev. 28, 2652–2662.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zimmer F., Harrison P. W., Dessimoz C. and Mank J. E. 2016 Compensation of dosage–sensitive genes on the chicken Z chromosome. Genome Biol. 8, 1233–1242.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John C. Lucchesi.

Additional information

Corresponding editor: H. A. Ranganath.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lucchesi, J.C. Transcriptional modulation of entire chromosomes: dosage compensation. J Genet 97, 357–364 (2018). https://doi.org/10.1007/s12041-018-0919-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-018-0919-7

Keywords

Navigation