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Dosage compensation, the origin and the afterlife of sex chromosomes

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Abstract

Over the past 100 years Drosophila has been developed into an outstanding model system for the study of evolutionary processes. A fascinating aspect of evolution is the differentiation of sex chromosomes. Organisms with highly differentiated sex chromosomes, such as the mammalian X and Y, must compensate for the imbalance in gene dosage that this creates. The need to adjust the expression of sex-linked genes is a potent force driving the rise of regulatory mechanisms that act on an entire chromosome. This review will contrast the process of dosage compensation in Drosophila with the divergent strategies adopted by other model organisms. While the machinery of sex chromosome compensation is different in each instance, all share the ability to direct chromatin modifications to an entire chromosome. This review will also explore the idea that chromosome-targeting systems are sometimes adapted for other purposes. This appears the likely source of a chromosome-wide targeting system displayed by the Drosophila fourth chromosome.

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References

  • Adler DA, Rugarli EI, Lingenfelter PA et al. (1997) Evidence of evolutionary up-regulation of the single active X chromosome in mammals based on Clc4 expression levels in Mus spretus and Mus musculus. Proc Natl Acad Sci USA 94: 9244–9248.

    Article  PubMed  CAS  Google Scholar 

  • Akhtar A, Becker PB (2000) Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol Cell 5: 367–375.

    Article  PubMed  CAS  Google Scholar 

  • Akhtar A, Zink D, Becker PB (2000) Chromodomains are protein–RNA interaction modules. Nature 407: 405–409.

    Article  PubMed  CAS  Google Scholar 

  • Alekseyenko AA, Park PJ, Larschan E, Lai WR, Kuroda MI (2006) High resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively indentifies active genes on the male X chromosome. Genes Dev 20: 848–857.

    Article  PubMed  CAS  Google Scholar 

  • Andersen AA, Panning B (2003) Epigenetic regulation by non-coding RNAs. Curr Opin Cell Biol 15: 281–289.

    Article  PubMed  CAS  Google Scholar 

  • Ashburner M, Golic KG, Hawley RS (2005) Drosophila, A Laboratory Handbook. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.

    Google Scholar 

  • Bachtrog D (2003a) Adaptation shapes patterns of genome evolution on sexual and asexual chromosomes of Drosophila. Nat Genet 34: 215–219.

    Article  PubMed  CAS  Google Scholar 

  • Bachtrog D (2003b) Protein evolution and codon bias on the neo-sex chromosomes of Drosophila miranda. Genetics 165: 1221–1232.

    PubMed  CAS  Google Scholar 

  • Bachtrog D (2005) Sex chromosome evolution: molecular aspects of Y-chromosome degeneration in Drosophila. Genome Res 15: 1393–1401.

    Article  PubMed  CAS  Google Scholar 

  • Bai X, Alekseyenko AA, Kuroda MI (2004) Sequence-specific targeting of MSL complex regulates transcription of the roX RNA genes. EMBO J 23: 2853–2861.

    Article  PubMed  CAS  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 USA 97: 6634–6639.

    Article  PubMed  CAS  Google Scholar 

  • Baker BS (1989) Sex in flies: the splice of life. Nature 340: 521–524.

    Article  PubMed  CAS  Google Scholar 

  • Baker BS, Gorman M, Marin I (1994) Dosage compensation in Drosophila. Annu Rev Genet 28: 491–521.

    Article  PubMed  CAS  Google Scholar 

  • Beckmann K, Grskovic M, Gebauer F, Hentze MW (2005) A dual inhibitory mechanism restricts msl2 translation for dosage compensation in Drosophila. Cell 122: 529–540.

    Article  PubMed  CAS  Google Scholar 

  • Belote JM (1983) Male-specific lethal mutations of Drosophila melanogaster. II. parameters of gene action during male development. Genetics 105: 881–896.

    PubMed  Google Scholar 

  • Birchler JA, Pal-Bhadra M, Bhadra U (2003) Dosage dependent gene regulation and the compensation of the X chromosome in Drosophila males. Genetica 117: 179–190.

    Article  PubMed  CAS  Google Scholar 

  • Bone JR, Kuroda MI (1996) Dosage compensation regulatory proteins and the evolution of sex chromosomes in Drosophila. Genetics 144: 705–713.

    PubMed  CAS  Google Scholar 

  • Bone JR, Lavender J, Richman R, Palmer MJ, Turner BM, Kuroda MI (1994) Acetylated histone H4 on the male X chromosome is associated with dosage compensation in Drosophila. Genes Dev 8: 96–104.

    PubMed  CAS  Google Scholar 

  • Bridges CB (1925) Sex in relation to chromosomes and genes. Am Nat 59: 127–137.

    Article  Google Scholar 

  • Bull JJ (1983) Evolution of Sex Determining Mechanisms. Menlo Park, California: Benjamin/Cummings.

    Google Scholar 

  • Buscaino A, Kocher T, Kind JH et al. (2003) MOF-regulated acetylation of MSL3 in the Drosophila dosage compensation complex. Mol Cell 11: 1265–1277.

    Article  PubMed  CAS  Google Scholar 

  • Carvalho AB (2002) Origin and evolution of the Drosophila Y chromosome. Curr Opin Genet Dev 12: 664–668.

    Article  PubMed  CAS  Google Scholar 

  • Carvalho AB, Lazzaro BP, Clark AG (2000) Y chromosome fetility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides. Proc Natl Acad Sci USA 97: 13239–13244.

    Article  PubMed  CAS  Google Scholar 

  • Chadwick BP, Willard HF (2003) Barring gene expression after XIST: maintaining facultative heterochromatin on the inactive X. Semin Cell Dev Biol 14: 359–367.

    Article  PubMed  CAS  Google Scholar 

  • Cline TW (1984) Autoregulation functioning of a Drosophila gene product that establishes and maintains the sexually determined state. Genetics 107: 231–277.

    PubMed  CAS  Google Scholar 

  • Cline TW, Meyer BJ (1996) Vive la difference: males vs females in flies vs worms. Annu Rev Genet 30: 637–702.

    Article  PubMed  CAS  Google Scholar 

  • Copps K, Richman R, Lyman LM, Chang KA, Rampersad-Ammons J, Kuroda MI (1998) Complex formation by the Drosophila MSL proteins: role of the MSL2 RING finger in protein complex assembly. EMBO J 17: 5409–5417.

    Article  PubMed  CAS  Google Scholar 

  • Csankovszki G, McDonel P, Meyer BJ (2004) Recruitment and spreading of the C. elegans dosage compensation complex along X chromosomes. Science 303: 182–185.

    Article  CAS  Google Scholar 

  • Dahlsveen IK, Gilfillan GD, Shelest VI, Lamm R, Becker PB (2006) Targeting determinants of dosage compensation in Drosophila. PLoS Genet 2: e5.

    Article  PubMed  CAS  Google Scholar 

  • Demakova OV, Kotlikova IV, Gordadze PR, Alekseyenko AA, Kuroda MI, Zhimulev IF (2003) The MSL complex levels are critical for its correct targeting to the chromosomes in Drosophila melanogaster. Chromosoma 112: 103–115.

    Article  PubMed  CAS  Google Scholar 

  • Ebert A, Schotta G, Lein S et al. (2004) Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18: 2973–2983.

    Article  PubMed  CAS  Google Scholar 

  • Eisen A, Utley RT, Nourani A et al. (2001) The yeast NuA4 and Drosophila MSL complexes contain homologous subunits important for transcription regulation. J Biol Chem 276: 3484–3491.

    Article  PubMed  CAS  Google Scholar 

  • Fagegaltier D, Baker BS (2004) X chromosome sites autonomously recruit the dosage compensation complex in Drosophila males. PLoS Biol 2: e341.

    Article  PubMed  CAS  Google Scholar 

  • Fitzsimons HL, Henry RA, Scott MJ (1999) Development of an insulated reporter system to search for cis-acting DNA sequences required for dosage compensation in Drosophila. Genetica 105: 215–226.

    Article  PubMed  CAS  Google Scholar 

  • Fung S-TC, Gowen JW (1960) Role of autosome-IV in Drosophila melanogaster sex balance. Genetics 45: 988–989.

    Google Scholar 

  • Gergen JP (1987) Dosage compensation in Drosophila: evidence that daughterless and Sexlethal control X chromosome activity at the blastoderm stage of embryogenesis. Genetics 117: 477–485.

    PubMed  Google Scholar 

  • Gilfillan GD, Straub T, de Wit E et al. (2006) Chromosome-wide gene-specific targeting of the Drosophila dosage compensation complex. Genes Dev 20: 858–870.

    Article  PubMed  CAS  Google Scholar 

  • Gupta A, Sharma GG, Young CS et al. (2005) Involvement of human MOF in ATM function. Mol Cell Biol 25: 5292–5305.

    Article  PubMed  CAS  Google Scholar 

  • Gupta V, Parisi M, Sturgill D et al. (2006) X-Chromosome compensation in Drosophila germ cells. J Biol 5: 3.

    Article  PubMed  CAS  Google Scholar 

  • Hagstrom KA, Meyer BJ (2003) Condensin and cohesin: more than chromosome compactor and glue. Nat Rev Genet 4: 520–534.

    Article  PubMed  CAS  Google Scholar 

  • Hamada FN, Park PJ, Gordadze PR, Kuroda MI (2005) Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster. Genes Dev 19: 2289–2294.

    Article  PubMed  CAS  Google Scholar 

  • Hilfiker A, Hilfiker-Kleiner D, Pannuti A, Lucchesi JC (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  CAS  Google Scholar 

  • Hochman B (1976) The fourth chromosome of Drosophila melanogaster. In Ashburner M, Novitski E, eds, The Genetics and Biology of Drosophila. New York: Academic Press, pp. 903–928

    Google Scholar 

  • Huynh KD, Lee JT (2001) Imprinted X inactivation in eutherians: a model of gametic execution and zygotic relaxation. Curr Opin Cell Biol 13: 690–697.

    Article  PubMed  CAS  Google Scholar 

  • Jegalian K, Page DC (1998) A proposed path by which genes common to mammalian X and Y chromosomes evolve to become X inactivated. Nature 394: 776–780.

    Article  PubMed  CAS  Google Scholar 

  • Jin Y, Wang Y, Walker DL et al. (1999) JIL-1: a novel chromosomal tandem kinase implicated in transcriptional regulation in Drosophila. Mol Cell 4: 129–135.

    Article  PubMed  CAS  Google Scholar 

  • Jin Y, Wang Y, Johansen J, Johansen KM (2000) JIL-1, a chromosomal kinase implicated in regulation of chromatin structure, associates with the male specific lethal (MSL) dosage compensation complex. J Cell Biol 149: 1005–1010.

    Article  PubMed  CAS  Google Scholar 

  • Jones BK, Levorse J, Tilghman SM (1998) Igf2 imprinting does not require its own DNA methylation or H19 RNA. Genes Dev 12: 2200–2297.

    PubMed  CAS  Google Scholar 

  • Kelley RL, Kuroda MI (2003) The Drosophila roX1 RNA gene can overcome silent chromatin by recruiting the Male-Specific Lethal dosage compensation complex. Genetics 164: 565–574.

    PubMed  CAS  Google Scholar 

  • Kelley RL, Solovyeva I, Lyman LM, Richman R, Solovyev V, Kuroda MI (1995) Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila. Cell 81: 867–877.

    Article  PubMed  CAS  Google Scholar 

  • Kelley RL, Meller VH, Gordadze PR, Roman G, Davis RL, Kuroda MI (1999) Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin. Cell 98: 513–522.

    Article  PubMed  CAS  Google Scholar 

  • Kotlikova IV, Demakova OV, Semeshin VF et al. (2006) The Drosophila dosage compensation complex binds to polytene chromosomes independently of developmental changes in transcription. Genetics 172: 963–974.

    Article  PubMed  CAS  Google Scholar 

  • Krivshenko JD (1952) A cytogenetic study of the Y chromosome in Drosophila buscki. Genetics 37: 500–518.

    PubMed  CAS  Google Scholar 

  • Krivshenko JD (1955) A cytogenetic study of the X chromosome of Drosophila busckii and its relation to phylogeny. Proc Natl Acad Sci USA 41: 1071–1079.

    Article  PubMed  CAS  Google Scholar 

  • Krivshenko JD (1959) New evidence for the homology of the short euchromatic elements of the X and Y chromosomes of Drosophila busckii with the microchromosome of Drosophila melanogaster. Genetics 44: 1027–1040.

    PubMed  CAS  Google Scholar 

  • Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286: 964–967.

    Article  PubMed  CAS  Google Scholar 

  • Larsson J, Chen JD, Rasheva V, Rasmuson-Lestander A, Pirrotta V (2001) Painting of fourth, a chromosome-specific protein in Drosophila. Proc Natl Acad Sci USA 98: 6273–6278.

    Article  PubMed  CAS  Google Scholar 

  • Larsson J, Svensson MJ, Stenberg P, Makitalo M (2004) Painting of fourth in genus Drosophila suggests autosome-specific gene regulation. Proc Natl Acad Sci USA 101: 9728–9733.

    Article  PubMed  CAS  Google Scholar 

  • Lee C-C, Hurwitz J (1993) Human RNA helicase A is homologous to the maleless protein of Drosophila. J Biol Chem 268: 16822–16830.

    PubMed  CAS  Google Scholar 

  • Lee C-G, Reichman TW, Baik T, Mathews MB (2004) MLE functions as a transcriptional regulator of the roX2 gene. J Biol Chem 46: 47740–47745.

    Article  CAS  Google Scholar 

  • Legube G, McWeeney SK, Lercher MJ, Akhtar A (2006) X chromosome wide profiling of MSL-1 distribution and dosage compensation in Drosophila. Genes Dev 20: 871–883.

    Article  PubMed  CAS  Google Scholar 

  • Lieb JD, de Solorzano CO, Rodriguez EG et al. (2000) The Caenorhabditis elegans dosage compensation machinery is recruited to X chromosome DNA attached to an autosome. Genetics 156: 1603–1621.

    PubMed  CAS  Google Scholar 

  • Lindsley DL, Sandler L, Baker BS et al. (1972) Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 71: 157–184.

    PubMed  CAS  Google Scholar 

  • Locke J, McDermid H (1993) Analysis of Drosophila chromosome four by pulse field electrophoresis. Chromosoma 102: 718–723.

    Article  PubMed  CAS  Google Scholar 

  • Lucchesi JC, Kelly WG, Panning B (2005) Chromatin remodeling in dosage compensation. Annu Rev Genet 39: 615–651.

    Article  PubMed  CAS  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: 8512–8520.

    Article  PubMed  CAS  Google Scholar 

  • Lyman LM, Copps K, Rastelli L, Kelley RL, Kuroda MI (1997) Drosophila male-specific lethal protein: structure/function analysis and dependence on MSL1 for chromosome association. Genetics 146: 1743–1753.

    Google Scholar 

  • Lyon MF (1998) X-chromosome inactivation: a repeat hypothesis. Cytogenet Cell Genet 80: 133–137.

    Article  PubMed  CAS  Google Scholar 

  • Marin I (2003) Evolution of chromatin remodelling complexes: comparative genomics reveals the ancient origin of ‘novel’ compensasome genes. J Mol Evol 56: 527–539.

    Article  PubMed  CAS  Google Scholar 

  • Marin I, Franke A, Bashaw GJ, Baker BS (1996) The dosage compensation system of Drosophila is co-opted by newly evolved X chromosomes. Nature 383: 160–163.

    Article  PubMed  CAS  Google Scholar 

  • Meller VH (2003) Initiation of dosage compensation in Drosophila embryos depends on expression of the roX RNAs. Mech Dev 120: 759–767.

    Article  PubMed  CAS  Google Scholar 

  • Meller VH, Kuroda MI (2002) Sex and the single chromosome. Adv Genet 46: 1–24.

    Article  PubMed  CAS  Google Scholar 

  • Meller VH, Rattner BP (2002) The roX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex. EMBO J 21: 1084–1091.

    Article  PubMed  CAS  Google Scholar 

  • Meller VH, Wu KH, Roman G, Kuroda MI, Davis RL (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 

  • Meller VH, Gordadze PR, Park Y et al. (2000) Ordered assembly of roX RNAs into MSL complexes on the dosage-compensated X chromosome in Drosophila. Curr Biol 10: 136–143.

    Article  PubMed  CAS  Google Scholar 

  • Miklos GLG., Yamamoto M-T, Davies J, Pirrotta V (1988) Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and b-heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci USA 85: 2051–2055.

    Article  PubMed  CAS  Google Scholar 

  • Mohandas T, Sparkes RS, Shapiro LJ (1981) Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation. Science 211: 393–396.

    PubMed  CAS  Google Scholar 

  • Muller HJ (1940) Bearings on the Drosophila work on systematics. In Huxley J, ed., The New Systematics. Oxford: Clarendon Press, pp. 185–268.

    Google Scholar 

  • Nguyen DK, Disteche CM (2006) Dosage compensation of the active X chromosome in mammals. Nat Genet 38: 47–53.

    PubMed  CAS  Google Scholar 

  • Nusinow DA, Panning B (2005) Recognition and modification of sex chromosomes. Curr Opin Genet Dev 15: 206–213.

    Article  PubMed  CAS  Google Scholar 

  • Oh H, Bone JR, Kuroda MI (2004) Multiple classes of MSL binding sites target dosage compensation to the X chromosome of Drosophila. Curr Biol 14: 481–487.

    Article  PubMed  CAS  Google Scholar 

  • O’Neill MJ (2005) The influence of non-coding RNAs on allele-specific gene expression in mammals. Hum Mol Genet 14: R113–R120.

    Article  PubMed  CAS  Google Scholar 

  • Pal Bhadra M, Bhadra U, Kundu J, Birchler JA (2005) Gene expression analysis of the function of the male-specific lethal complex in Drosophila. Genetics 169: 2061–2074.

    Article  CAS  Google Scholar 

  • Papaceit M, Juan E (1998) Fate of dot chromosome genes in Drosophila willistoni and Scaptodrosophila lebanonensis determined by in situ hybridization. Chromosome Res 6: 49–54.

    Article  PubMed  CAS  Google Scholar 

  • Park Y, Kelley RL, Oh H, Kuroda MI, Meller VH (2002) Extent of chromatin spreading determined by roX RNA recruitment of MSL proteins. Science 298: 1620–1623.

    Article  PubMed  CAS  Google Scholar 

  • Pfeifer GP, Tanguay RL, Steigerwald SD, Riggs AD (1990) In vivo footprint and methylation analysis by PCR-aided genomic sequencing: comparison of active and inactive X chromosomal DNA at the CpG island and promoter of human PGK-1. Genes Dev 4: 1277–1287.

    PubMed  CAS  Google Scholar 

  • Plath K, Fang J, Mlynarczyk-Evans SK et al. (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300: 131–135.

    Article  PubMed  CAS  Google Scholar 

  • Plath K, Talbot D, Hameer KM et al. (2004) Developmentally regulated alterations in Polycomb repressive complex 1 proteins on the inactive X chromosome. J Cell Biol 167: 1025–1035.

    Article  PubMed  CAS  Google Scholar 

  • Podemski L, Ferrer C, Locke J (2001) Whole arm inversion of chromosome 4 in Drosophila species. Chromosoma 110: 305–312.

    PubMed  CAS  Google Scholar 

  • Qian S, Pirrotta V (1995) Dosage compensation of the Drosophila white gene requires both the X chromosome environment and multiple intragenic elements. Genetics 139: 733–744.

    PubMed  CAS  Google Scholar 

  • Rattner BP, Meller VH (2004) Drosophila Male Specific Lethal 2 protein controls male-specific expression of the roX genes. Genetics 166: 1825–1832.

    Article  PubMed  CAS  Google Scholar 

  • Rice WR (1996) Evolution of the Y sex chromosome in animals. Bioscience 46: 331–343.

    Article  Google Scholar 

  • Richter L, Bone JR, Kuroda MI (1996) RNA-dependent association of the Drosophila maleless protein with the male X chromosome. Genes Cells 1: 325–336.

    Article  PubMed  CAS  Google Scholar 

  • Sandler L, Novitski E (1956) Evidence for genetic homology between chromosomes I and IV in Drosophila melanogaster, with a proposed explaination for the crowding effect in triploids. Genetics 41: 189–193.

    PubMed  CAS  Google Scholar 

  • Sass GL, Pannuti A, Lucchesi JC (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  CAS  Google Scholar 

  • Silva J, Mak W, Zvetkova I et al. (2003) Establishment of histone H3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev Cell 4: 481–495.

    Article  PubMed  CAS  Google Scholar 

  • Sleutels F, Zwart R, Barlow DP (2002) The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415: 810–813.

    PubMed  CAS  Google Scholar 

  • Smith ER, Pannuti A, Gu W 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  CAS  Google Scholar 

  • Smith ER, Allis CD, Lucchesi JC (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 

  • Smith ER, Cayrou C, Huang R, Lane WS, Cote J, Lucchesi JC (2005) A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16. Mol Cell Biol 25: 9175–9188.

    Article  PubMed  CAS  Google Scholar 

  • Steinmann M, Steinmann S (1998) Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda. a model for sex chromosome evolution. Genetica 102: 409–420.

    Article  Google Scholar 

  • Stenberg P, Pettersson F, Saura AO, Berglund A, Larsson J (2005) Sequence analysis of chromosome identity in three Drosophila species. BMC Bioinfomatics 6: 1–17.

    Article  CAS  Google Scholar 

  • Straub T, Gilfillan GD, Maier VK, Becker PB (2005) The Drosophila MSL complex activates the transcription of target genes. Genes Dev 19: 2284–2288.

    Article  PubMed  CAS  Google Scholar 

  • Sun FL, Cuaycong MH, Craig CA, Wallrath LL, Locke J, Elgin SC (2000) The fourth chromosome of Drosophila melanogaster: interspersed euchromatic and heterochromatic domains. Proc Natl Acad Sci USA 97: 5340–5345.

    Article  PubMed  CAS  Google Scholar 

  • Taipale M, Rea S, Richter K et al. (2005) hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells. Mol Cell Biol 25: 6798–6810.

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Subramanian S, Kumar S (2004) Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21: 36–44.

    Article  PubMed  CAS  Google Scholar 

  • Thakur N, Tiwari VK, Thomassin H et al. (2004) An antisense RNA regulates the bidirectional silencing property of the Kcnq1 imprinting control region. Mol Cell Biol 24: 7855–7862.

    Article  PubMed  CAS  Google Scholar 

  • Turner BM, Birley AJ, Lavender J (1992) Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69: 375–384.

    Article  PubMed  CAS  Google Scholar 

  • Verona RI, Mann MRW, Bartolomei MS (2003) Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu Rev Cell Dev Biol 19: 237–259.

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Zhang W, Jin Y, Johansen J, Johansen KM (2001) The JIL-1 tandem kinase mediates histone H3 phosphorylation and is required for maintenance of chromatin structure in Drosophila. Cell 105: 433–443.

    Article  PubMed  CAS  Google Scholar 

  • White WM, Willard HF, Van Dyke DL, Wolff DJ (1998) The spreading of X inactivation into autosomal material of an X;autosome translocation: evidence for a difference between autosomal and X-chromosomal DNA. Am J Hum Genet 63: 20–28.

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Deng H, Bao X et al. (2005) The JIL-1 histone H3S10 kinase regulates dimethyl H3K9 modifications and heterochromatic spreading in Drosophila. Development 133: 229–235.

    Article  PubMed  CAS  Google Scholar 

  • Zhou S, Yang Y, Scott MJ et al. (1995) Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cysteine cluster. EMBO J 14: 2884–2895.

    PubMed  CAS  Google Scholar 

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  1. Umeå Center for Molecular Pathogenesis, Umeå University, SE-901 87, Umeå, Sweden

    Jan Larsson

  2. Department of Biological Sciences, Wayne State University, Detroit, MI, 48070, USA

    Victoria H. Meller

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Larsson, J., Meller, V.H. Dosage compensation, the origin and the afterlife of sex chromosomes. Chromosome Res 14, 417–431 (2006). https://doi.org/10.1007/s10577-006-1064-3

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