1932

Abstract

X chromosome regulation represents a prime example of an epigenetic phenomenon where coordinated regulation of a whole chromosome is required. In flies, this is achieved by transcriptional upregulation of X chromosomal genes in males to equalize the gene dosage differences in females. Chromatin-bound proteins and long noncoding RNAs (lncRNAs) constituting a ribonucleoprotein complex known as the male-specific lethal (MSL) complex or the dosage compensation complex mediate this process. MSL complex members decorate the male X chromosome, and their absence leads to male lethality. The male X chromosome is also enriched with histone H4 lysine 16 acetylation (H4K16ac), indicating that the chromatin compaction status of the X chromosome also plays an important role in transcriptional activation. How the X chromosome is specifically targeted and how dosage compensation is mechanistically achieved are central questions for the field. Here, we review recent advances, which reveal a complex interplay among lncRNAs, the chromatin landscape, transcription, and chromosome conformation that fine-tune X chromosome gene expression.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-062917-011816
2018-06-20
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/biochem/87/1/annurev-biochem-062917-011816.html?itemId=/content/journals/10.1146/annurev-biochem-062917-011816&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Torres EM, Williams BR, Amon A 2008. Aneuploidy: cells losing their balance. Genetics 179:737–46
    [Google Scholar]
  2. 2.  Tang Y-C, Amon A 2013. Gene copy-number alterations: a cost-benefit analysis. Cell 152:394–405
    [Google Scholar]
  3. 3.  Disteche CM. 2016. Dosage compensation of the sex chromosomes and autosomes. Semin. Cell Dev. Biol. 56:9–18
    [Google Scholar]
  4. 4.  Ercan S. 2015. Mechanisms of X chromosome dosage compensation. J. Genomics 3:1–19
    [Google Scholar]
  5. 5.  Graves JAM. 2016. Evolution of vertebrate sex chromosomes and dosage compensation. Nat. Rev. Genet. 17:33–46
    [Google Scholar]
  6. 6.  Jiang X, Biedler JK, Qi Y, Hall AB, Tu Z 2015. Complete dosage compensation in Anopheles stephensi and the evolution of sex-biased genes in mosquitoes. Genome Biol. Evol. 7:1914–24
    [Google Scholar]
  7. 7.  Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D 2013. Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLOS Biol 11:e1001643
    [Google Scholar]
  8. 8.  Richard G, Legeai F, Prunier-Leterme N, Bretaudeau A, Tagu D et al. 2017. Dosage compensation and sex-specific epigenetic landscape of the X chromosome in the pea aphid. Epigenetics Chromatin 10:30
    [Google Scholar]
  9. 9.  Zhou Q, Ellison CE, Kaiser VB, Alekseyenko AA, Gorchakov AA, Bachtrog D 2013. The epigenome of evolving Drosophila neo-sex chromosomes: dosage compensation and heterochromatin formation. PLOS Biol 11:e1001711
    [Google Scholar]
  10. 10.  Prince EG, Kirkland D, Demuth JP 2010. Hyperexpression of the X chromosome in both sexes results in extensive female bias of X-linked genes in the flour beetle. Genome Biol. Evol. 2:336–46
    [Google Scholar]
  11. 11.  Chandler CH. 2017. When and why does sex chromosome dosage compensation evolve?. Ann. NY Acad. Sci. 1389:37–51
    [Google Scholar]
  12. 12.  Tanaka A, Fukunaga A, Oishi K 1976. Studies on the sex-specific lethals of Drosophila melanogaster. II. Further studies on a male-specific lethal gene, maleless. Genetics 84:257–66
    [Google Scholar]
  13. 13.  Belote JM, Lucchesi JC 1980. Male-specific lethal mutations of Drosophila melanogaster. Genetics 96:165–86
    [Google Scholar]
  14. 14.  Amrein H, Axel R 1997. Genes expressed in neurons of adult male Drosophila. Cell 88:459–69
    [Google Scholar]
  15. 15.  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 88:445–57
    [Google Scholar]
  16. 16.  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 81:867–77
    [Google Scholar]
  17. 17.  Gorman M, Franke A, Baker BS 1995. Molecular characterization of the male-specific lethal-3 gene and investigations of the regulation of dosage compensation in Drosophila. Development 121:463–75
    [Google Scholar]
  18. 18.  Bashaw GJ, Baker BS 1995. The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex specifically regulated by Sex-lethal. Development 121:3245–58
    [Google Scholar]
  19. 19.  Alekseyenko AA, Peng S, Larschan E, Gorchakov AA, Lee O-K et al. 2008. A sequence motif within chromatin entry sites directs MSL establishment on the Drosophila X chromosome. Cell 134:599–609
    [Google Scholar]
  20. 20.  Straub T, Grimaud C, Gilfillan GD, Mitterweger A, Becker PB 2008. The chromosomal high-affinity binding sites for the Drosophila dosage compensation complex. PLOS Genet 4:e1000302
    [Google Scholar]
  21. 21.  McElroy KA, Kang H, Kuroda MI 2014. Are we there yet? Initial targeting of the male-specific lethal and polycomb group chromatin complexes in Drosophila. Open Biol 4:140006
    [Google Scholar]
  22. 22.  Akhtar A, Becker PB 2000. Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol. Cell 5:367–75
    [Google Scholar]
  23. 23.  Conrad T, Cavalli F, Holz H, Hallacli E, Kind J et al. 2012. The MOF chromobarrel domain controls genome-wide H4K16 acetylation and spreading of the MSL complex. Dev. Cell 22:610–24
    [Google Scholar]
  24. 24.  Dunlap D, Yokoyama R, Ling H, Sun H-Y, McGill K et al. 2012. Distinct contributions of MSL complex subunits to the transcriptional enhancement responsible for dosage compensation in Drosophila. Nucleic Acids Res 40:11281–91
    [Google Scholar]
  25. 25.  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. 16:2054–60
    [Google Scholar]
  26. 26.  Piergentili R. 2010. Multiple roles of the Y chromosome in the biology of Drosophila melanogaster. Sci. World J 10:1749–67
    [Google Scholar]
  27. 27.  Erickson JW, Quintero JJ 2007. Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. PLOS Biol 5:e332
    [Google Scholar]
  28. 28.  Salz HK, Erickson JW 2010. Sex determination in Drosophila: the view from the top. Fly 4:60–70
    [Google Scholar]
  29. 29.  Pomiankowski A, Nöthiger R, Wilkins A 2004. The evolution of the Drosophila sex-determination pathway. Genetics 166:1761–73
    [Google Scholar]
  30. 30.  Schutt C, Nothiger R 2000. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127:667–77
    [Google Scholar]
  31. 31.  Penalva LOF, Sánchez L 2003. RNA binding protein sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol. Mol. Biol. Rev. 67:343–59
    [Google Scholar]
  32. 32.  Verhulst EC, van de Zande L 2015. Double nexus–doublesex is the connecting element in sex determination. Brief. Funct. Genomics 14:396–406
    [Google Scholar]
  33. 33.  Bashaw GJ, Baker BS 1997. The regulation of the Drosophila msl-2 gene reveals a function for Sex-lethal in translational control. Cell 89:789–98
    [Google Scholar]
  34. 34.  Kelley RL, Wang J, Bell L, Kuroda MI 1997. Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 387:195–99
    [Google Scholar]
  35. 35.  Hennig J, Militti C, Popowicz GM, Wang I, Sonntag M et al. 2014. Structural basis for the assembly of the Sxl-Unr translation regulatory complex. Nature 515:287–90
    [Google Scholar]
  36. 36.  Duncan K, Grskovic M, Strein C, Beckmann K, Niggeweg R et al. 2006. Sex-lethal imparts a sex-specific function to UNR by recruiting it to the msl-2 mRNA 3′ UTR: translational repression for dosage compensation. Genes Dev 20:368–79
    [Google Scholar]
  37. 37.  Beckmann K, Grskovic M, Gebauer F, Hentze MW 2005. A dual inhibitory mechanism restricts msl-2 mRNA translation for dosage compensation in Drosophila. Cell 122:529–40
    [Google Scholar]
  38. 38.  Graindorge A, Carré C, Gebauer F 2013. Sex-lethal promotes nuclear retention of msl2 mRNA via interactions with the STAR protein HOW. Genes Dev 27:1421–33
    [Google Scholar]
  39. 39.  Alekseyenko AA, Ho JW, Peng S, Gelbart M, Tolstorukov MY et al. 2012. Sequence-specific targeting of dosage compensation in Drosophila favors an active chromatin context. PLOS Genet 8:e1002646
    [Google Scholar]
  40. 40.  Clemente-Ruiz M, Murillo-Maldonado JM, Benhra N, Barrio L, Pérez L et al. 2016. Gene dosage imbalance contributes to chromosomal instability-induced tumorigenesis. Dev. Cell 36:290–302
    [Google Scholar]
  41. 41.  Kadlec J, Hallacli E, Lipp M, Holz H, Sanchez-Weatherby J et al. 2011. Structural basis for MOF and MSL3 recruitment into the dosage compensation complex by MSL1. Nat. Struct. Mol. Biol. 18:142–49
    [Google Scholar]
  42. 42.  Hallacli E, Lipp M, Georgiev P, Spielman C, Cusack S et al. 2012. Msl1-mediated dimerization of the dosage compensation complex is essential for male X-chromosome regulation in Drosophila. Mol. Cell 48:587–600
    [Google Scholar]
  43. 43.  Buscaino A, Köcher T, Kind JH, Holz H, Taipale M et al. 2003. MOF-regulated acetylation of MSL-3 in the Drosophila dosage compensation complex. Mol. Cell 11:1265–77
    [Google Scholar]
  44. 44.  Villa R, Forné I, Müller M, Imhof A, Straub T, Becker PB 2012. MSL2 combines sensor and effector functions in homeostatic control of the Drosophila dosage compensation machinery. Mol. Cell 48:647–54
    [Google Scholar]
  45. 45.  Chlamydas S, Holz H, Samata M, Chelmicki T, Georgiev P et al. 2016. Functional interplay between MSL1 and CDK7 controls RNA polymerase II Ser5 phosphorylation. Nat. Struct. Mol. Biol. 23:580–89
    [Google Scholar]
  46. 46.  Schunter S, Villa R, Flynn V, Heidelberger JB, Classen A-K et al. 2017. Ubiquitylation of the acetyltransferase MOF in Drosophila melanogaster. PLOS ONE 12:e0177408
    [Google Scholar]
  47. 47.  Morales V, Straub T, Neumann MF, Mengus G, Akhtar A, Becker PB 2004. Functional integration of the histone acetyltransferase MOF into the dosage compensation complex. EMBO J 23:2258–68
    [Google Scholar]
  48. 48.  Scott MJ, Pan LL, Cleland SB, Knox AL, Heinrich J 2000. MSL1 plays a central role in assembly of the MSL complex, essential for dosage compensation in Drosophila. EMBO J 19:144–55
    [Google Scholar]
  49. 49.  Li F, Parry DA, Scott MJ 2005. The amino-terminal region of Drosophila MSL1 contains basic, glycine-rich, and leucine zipper–like motifs that promote X chromosome binding, self-association, and MSL2 binding, respectively. Mol. Cell. Biol. 25:8913–24
    [Google Scholar]
  50. 50.  Meller VH, Gordadze PR, Park Y, Chu X, Stuckenholz C et al. 2000. Ordered assembly of roX RNAs into MSL complexes on the dosage-compensated X chromosome in Drosophila. Curr. Biol 10:136–43
    [Google Scholar]
  51. 51.  Menon DU, Meller VH 2009. Imprinting of the Y chromosome influences dosage compensation in roX1 roX2 Drosophila melanogaster. Genetics 183:811–20
    [Google Scholar]
  52. 52.  Deng X, Koya KS, Kong Y, Meller VH 2009. Coordinated regulation of heterochromatic genes in Drosophila melanogaster males. Genetics 182:481–91
    [Google Scholar]
  53. 53.  Zheng S, Villa R, Wang J, Feng Y, Wang J et al. 2014. Structural basis of X chromosome DNA recognition by the MSL2 CXC domain during Drosophila dosage compensation. Genes Dev 28:2652–62
    [Google Scholar]
  54. 54.  Zheng S, Wang J, Feng Y, Wang J, Ye K 2012. Solution structure of MSL2 CXC domain reveals an unusual Zn3Cys9 cluster and similarity to pre-SET domains of histone lysine methyltransferases. PLOS ONE 7:e45437
    [Google Scholar]
  55. 55.  Villa R, Schauer T, Smialowski P, Straub T, Becker PB 2016. PionX sites mark the X chromosome for dosage compensation. Nature 537:244–48
    [Google Scholar]
  56. 56.  Fauth T, Müller-Planitz F, König C, Straub T, Becker PB 2010. The DNA binding CXC domain of MSL2 is required for faithful targeting the dosage compensation complex to the X chromosome. Nucleic Acids Res 38:3209–21
    [Google Scholar]
  57. 57.  Li F, Schiemann AH, Scott MJ 2008. Incorporation of the noncoding roX RNAs alters the chromatin-binding specificity of the Drosophila MSL1/MSL2 complex. Mol. Cell. Biol. 28:1252–64
    [Google Scholar]
  58. 58.  Straub T, Zabel A, Gilfillan GD, Feller C, Becker PB 2013. Different chromatin interfaces of the Drosophila dosage compensation complex revealed by high-shear ChIP-seq. Genome Res 23:473–85
    [Google Scholar]
  59. 59.  Wu L, Zee BM, Wang Y, Garcia BA, 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 43:132–44
    [Google Scholar]
  60. 60.  Zhao X, Su J, Wang F, Liu D, Ding J et al. 2013. Crosstalk between NSL histone acetyltransferase and MLL/SET complexes: NSL complex functions in promoting histone H3K4 di-methylation activity by MLL/SET complexes. PLOS Genet 9:e1003940
    [Google Scholar]
  61. 61.  Buscaino A, Legube G, Akhtar A 2006. X-chromosome targeting and dosage compensation are mediated by distinct domains in MSL-3. EMBO Rep 7:531–38
    [Google Scholar]
  62. 62.  Sural TH, Peng S, Li B, Workman JL, Park PJ, Kuroda MI 2008. The MSL3 chromodomain directs a key targeting step for dosage compensation of the Drosophila melanogaster X chromosome. Nat. Struct. Mol. Biol. 15:1318–25
    [Google Scholar]
  63. 63.  Straub T, Zabel A, Gilfillan GD, Feller C, Becker PB 2013. Different chromatin interfaces of the Drosophila dosage compensation complex revealed by high-shear ChIP-seq. Genome Res 23:473–85
    [Google Scholar]
  64. 64.  Kim D, Blus BJ, Chandra V, Huang P, Rastinejad F, Khorasanizadeh S 2010. Corecognition of DNA and a methylated histone tail by the MSL3 chromodomain. Nat. Struct. Mol. Biol. 17:1027–29
    [Google Scholar]
  65. 65.  Larschan E, Alekseyenko AA, Gortchakov AA, Peng S, Li B et al. 2007. MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism. Mol. Cell 28:121–33
    [Google Scholar]
  66. 66.  Kind J, Akhtar A 2007. Cotranscriptional recruitment of the dosage compensation complex to X-linked target genes. Genes Dev 21:2030–40
    [Google Scholar]
  67. 67.  Moore SA, Ferhatoglu Y, Jia Y, Al-Jiab RA, Scott MJ 2010. Structural and biochemical studies on the chromo-barrel domain of male specific lethal 3 (MSL3) reveal a binding preference for mono- or dimethyllysine 20 on histone H4. J. Biol. Chem. 285:40879–90
    [Google Scholar]
  68. 68.  Robinson P, An W, Routh A, Martino F, Chapman L et al. 2008. 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J. Mol. Biol. 381:816–25
    [Google Scholar]
  69. 69.  Shogren-Knaak M, Ishii H, Sun J-M, Pazin MJ, Davie JR, Peterson CL 2006. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–47
    [Google Scholar]
  70. 70.  Lam KC, Mühlpfordt F, Vaquerizas JM, Raja SJ, Holz H et al. 2012. The NSL complex regulates housekeeping genes in Drosophila. PLOS Genet 8:e1002736
    [Google Scholar]
  71. 71.  Raja SJ, Charapitsa I, Conrad T, Vaquerizas JM, Gebhardt P et al. 2010. The nonspecific lethal complex is a transcriptional regulator in Drosophila. Mol. Cell 38:827–41
    [Google Scholar]
  72. 72.  Feller C, Prestel M, Hartmann H, Straub T, Soding J, Becker PB 2012. The MOF-containing NSL complex associates globally with housekeeping genes, but activates only a defined subset. Nucleic Acids Res 40:1509–22
    [Google Scholar]
  73. 73.  Mendjan S, Taipale M, Kind J, Holz H, Gebhardt P et al. 2006. Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol. Cell 21:811–23
    [Google Scholar]
  74. 74.  Cai Y, Jin J, Swanson SK, Cole MD, Choi S et al. 2010. Subunit composition and substrate specificity of a MOF-containing histone acetyltransferase distinct from the male-specific lethal (MSL) complex. J. Biol. Chem. 285:4268–72
    [Google Scholar]
  75. 75.  Gu W, Szauter P, Lucchesi JC 1998. Targeting of MOF, a putative histone acetyl transferase, to the X chromosome of Drosophila melanogaster. Dev. Genet 22:56–64
    [Google Scholar]
  76. 76.  Gu W, Wei X, Pannuti A, Lucchesi JC 2000. Targeting the chromatin-remodeling MSL complex of Drosophila to its sites of action on the X chromosome requires both acetyl transferase and ATPase activities. EMBO J 19:5202–11
    [Google Scholar]
  77. 77.  Akhtar A, Becker PB 2001. The histone H4 acetyltransferase MOF uses a C2HC zinc finger for substrate recognition. EMBO Rep 2:113–18
    [Google Scholar]
  78. 78.  Yang C, Wu J, Sinha SH, Neveu JM, Zheng YG 2012. Autoacetylation of the MYST lysine acetyltransferase MOF protein. J. Biol. Chem. 287:34917–26
    [Google Scholar]
  79. 79.  Akhtar A, Zink D, Becker PB 2000. Chromodomains are protein-RNA interaction modules. Nature 407:405–09
    [Google Scholar]
  80. 80.  Conrad T, Cavalli FM, Vaquerizas JM, Luscombe NM, Akhtar A 2012. Drosophila dosage compensation involves enhanced Pol II recruitment to male X-linked promoters. Science 337:742–46
    [Google Scholar]
  81. 81.  Suganuma T, Gutiérrez JL, Li B, Florens L, Swanson SK et al. 2008. ATAC is a double histone acetyltransferase complex that stimulates nucleosome sliding. Nat. Struct. Mol. Biol. 15:364–72
    [Google Scholar]
  82. 82.  Franke A, Baker BS 1999. The rox1 and rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila. Mol. Cell 4:117–22
    [Google Scholar]
  83. 83.  Ilik I, Quinn JJ, Georgiev P, Tavares-Cadete F, Maticzka D et al. 2013. Tandem stem-loops in roX RNAs act together to mediate X chromosome dosage compensation in Drosophila. Mol. Cell 51:156–73
    [Google Scholar]
  84. 84.  Figueiredo ML, Kim M, Philip P, Allgardsson A, Stenberg P, Larsson J 2014. Non-coding roX RNAs prevent the binding of the MSL-complex to heterochromatic regions. PLOS Genet 10:e1004865
    [Google Scholar]
  85. 85.  Gilfillan GD, Dahlsveen IK, Becker PB 2004. Lifting a chromosome: dosage compensation in Drosophila melanogaster. FEBS Lett 567:8–14
    [Google Scholar]
  86. 86.  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 17:5409–17
    [Google Scholar]
  87. 87.  Richter L, Bone JR, Kuroda MI 1996. RNA‐dependent association of the Drosophila maleless protein with the male X chromosome. Genes Cells 1:325–36
    [Google Scholar]
  88. 88.  Izzo A, Regnard C, Morales V, Kremmer E, Becker PB 2008. Structure-function analysis of the RNA helicase maleless. Nucleic Acids Res 36:950–62
    [Google Scholar]
  89. 89.  Prabu JR, Müller M, Thomae AW, Schüssler S, Bonneau F et al. 2015. Structure of the RNA helicase MLE reveals the molecular mechanisms for uridine specificity and RNA-ATP coupling. Mol. Cell 60:487–99
    [Google Scholar]
  90. 90.  Morra R, Yokoyama R, Ling H, Lucchesi JC 2011. Role of the ATPase/helicase maleless (MLE) in the assembly, targeting, spreading and function of the male-specific lethal (MSL) complex of Drosophila. Epigenetics Chromatin 4:1–13
    [Google Scholar]
  91. 91.  Aktaş T, Ilık İA, Maticzka D, Bhardwaj V, Rodrigues CP et al. 2017. DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome. Nature 544:115–19
    [Google Scholar]
  92. 92.  Reenan RA, Hanrahan CJ, Ganetzky B 2000. The mlenapts RNA helicase mutation in Drosophila results in a splicing catastrophe of the para Na+ channel transcript in a region of RNA editing. Neuron 25:139–49
    [Google Scholar]
  93. 93.  Cugusi S, Kallappagoudar S, Ling H, Lucchesi JC 2015. The Drosophila helicase maleless (MLE) is implicated in functions distinct from its role in dosage compensation. Mol. Cell. Proteomics 14:1478–88
    [Google Scholar]
  94. 94.  Ilik IA, Maticzka D, Georgiev P, Gutierrez NM, Backofen R, Akhtar A 2017. A mutually exclusive stem-loop arrangement in roX2 RNA is essential for X-chromosome regulation in Drosophila. Genes Dev 31:1973–87
    [Google Scholar]
  95. 95.  Aratani S, Kageyama Y, Nakamura A, Fujita H, Fujii R et al. 2008. MLE activates transcription via the minimal transactivation domain in Drosophila. Int. J. Mol. Med. 21:469–76
    [Google Scholar]
  96. 96.  Lee C-G, Reichman TW, Baik T, Mathews MB 2004. MLE functions as a transcriptional regulator of the roX2 gene. J. Biol. Chem. 279:47740–45
    [Google Scholar]
  97. 97.  Robert Finestra T, Gribnau J 2017. X chromosome inactivation: silencing, topology and reactivation. Curr. Opin. Cell Biol. 46:54–61
    [Google Scholar]
  98. 98.  Ilik I, Akhtar A 2009. roX RNAs: non-coding regulators of the male X chromosome in flies. RNA Biol 6:113–21
    [Google Scholar]
  99. 99.  Meller VH, Rattner BP 2002. The roX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex. EMBO J 21:1084–91
    [Google Scholar]
  100. 100.  Lim CK, Kelley RL 2012. Autoregulation of the Drosophila noncoding roX1 RNA gene. PLOS Genet 8:e1002564
    [Google Scholar]
  101. 101.  Park SW, Kuroda MI, Park Y 2008. Regulation of histone H4 Lys16 acetylation by predicted alternative secondary structures in roX noncoding RNAs. Mol. Cell. Biol. 28:4952–62
    [Google Scholar]
  102. 102.  Park SW, Kang Y, Sypula JG, Choi J, Oh H, Park Y 2007. An evolutionarily conserved domain of roX2 RNA is sufficient for induction of H4-Lys16 acetylation on the Drosophila X chromosome. Genetics 177:1429–37
    [Google Scholar]
  103. 103.  Kelley RL, Lee O-K, Shim Y-K 2008. Transcription rate of noncoding roX1 RNA controls local spreading of the Drosophila MSL chromatin remodeling complex. Mech. Dev. 125:1009–19
    [Google Scholar]
  104. 104.  Quinn JJ, Zhang QC, Georgiev P, Ilik IA, Akhtar A, Chang HY 2016. Rapid evolutionary turnover underlies conserved lncRNA-genome interactions. Genes Dev 30:191–207
    [Google Scholar]
  105. 105.  Quinn JJ, Ilik IA, Qu K, Georgiev P, Chu C et al. 2014. Revealing long noncoding RNA architecture and functions using domain-specific chromatin isolation by RNA purification. Nat. Biotechnol. 32:933–40
    [Google Scholar]
  106. 106.  Maenner S, Muller M, Frohlich J, Langer D, Becker PB 2013. ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Mol. Cell 51:174–84
    [Google Scholar]
  107. 107.  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 98:513–22
    [Google Scholar]
  108. 108.  Lyman LM, Copps K, Rastelli L, Kelley RL, Kuroda MI 1997. Drosophila male-specific lethal-2 protein: structure/function analysis and dependence on MSL-1 for chromosome association. Genetics 147:1743–53
    [Google Scholar]
  109. 109.  Ramírez F, Lingg T, Toscano S, Lam KC, Georgiev P 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 60:146–62
    [Google Scholar]
  110. 110.  Bai X, Alekseyenko AA, Kuroda MI 2004. Sequence-specific targeting of MSL complex regulates transcription of the roX RNA genes. EMBO J 23:2853–61
    [Google Scholar]
  111. 111.  Soruco MM, Larschan E 2014. A new player in X identification: the CLAMP protein is a key factor in Drosophila dosage compensation. Chromosome Res 22:505–15
    [Google Scholar]
  112. 112.  Urban JA, Doherty CA, Jordan WT, Bliss JE, Feng J et al. 2016. The essential Drosophila CLAMP protein differentially regulates non-coding roX RNAs in male and females. Chromosome Res 25:101–13
    [Google Scholar]
  113. 113.  Menon DU, Coarfa C, Xiao W, Gunaratne PH, Meller VH 2014. siRNAs from an X-linked satellite repeat promote X-chromosome recognition in Drosophila melanogaster. PNAS 111:16460–65
    [Google Scholar]
  114. 114.  Joshi SS, Meller VH 2017. Satellite repeats identify X chromatin for dosage compensation in Drosophila melanogaster males. Curr. Biol. 27:1393–402
    [Google Scholar]
  115. 115.  Menon DU, Meller VH 2015. Identification of the Drosophila X chromosome: the long and short of it. RNA Biol 12:1088–93
    [Google Scholar]
  116. 116.  Menon DU, Meller VH 2012. A role for siRNA in X-chromosome dosage compensation in Drosophila melanogaster. Genetics 191:1023–28
    [Google Scholar]
  117. 117.  Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93
    [Google Scholar]
  118. 118.  Sexton T, Cavalli G 2015. The role of chromosome domains in shaping the functional genome. Cell 160:1049–59
    [Google Scholar]
  119. 119.  Dixon JR, Selvaraj S, Yue F, Kim A, Li Y et al. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–80
    [Google Scholar]
  120. 120.  Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B et al. 2012. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148:458–72
    [Google Scholar]
  121. 121.  Denholtz M, Bonora G, Chronis C, Splinter E, de Laat W et al. 2013. Long-range chromatin contacts in embryonic stem cells reveal a role for pluripotency factors and polycomb proteins in genome organization. Cell Stem Cell 13:602–16
    [Google Scholar]
  122. 122.  Dixon JR, Jung I, Selvaraj S, Shen Y, Antosiewicz-Bourget JE et al. 2015. Chromatin architecture reorganization during stem cell differentiation. Nature 518:331–36
    [Google Scholar]
  123. 123.  Bantignies F, Roure V, Comet I, Leblanc B, Schuettengruber B et al. 2011. Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 144:214–26
    [Google Scholar]
  124. 124.  Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom DT et al. 2015. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep 10:1297–309
    [Google Scholar]
  125. 125.  Ulianov SV, Khrameeva EE, Gavrilov AA, Flyamer IM, Kos P et al. 2016. Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains. Genome Res 26:70–84
    [Google Scholar]
  126. 126.  Eagen KP, Hartl TA, Kornberg RD 2015. Stable chromosome condensation revealed by chromosome conformation capture. Cell 163:934–46
    [Google Scholar]
  127. 127.  Kind J, Vaquerizas JM, Gebhardt P, Gentzel M, Luscombe NM et al. 2008. Genome-wide analysis reveals MOF as a key regulator of dosage compensation and gene expression in Drosophila. Cell 133:813–28
    [Google Scholar]
  128. 128.  Gelbart ME, Larschan E, Peng S, Park PJ, Kuroda MI 2009. Drosophila MSL complex globally acetylates H4K16 on the male X chromosome for dosage compensation. Nat. Struct. Mol. Biol. 16:825–32
    [Google Scholar]
  129. 129.  Dou Y, Milne TA, Tackett AJ, Smith ER, Fukuda A et al. 2005. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121:873–85
    [Google Scholar]
  130. 130.  Kapoor-Vazirani P, Kagey JD, Powell DR, Vertino PM 2008. Role of hMOF-dependent histone H4 lysine 16 acetylation in the maintenance of TMS1/ASC gene activity. Cancer Res 68:6810–21
    [Google Scholar]
  131. 131.  Kapoor-Vazirani P, Kagey JD, Vertino PM 2011. SUV420H2-mediated H4K20 trimethylation enforces RNA polymerase II promoter-proximal pausing by blocking hMOF-dependent H4K16 acetylation. Mol. Cell. Biol. 31:1594–609
    [Google Scholar]
  132. 132.  Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, Oliviero S 2009. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138:1122–36
    [Google Scholar]
  133. 133.  Furuhashi H, Nakajima M, Hirose S 2006. DNA supercoiling factor contributes to dosage compensation in Drosophila. Development 133:4475–83
    [Google Scholar]
  134. 134.  Cugusi S, Ramos E, Ling H, Yokoyama R, Luk KM, Lucchesi JC 2013. Topoisomerase II plays a role in dosage compensation in Drosophila. Transcription 4:238–50
    [Google Scholar]
  135. 135.  Corless S, Gilbert N 2016. Effects of DNA supercoiling on chromatin architecture. Biophys. Rev. 8:245–58
    [Google Scholar]
  136. 136.  Muse GW, Gilchrist DA, Nechaev S, Shah R, Parker JS et al. 2007. RNA polymerase is poised for activation across the genome. Nat. Genet. 39:1507–11
    [Google Scholar]
  137. 137.  Ferrari F, Alekseyenko AA, Park PJ, Kuroda MI 2014. Transcriptional control of a whole chromosome: emerging models for dosage compensation. Nat. Struct. Mol. Biol. 21:118–25
    [Google Scholar]
  138. 138.  Straub T, Becker PB 2013. Comment on “Drosophila dosage compensation involves enhanced Pol II recruitment to male X-linked promoters. .” Science 340:273
    [Google Scholar]
  139. 139.  Ferrari F, Jung YL, Kharchenko PV, Plachetka A, Alekseyenko AA et al. 2013. Comment on “Drosophila dosage compensation involves enhanced Pol II recruitment to male X-linked promoters. .” Science 340:273
    [Google Scholar]
  140. 140.  Vaquerizas JM, Cavalli FM, Conrad T, Akhtar A, Luscombe NM 2013. Response to comments on “Drosophila dosage compensation involves enhanced Pol II recruitment to male X-linked promoters. .” Science 340:273
    [Google Scholar]
  141. 141.  Regnard C, Straub T, Mitterweger A, Dahlsveen IK, Fabian V, Becker PB 2011. Global analysis of the relationship between JIL-1 kinase and transcription. PLOS Genet 7:e1001327
    [Google Scholar]
  142. 142.  Ferrari F, Plachetka A, Alekseyenko AA, Jung YL, Ozsolak F et al. 2013. “Jump start and gain” model for dosage compensation in Drosophila based on direct sequencing of nascent transcripts. Cell Rep 5:629–36
    [Google Scholar]
  143. 143.  Larschan E, Bishop EP, Kharchenko PV, Core LJ, Lis JT et al. 2011. X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature 471:115–18
    [Google Scholar]
  144. 144.  Lladser ME, Azofeifa JG, Allen MA, Dowell RD 2017. RNA Pol II transcription model and interpretation of GRO-seq data. J. Math. Biol. 74:77–97
    [Google Scholar]
  145. 145.  Core LJ, Waterfall JJ, Gilchrist DA, Fargo DC, Kwak H et al. 2012. Defining the status of RNA polymerase at promoters. Cell Rep 2:1025–35
    [Google Scholar]
  146. 146.  Harlen KM, Churchman SL 2017. The code and beyond: transcription regulation by the RNA polymerase II carboxy-terminal domain. Nat. Rev. Mol. Cell Biol. 18:263–73
    [Google Scholar]
  147. 147.  Chelmicki T, Dündar F, Turley MJ, Khanam T, Aktas T et al. 2014. MOF-associated complexes ensure stem cell identity and Xist repression. eLife 3:e02024
    [Google Scholar]
  148. 148.  Faucillion M-LL, Larsson J 2015. Increased expression of X-linked genes in mammals is associated with a higher stability of transcripts and an increased ribosome density. Genome Biol. Evol. 7:1039–52
    [Google Scholar]
  149. 149.  Deng X, Berletch JB, Ma W, Nguyen DK, Hiatt JB et al. 2013. Mammalian X upregulation is associated with enhanced transcription initiation, RNA half-life, and MOF-mediated H4K16 acetylation. Dev. Cell 25:55–68
    [Google Scholar]
  150. 150.  Zhang Z, Presgraves DC 2016. Drosophila X-linked genes have lower translation rates than autosomal genes. Mol. Biol. Evol. 33:413–28
    [Google Scholar]
  151. 151.  Birchler JA. 2016. Parallel universes for models of X chromosome dosage compensation in Drosophila: a review. Cytogenet. Genome Res. 148:52–67
    [Google Scholar]
  152. 152.  Sun X, Birchler JA 2009. Interaction study of the male specific lethal (MSL) complex and trans-acting dosage effects in metafemales of Drosophila melanogaster. Cytogenet. Genome Res 124:298–311
    [Google Scholar]
  153. 153.  Sun L, Johnson AF, Donohue RC, Li J, Cheng J, Birchler JA 2013. Dosage compensation and inverse effects in triple X metafemales of Drosophila. PNAS 110:7383–88
    [Google Scholar]
  154. 154.  Sun L, Fernandez HR, Donohue RC, Li J, Cheng J, Birchler JA 2013. Male-specific lethal complex in Drosophila counteracts histone acetylation and does not mediate dosage compensation. PNAS 110:E808–17
    [Google Scholar]
  155. 155.  Landeen EL, Muirhead CA, Wright L, Meiklejohn CD, Presgraves DC 2016. Sex chromosome-wide transcriptional suppression and compensatory cis-regulatory evolution mediate gene expression in the Drosophila male germline. PLOS Biol 14:e1002499
    [Google Scholar]
  156. 156.  The UniProt C. 2017. UniProt: the universal protein knowledgebase. Nucleic Acids Res 45:D158–69
    [Google Scholar]
  157. 157.  Nielsen PR, Nietlispach D, Buscaino A, Warner RJ, Akhtar A et al. 2005. Structure of the chromo barrel domain from the MOF acetyltransferase. J. Biol. Chem. 280:32326–31
    [Google Scholar]
/content/journals/10.1146/annurev-biochem-062917-011816
Loading
/content/journals/10.1146/annurev-biochem-062917-011816
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error