Drosophila Dosage Compensation Loci Associate with a Boundary-Forming Insulator Complex

REFERENCES

• Hnisz D, Weintraub AS, Day DS, Valton A, Bak RO, Li CH, Goldmann J, Lajoie BR, Fan ZP, Sigova AA, Reddy J, Borges-Rivera D, Lee TI, Jaenisch R, Porteus MH, Dekker J, Young RA. 2016. Activation of proto-oncogenes by disruption of chromosome neighborhoods. Science 351:1454–1458. https://doi.org/10.1126/science.aad9024.
   PubMed Web of Science ®Google Scholar
• Chetverina D, Aoki T, Erokhin M, Georgiev P, Schedl P. 2014. Making connections: insulators organize eukaryotic chromosomes into independent cis-regulatory networks. Bioessays 36:163–172. https://doi.org/10.1002/bies.201300125.
   PubMed Web of Science ®Google Scholar
• Ribeiro de Almeida C, Hendriks RW, Stadhouders R. 2015. Dynamic control of long-range genomic interactions at the immunoglobulin κ light-chain locus. Adv Immunol 128:183–271. https://doi.org/10.1016/bs.ai.2015.07.004.
   PubMed Web of Science ®Google Scholar
• Dixon JR, Gorkin DU, Ren B. 2016. Chromatin domains: the unit of chromosome organization. Mol Cell 62:668–680. https://doi.org/10.1016/j.molcel.2016.05.018.
   PubMed Web of Science ®Google Scholar
• Dekker J, Heard E. 2015. Structural and functional diversity of topologically associating domains. FEBS Lett 589:2877–2884. https://doi.org/10.1016/j.febslet.2015.08.044.
   PubMed Web of Science ®Google Scholar
• Eagen K, Aiden EL, Kornberg R. 2017. Polycomb-mediated chromatin loops revealed by a sub-kilobase resolution chromatin interaction map. bioRxiv. https://doi.org/10.1101/099804.
   Google Scholar
• Fujioka M, Mistry H, Schedl P, Jaynes JB. 2016. Determinants of chromosome architecture: insulator pairing in cis and in trans. PLoS Genet 12:e1005889. https://doi.org/10.1371/journal.pgen.1005889.
   Google Scholar
• Kellum R, Schedl P. 1992. A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol Cell Biol 12:2424–2431. https://doi.org/10.1128/MCB.12.5.2424.
   PubMed Web of Science ®Google Scholar
• Kellum R, Schedl P. 1991. A position-effect assay for boundaries of higher order chromosomal domains. Cell 64:941–950. https://doi.org/10.1016/0092-8674(91)90318-S.
   PubMed Web of Science ®Google Scholar
• Vazquez J, Schedl P. 1994. Sequences required for enhancer blocking activity of scs are located within two nuclease-hypersensitive regions. EMBO J 13:5984–5993.
   PubMedGoogle Scholar
• Sigrist CJA, Pirrotta V. 1997. Chromatin insulator elements block the silencing of a target gene by the Drosophila polycomb response element (PRE) but allow trans interactions between PREs on different chromosomes. Genetics 147:209–221.
   PubMed Web of Science ®Google Scholar
• Muller M, Hagstrom K, Gyurkovics H, Pirrotta V, Schedl P. 1999. The Mcp element from the Drosophila melanogaster bithorax complex mediates long-distance regulatory interactions. Genetics 153:1333–1356.
   PubMedGoogle Scholar
• Muravyova E, Golovnin A, Gracheva E, Parshikov A, Belenkaya T, Pirrotta V, Georgiev P. 2001. Loss of insulator activity by paired Su(Hw) chromatin insulators. Science 291:495–498. https://doi.org/10.1126/science.291.5503.495.
   PubMedGoogle Scholar
• Cai Y, Jin J, Swanson SK, Cole MD, Choi SH, Florens L, Washburn MP, Conaway JW, Conaway RC. 2010. Subunit composition and substrate specificity of a MOF-containing histone acetyltransferase distinct from the male-specific lethal (MSL) complex. J Biol Chem 285:4268–4272. https://doi.org/10.1074/jbc.C109.087981.
   PubMed Web of Science ®Google Scholar
• Belote JM, Lucchesi JC. 1980. Male-specific lethal mutations of Drosophila melanogaster. Genetics 96:165–186.
   PubMed Web of Science ®Google Scholar
• Gelbart ME, Kuroda MI. 2009. Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136:1399–1410. https://doi.org/10.1242/dev.029645.
   PubMedGoogle Scholar
• Keller CI, Akhtar A. 2015. The MSL complex: juggling RNA-protein interactions for dosage compensation and beyond. Curr Opin Genet Dev 31:1–11. https://doi.org/10.1016/j.gde.2015.03.007.
   PubMedGoogle 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. https://doi.org/10.1093/emboj/21.5.1084.
   PubMed Web of Science ®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. https://doi.org/10.1074/jbc.C100351200.
   PubMed Web of Science ®Google Scholar
• Larschan E, Bishop EP, Kharchenko PV, Core LJ, Lis JT, Park PJ, Kuroda MI. 2011. X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature 471:115–118. https://doi.org/10.1038/nature09757.
   PubMedGoogle 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. https://doi.org/10.1016/S0092-8674(00)81979-0.
   PubMed Web of Science ®Google Scholar
• Kageyama Y, Mengus G, Gilfillan G, Kennedy HG, Stuckenholz C, Kelley RL, Becker PB, Kuroda MI. 2001. Association and spreading of the Drosophila dosage compensation complex from a discrete roX1 chromatin entry site. EMBO J 20:2236–2245. https://doi.org/10.1093/emboj/20.9.2236.
   PubMedGoogle Scholar
• Alekseyenko AA, Peng S, Larschan E, Gorchakov AA, Lee OK, Kharchenko P, McGrath SD, Wang CI, Mardis ER, Park PJ, Kuroda MI. 2008. A sequence motif within chromatin entry sites directs MSL establishment on the Drosophila X chromosome. Cell 134:599–609. https://doi.org/10.1016/j.cell.2008.06.033.
   PubMedGoogle Scholar
• Alekseyenko AA, Larschan E, Lai WR, Park PJ, Kuroda MI. 2006. High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome. Genes Dev 20:848–857. https://doi.org/10.1101/gad.1400206.
   PubMedGoogle Scholar
• Gorchakov AA, Alekseyenko AA, Kharchenko P, Park PJ, Kuroda MI. 2009. Long-range spreading of dosage compensation in Drosophila captures transcribed autosomal genes inserted on X. Genes Dev 23:2266–2271. https://doi.org/10.1101/gad.1840409.
   PubMed Web of Science ®Google Scholar
• Adkins NL, Hagerman T, Georgel P. 2006. GAGA protein: a multi-faceted transcription factor. Biochem Cell Biol 84:559–567. https://doi.org/10.1139/o06-062.
   PubMed Web of Science ®Google Scholar
• Meller VH, Kuroda MI. 2002. Sex and the single chromosome. Adv Genet 46:1–24.
   PubMed Web of Science ®Google Scholar
• Oh H, Park Y, Kuroda MI. 2003. Local spreading of MSL complexes from roX genes on the Drosophila X chromosome. Genes Dev 17:1334–1339. https://doi.org/10.1101/gad.1082003.
   PubMedGoogle Scholar
• Ramírez F, Lingg T, Toscano S, Lam KC, Georgiev P, Chung HR, Lajoie BR, de Wit E, Zhan Y, de Laat W, Dekker J, Manke T, Akhtar A. 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. https://doi.org/10.1016/j.molcel.2015.08.024.
   PubMedGoogle Scholar
• Larschan E, Soruco MML, Lee OK, Peng S, Bishop E, Chery J, Goebel K, Feng J, Park PJ, Kuroda MI. 2012. Identification of chromatin-associated regulators of MSL complex targeting in Drosophila dosage compensation. PLoS Genet 8:e1002830. https://doi.org/10.1371/journal.pgen.1002830.
   Google Scholar
• Soruco MML, Chery J, Bishop EP, Siggers T, Tolstorukov MY, Leydon AR, Sugden AU, Goebel K, Feng J, Xia P, Vedenko A, Bulyk ML, Park PJ, Larschan E. 2013. The CLAMP protein links the MSL complex to the X chromosome during Drosophila dosage compensation. Genes Dev 27:1551–1556. https://doi.org/10.1101/gad.214585.113.
   PubMedGoogle Scholar
• Kuzu G, Kaye EG, Chery J, Siggers T, Yang L, Dobson JR, Boor S, Bliss J, Liu W, Jogl G, Rohs R, Singh ND, Bulyk ML, Tolstorukov MY, Larschan E. 2016. Expansion of GA dinucleotide repeats increases the density of CLAMP binding sites on the X-chromosome to promote Drosophila dosage compensation. PLoS Genet 12:e1006120. https://doi.org/10.1371/journal.pgen.1006120.
   Google Scholar
• Greenberg AJ, Yanowitz JL, Schedl P. 2004. The Drosophila GAGA factor is required for dosage compensation in males and for the formation of the male-specific-lethal complex chromatin entry site at 12DE. Genetics 166:279–289. https://doi.org/10.1534/genetics.166.1.279.
   PubMedGoogle Scholar
• Urban J, Doherty C, Rieder L, Jordan W, Tsiarli M, Larschan E. 2017. The essential Drosophila CLAMP protein differentially regulates non-coding roX RNAs in male and females. Chromosome Res 25:101–113. https://doi.org/10.1007/s10577-016-9541-9.
   PubMedGoogle Scholar
• Ohtsuki S, Levine M. 1998. GAGA mediates the enhancer blocking activity of the eve promoter in the Drosophila embryo. Genes Dev 12:3325–3330. https://doi.org/10.1101/gad.12.21.3325.
   PubMedGoogle Scholar
• Belozerov VE, Majumder P, Shen P, Cai HN. 2003. A novel boundary element may facilitate independent gene regulation in the Antennapedia complex of Drosophila. EMBO J 22:3113–3121. https://doi.org/10.1093/emboj/cdg297.
   PubMedGoogle Scholar
• Wolle D, Cleard F, Aoki T, Deshpande G, Schedl P, Karch F. 2015. Functional requirements for Fab-7 boundary activity in the bithorax. Mol Cell Biol 35:3739–3752. https://doi.org/10.1128/MCB.00456-15.
   PubMedGoogle Scholar
• Schweinsberg SE, Schedl P. 2004. Developmental modulation of Fab-7 boundary function. Development 131:4743–4749. https://doi.org/10.1242/dev.01343.
   PubMedGoogle Scholar
• Zhou J, Barolo S, Szymanski P, Levine M. 1996. The Fab-7 element of the bithorax complex attenuates enhancer-promoter interactions in the Drosophila embryo. Genes Dev 10:3195–3201. https://doi.org/10.1101/gad.10.24.3195.
   PubMedGoogle Scholar
• Rodin S, Kyrchanova O, Pomerantseva E, Parshikov A, Georgiev P. 2007. New properties of Drosophila Fab-7 insulator. Genetics 177:113–121. https://doi.org/10.1534/genetics.107.075887.
   PubMedGoogle Scholar
• Hagstrom K, Muller M, Schedl P. 1997. A polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex. Genetics 146:1365–1380.
   PubMedGoogle Scholar
• Schweinsberg S, Hagstrom K, Gohl D, Schedl P, Kumar RP, Mishra R, Karch F. 2004. The enhancer-blocking activity of the Fab-7 boundary from the Drosophila bithorax complex requires GAGA-factor-binding sites. Genetics 168:1371–1384. https://doi.org/10.1534/genetics.104.029561.
   PubMedGoogle Scholar
• Cleard F, Wolle D, Taverner AM, Aoki T, Deshpande G, Andolfatto P, Karch F, Schedl P. 2017. Different evolutionary strategies to conserve chromatin boundary function in the bithorax complex. Genetics 205:589–603. https://doi.org/10.1534/genetics.116.195586.
   PubMedGoogle Scholar
• Kyrchanova O, Chetverina D, Maksimenko O, Kullyev A, Georgiev P. 2008. Orientation-dependent interaction between Drosophila insulators is a property of this class of regulatory elements. Nucleic Acids Res 36:7019–7028. https://doi.org/10.1093/nar/gkn781.
   PubMedGoogle Scholar
• Cai HN, Shen P. 2001. Effects of cis arrangement of chromatin insulators on enhancer-blocking activity. Science 291:493–495. https://doi.org/10.1126/science.291.5503.493.
   PubMedGoogle Scholar
• Gilfillan GD, König C, Dahlsveen IK, Prakoura N, Straub T, Lamm R, Fauth T, Becker PB. 2007. Cumulative contributions of weak DNA determinants to targeting the Drosophila dosage compensation complex. Nucleic Acids Res 35:3561–3572. https://doi.org/10.1093/nar/gkm282.
   PubMed Web of Science ®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. https://doi.org/10.1126/science.1076686.
   PubMed Web of Science ®Google Scholar
• Kyrchanova O, Mogila V, Wolle D, Magbanua JP, White R, Georgiev P, Schedl P. 2015. The boundary paradox in the Bithorax complex. Mech Dev 138:122–132. https://doi.org/10.1016/j.mod.2015.07.002.
   PubMedGoogle Scholar
• Dorn R, Krauss V. 2003. The modifier of mdg4 locus in Drosophila: functional complexity is resolved by trans splicing. Genetica 117:165–177. https://doi.org/10.1023/A:1022983810016.
   PubMed Web of Science ®Google Scholar
• Bonchuk A, Denisov S, Georgiev P, Maksimenko O. 2011. Drosophila BTB/POZ domains of “ttk group” can form multimers and selectively interact with each other. J Mol Biol 412:423–436. https://doi.org/10.1016/j.jmb.2011.07.052.
   PubMedGoogle Scholar
• Villa R, Schauer T, Smialowski P, Straub T, Becker PB. 2016. PionX sites mark the X chromosome for dosage compensation. Nature 537:244–248. https://doi.org/10.1038/nature19338.
   PubMedGoogle Scholar
• Aoki T, Schweinsberg S, Manasson J, Schedl P. 2008. A stage-specific factor confers Fab-7 boundary activity during early embryogenesis in Drosophila Mol Cell Biol 28:1047–1060. https://doi.org/10.1128/MCB.01622-07.
   PubMedGoogle 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. https://doi.org/10.1101/gad.1343705.
   PubMedGoogle Scholar
• Fuda NJ, Guertin MJ, Sharma S, Danko CG, Martins AL, Siepel A, Lis JT. 2015. GAGA factor maintains nucleosome-free regions and has a role in RNA polymerase II recruitment to promoters. PLoS Genet 11:e1005108. https://doi.org/10.1371/journal.pgen.1005108.
   Google Scholar
• Larschan E, Alekseyenko AA, Gortchakov AA, Peng S, Li B, Yang P, Workman JL, Park PJ, Kuroda MI. 2007. MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism. Mol Cell 28:121–133. https://doi.org/10.1016/j.molcel.2007.08.011.
   PubMed Web of Science ®Google Scholar