H3K27 modifications define segmental regulatory domains in the Drosophila bithorax complex

eLife

Volumn 3, Issue July2014, 2014, Pages 1-13

  Bowman, Sarah K ^a,b   Deaton, Aimee M ^a,b   Domingues, Heber ^b   Wang, Peggy I ^a,b   Sadreyev, Ruslan I ^a,b   Kingston, Robert E ^a,b   Bender, Welcome ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; CHROMATIN; CTCF PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; HISTONE; LYSINE; POLYCOMB PROTEIN, DROSOPHILA; PROTEIN BINDING; REPRESSOR PROTEIN;

ACETYLATION; ANIMAL; CHEMISTRY; CHROMATIN; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOBOX; MALE; METABOLISM; MORPHOGENESIS; NONMAMMALIAN EMBRYO; SIGNAL TRANSDUCTION;

ACETYLATION; ANIMALS; BODY PATTERNING; CHROMATIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HISTONES; LYSINE; MALE; POLYCOMB REPRESSIVE COMPLEX 1; PROTEIN BINDING; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84923804763     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02833     Document Type: Article

References (50)

1. Bae E, Calhoun VC, Levine M, Lewis EB, Drewell RA. 2002. Characterization of the intergenic RNA profile at abdominal-A and Abdominal-B in the Drosophila bithorax complex. Proceedings of the National Academy of Sciences of USA 99:16847-16852. doi: 10.1073/pnas.222671299.
2. Bender W, Hudson A. 2000. P element homing to the Drosophila bithorax complex. Development 127:3981-3992.
3. Bender W, Lucas M. 2013. The border between the Ultrabithorax and abdominal-A regulatory domains in the Drosophila bithorax complex. Genetics 193:1135-1147. doi: 10.1534/genetics.112.146340.
4. Blackledge NP, Farcas AM, Kondo T, King HW, McGouran JF, Hanssen LL, Ito S, Cooper S, Kondo K, Koseki Y, Ishikura T, Long HK, Sheahan TW, Brockdorff N, Kessler BM, Koseki H, Klose RJ. 2014. Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell 157:1445-1459. doi: 10.1016/j.cell.2014.05.004.
5. Boulet AM, Lloyd A, Sakonju S. 1991. Molecular definition of the morphogenetic and regulatory functions and the cis-regulatory elements of the Drosophila Abd-B homeotic gene. Development 111:393-405.
6. Bowman SK, Simon MD, Deaton AM, Tolstorukov M, Borowsky ML, Kingston RE. 2013. Multiplexed Illumina sequencing libraries from picogram quantities of DNA. BMC Genomics 14:466. doi: 10.1186/1471-2164-14-466.
7. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
8. Carroll SB, Laymon RA, McCutcheon MA, Riley PD, Scott MP. 1986. The localization and regulation of Antennapedia protein expression in Drosophila embryos. Cell 47:113-122. doi: 10.1016/0092-8674(86)90372-7.
9. Casares F, Bender W, Merriam J, Sanchez-Herrero E. 1997. Interactions of Drosophila Ultrabithorax regulatory regions with native and foreign promoters. Genetics 145:123-137.
10. Celniker SE, Sharma S, Keelan DJ, Lewis EB. 1990. The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. The EMBO Journal 9:4277-4286.
11. Chopra VS, Hong JW, Levine M. 2009. Regulation of hox gene activity by transcriptional elongation in Drosophila. Current Biology 19:688-693. doi: 10.1016/j.cub.2009.02.055.
12. Cooper S, Dienstbier M, Hassan R, Schermelleh L, Sharif J, Blackledge NP, de Marco V, Elderkin S, Koseki H, Klose R, Heger A, Brockdorff N. 2014. Targeting polycomb to pericentric heterochromatin in embryonic stem cells reveals a role for H2AK119u1 in PRC2 recruitment. Cell Reports 7:1456-1470. doi: 10.1016/j.celrep.2014.04.012.
13. Deal RB, Henikoff S. 2011. The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nature Protocols 6:56-68. doi: 10.1038/nprot.2010.175.
14. DeVido SK, Kwon D, Brown JL, Kassis JA. 2008. The role of Polycomb-group response elements in regulation of engrailed transcription in Drosophila. Development 135:669-676. doi: 10.1242/dev.014779.
15. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S. 2003. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes & Development 17:1870-1881. doi: 10.1101/gad.1110503.
16. Gonzalez I, Mateos-Langerak J, Thomas A, Cheutin T, Cavalli G. 2014. Identification of regulators of the three-dimensional polycomb organization by a microscopy-based genome-wide RNAi screen. Molecular Cell 54:485-499. doi: 10.1016/j.molcel.2014.03.004.
17. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108-112. doi: 10.1038/nature07829.
18. Kalb R, Latwiel S, Baymaz HI, Jansen PW, Müller CW, Vermeulen M, Müller J. 2014. Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression. Nature Structural & Molecular Biology 21:569-571. doi: 10.1038/nsmb.2833.
19. Karch F, Bender W, Weiffenbach B. 1990. abdA expression in Drosophila embryos. Genes & Development 4:1573-1587. doi: 10.1101/gad.4.9.1573.
20. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, Sabo PJ, Larschan E, Gorchakov AA, Gu T, Linder-Basso D, Plachetka A, Shanower G, Tolstorukov MY, Luquette LJ, Xi R, Jung YL, Park RW, Bishop EP, Canfield TK, Sandstrom R, Thurman RE, MacAlpine DM, Stamatoyannopoulos JA, Kellis M, Elgin SC, Kuroda MI, Pirrotta V, Karpen GH, Park PJ. 2011. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471:480-485. doi: 10.1038/nature09725.
21. Kharchenko PV, Tolstorukov MY, Park PJ. 2008. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nature Biotechnology 26:1351-1359. doi: 10.1038/nbt.1508.
22. Kwong C, Adryan B, Bell I, Meadows L, Russell S, Manak JR, White R. 2008. Stability and dynamics of polycomb target sites in Drosophila development. PLOS Genetics 4:e1000178. doi: 10.1371/journal.pgen.1000178.
23. Lewis EB. 1978. A gene complex controlling segmentation in Drosophila. Nature 276:565-570. doi: 10.1038/276565a0.
24. Lewis EB. 1981. Developmental genetics of the bithorax complex in Drosophila. In: Brown DD, Fox CF, editors. Developmental Biology Using Purified Genes ICN-UCLA Symposia on Molecular and Cellular Biology XXIII. New York: Academic Press.
25. Lewis PH. 1947. Melanogaster-new mutants: report of Pamela H. Lewis. Drosophila Information Service 21:69.
26. Maeda RK, Karch F. 2009. The bithorax complex of Drosophila: an exceptional Hox cluster. Current Topics in Developmental Biology 88:1-33. doi: 10.1016/S0070-2153(09)88001-0.
27. Mito Y, Henikoff JG, Henikoff S. 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nature Genetics 37:1090-1097. doi: 10.1038/ng1637.
28. Mohan M, Bartkuhn M, Herold M, Philippen A, Heinl N, Bardenhagen I, Leers J, White RA, Renkawitz-Pohl R, Saumweber H, Renkawitz R. 2007. The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning. The EMBO Journal 26:4203-4214. doi: 10.1038/sj.emboj.7601851.
29. Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O'Connor MB, Kingston RE, Simon JA. 2002. Histone Methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197-208. doi: 10.1016/S0092-8674(02)00976-5.
30. Nègre N, Brown CD, Ma L, Bristow CA, Miller SW, Wagner U, Kheradpour P, Eaton ML, Loriaux P, Sealfon R, Li Z, Ishii H, Spokony RF, Chen J, Hwang L, Cheng C, Auburn RP, Davis MB, Domanus M, Shah PK, Morrison CA, Zieba J, Suchy S, Senderowicz L, Victorsen A, Bild NA, Grundstad AJ, Hanley D, MacAlpine DM, Mannervik M, Venken K, Bellen H, White R, Gerstein M, Russell S, Grossman RL, Ren B, Posakony JW, Kellis M, White KP. 2011. A cis-regulatory map of the Drosophila genome. Nature 471:527-531. doi: 10.1038/nature09990.
31. Nègre N, Brown CD, Shah PK, Kheradpour P, Morrison CA, Henikoff JG, Feng X, Ahmad K, Russell S, White RA, Stein L, Henikoff S, Kellis M, White KP. 2010. A comprehensive map of insulator elements for the Drosophila genome. PLOS Genetics 6:e1000814. doi: 10.1371/journal.pgen.1000814.
32. Ohlsson R, Bartkuhn M, Renkawitz R. 2010. CTCF shapes chromatin by multiple mechanisms: the impact of 20 years of CTCF research on understanding the workings of chromatin. Chromosoma 119:351-360. doi: 10.1007/s00412-010-0262-0.
33. Oktaba K, Gutierrez L, Gagneur J, Girardot C, Sengupta AK, Furlong EE, Müller J. 2008. Dynamic regulation by polycomb group protein complexes controls pattern formation and the cell cycle in Drosophila. Developmental Cell 15:877-889. doi: 10.1016/j.devcel.2008.10.005.
34. Pai CY, Lei EP, Ghosh D, Corces VG. 2004. The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Molecular Cell 16:737-748. doi: 10.1016/j.molcel.2004.11.004.
35. Papp B, Müller J. 2006. Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes & Development 20:2041-2054. doi: 10.1101/gad.388706.
36. Pease B, Borges AC, Bender W. 2013. Noncoding RNAs of the Ultrabithorax domain of the Drosophila bithorax complex. Genetics 195:1253-1264. doi: 10.1534/genetics.113.155036.
37. Peifer M, Karch F, Bender W. 1987. The bithorax complex: control of segmental identity. Genes & Development 1:891-898. doi: 10.1101/gad.1.9.891.
38. Pengelly AR, Copur O, Jackle H, Herzig A, Müller J. 2013. A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science 339:698-699. doi: 10.1126/science.1231382.
39. Pinter SF, Sadreyev RI, Yildirim E, Jeon Y, Ohsumi TK, Borowsky M, Lee JT. 2012. Spreading of X chromosome inactivation via a hierarchy of defined Polycomb stations. Genome Research 22:1864-1876. doi: 10.1101/gr.133751.111.
40. Ruthenburg AJ, Allis CD, Wysocka J. 2007. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Molecular Cell 25:15-30. doi: 10.1016/j.molcel.2006.12.014.
41. Schuettengruber B, Ganapathi M, Leblanc B, Portoso M, Jaschek R, Tolhuis B, van Lohuizen M, Tanay A, Cavalli G. 2009. Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLOS Biology 7:e13. doi: 10.1371/journal.pbio.1000013.
42. Sepp KJ, Auld VJ. 1999. Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151:1093-1101.
43. Simon JA, Kingston RE. 2013. Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Molecular Cell 49:808-824. doi: 10.1016/j.molcel.2013.02.013.
44. Smith ST, Wickramasinghe P, Olson A, Loukinov D, Lin L, Deng J, Xiong Y, Rux J, Sachidanandam R, Sun H, Lobanenkov V, Zhou J. 2009. Genome wide ChIP-chip analyses reveal important roles for CTCF in Drosophila genome organization. Developmental Biology 328:518-528. doi: 10.1016/j.ydbio.2008.12.039.
45. Soshnikova N, Duboule D. 2009. Epigenetic temporal control of mouse HOX genes in vivo. Science 324:1320-1323. doi: 10.1126/science.1171468.
46. Steiner FA, Talbert PB, Kasinathan S, Deal RB, Henikoff S. 2012. Cell-type-specific nuclei purification from whole animals for genome-wide expression and chromatin profiling. Genome Research 22:766-777. doi: 10.1101/gr.131748.111.
47. Straub T, Zabel A, Gilfillan GD, Feller C, Becker PB. 2013. Different chromatin interfaces of the Drosophila doasge compensation complex revealed by high-shear ChIP-seq. Genome Research 23:473-485. doi: 10.1101/gr.146407.112.
48. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, Ryner L, Cheung LM, Chong A, Erickson C, Fisher WW, Greer K, Hartouni SR, Howie E, Jakkula L, Joo D, Killpack K, Laufer A, Mazzotta J, Smith RD, Stevens LM, Stuber C, Tan LR, Ventura R, Woo A, Zakrajsek I, Zhao L, Chen F, Swimmer C, Kopczynski C, Duyk G, Winberg ML, Margolis J. 2004. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nature Genetics 36:283-287. doi: 10.1038/ng1314.
49. Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, Zlobin A, Diaz MO, Scacheri PC, Harte PJ. 2009. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136:3131-3141. doi: 10.1242/dev.037127.
50. Yildirim E, Sadreyev RI, Pinter SF, Lee JT. 2012. X-chromosome hyperactivation in mammals via nonlinear relationships between chromatin states and transcription. Nature Structural & Molecular Biology 19:56-61. doi: 10.1038/nsmb.2195.