#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Analysis of cell-type-specific chromatin modifications and gene expression in Drosophila neurons that direct reproductive behavior


Autoři: Colleen M. Palmateer aff001;  Shawn C. Moseley aff001;  Surjyendu Ray aff001;  Savannah G. Brovero aff001;  Michelle N. Arbeitman aff001
Působiště autorů: Department of Biomedical Sciences, Florida State University, College of Medicine, Tallahassee, Florida, United States of America aff001;  Program of Neuroscience, Florida State University, Tallahassee, Florida, United States of America aff002
Vyšlo v časopise: Analysis of cell-type-specific chromatin modifications and gene expression in Drosophila neurons that direct reproductive behavior. PLoS Genet 17(4): e1009240. doi:10.1371/journal.pgen.1009240
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009240

Souhrn

Examining the role of chromatin modifications and gene expression in neurons is critical for understanding how the potential for behaviors are established and maintained. We investigate this question by examining Drosophila melanogaster fru P1 neurons that underlie reproductive behaviors in both sexes. We developed a method to purify cell-type-specific chromatin (Chromatag), using a tagged histone H2B variant that is expressed using the versatile Gal4/UAS gene expression system. Here, we use Chromatag to evaluate five chromatin modifications, at three life stages in both sexes. We find substantial changes in chromatin modification profiles across development and fewer differences between males and females. Additionally, we find chromatin modifications that persist in different sets of genes from pupal to adult stages, which may point to genes important for cell fate determination in fru P1 neurons. We generated cell-type-specific RNA-seq data sets, using translating ribosome affinity purification (TRAP). We identify actively translated genes in fru P1 neurons, revealing novel stage- and sex-differences in gene expression. We also find chromatin modification enrichment patterns that are associated with gene expression. Next, we use the chromatin modification data to identify cell-type-specific super-enhancer-containing genes. We show that genes with super-enhancers in fru P1 neurons differ across development and between the sexes. We validated that a set of genes are expressed in fru P1 neurons, which were chosen based on having a super-enhancer and TRAP-enriched expression in fru P1 neurons.

Klíčová slova:

Behavior – Gene expression – Gene ontologies – Histone modification – Chromatin – Chromatin modification – Neurons – Exon trapping


Zdroje

1. Dulac C. Brain function and chromatin plasticity. Nature. 2010;465(7299):728–35. doi: 10.1038/nature09231 WOS:000278551800035. 20535202

2. Graff J, Tsai LH. Histone acetylation: molecular mnemonics on the chromatin. Nature Reviews Neuroscience. 2013;14(2):97–111. doi: 10.1038/nrn3427 WOS:000314563200008. 23324667

3. Crepaldi L, Riccio A. Chromatin learns to behave. Epigenetics. 2009;4(1):23–6. doi: 10.4161/epi.4.1.7604 WOS:000263517400006. 19197164

4. Opachaloemphan C, Yan H, Leibholz A, Desplan C, Reinberg D. Recent Advances in Behavioral (Epi) Genetics in Eusocial Insects. Annual Review of Genetics, Vol 52. 2018;52:489–510. doi: 10.1146/annurev-genet-120116-024456 WOS:000453889500023. 30208294

5. Anreiter I, Biergans SD, Sokolowski MB. Epigenetic regulation of behavior in Drosophila melanogaster. Current Opinion in Behavioral Sciences. 2019;25:44–50. doi: 10.1016/j.cobeha.2018.06.010 WOS:000460484300008.

6. Yamamoto D, Sato K, Koganezawa M. Neuroethology of male courtship in Drosophila: from the gene to behavior. Journal of Comparative Physiology a-Neuroethology Sensory Neural and Behavioral Physiology. 2014;200(4):251–64. doi: 10.1007/s00359-014-0891-5 WOS:000333183800001. 24567257

7. Dauwalder B. THE ROLES OF FRUITLESS AND DOUBLESEX IN THE CONTROL OF MALE COURTSHIP. Recent Advances in the Use of Drosophila in Neurobiology and Neurodegeneration. 2011;99:87–105. doi: 10.1016/B978-0-12-387003-2.00004-5 WOS:000295818200004. 21906537

8. Kubli E, Bopp D. Sexual Behavior: How Sex Peptide Flips the Postmating Switch of Female Flies. Current Biology. 2012;22(13):R520–R2. doi: 10.1016/j.cub.2012.04.058 WOS:000306379600008. 22789998

9. Laturney M, Billeter JC. Neurogenetics of Female Reproductive Behaviors in Drosophila melanogaster. Advances in Genetics, Vol 85. 2014;85:1–108. doi: 10.1016/B978-0-12-800271-1.00001-9 WOS:000337493600001. 24880733

10. Burtis KC, Baker BS. DROSOPHILA DOUBLESEX GENE CONTROLS SOMATIC SEXUAL-DIFFERENTIATION BY PRODUCING ALTERNATIVELY SPLICED MESSENGER-RNAS ENCODING RELATED SEX-SPECIFIC POLYPEPTIDES. Cell. 1989;56(6):997–1010. doi: 10.1016/0092-8674(89)90633-8 WOS:A1989T944600014. 2493994

11. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, et al. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell. 1996;87(6):1079–89. doi: 10.1016/s0092-8674(00)81802-4 WOS:A1996VY44700013. 8978612

12. Ito H, Fujitani K, Usui K, ShimizuNishikawa K, Tanaka S, Yamamoto D. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. P Natl Acad Sci USA. 1996;93(18):9687–92. doi: 10.1073/pnas.93.18.9687 WOS:A1996VF61400068. 8790392

13. Villella A, Hall JC. Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics. 1996;143(1):331–44. WOS:A1996UH28300030. 8722785

14. Robinett CC, Vaughan AG, Knapp JM, Baker BS. Sex and the Single Cell. II. There Is a Time and Place for Sex. Plos Biology. 2010;8(5). doi: 10.1371/journal.pbio.1000365 WOS:000278759600003. 20454565

15. Rideout EJ, Dornan AJ, Neville MC, Eadie S, Goodwin SF. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nature Neuroscience. 2010;13(4):458–U79. doi: 10.1038/nn.2515 WOS:000276073500015. 20305646

16. Lee G, Hall JC, Park JH. Doublesex gene expression in the central nervous system of Drosophila melanogaster. Journal of Neurogenetics. 2002;16(4):229–48. doi: 10.1080/01677060216292 WOS:000183562400002. 12745633

17. Lee G, Foss M, Goodwin SF, Carlo T, Taylor BJ, Hall JC. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. Journal of Neurobiology. 2000;43(4):404–26. doi: 10.1002/1097-4695(20000615)43:4<404::aid-neu8>3.0.co;2-d WOS:000087713700008. 10861565

18. Sanders LE, Arbeitman MN. Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Developmental Biology. 2008;320(2):378–90. doi: 10.1016/j.ydbio.2008.05.543 WOS:000258603300006. 18599032

19. Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature. 2005;436(7049):395–400. Epub 2005/06/17. doi: 10.1038/nature03859 15959468

20. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ. Neural circuitry that governs Drosophila male courtship behavior. Cell. 2005;121(5):795–807. doi: 10.1016/j.cell.2005.04.026 WOS:000229658000017. 15935765

21. Hall JC. COURTSHIP AMONG MALES DUE TO A MALE-STERILE MUTATION IN DROSOPHILA-MELANOGASTER. Behavior Genetics. 1978;8(2):125–41. doi: 10.1007/BF01066870 WOS:A1978EU91600001. 99136

22. Anand A, Villella A, Ryner LC, Carlo T, Goodwin SF, Song HJ, et al. Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics. 2001;158(4):1569–95. WOS:000170603700016. 11514448

23. Goodwin SF, Taylor BJ, Villella A, Foss M, Ryner LC, Baker BS, et al. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics. 2000;154(2):725–45. WOS:000085178700021. 10655225

24. Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics. 1997;147(3):1107–30. WOS:A1997YF03500014. 9383056

25. Demir E, Dickson BJ. fruitless splicing specifies male courtship behavior in Drosophila. Cell. 2005;121(5):785–94. doi: 10.1016/j.cell.2005.04.027 WOS:000229658000016. 15935764

26. Kvitsiani D, Dickson BJ. Shared neural circuitry for female and male sexual behaviours in Drosophila. Current Biology. 2006;16(10):R355–R6. doi: 10.1016/j.cub.2006.04.025 WOS:000237874500009. 16713940

27. Kimura KI, Ote M, Tazawa T, Yamamoto D. Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature. 2005;438(7065):229–33. doi: 10.1038/nature04229 WOS:000233133500050. 16281036

28. Belote JM, Baker BS. SEXUAL-BEHAVIOR—ITS GENETIC-CONTROL DURING DEVELOPMENT AND ADULTHOOD IN DROSOPHILA-MELANOGASTER. Proceedings of the National Academy of Sciences of the United States of America. 1987;84(22):8026–30. doi: 10.1073/pnas.84.22.8026 WOS:A1987L051100048. 3120181

29. Arthur BI, Jallon JM, Caflisch B, Choffat Y, Nothiger R. Sexual behaviour in Drosophila is irreversibly programmed during a critical period. Current Biology. 1998;8(21):1187–90. doi: 10.1016/s0960-9822(07)00491-5 WOS:000076659300024. 9799737

30. Hueston CE, Olsen D, Li QY, Okuwa S, Peng B, Wu JN, et al. Chromatin Modulatory Proteins and Olfactory Receptor Signaling in the Refinement and Maintenance of Fruitless Expression in Olfactory Receptor Neurons. Plos Biology. 2016;14(4). doi: 10.1371/journal.pbio.1002443 WOS:000375094800014. 27093619

31. Zhao SH, Deanhardt B, Barlow GT, Schleske PG, Rossi AM, Volka PC. Chromatin-based reprogramming of a courtship regulator by concurrent pheromone perception and hormone signaling. Science Advances. 2020;6(21). doi: 10.1126/sciadv.aba6913 WOS:000537235300044. 32494751

32. Sethi S, Lin HH, Shepherd AK, Volkan PC, Su CY, Wang JW. Social Context Enhances Hormonal Modulation of Pheromone Detection in Drosophila. Current Biology. 2019;29(22):3887–+. doi: 10.1016/j.cub.2019.09.045 WOS:000497786500028. 31679932

33. Ito H, Sato K, Koganezawa M, Ote M, Matsumoto K, Hama C, et al. Fruitless Recruits Two Antagonistic Chromatin Factors to Establish Single-Neuron Sexual Dimorphism. Cell. 2012;149(6):1327–38. doi: 10.1016/j.cell.2012.04.025 WOS:000305119600016. 22682252

34. Handley A, Schauer T, Ladurner AG, Margulies CE. Designing Cell-Type-Specific Genome-wide Experiments. Molecular Cell. 2015;58(4):621–31. doi: 10.1016/j.molcel.2015.04.024 WOS:000355154000010. 26000847

35. van den Ameelel J, Krautz R, Brand AH. TaDa! Analysing cell type-specific chromatin in vivo with Targeted DamID. Current Opinion in Neurobiology. 2019;56:160–6. doi: 10.1016/j.conb.2019.01.021 WOS:000472704500020. 30844670

36. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Research. 2011;21(3):381–95. doi: 10.1038/cr.2011.22 WOS:000288064900003. 21321607

37. Cao R, Wang LJ, Wang HB, Xia L, Erdjument-Bromage H, Tempst P, et al. Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science. 2002;298(5595):1039–43. doi: 10.1126/science.1076997 WOS:000178932000061. 12351676

38. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(50):21931–6. doi: 10.1073/pnas.1016071107 WOS:000285521500125. 21106759

39. Fischle W, Wang YM, Jacobs SA, Kim YC, Allis CD, Khorasanizadeh S. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 bv Polvcomb and HP1 chromodomains. Genes & Development. 2003;17(15):1870–81. doi: 10.1101/gad.1110503 WOS:000184531500009. 12897054

40. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J. Differential chromatin marking of introns and expressed exons by H3K36me3. Nature Genetics. 2009;41(3):376–81. doi: 10.1038/ng.322 WOS:000263640200022. 19182803

41. Thomas A, Lee PJ, Dalton JE, Nomie KJ, Stoica L, Costa-Mattioli M, et al. A Versatile Method for Cell-Specific Profiling of Translated mRNAs in Drosophila. Plos One. 2012;7(7). doi: 10.1371/journal.pone.0040276 WOS:000306461800060. 22792260

42. Newell NR, New FN, Dalton JE, McIntyre LM, Arbeitman MN. Neurons That Underlie Drosophila melanogaster Reproductive Behaviors: Detection of a Large Male-Bias in Gene Expression in fruitless-Expressing Neurons. G3-Genes Genomes Genetics. 2016;6(8):2455–65. doi: 10.1534/g3.115.019265 WOS:000381282300020. 27247289

43. Brand AH, Perrimon N. TARGETED GENE-EXPRESSION AS A MEANS OF ALTERING CELL FATES AND GENERATING DOMINANT PHENOTYPES. Development. 1993;118(2):401–15. WOS:A1993LH32700009. 8223268

44. Duffy JB. GAL4 system in Drosophila: A fly geneticist’s Swiss army knife. Genesis. 2002;34(1–2):1–15. doi: 10.1002/gene.10150 WOS:000178412900001. 12324939

45. Beckett D, Kovaleva E, Schatz PJ. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Science. 1999;8(4):921–9. doi: 10.1110/ps.8.4.921 WOS:000079596800024. 10211839

46. Riddle NC, Elgin SCR. The Drosophila Dot Chromosome: Where Genes Flourish Amidst Repeats. Genetics. 2018;210(3):757–72. doi: 10.1534/genetics.118.301146 WOS:000449400500003. 30401762

47. Treangen TJ, Salzberg SL. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nature Reviews Genetics. 2012;13(1):36–46. doi: 10.1038/nrg3117 WOS:000298327300011. 22124482

48. Hall JC. THE MATING OF A FLY. Science. 1994;264(5166):1702–14. doi: 10.1126/science.8209251 WOS:A1994NR60000032. 8209251

49. Hing ALY, Carlson JR. Male-male courtship behavior induced by ectopic expression of the Drosophila white gene: Role of sensory function and age. Journal of Neurobiology. 1996;30(4):454–64. WOS:A1996UZ53000002. doi: 10.1002/(SICI)1097-4695(199608)30:4<454::AID-NEU2>3.0.CO;2-2 8844509

50. Yamamoto D, Jallon JM, Komatsu A. Genetic dissection of sexual behavior in Drosophila melanogaster. Annual Review of Entomology. 1997;42:551–85. doi: 10.1146/annurev.ento.42.1.551 WOS:A1997WD49500023. 9017901

51. Zhang SD, Odenwald WF. MISEXPRESSION OF THE WHITE (w) GENE TRIGGERS MALE-MADE COURTSHIP IN DROSOPHILA. Proceedings of the National Academy of Sciences of the United States of America. 1995;92(12):5525–9. doi: 10.1073/pnas.92.12.5525 WOS:A1995RB80400056. 7777542

52. Ramirez F, Ryan DP, Gruning B, Bhardwaj V, Kilpert F, Richter AS, et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Research. 2016;44(W1):W160–W5. doi: 10.1093/nar/gkw257 WOS:000379786800027. 27079975

53. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature. 2011;471(7339):480–+. doi: 10.1038/nature09725 WOS:000288702200055. 21179089

54. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693–705. doi: 10.1016/j.cell.2007.02.005 WOS:000245098600012. 17320507

55. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based Analysis of ChIP-Seq (MACS). Genome Biology. 2008;9(9). doi: 10.1186/gb-2008-9-9-r137 WOS:000260586900015. 18798982

56. Pal K, Forcato M, Jost D, Sexton T, Vaillant C, Salviato E, et al. Global chromatin conformation differences in the Drosophila dosage compensated chromosome X. Nature Communications. 2019;10. doi: 10.1038/s41467-018-07709-6 WOS:000503002300001. 30602777

57. Gelbart ME, Larschan E, Peng SY, Park PJ, Kuroda MI. Drosophila MSL complex globally acetylates H4K16 on the male X chromosome for dosage compensation. Nature Structural & Molecular Biology. 2009;16(8):825–U47. doi: 10.1038/nsmb.1644 WOS:000268738700009. 19648925

58. Voigt P, Tee WW, Reinberg D. A double take on bivalent promoters. Genes & Development. 2013;27(12):1318–38. doi: 10.1101/gad.219626.113 WOS:000320704000002. 23788621

59. Bernstein BE, Mikkelsen TS, Xie XH, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125(2):315–26. doi: 10.1016/j.cell.2006.02.041 WOS:000237241500021. 16630819

60. Zinn K, Ozkan E. Neural immunoglobulin superfamily interaction networks. Current Opinion in Neurobiology. 2017;45:99–105. doi: 10.1016/j.conb.2017.05.010 WOS:000408073900015. 28558267

61. Sanes JR, Zipursky SL. Synaptic Specificity, Recognition Molecules, and Assembly of Neural Circuits. Cell. 2020;181(3):536–56. doi: 10.1016/j.cell.2020.04.008 WOS:000530708400012. 32359437

62. Brovero SG, Fortier JC, Hu H, Lovejoy PC, Newell NR, Palmateer CM, et al. Investigation of Drosophilafruitless neurons that express Dpr/DIP cell adhesion molecules. eLife. 2021;10. doi: 10.7554/eLife.63101 MEDLINE:33616528. 33616528

63. Negre N, Brown CD, Ma LJ, Bristow CA, Miller SW, Wagner U, et al. A cis-regulatory map of the Drosophila genome. Nature. 2011;471(7339):527–31. doi: 10.1038/nature09990 WOS:000288702200065. 21430782

64. Marsano RM, Giordano E, Messina G, Dimitri P. A New Portrait of Constitutive Heterochromatin: Lessons from Drosophila melanogaster. Trends in Genetics. 2019;35(9):615–31. doi: 10.1016/j.tig.2019.06.002 WOS:000480475100001. 31320181

65. Lyne R, Smith R, Rutherford K, Wakeling M, Varley A, Guillier F, et al. FlyMine: an integrated database for Drosophila and Anopheles genomics. Genome Biology. 2007;8(7). doi: 10.1186/gb-2007-8-7-r129 WOS:000249416400009. 17615057

66. Shen LS, M. GeneOverlap: Test and visualize gene overlaps. 2019.

67. Dalton JE, Fear JM, Knott S, Baker BS, McIntyre LM, Arbeitman MN. Male-specific Fruitless isoforms have different regulatory roles conferred by distinct zinc finger DNA binding domains. Bmc Genomics. 2013;14. doi: 10.1186/1471-2164-14-659 WOS:000326172600001. 24074028

68. Neville MC, Nojima T, Ashley E, Parker DJ, Walker J, Southall T, et al. Male-Specific Fruitless Isoforms Target Neurodevelopmental Genes to Specify a Sexually Dimorphic Nervous System. Current Biology. 2014;24(3):229–41. doi: 10.1016/j.cub.2013.11.035 WOS:000330918900017. 24440396

69. Latham KL, Liu YS, Taylor BJ. A small cohort of FRUM and Engrailed-expressing neurons mediate successful copulation in Drosophila melanogaster. Bmc Neuroscience. 2013;14. doi: 10.1186/1471-2202-14-57 WOS:000319455800001. 23688386

70. Chen J, Jin S, Chen D, Cao J, Ji X, Peng Q, et al. fruitless tunes functional flexibility of courtship circuitry during development. eLife. 2021;10. doi: 10.7554/eLife.59224 MEDLINE:33463521. 33463521

71. Conway JR, Lex A, Gehlenborg N. UpSetR: an R package for the visualization of intersecting sets and their properties. Bioinformatics. 2017;33(18):2938–40. doi: 10.1093/bioinformatics/btx364 WOS:000409541400021. 28645171

72. Penalva LOF, Sanchez L. RNA binding protein sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiology and Molecular Biology Reviews. 2003;67(3):343–+. doi: 10.1128/mmbr.67.3.343-359.2003 WOS:000185342200002. 12966139

73. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, et al. Master Transcription Factors and Mediator Establish Super-Enhancers at Key Cell Identity Genes. Cell. 2013;153(2):307–19. doi: 10.1016/j.cell.2013.03.035 WOS:000317349700011. 23582322

74. Loven J, Hoke HA, Lin CY, Lau A, Orlando DA, Vakoc CR, et al. Selective Inhibition of Tumor Oncogenes by Disruption of Super-Enhancers. Cell. 2013;153(2):320–34. doi: 10.1016/j.cell.2013.03.036 WOS:000317349700012. 23582323

75. Yu JY, Kanai MI, Demir E, Jefferis G, Dickson BJ. Cellular Organization of the Neural Circuit that Drives Drosophila Courtship Behavior. Current Biology. 2010;20(18):1602–14. doi: 10.1016/j.cub.2010.08.025 WOS:000282385600020. 20832315

76. Gohl DM, Silies MA, Gao XJJ, Bhalerao S, Luongo FJ, Lin CC, et al. A versatile in vivo system for directed dissection of gene expression patterns. Nature Methods. 2011;8(3):231–U71. doi: 10.1038/nmeth.1561 WOS:000287734800014. 21473015

77. Diao FQ, Ironfield H, Luan HJ, Diao FC, Shropshire WC, Ewer J, et al. Plug-and-Play Genetic Access to Drosophila Cell Types using Exchangeable Exon Cassettes. Cell Reports. 2015;10(8):1410–21. doi: 10.1016/j.celrep.2015.01.059 WOS:000350564200017. 25732830

78. Wood JG, Hillenmeyer S, Lawrence C, Chang CY, Hosier S, Lightfoot W, et al. Chromatin remodeling in the aging genome of Drosophila. Aging Cell. 2010;9(6):971–8. doi: 10.1111/j.1474-9726.2010.00624.x WOS:000284071400005. 20961390

79. Barski A, Jothi R, Cuddapah S, Cui KR, Roh TY, Schones DE, et al. Chromatin poises miRNA- and protein-coding genes for expression (vol 19, pg 1742, 2009). Genome Research. 2009;19(12):2343–. WOS:000272273400019.

80. Goldman TD, Arbeitman MN. Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. Plos Genetics. 2007;3(11):2278–95. doi: 10.1371/journal.pgen.0030216 WOS:000251310200021. 18039034

81. Vernes SC. Genome wide identification of Fruitless targets suggests a role in upregulating genes important for neural circuit formation. Scientific Reports. 2014;4. doi: 10.1038/srep04412 WOS:000333018100001. 24642956

82. Arbeitman MN, Fleming AA, Siegal ML, Null BH, Baker BS. A genomic analysis of Drosophila somatic sexual differentiation and its regulation. Development. 2004;131(9):2007–21. doi: 10.1242/dev.01077 WOS:000221663600012. 15056610

83. Kwasnieski JC, Fiore C, Chaudhari HG, Cohen BA. High-throughput functional testing of ENCODE segmentation predictions. Genome Research. 2014;24(10):1595–602. doi: 10.1101/gr.173518.114 WOS:000342542800004. 25035418

84. Arvey A, Agius P, Noble WS, Leslie C. Sequence and chromatin determinants of cell-type-specific transcription factor binding. Genome Research. 2012;22(9):1723–34. doi: 10.1101/gr.127712.111 WOS:000308272800014. 22955984

85. Brown EJ, Bachtrog D. The chromatin landscape of Drosophila: comparisons between species, sexes, and chromosomes. Genome Research. 2014;24(7):1125–37. doi: 10.1101/gr.172155.114 WOS:000338185000007. 24840603

86. Pulecio J, Verma N, Mejia-Ramirez E, Huangfu D, Raya A. CRISPR/Cas9-Based Engineering of the Epigenome. Cell Stem Cell. 2017;21(4):431–47. doi: 10.1016/j.stem.2017.09.006 WOS:000412344700008. 28985525

87. Brezgin S, Kostyusheva A, Kostyushev D, Chulanov V. Dead Cas Systems: Types, Principles, and Applications. International Journal of Molecular Sciences. 2019;20(23). doi: 10.3390/ijms20236041 WOS:000504428300223. 31801211

88. Griffith LC, Ejima A. Courtship learning in Drosophila melanogaster: Diverse plasticity of a reproductive behavior. Learning & Memory. 2009;16(12):743–50. doi: 10.1101/lm.956309 WOS:000272187900001. 19926779

89. Andrew DJ, Chen EH, Manoli DS, Ryner LC, Arbeitman MN. Sex and the Single Fly: A Perspective on the Career of Bruce S. Baker. Genetics. 2019;212(2):365–76. doi: 10.1534/genetics.119.301928 WOS:000471058500002. 31167898

90. Ito K, Shinomiya K, Ito M, Armstrong JD, Boyan G, Hartenstein V, et al. A Systematic Nomenclature for the Insect Brain. Neuron. 2014;81(4):755–65. doi: 10.1016/j.neuron.2013.12.017 WOS:000331464400007. 24559671

91. Negre N, Lavrov S, Hennetin J, Bellis M, Cavalli G. Mapping the distribution of chromatin proteins by ChIP on chip. DNA Microarrays Part a: Array Platforms and Wet-Bench Protocols. 2006;410:316–+. doi: 10.1016/S0076-6879(06)10015-4 WOS:000244504800015. 16938558

92. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 WOS:000340049100004. 24695404

93. dos Santos G, Schroeder AJ, Goodman JL, Strelets VB, Crosby MA, Thurmond J, et al. FlyBase: introduction of the Drosophila melanogaster Release 6 reference genome assembly and large-scale migration of genome annotations. Nucleic Acids Research. 2015;43(D1):D690–D7. doi: 10.1093/nar/gku1099 WOS:000350210400101. 25398896

94. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105–11. doi: 10.1093/bioinformatics/btp120 WOS:000265523300002. 19289445

95. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. doi: 10.1093/bioinformatics/btp352 WOS:000268808600014. 19505943

96. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. doi: 10.1093/bioinformatics/bts635 WOS:000312654600003. 23104886

97. Kellis M, Wold B, Snyder MP, Bernstein BE, Kundaje A, Marinov GK, et al. Defining functional DNA elements in the human genome. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(17):6131–8. doi: 10.1073/pnas.1318948111 WOS:000335199000025. 24753594

98. Ross-Innes CS, Stark R, Teschendorff AE, Holmes KA, Ali HR, Dunning MJ, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature. 2012;481(7381):389–U177. doi: 10.1038/nature10730 WOS:000299210600048. 22217937

99. Yu GC, Wang LG, He QY. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics. 2015;31(14):2382–3. doi: 10.1093/bioinformatics/btv145 WOS:000358173500022. 25765347

100. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30. doi: 10.1093/bioinformatics/btt656 WOS:000334078300005. 24227677

101. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. doi: 10.1093/bioinformatics/btp616 WOS:000273116100025. 19910308

102. Yu GC, Wang LG, Han YY, He QY. clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters. Omics-a Journal of Integrative Biology. 2012;16(5):284–7. doi: 10.1089/omi.2011.0118 WOS:000303653300007. 22455463

103. Anti-Histone H3 (tri methyl K4) antibody—ChIP Grade (ab8580) Abcam. Available from: https://www.abcam.com/histone-h3-tri-methyl-k4-antibody-chip-grade-ab8580.html.

104. Cichewicz K, Hirsh J. ShinyR-DAM: a program analyzing Drosophila activity, sleep and circadian rhythms. Communications Biology. 2018;1. doi: 10.1038/s42003-018-0031-9 WOS:000461126500025. 29911688

105. Hulsen T, de Vlieg J, Alkema W. BioVenn—a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. Bmc Genomics. 2008;9. doi: 10.1186/1471-2164-9-488 WOS:000261169600001. 18925949

106. Court R, Namiki S, Armstrong JD, Borner J, Card G, Costa M, et al. A Systematic Nomenclature for the Drosophila Ventral Nerve Cord. Neuron. 2020;107(6):1071–+. doi: 10.1016/j.neuron.2020.08.005 32931755


Článek vyšel v časopise

PLOS Genetics


2021 Číslo 4
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

plice
INSIGHTS from European Respiratory Congress
nový kurz

Současné pohledy na riziko v parodontologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#