DOI: 10.1371/journal.pbio.1000435. Robust Target Gene Discovery through Transcriptome Perturbations and Genome-Wide Enhancer Predictions in Drosophila Uncovers a Regulatory Basis for Sensory Specification

Robust Target Gene Discovery through Transcriptome Perturbations and Genome-Wide Enhancer Predictions in Drosophila Uncovers a Regulatory Basis for Sensory Specification

10.1371/journal.pbio.1000435

Crossref journal-article

Public Library of Science (PLoS)

PLoS Biology (340)

Bibliography

Aerts, S., Quan, X.-J., Claeys, A., Naval Sanchez, M., Tate, P., Yan, J., & Hassan, B. A. (2010). Robust Target Gene Discovery through Transcriptome Perturbations and Genome-Wide Enhancer Predictions in Drosophila Uncovers a Regulatory Basis for Sensory Specification. PLoS Biology, 8(7), e1000435.

Authors 7

Stein Aerts (first)
Xiao-Jiang Quan (additional)
Annelies Claeys (additional)
Marina Naval Sanchez (additional)
Phillip Tate (additional)
Jiekun Yan (additional)
Bassem A. Hassan (additional)

References 72 Referenced 89

10.1038/ng2012 / Nat Genet / Genetic reconstruction of a functional transcriptional regulatory network. by Z Hu (2007)
10.1038/nature02800 / Nature / Transcriptional regulatory code of a eukaryotic genome. by C. T Harbison (2004)
10.1126/science.1123404 / Science / Regulatory blueprint for a chordate embryo. by K Imai (2006)
10.1126/science.1069883 / Science / A genomic regulatory network for development. by E Davidson (2002)
10.1016/j.devcel.2005.09.005 / Dev Cell / Genomic regulatory networks and animal development. by A Stathopoulos (2005)
10.1101/gad.1509007 / Genes Dev / A core transcriptional network for early mesoderm development in Drosophila melanogaster. by T Sandmann (2007)
10.1101/gad.1509607 / Genes Dev / Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. by J Zeitlinger (2007)
10.1016/j.ydbio.2009.02.029 / Dev Biol / A perturbation model of the gene regulatory network for oral and aboral ectoderm specification in the sea urchin embryo. by Y. H Su (2009)
10.1242/dev.026419 / Development / Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system. by K. S Imai (2009)
10.1073/pnas.0806501105 / Proc Natl Acad Sci U S A / A gene regulatory network armature for T lymphocyte specification. by C Georgescu (2008)
10.1093/nar/gkp464 / Nucleic Acids Res / Pscan: finding over-represented transcription factor binding site motifs in sequences from co-regulated or co-expressed genes. by F Zambelli (2009)
10.1093/bioinformatics/btn627 / Bioinformatics / PASTAA: identifying transcription factors associated with sets of co-regulated genes. by H. G Roider (2009)
10.1093/nar/gkm427 / Nucleic Acids Res / oPOSSUM: integrated tools for analysis of regulatory motif over-representation. by S. J Ho Sui (2007)
10.1093/nar/gkh299 / Nucleic Acids Res / Detection of functional DNA motifs via statistical over-representation. by M. C Frith (2004)
10.1093/nar/gkl224 / Nucleic Acids Res / Stubb: a program for discovery and analysis of cis-regulatory modules. by S Sinha (2006)
10.1371/journal.pcbi.1000652 / PLoS Comput Biol / Functional characterization of transcription factor motifs using cross-species comparison across large evolutionary distances. by J Kim
10.1093/nar/gkg540 / Nucleic Acids Res / Cluster-Buster: finding dense clusters of motifs in DNA sequences. by C. M Frith (2003)
10.1038/nmeth.1188 / Nat Methods / Systematic identification of mammalian regulatory motifs' target genes and functions. by J. B Warner (2008)
10.1101/gr.094144.109 / Genome Res / Distinguishing direct versus indirect transcription factor-DNA interactions. by R Gordan (2009)
10.1186/gb-2008-9-4-r66 / Genome Biol / ModuleMiner - improved computational detection of cis-regulatory modules: are there different modes of gene regulation in embryonic development and adult tissues? by P Van Loo (2008)
10.1016/j.gde.2007.05.003 / Curr Opin Genet Dev / Generating patterned arrays of photoreceptors. by J Morante (2007)
10.1038/nature04376 / Nature / Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing. by D Ferres-Marco (2006)
10.1371/journal.pbio.1000040 / PLoS Biol / The atonal proneural transcription factor links differentiation and tumor formation in Drosophila. by W Bossuyt (2009)
10.1101/gad.1509607 / Genes Dev / Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. by J Zeitlinger (2007)
10.1016/j.devcel.2005.09.005 / Dev Cell / Genomic regulatory networks and animal development. by A Stathopoulos (2005)
10.1016/S0092-8674(02)01087-5 / Cell / Whole-genome analysis of dorsal-ventral patterning in the Drosophila embryo. by A Stathopoulos (2002)
10.1093/nar/gkp939 / Nucleic Acids Res / The UCSC Genome Browser database: update 2010. by B Rhead
10.1371/journal.pone.0001115 / PLoS ONE / Fine-tuning enhancer models to predict transcriptional targets across multiple genomes. by S Aerts (2007)
10.1038/nbt1203 / Nat Biotechnol / Gene prioritization through genomic data fusion. by S Aerts (2006)
10.1128/MCB.01685-06 / Mol Cell Biol / Proneural basic helix-loop-helix proteins and epidermal growth factor receptor signaling coordinately regulate cell type specification and cdk inhibitor expression during development. by M. J Sukhanova (2007)
10.1128/MCB.24.21.9517-9526.2004 / Mol Cell Biol / The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites. by L. M Powell (2004)
10.1242/dev.028951 / Development / Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate. by K. L Pepple (2008)
10.1016/j.cell.2009.01.058 / Cell / A microRNA imparts robustness against environmental fluctuation during development. by X Li (2009)
10.1038/nature06340 / Nature / Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. by A Stark (2007)
10.1038/369398a0 / Nature / Atonal is the proneural gene for Drosophila photoreceptors. by A. P Jarman (1994)
10.1016/j.devcel.2005.01.020 / Dev Cell / Genetic programs activated by proneural proteins in the developing Drosophila PNS. by N Reeves (2005)
10.1006/dbio.1999.9324 / Dev Biol / Discrete enhancer elements mediate selective responsiveness of enhancer of split complex genes to common transcriptional activators. by D. T Nellesen (1999)
10.1101/gr.3642605 / Genome Res / Evaluation of regulatory potential and conservation scores for detecting cis-regulatory modules in aligned mammalian genome sequences. by D. C King (2005)
10.1073/pnas.0611511104 / Proc Natl Acad Sci U S A / An optimized transgenesis system for Drosophila using germ-line-specific varphiC31 integrases. by J Bischof (2007)
10.1534/genetics.166.4.1775 / Genetics / Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. by A. C Groth (2004)
10.1126/science.1134426 / Science / P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. by K. J Venken (2006)
10.1016/j.devcel.2004.09.015 / Dev Cell / EGF receptor signaling triggers recruitment of Drosophila sense organ precursors by stimulating proneural gene autoregulation. by P zur Lage (2004)
10.1242/dev.121.7.2019 / Development / Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. by A. P Jarman (1995)
10.1038/nrg2499 / Nat Rev Genet / The evolution of hierarchical gene regulatory networks. by D. H Erwin (2009)
10.1101/gr.4673006 / Genome Res / Genome-wide identification of direct targets of the Drosophila retinal determination protein Eyeless. by J. E Ostrin (2006)
10.1093/nar/gkn660 / Nucleic Acids Res / UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. by D. E Newburger (2009)
10.1093/nar/gkn048 / Nucleic Acids Res / A systematic characterization of factors that regulate Drosophila segmentation via a bacterial one-hybrid system. by M. B Noyes (2008)
10.1093/nar/gki439 / Nucleic Acids Res / enoLOGOS: a versatile web tool for energy normalized sequence logos. by C Workman (2005)
10.1038/nrg1315 / Nat Rev Genet / Applied bioinformatics for the identification of regulatory elements. by W Wasserman (2004)
10.1093/bioinformatics/16.1.16 / Bioinformatics / DNA binding sites: representation and discovery. by G. D Stormo (2000)
10.1242/dev.026054 / Development / Fasciclin 2, the Drosophila orthologue of neural cell-adhesion molecule, inhibits EGF receptor signalling. by Y Mao (2009)
10.1126/science.1181453 / Science / Deletion of Atoh1 disrupts Sonic Hedgehog signaling in the developing cerebellum and prevents medulloblastoma. by A Flora (2009)
10.1371/journal.pbio.1000039 / PLoS Biol / Atonal homolog 1 is a tumor suppressor gene. by W Bossuyt (2009)
10.1371/journal.pcbi.0020053 / PLoS Comput Biol / Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells. by A Philippakis (2006)
10.1016/j.devcel.2006.04.009 / Dev Cell / A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development. by T Sandmann (2006)
10.1016/S0960-9822(02)01144-2 / Curr Biol / Drosophila atonal fully rescues the phenotype of Math1 null mice: new functions evolve in new cellular contexts. by V. Y Wang (2002)
10.1186/gb-2004-5-10-r80 / Genome Biol / Bioconductor: open software development for computational biology and bioinformatics. by R. C Gentleman (2004)
10.2202/1544-6115.1027 / Stat Appl Genet Mol Biol / Linear models and empirical bayes methods for assessing differential expression in microarray experiments. by G. K Smyth (2004)
10.1111/j.2517-6161.1995.tb02031.x / J R Stat Soc Series B Stat Methodol / Controlling the false discovery rate: a practical and powerful approach to multiple testing. by Y Benjamini (1995)
10.1093/nar/gkg268 / Nucleic Acids Res / Toucan: deciphering the cis-regulatory logic of coregulated genes. by S Aerts (2003)
10.1093/nar/gkm876 / Nucleic Acids Res / REDfly 2.0: an integrated database of cis-regulatory modules and transcription factor binding sites in Drosophila. by M. S Halfon (2008)
{'key': 'ref62', 'article-title': 'ORegAnno: an open-access community-driven resource for regulatory annotation.', 'author': 'O Griffith', 'year': '2007', 'journal-title': 'Nucleic Acids Res'} / Nucleic Acids Res / ORegAnno: an open-access community-driven resource for regulatory annotation. by O Griffith (2007)
10.1093/bioinformatics/bti173 / Bioinformatics / Drosophila DNase I footprint database: a systematic genome annotation of transcription factor binding sites in the fruitfly, Drosophila. by M. C Bergman (2005)
10.2144/00294bm10 / Biotechniques / GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. by S Barolo (2000)
10.1101/gad.1122403 / Genes Dev / Senseless acts as a binary switch during sensory organ precursor selection. by H Jafar-Nejad (2003)
10.1016/0925-4773(95)00382-7 / Mech Dev / Dual organisation of the Drosophila neuropeptide receptor NKD gene promoter. by P Rosay (1995)
10.1242/dev.127.6.1185 / Development / Autoregulation and multiple enhancers control Math1 expression in the developing nervous system. by A. W Helms (2000)
10.1242/dev.01302 / Development / Highly specific interactions between bHLH transcription factors and chromatin during retina development. by D Skowronska-Krawczyk (2004)
10.1038/embor.2008.34 / EMBO Rep / Gene induction following wounding of wild-type versus macrophage-deficient Drosophila embryos. by B Stramer (2008)
10.1101/gad.437607 / Genes Dev / Temporal ChIP-on-chip reveals Biniou as a universal regulator of the visceral muscle transcriptional network. by J. S Jakobsen (2007)
10.1371/journal.pbio.0060027 / PLoS Biol / Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. by X. Y Li (2008)
10.1016/S0092-8674(00)00040-4 / Cell / Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. by R Nolo (2000)

Dates

Type	When
Created	15 years ago (July 27, 2010, 5:35 p.m.)
Deposited	6 months ago (Feb. 23, 2025, 7:22 a.m.)
Indexed	2 months ago (June 20, 2025, 8:06 a.m.)
Issued	15 years, 1 month ago (July 27, 2010)
Published	15 years, 1 month ago (July 27, 2010)
Published Online	15 years, 1 month ago (July 27, 2010)

Funders 0

None

BibTeX

@article{Aerts_2010, title={Robust Target Gene Discovery through Transcriptome Perturbations and Genome-Wide Enhancer Predictions in Drosophila Uncovers a Regulatory Basis for Sensory Specification}, volume={8}, ISSN={1545-7885}, url={http://dx.doi.org/10.1371/journal.pbio.1000435}, DOI={10.1371/journal.pbio.1000435}, number={7}, journal={PLoS Biology}, publisher={Public Library of Science (PLoS)}, author={Aerts, Stein and Quan, Xiao-Jiang and Claeys, Annelies and Naval Sanchez, Marina and Tate, Phillip and Yan, Jiekun and Hassan, Bassem A.}, editor={Eisen, Michael B.}, year={2010}, month=jul, pages={e1000435} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        20
      ]
    ],
    "date-time": "2025-06-20T12:06:48Z",
    "timestamp": 1750421208588,
    "version": "3.37.3"
  },
  "reference-count": 72,
  "publisher": "Public Library of Science (PLoS)",
  "issue": "7",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2010,
            7,
            27
          ]
        ],
        "date-time": "2010-07-27T00:00:00Z",
        "timestamp": 1280188800000
      },
      "content-version": "unspecified",
      "delay-in-days": 0,
      "URL": "http://creativecommons.org/licenses/by/4.0/"
    }
  ],
  "content-domain": {
    "domain": [
      "www.plosbiology.org"
    ],
    "crossmark-restriction": false
  },
  "DOI": "10.1371/journal.pbio.1000435",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2010,
        7,
        27
      ]
    ],
    "date-time": "2010-07-27T21:35:32Z",
    "timestamp": 1280266532000
  },
  "page": "e1000435",
  "update-policy": "https://doi.org/10.1371/journal.pbio.corrections_policy",
  "source": "Crossref",
  "is-referenced-by-count": 89,
  "title": "Robust Target Gene Discovery through Transcriptome Perturbations and Genome-Wide Enhancer Predictions in Drosophila Uncovers a Regulatory Basis for Sensory Specification",
  "prefix": "10.1371",
  "volume": "8",
  "author": [
    {
      "given": "Stein",
      "family": "Aerts",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Xiao-Jiang",
      "family": "Quan",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Annelies",
      "family": "Claeys",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Marina",
      "family": "Naval Sanchez",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Phillip",
      "family": "Tate",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Jiekun",
      "family": "Yan",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Bassem A.",
      "family": "Hassan",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "340",
  "published-online": {
    "date-parts": [
      [
        2010,
        7,
        27
      ]
    ]
  },
  "reference": [
    {
      "key": "ref1",
      "doi-asserted-by": "crossref",
      "first-page": "683",
      "DOI": "10.1038/ng2012",
      "article-title": "Genetic reconstruction of a functional transcriptional regulatory network.",
      "volume": "39",
      "author": "Z Hu",
      "year": "2007",
      "journal-title": "Nat Genet"
    },
    {
      "key": "ref2",
      "doi-asserted-by": "crossref",
      "first-page": "99",
      "DOI": "10.1038/nature02800",
      "article-title": "Transcriptional regulatory code of a eukaryotic genome.",
      "volume": "431",
      "author": "C. T Harbison",
      "year": "2004",
      "journal-title": "Nature"
    },
    {
      "key": "ref3",
      "doi-asserted-by": "crossref",
      "first-page": "1183",
      "DOI": "10.1126/science.1123404",
      "article-title": "Regulatory blueprint for a chordate embryo.",
      "volume": "312",
      "author": "K Imai",
      "year": "2006",
      "journal-title": "Science"
    },
    {
      "key": "ref4",
      "doi-asserted-by": "crossref",
      "first-page": "1669",
      "DOI": "10.1126/science.1069883",
      "article-title": "A genomic regulatory network for development.",
      "volume": "295",
      "author": "E Davidson",
      "year": "2002",
      "journal-title": "Science"
    },
    {
      "key": "ref5",
      "doi-asserted-by": "crossref",
      "first-page": "449",
      "DOI": "10.1016/j.devcel.2005.09.005",
      "article-title": "Genomic regulatory networks and animal development.",
      "volume": "9",
      "author": "A Stathopoulos",
      "year": "2005",
      "journal-title": "Dev Cell"
    },
    {
      "key": "ref6",
      "doi-asserted-by": "crossref",
      "first-page": "436",
      "DOI": "10.1101/gad.1509007",
      "article-title": "A core transcriptional network for early mesoderm development in Drosophila melanogaster.",
      "volume": "21",
      "author": "T Sandmann",
      "year": "2007",
      "journal-title": "Genes Dev"
    },
    {
      "key": "ref7",
      "doi-asserted-by": "crossref",
      "first-page": "385",
      "DOI": "10.1101/gad.1509607",
      "article-title": "Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo.",
      "volume": "21",
      "author": "J Zeitlinger",
      "year": "2007",
      "journal-title": "Genes Dev"
    },
    {
      "key": "ref8",
      "doi-asserted-by": "crossref",
      "first-page": "410",
      "DOI": "10.1016/j.ydbio.2009.02.029",
      "article-title": "A perturbation model of the gene regulatory network for oral and aboral ectoderm specification in the sea urchin embryo.",
      "volume": "329",
      "author": "Y. H Su",
      "year": "2009",
      "journal-title": "Dev Biol"
    },
    {
      "key": "ref9",
      "doi-asserted-by": "crossref",
      "first-page": "285",
      "DOI": "10.1242/dev.026419",
      "article-title": "Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system.",
      "volume": "136",
      "author": "K. S Imai",
      "year": "2009",
      "journal-title": "Development"
    },
    {
      "key": "ref10",
      "doi-asserted-by": "crossref",
      "first-page": "20100",
      "DOI": "10.1073/pnas.0806501105",
      "article-title": "A gene regulatory network armature for T lymphocyte specification.",
      "volume": "105",
      "author": "C Georgescu",
      "year": "2008",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "ref11",
      "doi-asserted-by": "crossref",
      "first-page": "W247",
      "DOI": "10.1093/nar/gkp464",
      "article-title": "Pscan: finding over-represented transcription factor binding site motifs in sequences from co-regulated or co-expressed genes.",
      "volume": "37",
      "author": "F Zambelli",
      "year": "2009",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref12",
      "doi-asserted-by": "crossref",
      "first-page": "435",
      "DOI": "10.1093/bioinformatics/btn627",
      "article-title": "PASTAA: identifying transcription factors associated with sets of co-regulated genes.",
      "volume": "25",
      "author": "H. G Roider",
      "year": "2009",
      "journal-title": "Bioinformatics"
    },
    {
      "key": "ref13",
      "doi-asserted-by": "crossref",
      "first-page": "W245",
      "DOI": "10.1093/nar/gkm427",
      "article-title": "oPOSSUM: integrated tools for analysis of regulatory motif over-representation.",
      "volume": "35",
      "author": "S. J Ho Sui",
      "year": "2007",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref14",
      "doi-asserted-by": "crossref",
      "first-page": "1372",
      "DOI": "10.1093/nar/gkh299",
      "article-title": "Detection of functional DNA motifs via statistical over-representation.",
      "volume": "32",
      "author": "M. C Frith",
      "year": "2004",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref15",
      "doi-asserted-by": "crossref",
      "first-page": "W555",
      "DOI": "10.1093/nar/gkl224",
      "article-title": "Stubb: a program for discovery and analysis of cis-regulatory modules.",
      "volume": "34",
      "author": "S Sinha",
      "year": "2006",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref16",
      "doi-asserted-by": "crossref",
      "first-page": "e1000652",
      "DOI": "10.1371/journal.pcbi.1000652",
      "article-title": "Functional characterization of transcription factor motifs using cross-species comparison across large evolutionary distances.",
      "volume": "6",
      "author": "J Kim",
      "journal-title": "PLoS Comput Biol"
    },
    {
      "key": "ref17",
      "doi-asserted-by": "crossref",
      "first-page": "3666",
      "DOI": "10.1093/nar/gkg540",
      "article-title": "Cluster-Buster: finding dense clusters of motifs in DNA sequences.",
      "volume": "31",
      "author": "C. M Frith",
      "year": "2003",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref18",
      "doi-asserted-by": "crossref",
      "first-page": "347",
      "DOI": "10.1038/nmeth.1188",
      "article-title": "Systematic identification of mammalian regulatory motifs&apos; target genes and functions.",
      "volume": "5",
      "author": "J. B Warner",
      "year": "2008",
      "journal-title": "Nat Methods"
    },
    {
      "key": "ref19",
      "doi-asserted-by": "crossref",
      "first-page": "2090",
      "DOI": "10.1101/gr.094144.109",
      "article-title": "Distinguishing direct versus indirect transcription factor-DNA interactions.",
      "volume": "19",
      "author": "R Gordan",
      "year": "2009",
      "journal-title": "Genome Res"
    },
    {
      "key": "ref20",
      "doi-asserted-by": "crossref",
      "first-page": "R66",
      "DOI": "10.1186/gb-2008-9-4-r66",
      "article-title": "ModuleMiner - improved computational detection of cis-regulatory modules: are there different modes of gene regulation in embryonic development and adult tissues?",
      "volume": "9",
      "author": "P Van Loo",
      "year": "2008",
      "journal-title": "Genome Biol"
    },
    {
      "key": "ref21",
      "doi-asserted-by": "crossref",
      "first-page": "314",
      "DOI": "10.1016/j.gde.2007.05.003",
      "article-title": "Generating patterned arrays of photoreceptors.",
      "volume": "17",
      "author": "J Morante",
      "year": "2007",
      "journal-title": "Curr Opin Genet Dev"
    },
    {
      "key": "ref22",
      "doi-asserted-by": "crossref",
      "first-page": "430",
      "DOI": "10.1038/nature04376",
      "article-title": "Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing.",
      "volume": "439",
      "author": "D Ferres-Marco",
      "year": "2006",
      "journal-title": "Nature"
    },
    {
      "key": "ref23",
      "doi-asserted-by": "crossref",
      "first-page": "e40",
      "DOI": "10.1371/journal.pbio.1000040",
      "article-title": "The atonal proneural transcription factor links differentiation and tumor formation in Drosophila.",
      "volume": "7",
      "author": "W Bossuyt",
      "year": "2009",
      "journal-title": "PLoS Biol"
    },
    {
      "key": "ref24",
      "doi-asserted-by": "crossref",
      "first-page": "385",
      "DOI": "10.1101/gad.1509607",
      "article-title": "Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo.",
      "volume": "21",
      "author": "J Zeitlinger",
      "year": "2007",
      "journal-title": "Genes Dev"
    },
    {
      "key": "ref25",
      "doi-asserted-by": "crossref",
      "first-page": "449",
      "DOI": "10.1016/j.devcel.2005.09.005",
      "article-title": "Genomic regulatory networks and animal development.",
      "volume": "9",
      "author": "A Stathopoulos",
      "year": "2005",
      "journal-title": "Dev Cell"
    },
    {
      "key": "ref26",
      "doi-asserted-by": "crossref",
      "first-page": "687",
      "DOI": "10.1016/S0092-8674(02)01087-5",
      "article-title": "Whole-genome analysis of dorsal-ventral patterning in the Drosophila embryo.",
      "volume": "111",
      "author": "A Stathopoulos",
      "year": "2002",
      "journal-title": "Cell"
    },
    {
      "key": "ref27",
      "doi-asserted-by": "crossref",
      "first-page": "D613",
      "DOI": "10.1093/nar/gkp939",
      "article-title": "The UCSC Genome Browser database: update 2010.",
      "volume": "38",
      "author": "B Rhead",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref28",
      "doi-asserted-by": "crossref",
      "first-page": "e1115",
      "DOI": "10.1371/journal.pone.0001115",
      "article-title": "Fine-tuning enhancer models to predict transcriptional targets across multiple genomes.",
      "volume": "2",
      "author": "S Aerts",
      "year": "2007",
      "journal-title": "PLoS ONE"
    },
    {
      "key": "ref29",
      "doi-asserted-by": "crossref",
      "first-page": "537",
      "DOI": "10.1038/nbt1203",
      "article-title": "Gene prioritization through genomic data fusion.",
      "volume": "24",
      "author": "S Aerts",
      "year": "2006",
      "journal-title": "Nat Biotechnol"
    },
    {
      "key": "ref30",
      "doi-asserted-by": "crossref",
      "first-page": "2987",
      "DOI": "10.1128/MCB.01685-06",
      "article-title": "Proneural basic helix-loop-helix proteins and epidermal growth factor receptor signaling coordinately regulate cell type specification and cdk inhibitor expression during development.",
      "volume": "27",
      "author": "M. J Sukhanova",
      "year": "2007",
      "journal-title": "Mol Cell Biol"
    },
    {
      "key": "ref31",
      "doi-asserted-by": "crossref",
      "first-page": "9517",
      "DOI": "10.1128/MCB.24.21.9517-9526.2004",
      "article-title": "The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites.",
      "volume": "24",
      "author": "L. M Powell",
      "year": "2004",
      "journal-title": "Mol Cell Biol"
    },
    {
      "key": "ref32",
      "doi-asserted-by": "crossref",
      "first-page": "4071",
      "DOI": "10.1242/dev.028951",
      "article-title": "Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate.",
      "volume": "135",
      "author": "K. L Pepple",
      "year": "2008",
      "journal-title": "Development"
    },
    {
      "key": "ref33",
      "doi-asserted-by": "crossref",
      "first-page": "273",
      "DOI": "10.1016/j.cell.2009.01.058",
      "article-title": "A microRNA imparts robustness against environmental fluctuation during development.",
      "volume": "137",
      "author": "X Li",
      "year": "2009",
      "journal-title": "Cell"
    },
    {
      "key": "ref34",
      "doi-asserted-by": "crossref",
      "first-page": "219",
      "DOI": "10.1038/nature06340",
      "article-title": "Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures.",
      "volume": "450",
      "author": "A Stark",
      "year": "2007",
      "journal-title": "Nature"
    },
    {
      "key": "ref35",
      "doi-asserted-by": "crossref",
      "first-page": "398",
      "DOI": "10.1038/369398a0",
      "article-title": "Atonal is the proneural gene for Drosophila photoreceptors.",
      "volume": "369",
      "author": "A. P Jarman",
      "year": "1994",
      "journal-title": "Nature"
    },
    {
      "key": "ref36",
      "doi-asserted-by": "crossref",
      "first-page": "413",
      "DOI": "10.1016/j.devcel.2005.01.020",
      "article-title": "Genetic programs activated by proneural proteins in the developing Drosophila PNS.",
      "volume": "8",
      "author": "N Reeves",
      "year": "2005",
      "journal-title": "Dev Cell"
    },
    {
      "key": "ref37",
      "doi-asserted-by": "crossref",
      "first-page": "33",
      "DOI": "10.1006/dbio.1999.9324",
      "article-title": "Discrete enhancer elements mediate selective responsiveness of enhancer of split complex genes to common transcriptional activators.",
      "volume": "213",
      "author": "D. T Nellesen",
      "year": "1999",
      "journal-title": "Dev Biol"
    },
    {
      "key": "ref38",
      "doi-asserted-by": "crossref",
      "first-page": "1051",
      "DOI": "10.1101/gr.3642605",
      "article-title": "Evaluation of regulatory potential and conservation scores for detecting cis-regulatory modules in aligned mammalian genome sequences.",
      "volume": "15",
      "author": "D. C King",
      "year": "2005",
      "journal-title": "Genome Res"
    },
    {
      "key": "ref39",
      "doi-asserted-by": "crossref",
      "first-page": "3312",
      "DOI": "10.1073/pnas.0611511104",
      "article-title": "An optimized transgenesis system for Drosophila using germ-line-specific varphiC31 integrases.",
      "volume": "104",
      "author": "J Bischof",
      "year": "2007",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "ref40",
      "doi-asserted-by": "crossref",
      "first-page": "1775",
      "DOI": "10.1534/genetics.166.4.1775",
      "article-title": "Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31.",
      "volume": "166",
      "author": "A. C Groth",
      "year": "2004",
      "journal-title": "Genetics"
    },
    {
      "key": "ref41",
      "doi-asserted-by": "crossref",
      "first-page": "1747",
      "DOI": "10.1126/science.1134426",
      "article-title": "P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster.",
      "volume": "314",
      "author": "K. J Venken",
      "year": "2006",
      "journal-title": "Science"
    },
    {
      "key": "ref42",
      "doi-asserted-by": "crossref",
      "first-page": "687",
      "DOI": "10.1016/j.devcel.2004.09.015",
      "article-title": "EGF receptor signaling triggers recruitment of Drosophila sense organ precursors by stimulating proneural gene autoregulation.",
      "volume": "7",
      "author": "P zur Lage",
      "year": "2004",
      "journal-title": "Dev Cell"
    },
    {
      "key": "ref43",
      "doi-asserted-by": "crossref",
      "first-page": "2019",
      "DOI": "10.1242/dev.121.7.2019",
      "article-title": "Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors.",
      "volume": "121",
      "author": "A. P Jarman",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "ref44",
      "doi-asserted-by": "crossref",
      "first-page": "141",
      "DOI": "10.1038/nrg2499",
      "article-title": "The evolution of hierarchical gene regulatory networks.",
      "volume": "10",
      "author": "D. H Erwin",
      "year": "2009",
      "journal-title": "Nat Rev Genet"
    },
    {
      "key": "ref45",
      "doi-asserted-by": "crossref",
      "first-page": "466",
      "DOI": "10.1101/gr.4673006",
      "article-title": "Genome-wide identification of direct targets of the Drosophila retinal determination protein Eyeless.",
      "volume": "16",
      "author": "J. E Ostrin",
      "year": "2006",
      "journal-title": "Genome Res"
    },
    {
      "key": "ref46",
      "doi-asserted-by": "crossref",
      "first-page": "D77",
      "DOI": "10.1093/nar/gkn660",
      "article-title": "UniPROBE: an online database of protein binding microarray data on protein-DNA interactions.",
      "volume": "37",
      "author": "D. E Newburger",
      "year": "2009",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref47",
      "doi-asserted-by": "crossref",
      "first-page": "2547",
      "DOI": "10.1093/nar/gkn048",
      "article-title": "A systematic characterization of factors that regulate Drosophila segmentation via a bacterial one-hybrid system.",
      "volume": "36",
      "author": "M. B Noyes",
      "year": "2008",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref48",
      "doi-asserted-by": "crossref",
      "first-page": "W389",
      "DOI": "10.1093/nar/gki439",
      "article-title": "enoLOGOS: a versatile web tool for energy normalized sequence logos.",
      "volume": "33",
      "author": "C Workman",
      "year": "2005",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref49",
      "doi-asserted-by": "crossref",
      "first-page": "276",
      "DOI": "10.1038/nrg1315",
      "article-title": "Applied bioinformatics for the identification of regulatory elements.",
      "volume": "5",
      "author": "W Wasserman",
      "year": "2004",
      "journal-title": "Nat Rev Genet"
    },
    {
      "key": "ref50",
      "doi-asserted-by": "crossref",
      "first-page": "16",
      "DOI": "10.1093/bioinformatics/16.1.16",
      "article-title": "DNA binding sites: representation and discovery.",
      "volume": "16",
      "author": "G. D Stormo",
      "year": "2000",
      "journal-title": "Bioinformatics"
    },
    {
      "key": "ref51",
      "doi-asserted-by": "crossref",
      "first-page": "473",
      "DOI": "10.1242/dev.026054",
      "article-title": "Fasciclin 2, the Drosophila orthologue of neural cell-adhesion molecule, inhibits EGF receptor signalling.",
      "volume": "136",
      "author": "Y Mao",
      "year": "2009",
      "journal-title": "Development"
    },
    {
      "key": "ref52",
      "doi-asserted-by": "crossref",
      "first-page": "1424",
      "DOI": "10.1126/science.1181453",
      "article-title": "Deletion of Atoh1 disrupts Sonic Hedgehog signaling in the developing cerebellum and prevents medulloblastoma.",
      "volume": "326",
      "author": "A Flora",
      "year": "2009",
      "journal-title": "Science"
    },
    {
      "key": "ref53",
      "doi-asserted-by": "crossref",
      "first-page": "e39",
      "DOI": "10.1371/journal.pbio.1000039",
      "article-title": "Atonal homolog 1 is a tumor suppressor gene.",
      "volume": "7",
      "author": "W Bossuyt",
      "year": "2009",
      "journal-title": "PLoS Biol"
    },
    {
      "key": "ref54",
      "doi-asserted-by": "crossref",
      "first-page": "e53",
      "DOI": "10.1371/journal.pcbi.0020053",
      "article-title": "Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells.",
      "volume": "2",
      "author": "A Philippakis",
      "year": "2006",
      "journal-title": "PLoS Comput Biol"
    },
    {
      "key": "ref55",
      "doi-asserted-by": "crossref",
      "first-page": "797",
      "DOI": "10.1016/j.devcel.2006.04.009",
      "article-title": "A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development.",
      "volume": "10",
      "author": "T Sandmann",
      "year": "2006",
      "journal-title": "Dev Cell"
    },
    {
      "key": "ref56",
      "doi-asserted-by": "crossref",
      "first-page": "1611",
      "DOI": "10.1016/S0960-9822(02)01144-2",
      "article-title": "Drosophila atonal fully rescues the phenotype of Math1 null mice: new functions evolve in new cellular contexts.",
      "volume": "12",
      "author": "V. Y Wang",
      "year": "2002",
      "journal-title": "Curr Biol"
    },
    {
      "key": "ref57",
      "doi-asserted-by": "crossref",
      "first-page": "R80",
      "DOI": "10.1186/gb-2004-5-10-r80",
      "article-title": "Bioconductor: open software development for computational biology and bioinformatics.",
      "volume": "5",
      "author": "R. C Gentleman",
      "year": "2004",
      "journal-title": "Genome Biol"
    },
    {
      "key": "ref58",
      "doi-asserted-by": "crossref",
      "first-page": "Article3",
      "DOI": "10.2202/1544-6115.1027",
      "article-title": "Linear models and empirical bayes methods for assessing differential expression in microarray experiments.",
      "volume": "3",
      "author": "G. K Smyth",
      "year": "2004",
      "journal-title": "Stat Appl Genet Mol Biol"
    },
    {
      "key": "ref59",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1111/j.2517-6161.1995.tb02031.x",
      "article-title": "Controlling the false discovery rate: a practical and powerful approach to multiple testing.",
      "volume": "57",
      "author": "Y Benjamini",
      "year": "1995",
      "journal-title": "J R Stat Soc Series B Stat Methodol"
    },
    {
      "key": "ref60",
      "doi-asserted-by": "crossref",
      "first-page": "1753",
      "DOI": "10.1093/nar/gkg268",
      "article-title": "Toucan: deciphering the cis-regulatory logic of coregulated genes.",
      "volume": "31",
      "author": "S Aerts",
      "year": "2003",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref61",
      "doi-asserted-by": "crossref",
      "first-page": "D594",
      "DOI": "10.1093/nar/gkm876",
      "article-title": "REDfly 2.0: an integrated database of cis-regulatory modules and transcription factor binding sites in Drosophila.",
      "volume": "36",
      "author": "M. S Halfon",
      "year": "2008",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref62",
      "article-title": "ORegAnno: an open-access community-driven resource for regulatory annotation.",
      "author": "O Griffith",
      "year": "2007",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "ref63",
      "doi-asserted-by": "crossref",
      "first-page": "1747",
      "DOI": "10.1093/bioinformatics/bti173",
      "article-title": "Drosophila DNase I footprint database: a systematic genome annotation of transcription factor binding sites in the fruitfly, Drosophila.",
      "volume": "21",
      "author": "M. C Bergman",
      "year": "2005",
      "journal-title": "Bioinformatics"
    },
    {
      "key": "ref64",
      "doi-asserted-by": "crossref",
      "first-page": "726",
      "DOI": "10.2144/00294bm10",
      "article-title": "GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila.",
      "volume": "29",
      "author": "S Barolo",
      "year": "2000",
      "journal-title": "Biotechniques"
    },
    {
      "key": "ref65",
      "doi-asserted-by": "crossref",
      "first-page": "2966",
      "DOI": "10.1101/gad.1122403",
      "article-title": "Senseless acts as a binary switch during sensory organ precursor selection.",
      "volume": "17",
      "author": "H Jafar-Nejad",
      "year": "2003",
      "journal-title": "Genes Dev"
    },
    {
      "key": "ref66",
      "doi-asserted-by": "crossref",
      "first-page": "329",
      "DOI": "10.1016/0925-4773(95)00382-7",
      "article-title": "Dual organisation of the Drosophila neuropeptide receptor NKD gene promoter.",
      "volume": "51",
      "author": "P Rosay",
      "year": "1995",
      "journal-title": "Mech Dev"
    },
    {
      "key": "ref67",
      "doi-asserted-by": "crossref",
      "first-page": "1185",
      "DOI": "10.1242/dev.127.6.1185",
      "article-title": "Autoregulation and multiple enhancers control Math1 expression in the developing nervous system.",
      "volume": "127",
      "author": "A. W Helms",
      "year": "2000",
      "journal-title": "Development"
    },
    {
      "key": "ref68",
      "doi-asserted-by": "crossref",
      "first-page": "4447",
      "DOI": "10.1242/dev.01302",
      "article-title": "Highly specific interactions between bHLH transcription factors and chromatin during retina development.",
      "volume": "131",
      "author": "D Skowronska-Krawczyk",
      "year": "2004",
      "journal-title": "Development"
    },
    {
      "key": "ref69",
      "doi-asserted-by": "crossref",
      "first-page": "465",
      "DOI": "10.1038/embor.2008.34",
      "article-title": "Gene induction following wounding of wild-type versus macrophage-deficient Drosophila embryos.",
      "volume": "9",
      "author": "B Stramer",
      "year": "2008",
      "journal-title": "EMBO Rep"
    },
    {
      "key": "ref70",
      "doi-asserted-by": "crossref",
      "first-page": "2448",
      "DOI": "10.1101/gad.437607",
      "article-title": "Temporal ChIP-on-chip reveals Biniou as a universal regulator of the visceral muscle transcriptional network.",
      "volume": "21",
      "author": "J. S Jakobsen",
      "year": "2007",
      "journal-title": "Genes Dev"
    },
    {
      "key": "ref71",
      "doi-asserted-by": "crossref",
      "first-page": "e27",
      "DOI": "10.1371/journal.pbio.0060027",
      "article-title": "Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm.",
      "volume": "6",
      "author": "X. Y Li",
      "year": "2008",
      "journal-title": "PLoS Biol"
    },
    {
      "key": "ref72",
      "doi-asserted-by": "crossref",
      "first-page": "349",
      "DOI": "10.1016/S0092-8674(00)00040-4",
      "article-title": "Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila.",
      "volume": "102",
      "author": "R Nolo",
      "year": "2000",
      "journal-title": "Cell"
    }
  ],
  "container-title": "PLoS Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "http://dx.plos.org/10.1371/journal.pbio.1000435",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        2,
        23
      ]
    ],
    "date-time": "2025-02-23T12:22:31Z",
    "timestamp": 1740313351000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://dx.plos.org/10.1371/journal.pbio.1000435"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "Michael B.",
      "family": "Eisen",
      "sequence": "first",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2010,
        7,
        27
      ]
    ]
  },
  "references-count": 72,
  "journal-issue": {
    "issue": "7",
    "published-online": {
      "date-parts": [
        [
          2010,
          7,
          27
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1371/journal.pbio.1000435",
  "relation": {},
  "ISSN": [
    "1545-7885"
  ],
  "subject": [],
  "container-title-short": "PLoS Biol",
  "published": {
    "date-parts": [
      [
        2010,
        7,
        27
      ]
    ]
  }
}