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JOURNAL ARTICLES
Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis
M.P. Ward, J.T. Mosher, S.T. Crews
Development 1998 125: 1599-1608;
M.P. Ward
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J.T. Mosher
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S.T. Crews
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Summary

The Drosophila Single-minded and Tango basic-helix-loop-helix-PAS protein heterodimer controls transcription and embryonic development of the CNS midline cells, while the Trachealess and Tango heterodimer controls tracheal cell and salivary duct transcription and development. Expression of both single-minded and trachealess is highly restricted to their respective cell lineages, however tango is broadly expressed. The developmental control of subcellular localization of these proteins is investigated because of their similarity to the mammalian basic-helix-loop-helix-PAS Aromatic hydrocarbon receptor whose nuclear localization is dependent on ligand binding. Confocal imaging of Single-minded and Trachealess protein localization indicate that they accumulate in cell nuclei when initially synthesized in their respective cell lineages and remain nuclear throughout embryogenesis. Ectopic expression experiments show that Single-minded and Trachealess are localized to nuclei in cells throughout the ectoderm and mesoderm, indicating that nuclear accumulation is not regulated in a cell-specific fashion and unlikely to be ligand dependent. In contrast, nuclear localization of Tango is developmentally regulated; it is localized to the cytoplasm in most cells except the CNS midline, salivary duct, and tracheal cells where it accumulates in nuclei. Genetic and ectopic expression experiments indicate that Tango nuclear localization is dependent on the presence of a basic-helix-loop-helix-PAS protein such as Single-minded or Trachealess. Conversely, Drosophila cell culture experiments show that Single-minded and Trachealess nuclear localization is dependent on Tango since they are cytoplasmic in the absence of Tango. These results suggest a model in which Single-minded and Trachealess dimerize with Tango in the cytoplasm of the CNS midline cells and trachea, respectively, and the dimeric complex accumulates in nuclei in a ligand-independent mode and regulates lineage-specific transcription. The lineage-specific action of Single-minded and Trachealess derives from transcriptional activation of their genes in their respective lineages, not from extracellular signaling.

REFERENCES

    1. Abbott B. D.,
    2. Birnbaum L. S.,
    3. Perdew G. H.
    (1995) Developmental expression of two members of a new class of transcription factors: I. Expression of aryl hydrocarbon receptor in the C57BL/6N mouse embryo. Dev. Dyn 204, 133–143
    OpenUrlCrossRefPubMedWeb of Science
    1. Abbott B. D.,
    2. Probst M. R.
    (1995) Developmental expression of two members of a new class of transcription factors: II. Expression of aryl hydrocarbon receptor nuclear translocator in the C57BL/6N mouse embryo. Dev. Dyn 204, 144–155
    OpenUrlCrossRefPubMedWeb of Science
    1. Antonsson C.,
    2. Arulampalam V.,
    3. Whitelaw M. L.,
    4. Petterson S.,
    5. Poellinger L.
    (1995) Constitutive function of the basic helix-loop-helix/PAS factor Arnt. Regulation of target promoters via the E box motif. J. Biol. Chem 270, 13968–13972
    OpenUrlAbstract/FREE Full Text
    1. Brand A. H.,
    2. Perrimon N.
    (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Burbach K. M.,
    2. Poland A.,
    3. Bradfield C. A.
    (1992) Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor. Proc. Nat. Acad. Sci. USA 89, 8185–8189
    OpenUrlAbstract/FREE Full Text
    1. Chen H.,
    2. Chrast R.,
    3. Rossier C.,
    4. Gos A.,
    5. Antonarakis S. E.,
    6. Kudoh J.,
    7. Yamaki A.,
    8. Shindoh N.,
    9. Maeda H.,
    10. Minoshima S.,
    11. Shimizu N.
    (1995) Single-minded and Down syndrome. Nature Genet 10, 9–10
    OpenUrlCrossRefPubMedWeb of Science
    1. Crews S. T.,
    2. Thomas J. B.,
    3. Goodman C. S.
    (1988) The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product. Cell 52, 143–151
    OpenUrlCrossRefPubMedWeb of Science
    1. Dahmane N.,
    2. Charron G.,
    3. Lopes C.,
    4. Yaspo M. L.,
    5. Maunoury C.,
    6. Decorte L.,
    7. Sinet P. M.,
    8. Bloch B.,
    9. Delabar J. M.
    (1995) Down syndrome-critical region contains a gene homologous to Drosophila sim expressed during rat and human central nervous system development. Proc. Natl. Acad. Sci. USA 92, 9191–9195
    OpenUrlAbstract/FREE Full Text
    1. Denis M.,
    2. Cuthill S.,
    3. Wikstrom A. C.,
    4. Poellinger L.,
    5. Gustafsson J.-A.
    (1988) Association of the dioxin receptor with the Mr 90,000 heat shock protein: a structural kinship with the glucocorticoid receptor. Biochem. Biophys. Res. Comm 155, 801–807
    OpenUrlCrossRefPubMedWeb of Science
    1. Edwards D. N.,
    2. Towb P.,
    3. Wasserman S. A.
    (1997) An activity-dependent network of interactions links the Rel protein Dorsal with its cytoplasmic regulators. Development 124, 3855–3864
    OpenUrlAbstract
    1. Eguchi H.,
    2. Ikuta T.,
    3. Tachibana T.,
    4. Yoneda Y.,
    5. Kawajiri K.
    (1997) A nuclear localization signal of human aryl hydrocarbon receptor nuclear translocator/hypoxia-inducible factor 1is a novel bipartite type recognized by the two components of nuclear pore-targeting complex. J. Biol. Chem 272, 17640–17647
    OpenUrlAbstract/FREE Full Text
    1. Ema M.,
    2. Morita M.,
    3. Ikawa S.,
    4. Tanaka M.,
    5. Matsuda Y.,
    6. Gotoh O.,
    7. Saijoh Y.,
    8. Fujii H.,
    9. Hamada H.,
    10. Fujii-Kuriyama Y.
    (1997) Two new members of murine Sim gene family are transcriptional repressors and show different expression patterns during mouse embryogenesis. Mol. Cell. Biol 16, 5865–5875
    OpenUrlAbstract/FREE Full Text
    1. Ema M.,
    2. Sogawa K.,
    3. Watanabe N.,
    4. Chujoh Y.,
    5. Matsushita N.,
    6. Gotoh O.,
    7. Funae Y.,
    8. Fujii-Kuriyama Y.
    (1992) cDNA cloning and structure of mouse putative Ah receptor. Biochem. Biophys. Res. Comm 184, 246–253
    OpenUrlCrossRefPubMedWeb of Science
    1. Fan C.-M.,
    2. Kuwana E.,
    3. Bulfone A.,
    4. Fletcher C. F.,
    5. Copeland N. G.,
    6. Jenkins N. A.,
    7. Crews S.,
    8. Martinez S.,
    9. Puelles L.,
    10. Rubenstein J. L. R.,
    11. Tessier-Lavigne M.
    (1996) Expression patterns of two murine homologs of Drosophila single-minded suggest possible roles in embryonic patterning and in the pathogenesis of Down Syndrome. Mol. Cell. Neuro 7, 1–16
    OpenUrlCrossRefPubMedWeb of Science
    1. Foe V. E.
    (1989) Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107, 1–22
    OpenUrlAbstract
    1. Hoffman E. C.,
    2. Reyes H.,
    3. Chu F.,
    4. Sander F.,
    5. Conley L. H.,
    6. Brooks B. A.,
    7. Hankinson O.
    (1991) Cloning of a subunit of the DNA-binding form of the Ah (dioxin) receptor. Science 252, 954–958
    OpenUrlAbstract/FREE Full Text
    1. Isaac D. D.,
    2. Andrew D. J.
    (1996) Tubulogenesis in Drosophila: a requirement for the trachealess gene product. Genes Dev 10, 103–117
    OpenUrlAbstract/FREE Full Text
    1. Ma Q.,
    2. Whitlock J. J. P.
    (1997) A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. J. Biol. Chem 272, 8878–8884
    OpenUrlAbstract/FREE Full Text
    1. Nambu J. R.,
    2. Chen W.,
    3. Hu S.,
    4. Crews S. T.
    (1996) The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human Hypoxia-inducible factor 1and Drosophila Single-minded. Gene 172, 249–254
    OpenUrlCrossRefPubMedWeb of Science
    1. Nambu J. R.,
    2. Franks R. G.,
    3. Hu S.,
    4. Crews S. T.
    (1990) The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells. Cell 63, 63–75
    OpenUrlCrossRefPubMedWeb of Science
    1. Nambu J. R.,
    2. Lewis J. L.,
    3. Wharton K. A.,
    4. Crews S. T.
    (1991) The Drosophila single-minded gene encodes a helix-loop-helix protein which acts as a master regulator of CNS midline development. Cell 67, 1157–1167
    OpenUrlCrossRefPubMedWeb of Science
    1. Ohshiro T.,
    2. Saigo K.
    (1997) Transcriptional regulation of breathless FGF receptor gene by binding of TRACHEALESS/dARNT heterodimers to three central midline elements in Drosophila developing trachea. Development 124, 3975–3986
    OpenUrlAbstract
    1. Orsulic S.,
    2. Peifer M.
    (1996) Cell-cell signalling: Wingless lands at last. Curr. Biol 6, 1363–1367
    OpenUrlCrossRefPubMedWeb of Science
    1. Patel N. H.,
    2. Snow P. M.,
    3. Goodman C. S.
    (1987) Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 48, 975–988
    OpenUrlCrossRefPubMedWeb of Science
    1. Perdew G. H.
    (1988) Association of the Ah receptor with the 90-kDa heat shock protein. J. Biol. Chem 263, 13802–13805
    OpenUrlAbstract/FREE Full Text
    1. Pollenz R. S.,
    2. Sattler C. A.,
    3. Poland A.
    (1994) The aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator protein show distinct subcellular localizations in Hepa 1c1c7 cells by immunofluorescence microscopy. Mol. Pharmacol 45, 428–438
    OpenUrlAbstract
    1. Probst M. R.,
    2. Fan C.-M.,
    3. Tessier-Lavigne M.,
    4. Hankinson O.
    (1997) Two murine homologs of the Drosophila Single-minded protein that interact with the mouse aryl hydrocarbon receptor nuclear translocator protein. J. Biol. Chem 272, 4451–4457
    OpenUrlAbstract/FREE Full Text
    1. Roth S.,
    2. Stein D.,
    3. Nusslein-Volhard C.
    (1989) A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell 59, 1189–1202
    OpenUrlCrossRefPubMedWeb of Science
    1. Rowlands J. C.,
    2. Gustafsson J.-A.
    (1997) Aryl hydrocarbon receptor-mediated signal transduction. Crit. Rev. Toxicol 27, 109–134
    OpenUrlCrossRefPubMedWeb of Science
    1. Rupp R. A.,
    2. Snider L.,
    3. Weintraub H.
    (1994) Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev 8, 1311–1323
    OpenUrlAbstract/FREE Full Text
    1. Rusch J.,
    2. Levine M.
    (1996) Threshold responses to the dorsal regulatory gradient and the subdivision of primary tissue territories in the Drosophila embryo. Curr. Opin. Genet. Dev 6, 416–423
    OpenUrlCrossRefPubMedWeb of Science
    1. Rushlow C.,
    2. Han K.,
    3. Manley J. L.,
    4. Levine M.
    (1989) The graded distribution of the dorsal morphogen is initiated by selective nuclear transport in Drosophila. Cell 59, 1165–1177
    OpenUrlCrossRefPubMedWeb of Science
    1. Sogawa K. R.,
    2. Nakano A.,
    3. Kobayashi Y.,
    4. Kikuchi N.,
    5. Ohe N.,
    6. Matsushita N.,
    7. Fujii-Kuriyama Y.
    (1995) Possible function of Ah receptor nuclear translocator (Arnt) homodimer in transcriptional regulation. Proc. Nat. Acad. Sci USA 92, 1936–1940
    OpenUrlAbstract/FREE Full Text
    1. Sonnenfeld M.,
    2. Ward M.,
    3. Nystrom G.,
    4. Mosher J.,
    5. Stahl S.,
    6. Crews S.
    (1997) The Drosophila tango gene encodes a bHLH-PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development 124, 4583–4594
    OpenUrlAbstract
    1. Steward R.
    (1989) Relocalization of the dorsal protein from the cytoplasm correlates with its function. Cell 59, 1179–1188
    OpenUrlCrossRefPubMedWeb of Science
    1. Swanson H. I.,
    2. Chan W. K.,
    3. Bradfield C. A.
    (1995) DNA binding specificities and pairing rules of the Ah receptor, ARNT, and SIM proteins. J. Biol. Chem 280, 26292–26302
    1. Thomas J. B.,
    2. Crews S. T.,
    3. Goodman C. S.
    (1988) Molecular genetics of the single-minded locus: a gene involved in the development of the Drosophila nervous system. Cell 52, 133–141
    OpenUrlCrossRefPubMedWeb of Science
    1. Vandromme M.,
    2. Gauthier-Rouviere C.,
    3. Lamb N.,
    4. Fernandez A.
    (1996) Regulation of transcription factor localization: fine-tuning of gene expression. Trends Biochem. Sci 21, 59–64
    OpenUrlCrossRefPubMedWeb of Science
    1. Wang G. L.,
    2. Jaing B.-H.,
    3. Rue E.,
    4. Semenza G. L.
    (1995) Hypoxia-inducible factor 1 is a basic helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA 92, 5510–5514
    OpenUrlAbstract/FREE Full Text
    1. Wharton K. A., Jr.,
    2. Franks R. G.,
    3. Kasai Y.,
    4. Crews S. T.
    (1994) Control of CNS midline transcription by asymmetric E-box elements: similarity to xenobiotic responsive regulation. Development 120, 3563–3569
    OpenUrlAbstract
    1. Wiener C. M.,
    2. Booth G.,
    3. Semenza G. L.
    (1996) In vivo expression of mRNAs encoding hypoxia-inducible factor 1. Biochem. Biophys. Res. Comm 225, 485–488
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilk R.,
    2. Weizman I.,
    3. Glazer L.,
    4. Shilo B.-Z.
    (1996) trachealess encodes a bHLH-PAS protein and is a master regulator gene in the Drosophila tracheal system. Genes Dev 10, 93–102
    OpenUrlAbstract/FREE Full Text
    1. Zelzer E.,
    2. Wappner P.,
    3. Shilo B.-Z.
    (1997) The PAS domain confers target gene specificity of Drosophila bHLH/PAS proteins. Genes Dev 11, 2079–2089
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis
M.P. Ward, J.T. Mosher, S.T. Crews
Development 1998 125: 1599-1608;
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JOURNAL ARTICLES
Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis
M.P. Ward, J.T. Mosher, S.T. Crews
Development 1998 125: 1599-1608;

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