tango

DEVELOPMENTAL BIOLOGY

Embryonic

See the embryonic expression pattern of tgo at the Berkeley Drosophila Genome Project Patterns of Gene Expression Site.

Tango protein is found either in cell nuclei or cytoplasm, depending on the cell type and time of development. In the precellular blastoderm, Tango protein is uniformly distributed, presumable due to maternal contribution. Staining is more intense in the cytoplasm than in the nucleus. During the extended germband stage, Tgo protein is detected in all three germ layers. As tracheal pits form, the cells surrounding the pits show enhanced levels of Tgo protein and RNA, as compared to surrounding cells. Amounts of Tgo protein above ubiquitous levels continue to be observed in the tracheal cells, including the posterior spiracles, from stage 11 to the end of embryogenesis at stage 17. As the CNS forms, uniformly high levels of Tgo protein are found in the brain and ventral nerve cord (Sonnenfeld, 1997)

Effects of Mutation or Deletion

Isolation and analysis of tango mutants reveal CNS midline and tracheal defects, and gene dosage studies demonstrate in vivo interactions between single-minded::tango and trachealess::tango. Defects in CNS midline neurons and glia were examined using enhancer trap reporters. In wild-type embryos, the AA142 enhancer trap is expressed in an average of 3.5 midline glia per segment by stage 14 of embryogenesis. In tango mutant embryos, there is a reduction in the number of stained midline glia to approximately one cell per segment. The X55 enhancer trap gene stains the ventral unpaired median neurons (VUMs) and the median neuroblast (MNB) and its progeny in the ventral region of the CNS. In tango mutant embryos, the number of VUM neurons and MNB progeny are reduced in number (60% of wild-type) and do not migrate into the ventral regions of the ventral cord. The role of tango in tracheal development was examined by staining tango mutant embryos with monoclonal antibody 2A12, which stains the lumen of the tracheal tubes. tango mutant embryos are shown to have a variety of tracheal defects. Experiments with heterozygotes show that tango interacts genetically with both trachealess and single minded (Sonnenfeld, 1997).

Abbott, B. D. and 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(2): 144-155.

Antonsson, C., et al. (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(23): 13968-13972.

Ashok, M., Turner, C. and Wilson, T. G. (1998). Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc. Natl. Acad. Sci. 95(6): 2761-2766.

Bacsi, S. G. and Hankinson, O. (1996). Functional characterization of DNA-binding domains of the subunits of the heterodimeric aryl hydrocarbon receptor complex imputing novel and canonical basic helix-loop-helix protein-DNA interactions. J. Biol. Chem. 271(15): 8843-8850.

Brown, R. P., McDonnell, C. M., Berenbaum, M. R. and Schuler, M. A. (2005). Regulation of an insect cytochrome P450 monooxygenase gene (CYP6B1) by aryl hydrocarbon and xanthotoxin response cascades. Gene 358: 39-52. Medline abstract: 16099607

Chang, C. Y. and Puga, A. (1998). Constitutive activation of the aromatic hydrocarbon receptor. Mol. Cell. Biol. 18(1): 525-535.

Chapman-Smith, A., Lutwyche, J. K. and Whitelaw, M. L. (2004). Contribution of the Per/Arnt/Sim (PAS) domains to DNA binding by the basic helix-loop-helix PAS transcriptional regulators. J. Biol. Chem. 279(7): 5353-62. 14638687

Chen, Y. H. and Tukey, R. H. (1996). Protein kinase C modulates regulation of the CYP1A1 gene by the aryl hydrocarbon receptor. J. Biol. Chem. 1271(42): 26261-26266.

Drutel, G., et al. (1996). Cloning and selective expression in brain and kidney of ARNT2 homologous to the Ah receptor nuclear translocator (ARNT). Biochem. Biophys. Res. Commun. 225(2): 333-339.

Emmons, R. B., et al. (1999). The Spineless-Aristapedia and Tango bHLH-PAS proteins interact to control antennal and tarsal development in Drosophila. Development 126: 3937-3945

Erbel, P. J., Card, P. B., Karakuzu, O., Bruick, R. K. and Gardner, K. H. (2003). Structural basis for PAS domain heterodimerization in the basic helix--loop--helix-PAS transcription factor hypoxia-inducible factor. Proc. Natl. Acad. Sci. 100(26): 15504-9. 14668441

Estes, P., Mosher, J. and Crews, S. T. (2001). Drosophila Single-minded represses gene transcription by activating the expression of repressive factors. Dev. Bio. 232: 157-175

Forsythe, J. A., et al. (1996). Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16(9): 4604-4613.

Fukunaga, B. N., et al. (1995). Identification of functional domains of the aryl hydrocarbon receptor. J. Biol. Chem. 270(49): 29270-29278.

Gergely, F., et al. (2000). The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc. Natl. Acad. Sci. 97(26): 14352-14357

Gradin, K., et al. (1996). Functional interference between hypoxia and dioxin signal transduction pathways: competition for recruitment of the Arnt transcription factor. Mol. Cell. Biol. 16(10): 5221-5231.

Gustafsson, M. V., et al. (2005). Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9(5): 617-28. 16256737

Hogenesch. J. B., et al. (1997). Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J. Biol. Chem. 272(13):8581-8593.

Jiang, G., Guo, R. and Powell-Coffman, J. A. (2001). The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia Proc. Natl. Acad. Sci. 98: 7916-7921. 11427734

Jiang, L. and Crews, S. T. (2003). The Drosophila dysfusion basic helix-loop-helix (bHLH)-PAS gene controls tracheal fusion and levels of the Trachealess bHLH-PAS protein. Molec. Cell. Biol. 23: 5625-5637. 12897136

Kainu, T., Gustafsson, J. A., Pelto-Huikko, M. (1995). The dioxin receptor and its nuclear translocator (Arnt) in the rat brain. Neuroreport 6(18): 2557-2560.

Kallio, P. J., et al. (1997). Activation of hypoxia-inducible factor 1alpha: posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proc. Natl. Acad. Sci. 94(11): 5667-5672.

Kobayashi, A., Sogawa, K, and Fujii-Kuriyama, Y. (1996). Cooperative interaction between AhR.Arnt and Sp1 for the drug-inducible expression of CYP1A1 gene. J. Biol. Chem. 271(21): 12310-12316.

Kobayashi, A., et al. (1997). CBP/p300 functions as a possible transcriptional coactivator of Ah receptor nuclear translocator. J Biochem (Tokyo) 122(4): 703-710.

Kozak, K. R., Abbott, B. and Hankinson, O. (1997). ARNT-deficient mice and placental differentiation. Dev. Biol. 191(2): 297-305.

Lavista-Llanos, S., Centanin, L., Irisarri, M., Russo, D. M., Gleadle, J. M., Bocca, S. N., Muzzopappa, M., Ratcliffe, P. J. and Wappner, P. (2002). Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein Similar. Mol. Cell. Biol. 22: 6842-6853. 12215541

Li, S. Y., Dougherty, J. J. (1997). Inhibitors of serine/threonine-specific protein phosphatases stimulate transcription by the Ah receptor/Arnt dimer by affecting a step subsequent to XRE binding. Arch Biochem Biophys 340(1): 73-82.

Lindebro, M. C., Poellinger, L. and Whitelaw, M. L. (1995). Protein-protein interaction via PAS domains: role of the PAS domain in positive and negative regulation of the bHLH/PAS dioxin receptor-Arnt transcription factor complex. EMBO J. 1995 Jul 17;14(14): 3528-3539.

Maltepe, E., et al. (1997). Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386(6623): 403-407.

Maltepe, E., et al. (2005). Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development 132(15): 3393-403. 15987772

Miller, C. A. (1997). Expression of the human aryl hydrocarbon receptor complex in yeast. Activation of transcription by indole compounds. J. Biol. Chem. 272(52): 32824-32829.

Nagao, et al. (1996). Drosophila melanogaster SL2 cells contain a hypoxically inducible DNA binding complex which recognises mammalian HIF-1 binding sites. FEGS Lett. 387: 161-166.

Nambu, J. R., et al. (1996). A Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia-inducible factor 1alpha and Drosophila single minded. Gene 172: 249-254

Ohshiro, T. and 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

Ohshiro, T., Emori, Y. and Saigo, K. (2002). Ligand-dependent activation of breathless FGF receptor gene in Drosophila developing trachea. Mech. Dev. 114: 3-11. 12175485

Okino, S. T. and Whitlock, J. P. (1995). Dioxin induces localized, graded changes in chromatin structure: implications for Cyp1A1 gene transcription. Mol. Cell. Biol. 15(7): 3714-3721.

Perdew, G. H. and Bradfield, C. A. (1996). Mapping the 90 kDa heat shock protein binding region of the Ah receptor. Biochem. Mol. Biol. Int. 39(3): 589-593.

Pollenz, R. S., et al. (1996). Isolation and expression of cDNAs from rainbow trout (Oncorhynchus mykiss) that encode two novel basic helix-loop-Helix/PER-ARNT-SIM (bHLH/PAS) proteins with distinct functions in the presence of the aryl hydrocarbon receptor. Evidence for alternative mRNA splicing and dominant negative activity in the bHLH/PAS family. J. Biol. Chem. 271(48): 30886-30896.

Rowlands, J. C., McEwan, I. J. and Gustafsson, J. A. (1996). Trans-activation by the human aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator proteins: direct interactions with basal transcription factors. Mol Pharmacol 50(3): 538-548.

Sadek, C. M., et al. (2000). Isolation and characterization of AINT: a novel ARNT interacting protein expressed during murine embryonic development. Mech. Dev. 97: 13-26.

Salceda, S., Beck, I. and Caro, J. (1996). Absolute requirement of aryl hydrocarbon receptor nuclear translocator protein for gene activation by hypoxia. Arch. Biochem. Biophys. 334(2): 389-394.

Sonnenfeld, M., et al. (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(22): 4571-4582.

Sun, W., Zhang, J. and Hankinson, O. (1997). A mutation in the aryl hydrocarbon receptor (AHR) in a cultured mammalian cell line identifies a novel region of AHR that affects DNA binding. J. Biol. Chem. 272(50): 31845-31854.

Swanson, H. I., Chan, W. K. and Bradfield, C. A. (1995). DNA binding specificities and pairing rules of the Ah receptor, ARNT and SIM proteins. J. Biol. Chem. 270: 26292-26302.

Swanson, H. I. and Yang, J. h. (1996). Mapping the protein/DNA contact sites of the Ah receptor and Ah receptor nuclear translocator. J. Biol. Chem. 271(49): 31657-31665.

Takahashi, Y., et al. (1997). Inhibition of the transcription of CYP1A1 gene by the upstream stimulatory factor 1 in rabbits. Competitive binding of USF1 with AhR.Arnt complex. J. Biol. Chem. 272(48): 30025-30031.

Ward, M. P., Mosher, J. T. and Crews, S. T. (1998). Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis. Development 125: 1599-1608.

Wood, S. M., et al. (1996). The role of the aryl hydrocarbon receptor nuclear translocator (ARNT) in hypoxic induction of gene expression. Studies in ARNT-deficient cells. J. Biol. Chem. 271(25): 15117-15123.

Zelzer, E., Wappner, P. and Shilo, B. Z. (1997). The PAS domain confers target gene specificity of Drosophila bHLH/PAS proteins. Genes Dev. 11(16): 2079-2089.

date revised: 15 March 2007 

Home page: The Interactive Fly © 1997 Thomas B. Brody, Ph.D.

The Interactive Fly resides on the
Society for Developmental Biology's Web server.