tango


DEVELOPMENTAL BIOLOGY

Embryonic

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).


REFERENCES

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. PubMed Citation: 8589438

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. PubMed Citation: 7775458

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. PubMed Citation: 9501163

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. PubMed Citation: 8621524

Bailey, P., et al. (2006). A global genomic transcriptional code associated with CNS-expressed genes. Exp. Cell Res. 16: 3108-3119. PubMed Citation: 16919269

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. PubMed Citation: 9418899

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. PubMed Citation: 8824276

Cordoba, S. and Estella, C. (2014). The bHLH-PAS transcription factor Dysfusion regulates tarsal joint formation in response to Notch activity during Drosophila leg development. PLoS Genet 10: e1004621. PubMed ID: 25329825

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. PubMed Citation: 8753765

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. PubMed Citation: 10433921

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

Fulkerson, E. and Estes, P. A. (2010). Common motifs shared by conserved enhancers of Drosophila midline glial genes. J. Exp. Zool. B Mol. Dev. Evol. 316(1): 61-75. PubMed Citation: 21154525

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

Morozova, T., Hackett, J., Sedaghat, Y. and Sonnenfeld, M. (2010). The Drosophila jing gene is a downstream target in the Trachealess/Tango tracheal pathway. Dev. Genes Evol. 220(7-8): 191-206. PubMed Citation: 21061019

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, C., Evans, N. C. and Barolo, S. (2010). Structural rules and complex regulatory circuitry constrain expression of a Notch- and EGFR-regulated eye enhancer. Dev Cell 18: 359-370. PubMed Citation: 20230745

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


tango: Biological Overview | Evolutionary Homologs | Regulation | Developmental Biology | Effects of Mutation

date revised: 23 July 2014 

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