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AIMS Molecular Science

2015, Volume 2, Issue 2: 64-76. doi: 10.3934/molsci.2015.2.64
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A role for the non-conserved N-terminal domain of the TATA-binding protein in the crosstalk between cell signaling pathways and steroid receptors

  • Department of Pathology, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA
  • Transcriptional induction by steroid receptors is coupled to cellular signal transduction pathways although,in general,the mechanisms governing these events are not well defined. Using TATA-binding protein (TBP) specificity mutants that recognize a TGTA box,we show that yeast TBP expressed in mammalian cells can support steroid-mediated gene induction to a similar degree as human TBP,however yeast TBP does not support the 8-Bromo-cAMP-mediated potentiation of glucocorticoid receptor (GR)-dependent transactivation. Chimeras between yeast and human TBP reveal that it is the non-conserved N-terminus of TBP that governs the potentiation of GR action. While the conserved core of TBP is sufficient for TATA-element binding and preinitiation complex formation,the role of the N-terminus has remained elusive. Our results suggest a role of the N-terminus of human TBP in coupling cell signaling events to steroid-mediated transcription,thereby establishing one of the few described functional roles of this polypeptide domain in a physiological process.

    Citation: James R. Lambert, Steven K. Nordeen. A role for the non-conserved N-terminal domain of the TATA-binding protein in the crosstalk between cell signaling pathways and steroid receptors[J]. AIMS Molecular Science, 2015, 2(2): 64-76. doi: 10.3934/molsci.2015.2.64

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  • Transcriptional induction by steroid receptors is coupled to cellular signal transduction pathways although,in general,the mechanisms governing these events are not well defined. Using TATA-binding protein (TBP) specificity mutants that recognize a TGTA box,we show that yeast TBP expressed in mammalian cells can support steroid-mediated gene induction to a similar degree as human TBP,however yeast TBP does not support the 8-Bromo-cAMP-mediated potentiation of glucocorticoid receptor (GR)-dependent transactivation. Chimeras between yeast and human TBP reveal that it is the non-conserved N-terminus of TBP that governs the potentiation of GR action. While the conserved core of TBP is sufficient for TATA-element binding and preinitiation complex formation,the role of the N-terminus has remained elusive. Our results suggest a role of the N-terminus of human TBP in coupling cell signaling events to steroid-mediated transcription,thereby establishing one of the few described functional roles of this polypeptide domain in a physiological process.


    [1] Goodrich JA,Tjian R (1994) TBP-TAF complexes: selectivity factors for eukaryotic transcription. Curr Opin Cell Biol 6: 403-409. doi: 10.1016/0955-0674(94)90033-7
    [2] Buratowski S (1994) The basics of basal transcription by RNA polymerase II. Cell 77: 1-3. doi: 10.1016/0092-8674(94)90226-7
    [3] Evans RM (1998) The steroid and thyroid hormone receptor superfamily. Science 240: 889-895.
    [4] Dasgupta AB,Lonard DM,O'Malley BW (2014) Nuclear receptor coactivators: master regulators of human health and disease. Annu Rev Med 65: 279-292. doi: 10.1146/annurev-med-051812-145316
    [5] Xu J,Li Q (2003) Review of the in vivo Functions of the p160 Steroid Receptor Coactivator Family. Mol Endocrinol 17:1681-1692. doi: 10.1210/me.2003-0116
    [6] Smith CL,DeVera DG,Lamb DJ,et al. (2002) Genetic ablation of the steroid receptor coactivator-ubiquitin ligase,E6-AP,results in tissue-selective steroid hormone resistance and defects in reproduction. Mol Cell Biol 22: 525-535. doi: 10.1128/MCB.22.2.525-535.2002
    [7] Beitel LK,Elhaji YA,Lumbroso R,et al. (2002) Cloning and characterization of an androgen receptor N-terminal-interacting protein with ubiquitin-protein ligase activity. J Mol Endocrinol 29: 41-60. doi: 10.1677/jme.0.0290041
    [8] Khan SH,Ling J,Kumar R (2011) TBP binding-induced folding of the glucocorticoid receptor AF1 domain facilitates its interaction with steroid receptor coactivator-1. PLoS One 6: e21939
    [9] Kumar R,Moure CM,Khan SH,et al. (2013) Regulation of the structurally dynamic N-terminal domain of progesterone receptor by protein-induced folding. J Biol 288: 30285-3099.
    [10] Warnmark A,Wikstrom A,Wright AP,et al. (2001) The N-terminal regions of estrogen receptor alpha and beta are unstructured in vitro and show different TBP binding properties. J Biol Chem 276: 45939-45944. doi: 10.1074/jbc.M107875200
    [11] Keaveney M,Berkenstam A,Feigenbutz M,et al. (1993) Residues in the TATA-binding protein required to mediate a transcriptional response to retinoic acid in EC cells. Nature 365: 562-566. doi: 10.1038/365562a0
    [12] Pugh BF,Tjian R (1990) Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell 61: 1187-1197. doi: 10.1016/0092-8674(90)90683-6
    [13] Strubin M,Struhl K (1992) Yeast and human TFIID with altered DNA-binding specificity for TATA elements. Cell 68:721-730. doi: 10.1016/0092-8674(92)90147-5
    [14] Nordeen SK,Moyer ML,Bona BJ (1995) Modulation of glucocorticoid-regulated transcription by purines: novel characteristics and implications for tissue specificity of steroid responses. Endocrinology 136: 1120-1127.
    [15] Beck CA,Weigel NL,Moyer ML,et al. (1993) The progesterone antagonist RU486 acquires agonist activity upon stimulation of cAMP signaling pathways. Proc Natl Acad Sci U S A 90: 4441-4445. doi: 10.1073/pnas.90.10.4441
    [16] Nordeen SK,Bona BJ,Moyer ML (1993) Latent agonist activity of the steroid antagonist,RU486,is unmasked in cells treated with activators of protein kinase A. Mol Endocrinol 7: 731-742.
    [17] Moyer ML,Borror KC,Bona BJ,et al. (1993) Modulation of cell signaling pathways can enhance or impair glucocorticoid-induced gene expression without altering the state of receptor phosphorylation. J Biol Chem 268: 22933-22940.
    [18] Nordeen SK,Moyer ML,Bona BJ (1994) The coupling of multiple signal transduction pathways with steroid response mechanisms. Endocrinology 134: 1723-1732.
    [19] Nordeen SK (1994) Potentiation of glucocorticoid-mediated induction of the mouse mammary tumor virus promoter in mammary carcinoma cells by activation of protein kinase C. Biochem Biophys Res Commun 198: 1183-1188. doi: 10.1006/bbrc.1994.1167
    [20] Dutertre M,Smith CL (2003) Ligand-independent interactions of p160/steroid receptor coactivators and CREB-binding protein (CBP) with estrogen receptor-alpha: regulation by phosphorylation sites in the A/B region depends on other receptor domains. Mol Endocrinol 17: 1296-1314. doi: 10.1210/me.2001-0316
    [21] Wu RC,Smith CL,O'Malley BW (2005) Transcriptional regulation by steroid receptor coactivator phosphorylation. Endocr Rev 26: 393-399. doi: 10.1210/er.2004-0018
    [22] Kato S,Masuhiro Y,Watanabe M (2000) Molecular mechanism of a cross-talk between oestrogen and growth factor signaling pathways. Genes Cells 5: 593-601. doi: 10.1046/j.1365-2443.2000.00354.x
    [23] Kit S,Dubbs DR,Piekarksi LJ,et al. (1963) Deletion of thymidine kinase activity from L cells resistant to bromodeoxyuridine. Exp Cell Res 31: 297-312. doi: 10.1016/0014-4827(63)90007-7
    [24] Ralph P,Moore MA,Milsson K (1976) Lysozyme synthesis by established human and murine histiocytic lymphoma cell lines. J Exp Med 143: 1528-1533. doi: 10.1084/jem.143.6.1528
    [25] Gatlin J,Campbell LH,Schmidt MG,et al. (1995) Direct-rapid (DR) mutagenesis of large plasmids using PCR. Biotechniques 19: 559-564.
    [26] Nordeen SK (1988) Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques 6: 454-458.
    [27] Lieberman BA,Bona BJ,Edwards DP,et al. (1993) The constitution of a progesterone response element. Mol Endocrinol 7: 515-527.
    [28] Biggs JR,Ahn NG,Kraft AS (1998) Activation of the mitogen-activated protein kinase pathway in U937 leukemic cells induces phosphorylation of the amino terminus of the TATA-binding protein. Cell Growth Differ 9: 667-676.
    [29] Fujimoto N,Katzenellenbogen BS (1994) Alteration in the agonist/antagonist balance of antiestrogens by activation of protein kinase A signaling pathways in breast cancer cells: antiestrogen selectivity and promoter dependence. Mol Endocrinol 8: 296-304.
    [30] Keenan CR,Mok JS,Harris T,et al (2014) Bronchial epithelial cells are rendered insensitive to glucocorticoid transactivation by transforming growth factor-β1. Respiratory Res 15: 55
    [31] Piovan E,Yu J,Tosello V,et al. (2013) Direct reversal of glucocorticoid resistance by AKT inhibition in acute lymphoblastic leukemia. Cancer Cell 24: 766-776. doi: 10.1016/j.ccr.2013.10.022
    [32] Beck IM,Vanden Berghe W,Vermeulen L (2009) Crosstalk in inflammation: the interplay of glucocorticoid receptor-based mechanisms and kinases and phosphatases. Endocr Rev 30: 830-882. doi: 10.1210/er.2009-0013
    [33] Kumar R,Calhoun WJ (2008) Differential regulation of the transcriptional activity of the glucocorticoid receptor through site-specific phosphorylation. Biologics 2: 845-854.
    [34] Ward RD,Weigel NL (2009) Steroid receptor phosphorylation: Assigning function to site-specific phosphorylation. Biofactors 35: 528-536. doi: 10.1002/biof.66
    [35] Chen W,Dang T,Blind RD,et al. (2008) Glucocorticoid receptor phosphorylation differentially affects target gene expression. Mol Endocrinol 22: 1754-66. doi: 10.1210/me.2007-0219
    [36] Espinas ML,Roux J,Pictet R,et al. (1995) Glucocorticoids and protein kinase A coordinately modulate transcription factor recruitment at a glucocorticoid-responsive unit. Mol Cell Biol 15: 5346-5354.
    [37] Rowan BG,Garrison N,Weigel NL,et al. (2000) 8-Bromo-cyclic AMP induces phosphorylation of two sites in SRC-1 that facilitate ligand-independent activation of the chicken progesterone receptor and are critical for functional cooperation between SRC-1 and CREB binding protein. Mol Cell Biol 20: 8720-8730. doi: 10.1128/MCB.20.23.8720-8730.2000
    [38] Johnson AB,O'Malley BW (2012) Steroid receptor coactivators 1,2,and 3: critical regulators of nuclear receptor activity and steroid receptor modulator (SRM)-based cancer therapy. Mol Cell Endocrinol 348: 430-439. doi: 10.1016/j.mce.2011.04.021
    [39] Das D,Scovell WM (2001) The binding interaction of HMG-1 with the TATA-binding protein/TATA complex. J Biol Chem 276: 32597-32605. doi: 10.1074/jbc.M011792200
    [40] Boonyaratanakornkit V,Melvin V,Prendergast P,et al. (1998) High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells. Mol Cell Biol 18: 4471-4487.
    [41] Melvin VS,Edwards DP (1999) Coregulatory proteins in steroid hormone receptor action: the role of chromatin high mobility group proteins HMG-1 and -2. Steroids 64: 576-586. doi: 10.1016/S0039-128X(99)00036-7
    [42] Hernandez N (1993) TBP,a universal eukaryotic transcription factor? Genes Dev 7:1291-1308. doi: 10.1101/gad.7.7b.1291
    [43] Mittal V,Hernandez N (1997) Role for the amino-terminal region of human TBP in U6 snRNA transcription. Science 275: 1136-1140. doi: 10.1126/science.275.5303.1136
    [44] Mittal V,Ma B,Hernandez N (1999) SNAP(c): a core promoter factor with a built-in DNA-binding damper that is deactivated by the Oct-1 POU domain. Genes Dev 13: 1807-1821. doi: 10.1101/gad.13.14.1807
    [45] Zhao X,Herr W (2002) A regulated two-step mechanism of TBP binding to DNA: a solvent-exposed surface of TBP inhibits TATA box recognition. Cell 108: 615-627. doi: 10.1016/S0092-8674(02)00648-7
    [46] Um M,Yamauchi J,Kato S,et al. (2001) Heterozygous disruption of the TATA-binding protein gene in DT40 cells causes reduced cdc25B phosphatase expression and delayed mitosis. Mol Cell Biol 21: 2435-2448. doi: 10.1128/MCB.21.7.2435-2448.2001
    [47] Schmidt EE,Bondareva AA,Radke JR,et al. (2003) Fundamental cellular processes do not require vertebrate-specific sequences within the TATA-binding protein. J Biol Chem 278: 6168-6174. doi: 10.1074/jbc.M211205200
    [48] Hobbs NK,Bondareva AA,Barnett S,et al. (2002) Removing the vertebrate-specific TBP N terminus disrupts placental beta2m-dependent interactions with the maternal immune system. Cell 110: 43-54. doi: 10.1016/S0092-8674(02)00806-1
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