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. 1999 Aug;11(8):1591–1602. doi: 10.1105/tpc.11.8.1591

Specific interactions with TBP and TFIIB in vitro suggest that 14-3-3 proteins may participate in the regulation of transcription when part of a DNA binding complex.

S Pan 1, P C Sehnke 1, R J Ferl 1, W B Gurley 1
PMCID: PMC144297  PMID: 10449590

Abstract

The 14-3-3 family of multifunctional proteins is highly conserved among animals, plants, and yeast. Several studies have shown that these proteins are associated with a G-box DNA binding complex and are present in the nucleus in several plant and animal species. In this study, 14-3-3 proteins are shown to bind the TATA box binding protein (TBP), transcription factor IIB (TFIIB), and the human TBP-associated factor hTAF(II)32 in vitro but not hTAF(II)55. The interactions with TBP and TFIIB were highly specific, requiring amino acid residues in the box 1 domain of the 14-3-3 protein. These interactions do not require formation of the 14-3-3 dimer and are not dependent on known 14-3-3 recognition motifs containing phosphoserine. The 14-3-3-TFIIB interaction appears to occur within the same domain of TFIIB that binds the human herpes simplex virus transcriptional activator VP16, because VP16 and 14-3-3 were able to compete for interaction with TFIIB in vitro. In a plant transient expression system, 14-3-3 was able to activate GAL4-dependent beta-glucuronidase reporter gene expression at low levels when translationally fused with the GAL4 DNA binding domain. The in vitro binding with general transcription factors TBP and TFIIB together with its nuclear location provide evidence supporting a role for 14-3-3 proteins as transcriptional activators or coactivators when part of a DNA binding complex.

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Selected References

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  1. Alam R., Hachiya N., Sakaguchi M., Kawabata S., Iwanaga S., Kitajima M., Mihara K., Omura T. cDNA cloning and characterization of mitochondrial import stimulation factor (MSF) purified from rat liver cytosol. J Biochem. 1994 Aug;116(2):416–425. doi: 10.1093/oxfordjournals.jbchem.a124541. [DOI] [PubMed] [Google Scholar]
  2. Andrews R. K., Harris S. J., McNally T., Berndt M. C. Binding of purified 14-3-3 zeta signaling protein to discrete amino acid sequences within the cytoplasmic domain of the platelet membrane glycoprotein Ib-IX-V complex. Biochemistry. 1998 Jan 13;37(2):638–647. doi: 10.1021/bi970893g. [DOI] [PubMed] [Google Scholar]
  3. Bachmann M., Huber J. L., Athwal G. S., Wu K., Ferl R. J., Huber S. C. 14-3-3 proteins associate with the regulatory phosphorylation site of spinach leaf nitrate reductase in an isoform-specific manner and reduce dephosphorylation of Ser-543 by endogenous protein phosphatases. FEBS Lett. 1996 Nov 25;398(1):26–30. doi: 10.1016/s0014-5793(96)01188-x. [DOI] [PubMed] [Google Scholar]
  4. Baldwin D. A., Gurley W. B. Isolation and characterization of cDNAs encoding transcription factor IIB from Arabidopsis and soybean. Plant J. 1996 Sep;10(3):561–568. doi: 10.1046/j.1365-313x.1996.10030561.x. [DOI] [PubMed] [Google Scholar]
  5. Banik U., Wang G. A., Wagner P. D., Kaufman S. Interaction of phosphorylated tryptophan hydroxylase with 14-3-3 proteins. J Biol Chem. 1997 Oct 17;272(42):26219–26225. doi: 10.1074/jbc.272.42.26219. [DOI] [PubMed] [Google Scholar]
  6. Bihn E. A., Paul A. L., Wang S. W., Erdos G. W., Ferl R. J. Localization of 14-3-3 proteins in the nuclei of arabidopsis and maize. Plant J. 1997 Dec;12(6):1439–1445. doi: 10.1046/j.1365-313x.1997.12061439.x. [DOI] [PubMed] [Google Scholar]
  7. Braselmann S., McCormick F. Bcr and Raf form a complex in vivo via 14-3-3 proteins. EMBO J. 1995 Oct 2;14(19):4839–4848. doi: 10.1002/j.1460-2075.1995.tb00165.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chiang C. M., Roeder R. G. Cloning of an intrinsic human TFIID subunit that interacts with multiple transcriptional activators. Science. 1995 Jan 27;267(5197):531–536. doi: 10.1126/science.7824954. [DOI] [PubMed] [Google Scholar]
  9. Christensen A. H., Quail P. H. Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res. 1996 May;5(3):213–218. doi: 10.1007/BF01969712. [DOI] [PubMed] [Google Scholar]
  10. Colgan J., Ashali H., Manley J. L. A direct interaction between a glutamine-rich activator and the N terminus of TFIIB can mediate transcriptional activation in vivo. Mol Cell Biol. 1995 Apr;15(4):2311–2320. doi: 10.1128/mcb.15.4.2311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Colgan J., Wampler S., Manley J. L. Interaction between a transcriptional activator and transcription factor IIB in vivo. Nature. 1993 Apr 8;362(6420):549–553. doi: 10.1038/362549a0. [DOI] [PubMed] [Google Scholar]
  12. Dellambra E., Patrone M., Sparatore B., Negri A., Ceciliani F., Bondanza S., Molina F., Cancedda F. D., De Luca M. Stratifin, a keratinocyte specific 14-3-3 protein, harbors a pleckstrin homology (PH) domain and enhances protein kinase C activity. J Cell Sci. 1995 Nov;108(Pt 11):3569–3579. doi: 10.1242/jcs.108.11.3569. [DOI] [PubMed] [Google Scholar]
  13. Ferl Robert J. 14-3-3 PROTEINS AND SIGNAL TRANSDUCTION. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):49–73. doi: 10.1146/annurev.arplant.47.1.49. [DOI] [PubMed] [Google Scholar]
  14. Ford J. C., al-Khodairy F., Fotou E., Sheldrick K. S., Griffiths D. J., Carr A. M. 14-3-3 protein homologs required for the DNA damage checkpoint in fission yeast. Science. 1994 Jul 22;265(5171):533–535. doi: 10.1126/science.8036497. [DOI] [PubMed] [Google Scholar]
  15. Freed E., Symons M., Macdonald S. G., McCormick F., Ruggieri R. Binding of 14-3-3 proteins to the protein kinase Raf and effects on its activation. Science. 1994 Sep 16;265(5179):1713–1716. doi: 10.1126/science.8085158. [DOI] [PubMed] [Google Scholar]
  16. Gelperin D., Weigle J., Nelson K., Roseboom P., Irie K., Matsumoto K., Lemmon S. 14-3-3 proteins: potential roles in vesicular transport and Ras signaling in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11539–11543. doi: 10.1073/pnas.92.25.11539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gu M., Du X. A novel ligand-binding site in the zeta-form 14-3-3 protein recognizing the platelet glycoprotein Ibalpha and distinct from the c-Raf-binding site. J Biol Chem. 1998 Dec 11;273(50):33465–33471. doi: 10.1074/jbc.273.50.33465. [DOI] [PubMed] [Google Scholar]
  18. Hadzic E., Desai-Yajnik V., Helmer E., Guo S., Wu S., Koudinova N., Casanova J., Raaka B. M., Samuels H. H. A 10-amino-acid sequence in the N-terminal A/B domain of thyroid hormone receptor alpha is essential for transcriptional activation and interaction with the general transcription factor TFIIB. Mol Cell Biol. 1995 Aug;15(8):4507–4517. doi: 10.1128/mcb.15.8.4507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ichimura T., Isobe T., Okuyama T., Yamauchi T., Fujisawa H. Brain 14-3-3 protein is an activator protein that activates tryptophan 5-monooxygenase and tyrosine 3-monooxygenase in the presence of Ca2+,calmodulin-dependent protein kinase II. FEBS Lett. 1987 Jul 13;219(1):79–82. doi: 10.1016/0014-5793(87)81194-8. [DOI] [PubMed] [Google Scholar]
  20. Ichimura T., Ito M., Itagaki C., Takahashi M., Horigome T., Omata S., Ohno S., Isobe T. The 14-3-3 protein binds its target proteins with a common site located towards the C-terminus. FEBS Lett. 1997 Aug 18;413(2):273–276. doi: 10.1016/s0014-5793(97)00910-1. [DOI] [PubMed] [Google Scholar]
  21. Ichimura T., Uchiyama J., Kunihiro O., Ito M., Horigome T., Omata S., Shinkai F., Kaji H., Isobe T. Identification of the site of interaction of the 14-3-3 protein with phosphorylated tryptophan hydroxylase. J Biol Chem. 1995 Dec 1;270(48):28515–28518. doi: 10.1074/jbc.270.48.28515. [DOI] [PubMed] [Google Scholar]
  22. Irie K., Gotoh Y., Yashar B. M., Errede B., Nishida E., Matsumoto K. Stimulatory effects of yeast and mammalian 14-3-3 proteins on the Raf protein kinase. Science. 1994 Sep 16;265(5179):1716–1719. doi: 10.1126/science.8085159. [DOI] [PubMed] [Google Scholar]
  23. Jones D. H., Martin H., Madrazo J., Robinson K. A., Nielsen P., Roseboom P. H., Patel Y., Howell S. A., Aitken A. Expression and structural analysis of 14-3-3 proteins. J Mol Biol. 1995 Jan 27;245(4):375–384. doi: 10.1006/jmbi.1994.0031. [DOI] [PubMed] [Google Scholar]
  24. Kim T. K., Hashimoto S., Kelleher R. J., 3rd, Flanagan P. M., Kornberg R. D., Horikoshi M., Roeder R. G. Effects of activation-defective TBP mutations on transcription initiation in yeast. Nature. 1994 May 19;369(6477):252–255. doi: 10.1038/369252a0. [DOI] [PubMed] [Google Scholar]
  25. Kim T. K., Roeder R. G. Proline-rich activator CTF1 targets the TFIIB assembly step during transcriptional activation. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4170–4174. doi: 10.1073/pnas.91.10.4170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Klemm R. D., Goodrich J. A., Zhou S., Tjian R. Molecular cloning and expression of the 32-kDa subunit of human TFIID reveals interactions with VP16 and TFIIB that mediate transcriptional activation. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5788–5792. doi: 10.1073/pnas.92.13.5788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Li S., Janosch P., Tanji M., Rosenfeld G. C., Waymire J. C., Mischak H., Kolch W., Sedivy J. M. Regulation of Raf-1 kinase activity by the 14-3-3 family of proteins. EMBO J. 1995 Feb 15;14(4):685–696. doi: 10.1002/j.1460-2075.1995.tb07047.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lin Y. S., Ha I., Maldonado E., Reinberg D., Green M. R. Binding of general transcription factor TFIIB to an acidic activating region. Nature. 1991 Oct 10;353(6344):569–571. doi: 10.1038/353569a0. [DOI] [PubMed] [Google Scholar]
  29. Liu D., Bienkowska J., Petosa C., Collier R. J., Fu H., Liddington R. Crystal structure of the zeta isoform of the 14-3-3 protein. Nature. 1995 Jul 13;376(6536):191–194. doi: 10.1038/376191a0. [DOI] [PubMed] [Google Scholar]
  30. Liu Y. C., Liu Y., Elly C., Yoshida H., Lipkowitz S., Altman A. Serine phosphorylation of Cbl induced by phorbol ester enhances its association with 14-3-3 proteins in T cells via a novel serine-rich 14-3-3-binding motif. J Biol Chem. 1997 Apr 11;272(15):9979–9985. doi: 10.1074/jbc.272.15.9979. [DOI] [PubMed] [Google Scholar]
  31. Lu G., DeLisle A. J., de Vetten N. C., Ferl R. J. Brain proteins in plants: an Arabidopsis homolog to neurotransmitter pathway activators is part of a DNA binding complex. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11490–11494. doi: 10.1073/pnas.89.23.11490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Luo Z. J., Zhang X. F., Rapp U., Avruch J. Identification of the 14.3.3 zeta domains important for self-association and Raf binding. J Biol Chem. 1995 Oct 6;270(40):23681–23687. doi: 10.1074/jbc.270.40.23681. [DOI] [PubMed] [Google Scholar]
  33. Marra M., Fullone M. R., Fogliano V., Pen J., Mattei M., Masi S., Aducci P. The 30-kilodalton protein present in purified fusicoccin receptor preparations is a 14-3-3-like protein. Plant Physiol. 1994 Dec;106(4):1497–1501. doi: 10.1104/pp.106.4.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Matto-Yelin M., Aitken A., Ravid S. 14-3-3 inhibits the Dictyostelium myosin II heavy-chain-specific protein kinase C activity by a direct interaction: identification of the 14-3-3 binding domain. Mol Biol Cell. 1997 Oct;8(10):1889–1899. doi: 10.1091/mbc.8.10.1889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Morgan A., Burgoyne R. D. Exo1 and Exo2 proteins stimulate calcium-dependent exocytosis in permeabilized adrenal chromaffin cells. Nature. 1992 Feb 27;355(6363):833–836. doi: 10.1038/355833a0. [DOI] [PubMed] [Google Scholar]
  36. Muslin A. J., Tanner J. W., Allen P. M., Shaw A. S. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell. 1996 Mar 22;84(6):889–897. doi: 10.1016/s0092-8674(00)81067-3. [DOI] [PubMed] [Google Scholar]
  37. Nakshatri H., Nakshatri P., Currie R. A. Interaction of Oct-1 with TFIIB. Implications for a novel response elicited through the proximal octamer site of the lipoprotein lipase promoter. J Biol Chem. 1995 Aug 18;270(33):19613–19623. doi: 10.1074/jbc.270.33.19613. [DOI] [PubMed] [Google Scholar]
  38. Odell J. T., Nagy F., Chua N. H. Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. 1985 Feb 28-Mar 6Nature. 313(6005):810–812. doi: 10.1038/313810a0. [DOI] [PubMed] [Google Scholar]
  39. Petosa C., Masters S. C., Bankston L. A., Pohl J., Wang B., Fu H., Liddington R. C. 14-3-3zeta binds a phosphorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. J Biol Chem. 1998 Jun 26;273(26):16305–16310. doi: 10.1074/jbc.273.26.16305. [DOI] [PubMed] [Google Scholar]
  40. Reuther G. W., Fu H., Cripe L. D., Collier R. J., Pendergast A. M. Association of the protein kinases c-Bcr and Bcr-Abl with proteins of the 14-3-3 family. Science. 1994 Oct 7;266(5182):129–133. doi: 10.1126/science.7939633. [DOI] [PubMed] [Google Scholar]
  41. Roberts S. G., Green M. R. Activator-induced conformational change in general transcription factor TFIIB. Nature. 1994 Oct 20;371(6499):717–720. doi: 10.1038/371717a0. [DOI] [PubMed] [Google Scholar]
  42. Roberts S. G., Ha I., Maldonado E., Reinberg D., Green M. R. Interaction between an acidic activator and transcription factor TFIIB is required for transcriptional activation. Nature. 1993 Jun 24;363(6431):741–744. doi: 10.1038/363741a0. [DOI] [PubMed] [Google Scholar]
  43. Rommel C., Radziwill G., Lovrić J., Noeldeke J., Heinicke T., Jones D., Aitken A., Moelling K. Activated Ras displaces 14-3-3 protein from the amino terminus of c-Raf-1. Oncogene. 1996 Feb 1;12(3):609–619. [PubMed] [Google Scholar]
  44. Schultz T. F., Medina J., Hill A., Quatrano R. S. 14-3-3 proteins are part of an abscisic acid-VIVIPAROUS1 (VP1) response complex in the Em promoter and interact with VP1 and EmBP1. Plant Cell. 1998 May;10(5):837–847. doi: 10.1105/tpc.10.5.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tang S. J., Suen T. C., McInnes R. R., Buchwald M. Association of the TLX-2 homeodomain and 14-3-3eta signaling proteins. J Biol Chem. 1998 Sep 25;273(39):25356–25363. doi: 10.1074/jbc.273.39.25356. [DOI] [PubMed] [Google Scholar]
  46. Toker A., Sellers L. A., Amess B., Patel Y., Harris A., Aitken A. Multiple isoforms of a protein kinase C inhibitor (KCIP-1/14-3-3) from sheep brain. Amino acid sequence of phosphorylated forms. Eur J Biochem. 1992 Jun 1;206(2):453–461. doi: 10.1111/j.1432-1033.1992.tb16946.x. [DOI] [PubMed] [Google Scholar]
  47. Vincenz C., Dixit V. M. 14-3-3 proteins associate with A20 in an isoform-specific manner and function both as chaperone and adapter molecules. J Biol Chem. 1996 Aug 16;271(33):20029–20034. doi: 10.1074/jbc.271.33.20029. [DOI] [PubMed] [Google Scholar]
  48. Wakui H., Wright A. P., Gustafsson J., Zilliacus J. Interaction of the ligand-activated glucocorticoid receptor with the 14-3-3 eta protein. J Biol Chem. 1997 Mar 28;272(13):8153–8156. doi: 10.1074/jbc.272.13.8153. [DOI] [PubMed] [Google Scholar]
  49. Wang J., Goodman H. M., Zhang H. An Arabidopsis 14-3-3 protein can act as a transcriptional activator in yeast. FEBS Lett. 1999 Jan 29;443(3):282–284. doi: 10.1016/s0014-5793(98)01739-6. [DOI] [PubMed] [Google Scholar]
  50. Wang W., Shakes D. C. Molecular evolution of the 14-3-3 protein family. J Mol Evol. 1996 Oct;43(4):384–398. doi: 10.1007/BF02339012. [DOI] [PubMed] [Google Scholar]
  51. Wu K., Lu G., Sehnke P., Ferl R. J. The heterologous interactions among plant 14-3-3 proteins and identification of regions that are important for dimerization. Arch Biochem Biophys. 1997 Mar 1;339(1):2–8. doi: 10.1006/abbi.1996.9841. [DOI] [PubMed] [Google Scholar]
  52. Xiao B., Smerdon S. J., Jones D. H., Dodson G. G., Soneji Y., Aitken A., Gamblin S. J. Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature. 1995 Jul 13;376(6536):188–191. doi: 10.1038/376188a0. [DOI] [PubMed] [Google Scholar]
  53. Yaffe M. B., Rittinger K., Volinia S., Caron P. R., Aitken A., Leffers H., Gamblin S. J., Smerdon S. J., Cantley L. C. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell. 1997 Dec 26;91(7):961–971. doi: 10.1016/s0092-8674(00)80487-0. [DOI] [PubMed] [Google Scholar]
  54. Yamauchi T., Nakata H., Fujisawa H. A new activator protein that activates tryptophan 5-monooxygenase and tyrosine 3-monooxygenase in the presence of Ca2+-, calmodulin-dependent protein kinase. Purification and characterization. J Biol Chem. 1981 Jun 10;256(11):5404–5409. [PubMed] [Google Scholar]
  55. de Vetten N. C., Ferl R. J. Two genes encoding GF14 (14-3-3) proteins in Zea mays. Structure, expression, and potential regulation by the G-box binding complex. Plant Physiol. 1994 Dec;106(4):1593–1604. doi: 10.1104/pp.106.4.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. de Vetten N. C., Lu G., Feri R. J. A maize protein associated with the G-box binding complex has homology to brain regulatory proteins. Plant Cell. 1992 Oct;4(10):1295–1307. doi: 10.1105/tpc.4.10.1295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. van Heusden G. P., Griffiths D. J., Ford J. C., Chin-A-Woeng T. F., Schrader P. A., Carr A. M., Steensma H. Y. The 14-3-3 proteins encoded by the BMH1 and BMH2 genes are essential in the yeast Saccharomyces cerevisiae and can be replaced by a plant homologue. Eur J Biochem. 1995 Apr 1;229(1):45–53. [PubMed] [Google Scholar]

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