Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1998 May 1;26(9):2112–2119. doi: 10.1093/nar/26.9.2112

TFIID (TBP) stabilizes the binding of MyoD to its DNA site at the promoter and MyoD facilitates the association of TFIIB with the preinitiation complex.

H Heller 1, E Bengal 1
PMCID: PMC147529  PMID: 9547268

Abstract

The myogenic determination factor MyoD activates the transcription of muscle-specific genes by binding to consensus DNA sites found in the regulatory sequences of these genes. The interaction of MyoD with the basal transcription machinery is not known. Several activators induce transcription by recruiting TFIID and/or TFIIB to the promoter. We asked whether MyoD interacted functionally with TFIID and TFIIB in transcription. We reconstituted in vitro DNA binding and transcription systems of MyoD and basal transcription factors, and found that MyoD function in transcription occurred during the assembly of the preinitiation complex. Interestingly, MyoD activated transcription without affecting the binding of TFIID to the promoter. However, TFIID or TBP dramatically stabilized the binding of MyoD to its recognition site. MyoD and TBP interacted in solution. Deletion analysis of MyoD suggested that interaction of MyoD with TBP is needed for its activity in transcription. At a later stage of assembly, MyoD stabilized the binding of TFIIB to the preinitiation complex. These findings suggest that MyoD is involved in two steps of preinitiation; first, TFIID stabilizes MyoD binding to its DNA recognition site and at a later stage MyoD facilitates the association of TFIIB with the preinitiation complex.

Full Text

The Full Text of this article is available as a PDF (290.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abmayr S. M., Workman J. L., Roeder R. G. The pseudorabies immediate early protein stimulates in vitro transcription by facilitating TFIID: promoter interactions. Genes Dev. 1988 May;2(5):542–553. doi: 10.1101/gad.2.5.542. [DOI] [PubMed] [Google Scholar]
  2. Agostini I., Navarro J. M., Rey F., Bouhamdan M., Spire B., Vigne R., Sire J. The human immunodeficiency virus type 1 Vpr transactivator: cooperation with promoter-bound activator domains and binding to TFIIB. J Mol Biol. 1996 Sep 6;261(5):599–606. doi: 10.1006/jmbi.1996.0485. [DOI] [PubMed] [Google Scholar]
  3. Arias J. A., Dynan W. S. Promoter-dependent transcription by RNA polymerase II using immobilized enzyme complexes. J Biol Chem. 1989 Feb 25;264(6):3223–3229. [PubMed] [Google Scholar]
  4. Baniahmad A., Ha I., Reinberg D., Tsai S., Tsai M. J., O'Malley B. W. Interaction of human thyroid hormone receptor beta with transcription factor TFIIB may mediate target gene derepression and activation by thyroid hormone. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8832–8836. doi: 10.1073/pnas.90.19.8832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bengal E., Flores O., Rangarajan P. N., Chen A., Weintraub H., Verma I. M. Positive control mutations in the MyoD basic region fail to show cooperative DNA binding and transcriptional activation in vitro. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6221–6225. doi: 10.1073/pnas.91.13.6221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blackwell T. K., Weintraub H. Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science. 1990 Nov 23;250(4984):1104–1110. doi: 10.1126/science.2174572. [DOI] [PubMed] [Google Scholar]
  7. Blanco J. C., Wang I. M., Tsai S. Y., Tsai M. J., O'Malley B. W., Jurutka P. W., Haussler M. R., Ozato K. Transcription factor TFIIB and the vitamin D receptor cooperatively activate ligand-dependent transcription. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1535–1539. doi: 10.1073/pnas.92.5.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buskin J. N., Hauschka S. D. Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol Cell Biol. 1989 Jun;9(6):2627–2640. doi: 10.1128/mcb.9.6.2627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chatterjee S., Struhl K. Connecting a promoter-bound protein to TBP bypasses the need for a transcriptional activation domain. Nature. 1995 Apr 27;374(6525):820–822. doi: 10.1038/374820a0. [DOI] [PubMed] [Google Scholar]
  10. Chen J. L., Attardi L. D., Verrijzer C. P., Yokomori K., Tjian R. Assembly of recombinant TFIID reveals differential coactivator requirements for distinct transcriptional activators. Cell. 1994 Oct 7;79(1):93–105. doi: 10.1016/0092-8674(94)90403-0. [DOI] [PubMed] [Google Scholar]
  11. Chen X., Farmer G., Zhu H., Prywes R., Prives C. Cooperative DNA binding of p53 with TFIID (TBP): a possible mechanism for transcriptional activation. Genes Dev. 1993 Oct;7(10):1837–1849. doi: 10.1101/gad.7.10.1837. [DOI] [PubMed] [Google Scholar]
  12. Choy B., Green M. R. Eukaryotic activators function during multiple steps of preinitiation complex assembly. Nature. 1993 Dec 9;366(6455):531–536. doi: 10.1038/366531a0. [DOI] [PubMed] [Google Scholar]
  13. Coleman R. A., Pugh B. F. Evidence for functional binding and stable sliding of the TATA binding protein on nonspecific DNA. J Biol Chem. 1995 Jun 9;270(23):13850–13859. doi: 10.1074/jbc.270.23.13850. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Emerson C. P., Jr Skeletal myogenesis: genetics and embryology to the fore. Curr Opin Genet Dev. 1993 Apr;3(2):265–274. doi: 10.1016/0959-437x(93)90033-l. [DOI] [PubMed] [Google Scholar]
  18. Flores O., Lu H., Reinberg D. Factors involved in specific transcription by mammalian RNA polymerase II. Identification and characterization of factor IIH. J Biol Chem. 1992 Feb 5;267(4):2786–2793. [PubMed] [Google Scholar]
  19. Gerber A. N., Klesert T. R., Bergstrom D. A., Tapscott S. J. Two domains of MyoD mediate transcriptional activation of genes in repressive chromatin: a mechanism for lineage determination in myogenesis. Genes Dev. 1997 Feb 15;11(4):436–450. doi: 10.1101/gad.11.4.436. [DOI] [PubMed] [Google Scholar]
  20. Gonzalez-Couto E., Klages N., Strubin M. Synergistic and promoter-selective activation of transcription by recruitment of transcription factors TFIID and TFIIB. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8036–8041. doi: 10.1073/pnas.94.15.8036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Goodrich J. A., Tjian R. TBP-TAF complexes: selectivity factors for eukaryotic transcription. Curr Opin Cell Biol. 1994 Jun;6(3):403–409. doi: 10.1016/0955-0674(94)90033-7. [DOI] [PubMed] [Google Scholar]
  22. Ha I., Lane W. S., Reinberg D. Cloning of a human gene encoding the general transcription initiation factor IIB. Nature. 1991 Aug 22;352(6337):689–695. doi: 10.1038/352689a0. [DOI] [PubMed] [Google Scholar]
  23. Ho S. N., Biggar S. R., Spencer D. M., Schreiber S. L., Crabtree G. R. Dimeric ligands define a role for transcriptional activation domains in reinitiation. Nature. 1996 Aug 29;382(6594):822–826. doi: 10.1038/382822a0. [DOI] [PubMed] [Google Scholar]
  24. Horikoshi M., Carey M. F., Kakidani H., Roeder R. G. Mechanism of action of a yeast activator: direct effect of GAL4 derivatives on mammalian TFIID-promoter interactions. Cell. 1988 Aug 26;54(5):665–669. doi: 10.1016/s0092-8674(88)80011-4. [DOI] [PubMed] [Google Scholar]
  25. Horikoshi M., Hai T., Lin Y. S., Green M. R., Roeder R. G. Transcription factor ATF interacts with the TATA factor to facilitate establishment of a preinitiation complex. Cell. 1988 Sep 23;54(7):1033–1042. doi: 10.1016/0092-8674(88)90118-3. [DOI] [PubMed] [Google Scholar]
  26. Ing N. H., Beekman J. M., Tsai S. Y., Tsai M. J., O'Malley B. W. Members of the steroid hormone receptor superfamily interact with TFIIB (S300-II). J Biol Chem. 1992 Sep 5;267(25):17617–17623. [PubMed] [Google Scholar]
  27. Jacq X., Brou C., Lutz Y., Davidson I., Chambon P., Tora L. Human TAFII30 is present in a distinct TFIID complex and is required for transcriptional activation by the estrogen receptor. Cell. 1994 Oct 7;79(1):107–117. doi: 10.1016/0092-8674(94)90404-9. [DOI] [PubMed] [Google Scholar]
  28. Kerr L. D., Ransone L. J., Wamsley P., Schmitt M. J., Boyer T. G., Zhou Q., Berk A. J., Verma I. M. Association between proto-oncoprotein Rel and TATA-binding protein mediates transcriptional activation by NF-kappa B. Nature. 1993 Sep 30;365(6445):412–419. doi: 10.1038/365412a0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Klages N., Strubin M. Stimulation of RNA polymerase II transcription initiation by recruitment of TBP in vivo. Nature. 1995 Apr 27;374(6525):822–823. doi: 10.1038/374822a0. [DOI] [PubMed] [Google Scholar]
  31. Lassar A. B., Davis R. L., Wright W. E., Kadesch T., Murre C., Voronova A., Baltimore D., Weintraub H. Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell. 1991 Jul 26;66(2):305–315. doi: 10.1016/0092-8674(91)90620-e. [DOI] [PubMed] [Google Scholar]
  32. Lieberman P. M., Berk A. J. A mechanism for TAFs in transcriptional activation: activation domain enhancement of TFIID-TFIIA--promoter DNA complex formation. Genes Dev. 1994 May 1;8(9):995–1006. doi: 10.1101/gad.8.9.995. [DOI] [PubMed] [Google Scholar]
  33. Lin Y. S., Green M. R. Mechanism of action of an acidic transcriptional activator in vitro. Cell. 1991 Mar 8;64(5):971–981. doi: 10.1016/0092-8674(91)90321-o. [DOI] [PubMed] [Google Scholar]
  34. Liu X., Berk A. J. Reversal of in vitro p53 squelching by both TFIIB and TFIID. Mol Cell Biol. 1995 Nov;15(11):6474–6478. doi: 10.1128/mcb.15.11.6474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lu H., Flores O., Weinmann R., Reinberg D. The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10004–10008. doi: 10.1073/pnas.88.22.10004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. MacDonald P. N., Sherman D. R., Dowd D. R., Jefcoat S. C., Jr, DeLisle R. K. The vitamin D receptor interacts with general transcription factor IIB. J Biol Chem. 1995 Mar 3;270(9):4748–4752. doi: 10.1074/jbc.270.9.4748. [DOI] [PubMed] [Google Scholar]
  37. Maldonado E., Ha I., Cortes P., Weis L., Reinberg D. Factors involved in specific transcription by mammalian RNA polymerase II: role of transcription factors IIA, IID, and IIB during formation of a transcription-competent complex. Mol Cell Biol. 1990 Dec;10(12):6335–6347. doi: 10.1128/mcb.10.12.6335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3855–3859. doi: 10.1073/pnas.77.7.3855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Olson E. N., Klein W. H. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 1994 Jan;8(1):1–8. doi: 10.1101/gad.8.1.1. [DOI] [PubMed] [Google Scholar]
  40. Peterson M. G., Inostroza J., Maxon M. E., Flores O., Admon A., Reinberg D., Tjian R. Structure and functional properties of human general transcription factor IIE. Nature. 1991 Dec 5;354(6352):369–373. doi: 10.1038/354369a0. [DOI] [PubMed] [Google Scholar]
  41. Reinberg D., Horikoshi M., Roeder R. G. Factors involved in specific transcription in mammalian RNA polymerase II. Functional analysis of initiation factors IIA and IID and identification of a new factor operating at sequences downstream of the initiation site. J Biol Chem. 1987 Mar 5;262(7):3322–3330. [PubMed] [Google Scholar]
  42. Roberts S. G., Choy B., Walker S. S., Lin Y. S., Green M. R. A role for activator-mediated TFIIB recruitment in diverse aspects of transcriptional regulation. Curr Biol. 1995 May 1;5(5):508–516. doi: 10.1016/s0960-9822(95)00103-5. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. 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]
  45. Sauer F., Fondell J. D., Ohkuma Y., Roeder R. G., Jäckle H. Control of transcription by Krüppel through interactions with TFIIB and TFIIE beta. Nature. 1995 May 11;375(6527):162–164. doi: 10.1038/375162a0. [DOI] [PubMed] [Google Scholar]
  46. Sawadogo M., Roeder R. G. Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region. Cell. 1985 Nov;43(1):165–175. doi: 10.1016/0092-8674(85)90021-2. [DOI] [PubMed] [Google Scholar]
  47. Schmidt M. C., Zhou Q., Berk A. J. Sp1 activates transcription without enhancing DNA-binding activity of the TATA box factor. Mol Cell Biol. 1989 Aug;9(8):3299–3307. doi: 10.1128/mcb.9.8.3299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Schmitz M. L., Stelzer G., Altmann H., Meisterernst M., Baeuerle P. A. Interaction of the COOH-terminal transactivation domain of p65 NF-kappa B with TATA-binding protein, transcription factor IIB, and coactivators. J Biol Chem. 1995 Mar 31;270(13):7219–7226. doi: 10.1074/jbc.270.13.7219. [DOI] [PubMed] [Google Scholar]
  49. Stargell L. A., Struhl K. Mechanisms of transcriptional activation in vivo: two steps forward. Trends Genet. 1996 Aug;12(8):311–315. doi: 10.1016/0168-9525(96)10028-7. [DOI] [PubMed] [Google Scholar]
  50. Starr D. B., Hoopes B. C., Hawley D. K. DNA bending is an important component of site-specific recognition by the TATA binding protein. J Mol Biol. 1995 Jul 21;250(4):434–446. doi: 10.1006/jmbi.1995.0388. [DOI] [PubMed] [Google Scholar]
  51. Sundseth R., Hansen U. Activation of RNA polymerase II transcription by the specific DNA-binding protein LSF. Increased rate of binding of the basal promoter factor TFIIB. J Biol Chem. 1992 Apr 15;267(11):7845–7855. [PubMed] [Google Scholar]
  52. Wang I. M., Blanco J. C., Tsai S. Y., Tsai M. J., Ozato K. Interferon regulatory factors and TFIIB cooperatively regulate interferon-responsive promoter activity in vivo and in vitro. Mol Cell Biol. 1996 Nov;16(11):6313–6324. doi: 10.1128/mcb.16.11.6313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Weideman C. A., Netter R. C., Benjamin L. R., McAllister J. J., Schmiedekamp L. A., Coleman R. A., Pugh B. F. Dynamic interplay of TFIIA, TBP and TATA DNA. J Mol Biol. 1997 Aug 8;271(1):61–75. doi: 10.1006/jmbi.1997.1152. [DOI] [PubMed] [Google Scholar]
  54. Weintraub H., Davis R., Lockshon D., Lassar A. MyoD binds cooperatively to two sites in a target enhancer sequence: occupancy of two sites is required for activation. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5623–5627. doi: 10.1073/pnas.87.15.5623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Weintraub H., Dwarki V. J., Verma I., Davis R., Hollenberg S., Snider L., Lassar A., Tapscott S. J. Muscle-specific transcriptional activation by MyoD. Genes Dev. 1991 Aug;5(8):1377–1386. doi: 10.1101/gad.5.8.1377. [DOI] [PubMed] [Google Scholar]
  56. Weintraub H. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell. 1993 Dec 31;75(7):1241–1244. doi: 10.1016/0092-8674(93)90610-3. [DOI] [PubMed] [Google Scholar]
  57. White J., Brou C., Wu J., Lutz Y., Moncollin V., Chambon P. The acidic transcriptional activator GAL-VP16 acts on preformed template-committed complexes. EMBO J. 1992 Jun;11(6):2229–2240. doi: 10.1002/j.1460-2075.1992.tb05282.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Zawel L., Kumar K. P., Reinberg D. Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev. 1995 Jun 15;9(12):1479–1490. doi: 10.1101/gad.9.12.1479. [DOI] [PubMed] [Google Scholar]
  59. Zawel L., Reinberg D. Initiation of transcription by RNA polymerase II: a multi-step process. Prog Nucleic Acid Res Mol Biol. 1993;44:67–108. doi: 10.1016/s0079-6603(08)60217-2. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES