The DPE, a core promoter element for transcription by RNA polymerase II

Kadonaga, James T.

  • Published : 2002.09.30

Abstract

The core promoter is an important yet often overlooked component in the regulation of transcription by RNA polymerase II. In fact, the core promoter is the ultimate target of action of all of the factors and coregulators that control the transcriptional activity of every gene. In this review, I describe our current knowledge of a downstream core promoter element termed the DPE, which is a TFIID recognition site that is conserved from Drosophila to humans. The DPE is located from +28 to +32 relative to the +1 transcription start site, and is mainly present in core promoters that lack a TATA box motif. Moreover, in Drosophila, the DPE appears to be about as common as the TATA box. There are distinct mechanisms of basal transcription from DPE- versus TATA-dependent core promoters. For instance, NC2/Dr1-Drap1 is a repressor of TATA-dependent transcription and an activator of DPE-dependent transcription. In addition, DPE-specific and TATA-specific transcriptional enhancers have been identified. These findings further indicate that the core promoter is an active participant in the regulation of eukaryotic gene expression.

Keywords

References

  1. Mol Cell Biol v.21 Developmental and transcriptional consequences of mutations in Drosophila $TAF_{II}60$ Aoyagi, N.;Wassarman, D.A. https://doi.org/10.1128/MCB.21.20.6808-6819.2001
  2. Genetics v.139 Promoter elements in Drosophila melanogaster revealed by sequence analysis Arkhipova, I.R.
  3. Science v.281 Going the distance: a current view of enhancer action Blackwood, E.M.;Kadonaga, J.T. https://doi.org/10.1126/science.281.5373.60
  4. Annu Rev Biochem v.50 Organization and expression of eucaryotic split genes coding for proteins Breathnach, R.;Chambon, P. https://doi.org/10.1146/annurev.bi.50.070181.002025
  5. J Mol Biol v.212 Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences Bucher, P. https://doi.org/10.1016/0022-2836(90)90223-9
  6. Genes Dev v.13 Looping versus linking: toward a model for long-distance gene activation Bulger, M.;Groudine, M. https://doi.org/10.1101/gad.13.19.2465
  7. Annu Rev Biochem v.65 Biochemistry and structural biology of transcription factor IID (TFIID) Burley, S.K.;Roeder, R.G. https://doi.org/10.1146/annurev.bi.65.070196.004005
  8. Genes Dev v.10 Drosophila TFIID binds to a conserved downstream basal promoter element that is present in many TATA-box-deficient promoters Burke, T.W.;Kadonaga, J.T. https://doi.org/10.1101/gad.10.6.711
  9. Genes Dev v.11 The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by $TAF_{II}60$ of Drosophila Burke, T.W.;Kadonaga, J.T. https://doi.org/10.1101/gad.11.22.3020
  10. Genes Dev v.15 Enhancer-promoter specificity mediated by DPE or TATA core promoter motifs Butler, J.E.F.;Kadonaga, J.T. https://doi.org/10.1101/gad.924301
  11. Genes Dev The RNA polymerase II core promoter: a key component in the regulation of gene expression Butler, J.E.F.;Kadonaga, J.T.
  12. Science v.209 Promoter sequences of eukaryotic protein-coding genes Corden, J.;Wasylyk, B.;Buchwalder, A.;Sassone-Corsi, P.;Kedinger, C.;Chambon, P. https://doi.org/10.1126/science.6251548
  13. Genes Dev v.15 Transcriptional repression: the long and the short of it Courey, A.J.;Jia, S.
  14. Curr Opin Genet Dev v.11 Mechanism of transcription initiation and promoter escape by RNA polymerase II Dvir, A.;Conaway, J.W.;Conaway, R.C. https://doi.org/10.1016/S0959-437X(00)00181-7
  15. Cell v.109 Specificity of gene regulation Emerson, B. https://doi.org/10.1016/S0092-8674(02)00740-7
  16. Genes Dev v.15 Activator-mediated disruption of sequence-specific DNA contacts by the general transcription factor TFIIB Evans, R.;Fairley, J.A.;Roberts, S.G.E. https://doi.org/10.1101/gad.206901
  17. Genes Dev v.14 The coregulator exchange in transcriptional functions of nuclear receptors Glass, C.K.;Rosenfeld, M.G.
  18. Sequence analysis of Drosophila histone genes Goldberg, M.L.
  19. Microbiology and Molecular Biology Reviews v.62 Molecular genetics of the RNA polymerase II general transcription machinery Hampsey, M.
  20. Cell v.44 Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22 Hultmark, D.;Klemenz, R.;Gehring, W.J. https://doi.org/10.1016/0092-8674(86)90464-2
  21. Mol Cell Biol v.14 DNA sequence requirements for transcriptional initiator activity in mammalian cells Javahery, R.;Khachi, A.;Lo, K.;Zenzie-Gregory, B.;Smale, S.T. https://doi.org/10.1128/MCB.14.1.116
  22. Mol Cell Biol v.20 The downstream promoter element DPE appears to be as widely used as the TATA box in Drosophila core promoters Kutach, A.K.;Kadonaga, J.T. https://doi.org/10.1128/MCB.20.13.4754-4764.2000
  23. Genes Dev v.12 New core promoter element in RNA polymerase II-dependent transcription: sequence-specific DNA binding by transcription factor IIB Lagrange, T.;Kapanidis, A.N.;Tang, H.;Reinberg, D.;Ebright, R.H. https://doi.org/10.1101/gad.12.1.34
  24. Annu Rev Genet v.34 Transcription of eukaryotic protein-coding genes Lee, T.I.;Young, R.A. https://doi.org/10.1146/annurev.genet.34.1.77
  25. Nature v.392 Allosteric effects of DNA on transcriptional regulators Lefstin, J.A.;Yamamoto, K.R. https://doi.org/10.1038/31860
  26. Genes Dev v.14 Orchestrated response: a symphony of transcription factors for gene control Lemon, B.;Tjian, R. https://doi.org/10.1101/gad.831000
  27. Gene v.182 Generality of a functional initiator consensus sequence Lo, K.;Smale, S.T. https://doi.org/10.1016/S0378-1119(96)00438-6
  28. Cell v.99 Repression: targeting the heart of the matter Maldonado, E.;Hampsey, M.;Reinberg, D. https://doi.org/10.1016/S0092-8674(00)81533-0
  29. Cell v.108 Combinatorial control of gene expression by nuclear receptors and coregulators McKenna, N.J.;O'Malley, B.W. https://doi.org/10.1016/S0092-8674(02)00641-4
  30. J Biol Chem v.273 RNA polymerase II holoenzymes and subcomplexes Myer, V.E.;Young, R.A. https://doi.org/10.1074/jbc.273.43.27757
  31. Cell v.108 Cooperation between complexes that regulate chromatin structure and transcription Narlikar, G.J.;Fan, H.Y.;Kingston, R.E. https://doi.org/10.1016/S0092-8674(02)00654-2
  32. Genes Dev v.12 Different core promoters possess distinct regulatory activities in the Drosophila embryo Ohtsuki, S.;Levine, M.;Cai, H.N. https://doi.org/10.1101/gad.12.4.547
  33. Genes Dev v.10 The general transcription factors of RNA polymerase II Orphanides, G.;Lagrange, T.;Reinberg, D. https://doi.org/10.1101/gad.10.21.2657
  34. Cell v.108 A unified theory of gene expression Orphanides, G.;Reinberg, D. https://doi.org/10.1016/S0092-8674(02)00655-4
  35. Genes Dev v.8 TFIID sequence recognition of the initiator and sequences farther downstream in Drosophila class II genes Purnell, B.A.;Emanuel, P.A.;Gilmour, D.S. https://doi.org/10.1101/gad.8.7.830
  36. Cold Spring Harbor Symp Quant Biol v.58 Role of general and gene-specific cofactors in the regulation of eukaryotic transcription Roeder, R.G.
  37. Cell v.57 The initiator as a transcription control element Smale, S.T.;Baltimore, D. https://doi.org/10.1016/0092-8674(89)90176-1
  38. Core promoter architecture for eukaryotic proteincoding genes;Transcription: Mechanisms and Regulation Smale, S.T.;Conaway, R.C.(ed.);Conaway, J.W.(ed.)
  39. Biochim Biophys Acta v.1351 Transcription initiation from TATA-less promoters within eukaryotic protein-coding genes Smale, S.T. https://doi.org/10.1016/S0167-4781(96)00206-0
  40. Cold Spring Harbor Symp Quant Biol v.58 The initiator element: a paradigm for core promoter heterogeneity within metazoan protein-coding genes Smale, S.T.;Jain, A.;Kaufmann, J.;Emami, K.H.;Lo, K.;Garraway, I.P.
  41. Genes Dev v.15 Core promoters: active contributors to combinatorial gene regulation Smale, S.T. https://doi.org/10.1101/gad.937701
  42. Mol Cell Biol v.19 $TAF_{II}40$ protein is encoded by the e(y)1 gene: biological consequences of mutations Soldatov, A.;Nabirochkina, E.;Georgieva, S.;Belenkaja, T.;Georgiev, P. https://doi.org/10.1128/MCB.19.5.3769
  43. Nature v.403 The language of covalent histone modifications Strahl, B.D.;Allis, C.D. https://doi.org/10.1038/47412
  44. Cell v.49 Promoters, activator proteins, and the mechanism of transcriptional initiation in yeast Struhl, K. https://doi.org/10.1016/0092-8674(87)90277-7
  45. Cell v.98 Fundamentally different logic of gene regulation in eukaryotes and prokaryotes Struhl, K. https://doi.org/10.1016/S0092-8674(00)80599-1
  46. Genome Res v.11 Identification and characterization of the potential promoter regions of 1031 kinds of human genes Suzuki, Y.;Tsunoda, T.;Sese, J.;Taira, H.;Mizushima-Sugano, J.;Hata, H.;Ota, T.;Isogai, T.;Tanaka, T.;Nakamura, Y.;Suyama, A.;Sakaki, Y.;Morishita, S.;Okubo, K.;Sugano, S. https://doi.org/10.1101/gr.GR-1640R
  47. Genes Dev v.16 A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription Tora, L. https://doi.org/10.1101/gad.976402
  48. FASEB J v.6 Transcription by RNA polymerase II: initiator-directed formation of transcription-competent complexes Weis, L.;Reinberg, D. https://doi.org/10.1096/fasebj.6.14.1426767
  49. Genes Dev v.16 Insulators: many functions, many mechanisms West, A.G.;Gaszner, M.;Felsenfeld, G. https://doi.org/10.1101/gad.954702
  50. Gene Transcription: Mechanisms and Control White, R.J.
  51. Science v.290 A basal transcription factor that activates or represses transcription Willy, P.J.;Kobayashi, R.;Kadonaga, J.T. https://doi.org/10.1126/science.290.5493.982
  52. Genes Dev v.15 Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails Zhang, Y.;Reinberg, D. https://doi.org/10.1101/gad.927301
  53. J Biol Chem v.276 The intronless and TATA-less human $TAF_{II}55$ gene contains a functional initiator and a downstream promoter element Zhou, T.;Chiang, C.M. https://doi.org/10.1074/jbc.M102875200