Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1997 Jun 1;25(11):2174–2181. doi: 10.1093/nar/25.11.2174

CCAAT binding NF-Y-TBP interactions: NF-YB and NF-YC require short domains adjacent to their histone fold motifs for association with TBP basic residues.

M Bellorini 1, D K Lee 1, J C Dantonel 1, K Zemzoumi 1, R G Roeder 1, L Tora 1, R Mantovani 1
PMCID: PMC146709  PMID: 9153318

Abstract

Both the TATA and CCAAT boxes are widespread promoter elements and their binding proteins, TBP and NF-Y, are extremely conserved in evolution. NF-Y is composed of three subunits, NF-YA, NF-YB and NF-YC, all necessary for DNA binding. NF-YB and NF-YC contain a putative histone-like motif, a domain also present in TBP-associated factors (TAFIIs) and in the subunits of the transcriptional repressor NC2. Immunopurification of holo-TFIID with anti-TBP and anti-TAFII100 antibodies indicates that a fraction of NF-YB associates with TFIID in the absence of NF-YA. Sedimentation velocity centrifugation experiments confirm that two pools of NF-YB, and most likely NF-YC, exist: one associated with NF-YA and binding to the CCAAT box; another involved in high molecular weight complexes. We started to dissect NF-Y-TFIID interactions by showing that: (i) NF-YB and NF-YC interact with TBP in solution, both separately and once bound to each other; (ii) short stretches of both NF-YB and NF-YC located within the evolutionary conserved domains, adjacent to the putative histone fold motifs, are necessary for TBP binding; (iii) TBP single amino acid mutants in the HS2 helix, previously shown to be defective in NC2 binding, are also unable to bind NF-YB and NF-YC.

Full Text

The Full Text of this article is available as a PDF (178.5 KB).

Selected References

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

  1. Arents G., Moudrianakis E. N. The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11170–11174. doi: 10.1073/pnas.92.24.11170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arents G., Moudrianakis E. N. Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10489–10493. doi: 10.1073/pnas.90.22.10489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baxevanis A. D., Arents G., Moudrianakis E. N., Landsman D. A variety of DNA-binding and multimeric proteins contain the histone fold motif. Nucleic Acids Res. 1995 Jul 25;23(14):2685–2691. doi: 10.1093/nar/23.14.2685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bellorini M., Dantonel J. C., Yoon J. B., Roeder R. G., Tora L., Mantovani R. The major histocompatibility complex class II Ea promoter requires TFIID binding to an initiator sequence. Mol Cell Biol. 1996 Feb;16(2):503–512. doi: 10.1128/mcb.16.2.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benoist C., Mathis D. Regulation of major histocompatibility complex class-II genes: X, Y and other letters of the alphabet. Annu Rev Immunol. 1990;8:681–715. doi: 10.1146/annurev.iy.08.040190.003341. [DOI] [PubMed] [Google Scholar]
  6. Brou C., Chaudhary S., Davidson I., Lutz Y., Wu J., Egly J. M., Tora L., Chambon P. Distinct TFIID complexes mediate the effect of different transcriptional activators. EMBO J. 1993 Feb;12(2):489–499. doi: 10.1002/j.1460-2075.1993.tb05681.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol. 1990 Apr 20;212(4):563–578. doi: 10.1016/0022-2836(90)90223-9. [DOI] [PubMed] [Google Scholar]
  8. Burley S. K., Roeder R. G. Biochemistry and structural biology of transcription factor IID (TFIID). Annu Rev Biochem. 1996;65:769–799. doi: 10.1146/annurev.bi.65.070196.004005. [DOI] [PubMed] [Google Scholar]
  9. Caron C., Rousset R., Béraud C., Moncollin V., Egly J. M., Jalinot P. Functional and biochemical interaction of the HTLV-I Tax1 transactivator with TBP. EMBO J. 1993 Nov;12(11):4269–4278. doi: 10.1002/j.1460-2075.1993.tb06111.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chang J., Kim D. H., Lee S. W., Choi K. Y., Sung Y. C. Transactivation ability of p53 transcriptional activation domain is directly related to the binding affinity to TATA-binding protein. J Biol Chem. 1995 Oct 20;270(42):25014–25019. doi: 10.1074/jbc.270.42.25014. [DOI] [PubMed] [Google Scholar]
  11. Dorn A., Bollekens J., Staub A., Benoist C., Mathis D. A multiplicity of CCAAT box-binding proteins. Cell. 1987 Sep 11;50(6):863–872. doi: 10.1016/0092-8674(87)90513-7. [DOI] [PubMed] [Google Scholar]
  12. Emili A., Greenblatt J., Ingles C. J. Species-specific interaction of the glutamine-rich activation domains of Sp1 with the TATA box-binding protein. Mol Cell Biol. 1994 Mar;14(3):1582–1593. doi: 10.1128/mcb.14.3.1582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goppelt A., Stelzer G., Lottspeich F., Meisterernst M. A mechanism for repression of class II gene transcription through specific binding of NC2 to TBP-promoter complexes via heterodimeric histone fold domains. EMBO J. 1996 Jun 17;15(12):3105–3116. [PMC free article] [PubMed] [Google Scholar]
  14. Hahn S., Pinkham J., Wei R., Miller R., Guarente L. The HAP3 regulatory locus of Saccharomyces cerevisiae encodes divergent overlapping transcripts. Mol Cell Biol. 1988 Feb;8(2):655–663. doi: 10.1128/mcb.8.2.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hoffmann A., Chiang C. M., Oelgeschläger T., Xie X., Burley S. K., Nakatani Y., Roeder R. G. A histone octamer-like structure within TFIID. Nature. 1996 Mar 28;380(6572):356–359. doi: 10.1038/380356a0. [DOI] [PubMed] [Google Scholar]
  16. Hoffmann A., Roeder R. G. Cloning and characterization of human TAF20/15. Multiple interactions suggest a central role in TFIID complex formation. J Biol Chem. 1996 Jul 26;271(30):18194–18202. doi: 10.1074/jbc.271.30.18194. [DOI] [PubMed] [Google Scholar]
  17. Hooft van Huijsduijnen R. A., Bollekens J., Dorn A., Benoist C., Mathis D. Properties of a CCAAT box-binding protein. Nucleic Acids Res. 1987 Sep 25;15(18):7265–7282. doi: 10.1093/nar/15.18.7265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hooft van Huijsduijnen R., Li X. Y., Black D., Matthes H., Benoist C., Mathis D. Co-evolution from yeast to mouse: cDNA cloning of the two NF-Y (CP-1/CBF) subunits. EMBO J. 1990 Oct;9(10):3119–3127. doi: 10.1002/j.1460-2075.1990.tb07509.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ingles C. J., Shales M., Cress W. D., Triezenberg S. J., Greenblatt J. Reduced binding of TFIID to transcriptionally compromised mutants of VP16. Nature. 1991 Jun 13;351(6327):588–590. doi: 10.1038/351588a0. [DOI] [PubMed] [Google Scholar]
  20. Inostroza J. A., Mermelstein F. H., Ha I., Lane W. S., Reinberg D. Dr1, a TATA-binding protein-associated phosphoprotein and inhibitor of class II gene transcription. Cell. 1992 Aug 7;70(3):477–489. doi: 10.1016/0092-8674(92)90172-9. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Kim C. G., Sheffery M. Physical characterization of the purified CCAAT transcription factor, alpha-CP1. J Biol Chem. 1990 Aug 5;265(22):13362–13369. [PubMed] [Google Scholar]
  23. Kim I. S., Sinha S., de Crombrugghe B., Maity S. N. Determination of functional domains in the C subunit of the CCAAT-binding factor (CBF) necessary for formation of a CBF-DNA complex: CBF-B interacts simultaneously with both the CBF-A and CBF-C subunits to form a heterotrimeric CBF molecule. Mol Cell Biol. 1996 Aug;16(8):4003–4013. doi: 10.1128/mcb.16.8.4003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kim T. K., Zhao Y., Ge H., Bernstein R., Roeder R. G. TATA-binding protein residues implicated in a functional interplay between negative cofactor NC2 (Dr1) and general factors TFIIA and TFIIB. J Biol Chem. 1995 May 5;270(18):10976–10981. doi: 10.1074/jbc.270.18.10976. [DOI] [PubMed] [Google Scholar]
  25. Kokubo T., Yamashita S., Horikoshi M., Roeder R. G., Nakatani Y. Interaction between the N-terminal domain of the 230-kDa subunit and the TATA box-binding subunit of TFIID negatively regulates TATA-box binding. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3520–3524. doi: 10.1073/pnas.91.9.3520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kuromori T., Yamamoto M. Cloning of cDNAs from Arabidopsis thaliana that encode putative protein phosphatase 2C and a human Dr1-like protein by transformation of a fission yeast mutant. Nucleic Acids Res. 1994 Dec 11;22(24):5296–5301. doi: 10.1093/nar/22.24.5296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lee D. K., DeJong J., Hashimoto S., Horikoshi M., Roeder R. G. TFIIA induces conformational changes in TFIID via interactions with the basic repeat. Mol Cell Biol. 1992 Nov;12(11):5189–5196. doi: 10.1128/mcb.12.11.5189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lee W. S., Kao C. C., Bryant G. O., Liu X., Berk A. J. Adenovirus E1A activation domain binds the basic repeat in the TATA box transcription factor. Cell. 1991 Oct 18;67(2):365–376. doi: 10.1016/0092-8674(91)90188-5. [DOI] [PubMed] [Google Scholar]
  29. Li X. Y., Hooft van Huijsduijnen R., Mantovani R., Benoist C., Mathis D. Intron-exon organization of the NF-Y genes. Tissue-specific splicing modifies an activation domain. J Biol Chem. 1992 May 5;267(13):8984–8990. [PubMed] [Google Scholar]
  30. Li X. Y., Mantovani R., Hooft van Huijsduijnen R., Andre I., Benoist C., Mathis D. Evolutionary variation of the CCAAT-binding transcription factor NF-Y. Nucleic Acids Res. 1992 Mar 11;20(5):1087–1091. doi: 10.1093/nar/20.5.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Mantovani R., Li X. Y., Pessara U., Hooft van Huisjduijnen R., Benoist C., Mathis D. Dominant negative analogs of NF-YA. J Biol Chem. 1994 Aug 12;269(32):20340–20346. [PubMed] [Google Scholar]
  32. Mantovani R., Pessara U., Tronche F., Li X. Y., Knapp A. M., Pasquali J. L., Benoist C., Mathis D. Monoclonal antibodies to NF-Y define its function in MHC class II and albumin gene transcription. EMBO J. 1992 Sep;11(9):3315–3322. doi: 10.1002/j.1460-2075.1992.tb05410.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mantovani R., Tora L., Moncollin V., Egly J. M., Benoist C., Mathis D. The major histocompatibility complex (MHC) Ea promoter: sequences and factors at the initiation site. Nucleic Acids Res. 1993 Oct 25;21(21):4873–4878. doi: 10.1093/nar/21.21.4873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. McNabb D. S., Xing Y., Guarente L. Cloning of yeast HAP5: a novel subunit of a heterotrimeric complex required for CCAAT binding. Genes Dev. 1995 Jan 1;9(1):47–58. doi: 10.1101/gad.9.1.47. [DOI] [PubMed] [Google Scholar]
  35. Mengus G., May M., Jacq X., Staub A., Tora L., Chambon P., Davidson I. Cloning and characterization of hTAFII18, hTAFII20 and hTAFII28: three subunits of the human transcription factor TFIID. EMBO J. 1995 Apr 3;14(7):1520–1531. doi: 10.1002/j.1460-2075.1995.tb07138.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mermelstein F., Yeung K., Cao J., Inostroza J. A., Erdjument-Bromage H., Eagelson K., Landsman D., Levitt P., Tempst P., Reinberg D. Requirement of a corepressor for Dr1-mediated repression of transcription. Genes Dev. 1996 Apr 15;10(8):1033–1048. doi: 10.1101/gad.10.8.1033. [DOI] [PubMed] [Google Scholar]
  37. Metz R., Bannister A. J., Sutherland J. A., Hagemeier C., O'Rourke E. C., Cook A., Bravo R., Kouzarides T. c-Fos-induced activation of a TATA-box-containing promoter involves direct contact with TATA-box-binding protein. Mol Cell Biol. 1994 Sep;14(9):6021–6029. doi: 10.1128/mcb.14.9.6021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Milos P. M., Zaret K. S. A ubiquitous factor is required for C/EBP-related proteins to form stable transcription complexes on an albumin promoter segment in vitro. Genes Dev. 1992 Jun;6(6):991–1004. doi: 10.1101/gad.6.6.991. [DOI] [PubMed] [Google Scholar]
  39. Nerlov C., Ziff E. B. CCAAT/enhancer binding protein-alpha amino acid motifs with dual TBP and TFIIB binding ability co-operate to activate transcription in both yeast and mammalian cells. EMBO J. 1995 Sep 1;14(17):4318–4328. doi: 10.1002/j.1460-2075.1995.tb00106.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Osada S., Yamamoto H., Nishihara T., Imagawa M. DNA binding specificity of the CCAAT/enhancer-binding protein transcription factor family. J Biol Chem. 1996 Feb 16;271(7):3891–3896. doi: 10.1074/jbc.271.7.3891. [DOI] [PubMed] [Google Scholar]
  41. Pinkham J. L., Olesen J. T., Guarente L. P. Sequence and nuclear localization of the Saccharomyces cerevisiae HAP2 protein, a transcriptional activator. Mol Cell Biol. 1987 Feb;7(2):578–585. doi: 10.1128/mcb.7.2.578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Reith W., Siegrist C. A., Durand B., Barras E., Mach B. Function of major histocompatibility complex class II promoters requires cooperative binding between factors RFX and NF-Y. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):554–558. doi: 10.1073/pnas.91.2.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ronchi A., Bellorini M., Mongelli N., Mantovani R. CCAAT-box binding protein NF-Y (CBF, CP1) recognizes the minor groove and distorts DNA. Nucleic Acids Res. 1995 Nov 25;23(22):4565–4572. doi: 10.1093/nar/23.22.4565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Schulman I. G., Chakravarti D., Juguilon H., Romo A., Evans R. M. Interactions between the retinoid X receptor and a conserved region of the TATA-binding protein mediate hormone-dependent transactivation. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8288–8292. doi: 10.1073/pnas.92.18.8288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sinha S., Kim I. S., Sohn K. Y., de Crombrugghe B., Maity S. N. Three classes of mutations in the A subunit of the CCAAT-binding factor CBF delineate functional domains involved in the three-step assembly of the CBF-DNA complex. Mol Cell Biol. 1996 Jan;16(1):328–337. doi: 10.1128/mcb.16.1.328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sinha S., Maity S. N., Lu J., de Crombrugghe B. Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1624–1628. doi: 10.1073/pnas.92.5.1624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Steger G., Ham J., Lefebvre O., Yaniv M. The bovine papillomavirus 1 E2 protein contains two activation domains: one that interacts with TBP and another that functions after TBP binding. EMBO J. 1995 Jan 16;14(2):329–340. doi: 10.1002/j.1460-2075.1995.tb07007.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Timmers H. T., Sharp P. A. The mammalian TFIID protein is present in two functionally distinct complexes. Genes Dev. 1991 Nov;5(11):1946–1956. doi: 10.1101/gad.5.11.1946. [DOI] [PubMed] [Google Scholar]
  49. Um M., Li C., Manley J. L. The transcriptional repressor even-skipped interacts directly with TATA-binding protein. Mol Cell Biol. 1995 Sep;15(9):5007–5016. doi: 10.1128/mcb.15.9.5007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wright K. L., Moore T. L., Vilen B. J., Brown A. M., Ting J. P. Major histocompatibility complex class II-associated invariant chain gene expression is up-regulated by cooperative interactions of Sp1 and NF-Y. J Biol Chem. 1995 Sep 8;270(36):20978–20986. doi: 10.1074/jbc.270.36.20978. [DOI] [PubMed] [Google Scholar]
  51. Xiao H., Friesen J. D., Lis J. T. A highly conserved domain of RNA polymerase II shares a functional element with acidic activation domains of upstream transcription factors. Mol Cell Biol. 1994 Nov;14(11):7507–7516. doi: 10.1128/mcb.14.11.7507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Xie X., Kokubo T., Cohen S. L., Mirza U. A., Hoffmann A., Chait B. T., Roeder R. G., Nakatani Y., Burley S. K. Structural similarity between TAFs and the heterotetrameric core of the histone octamer. Nature. 1996 Mar 28;380(6572):316–322. doi: 10.1038/380316a0. [DOI] [PubMed] [Google Scholar]
  53. Xing Y., Fikes J. D., Guarente L. Mutations in yeast HAP2/HAP3 define a hybrid CCAAT box binding domain. EMBO J. 1993 Dec;12(12):4647–4655. doi: 10.1002/j.1460-2075.1993.tb06153.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Yeung K. C., Inostroza J. A., Mermelstein F. H., Kannabiran C., Reinberg D. Structure-function analysis of the TBP-binding protein Dr1 reveals a mechanism for repression of class II gene transcription. Genes Dev. 1994 Sep 1;8(17):2097–2109. doi: 10.1101/gad.8.17.2097. [DOI] [PubMed] [Google Scholar]
  55. Zorbas H., Rein T., Krause A., Hoffmann K., Winnacker E. L. Nuclear factor I (NF I) binds to an NF I-type site but not to the CCAAT site in the human alpha-globin gene promoter. J Biol Chem. 1992 Apr 25;267(12):8478–8484. [PubMed] [Google Scholar]
  56. Zwilling S., Annweiler A., Wirth T. The POU domains of the Oct1 and Oct2 transcription factors mediate specific interaction with TBP. Nucleic Acids Res. 1994 May 11;22(9):1655–1662. doi: 10.1093/nar/22.9.1655. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES