Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1995 Apr;15(4):1983–1992. doi: 10.1128/mcb.15.4.1983

Mitotic regulation of a TATA-binding-protein-containing complex.

R J White 1, T M Gottlieb 1, C S Downes 1, S P Jackson 1
PMCID: PMC230425  PMID: 7891693

Abstract

The mitotic state is associated with a generalized repression of transcription. We show that mitotic repression of RNA polymerase III transcription can be reproduced by using extracts of synchronized HeLa cells. We have used this system to investigate the molecular basis of transcriptional repression during mitosis. We find a specific decrease in the activity of the TATA-binding-protein (TBP)-containing complex TFIIIB. TBP itself is hyperphosphorylated at mitosis, but this does not appear to account for the loss of TFIIIB activity. Instead, one or more TBP-associated components appear to be regulated. The data suggest that changes in the activity of TBP-associated components contribute to the coordinate repression of gene expression that occurs at mitosis.

Full Text

The Full Text of this article is available as a PDF (439.4 KB).

Selected References

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

  1. Bradbury E. M., Inglis R. J., Matthews H. R. Control of cell division by very lysine rich histone (F1) phosphorylation. Nature. 1974 Feb 1;247(5439):257–261. doi: 10.1038/247257a0. [DOI] [PubMed] [Google Scholar]
  2. Chiang C. M., Ge H., Wang Z., Hoffmann A., Roeder R. G. Unique TATA-binding protein-containing complexes and cofactors involved in transcription by RNA polymerases II and III. EMBO J. 1993 Jul;12(7):2749–2762. doi: 10.1002/j.1460-2075.1993.tb05936.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cormack B. P., Struhl K. The TATA-binding protein is required for transcription by all three nuclear RNA polymerases in yeast cells. Cell. 1992 May 15;69(4):685–696. doi: 10.1016/0092-8674(92)90232-2. [DOI] [PubMed] [Google Scholar]
  4. DAVIDSON D. RNA SYNTHESIS IN ROOTS OF VICIA FABA. Exp Cell Res. 1964 Jul;35:317–325. doi: 10.1016/0014-4827(64)90098-9. [DOI] [PubMed] [Google Scholar]
  5. Dean N., Berk A. J. Ordering promoter binding of class III transcription factors TFIIIC1 and TFIIIC2. Mol Cell Biol. 1988 Aug;8(8):3017–3025. doi: 10.1128/mcb.8.8.3017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Edgar B. A., Schubiger G. Parameters controlling transcriptional activation during early Drosophila development. Cell. 1986 Mar 28;44(6):871–877. doi: 10.1016/0092-8674(86)90009-7. [DOI] [PubMed] [Google Scholar]
  8. Evans T., Rosenthal E. T., Youngblom J., Distel D., Hunt T. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell. 1983 Jun;33(2):389–396. doi: 10.1016/0092-8674(83)90420-8. [DOI] [PubMed] [Google Scholar]
  9. Fink K., Turnock G. Synthesis of transfer RNA during the synchronous nuclear division cycle in Physarum polycephalum. Eur J Biochem. 1977 Oct 17;80(1):93–96. doi: 10.1111/j.1432-1033.1977.tb11860.x. [DOI] [PubMed] [Google Scholar]
  10. Fradkin L. G., Yoshinaga S. K., Berk A. J., Dasgupta A. Inhibition of host cell RNA polymerase III-mediated transcription by poliovirus: inactivation of specific transcription factors. Mol Cell Biol. 1987 Nov;7(11):3880–3887. doi: 10.1128/mcb.7.11.3880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Garber M. E., Vilalta A., Johnson D. L. Induction of Drosophila RNA polymerase III gene expression by the phorbol ester 12-O-tetradecanoylphorbol-13-acetate (TPA) is mediated by transcription factor IIIB. Mol Cell Biol. 1994 Jan;14(1):339–347. doi: 10.1128/mcb.14.1.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goddard J. P., Squire M., Bienz M., Smith J. D. A human tRNAGlu gene of high transcriptional activity. Nucleic Acids Res. 1983 May 11;11(9):2551–2562. doi: 10.1093/nar/11.9.2551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gottesfeld J. M., Wolf V. J., Dang T., Forbes D. J., Hartl P. Mitotic repression of RNA polymerase III transcription in vitro mediated by phosphorylation of a TFIIIB component. Science. 1994 Jan 7;263(5143):81–84. doi: 10.1126/science.8272869. [DOI] [PubMed] [Google Scholar]
  14. Hansen J. C., Wolffe A. P. Influence of chromatin folding on transcription initiation and elongation by RNA polymerase III. Biochemistry. 1992 Sep 1;31(34):7977–7988. doi: 10.1021/bi00149a032. [DOI] [PubMed] [Google Scholar]
  15. Hartl P., Gottesfeld J., Forbes D. J. Mitotic repression of transcription in vitro. J Cell Biol. 1993 Feb;120(3):613–624. doi: 10.1083/jcb.120.3.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hernandez N. TBP, a universal eukaryotic transcription factor? Genes Dev. 1993 Jul;7(7B):1291–1308. doi: 10.1101/gad.7.7b.1291. [DOI] [PubMed] [Google Scholar]
  17. Hisatake K., Hasegawa S., Takada R., Nakatani Y., Horikoshi M., Roeder R. G. The p250 subunit of native TATA box-binding factor TFIID is the cell-cycle regulatory protein CCG1. Nature. 1993 Mar 11;362(6416):179–181. doi: 10.1038/362179a0. [DOI] [PubMed] [Google Scholar]
  18. Hoeffler W. K., Roeder R. G. Enhancement of RNA polymerase III transcription by the E1A gene product of adenovirus. Cell. 1985 Jul;41(3):955–963. doi: 10.1016/s0092-8674(85)80076-3. [DOI] [PubMed] [Google Scholar]
  19. Huet J., Sentenac A. The TATA-binding protein participates in TFIIIB assembly on tRNA genes. Nucleic Acids Res. 1992 Dec 25;20(24):6451–6454. doi: 10.1093/nar/20.24.6451. [DOI] [PMC free article] [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. Kassavetis G. A., Joazeiro C. A., Pisano M., Geiduschek E. P., Colbert T., Hahn S., Blanco J. A. The role of the TATA-binding protein in the assembly and function of the multisubunit yeast RNA polymerase III transcription factor, TFIIIB. Cell. 1992 Dec 11;71(6):1055–1064. doi: 10.1016/0092-8674(92)90399-w. [DOI] [PubMed] [Google Scholar]
  22. Kovelman R., Roeder R. G. Purification and characterization of two forms of human transcription factor IIIC. J Biol Chem. 1992 Dec 5;267(34):24446–24456. [PubMed] [Google Scholar]
  23. Lobo S. M., Ifill S., Hernandez N. cis-acting elements required for RNA polymerase II and III transcription in the human U2 and U6 snRNA promoters. Nucleic Acids Res. 1990 May 25;18(10):2891–2899. doi: 10.1093/nar/18.10.2891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lobo S. M., Tanaka M., Sullivan M. L., Hernandez N. A TBP complex essential for transcription from TATA-less but not TATA-containing RNA polymerase III promoters is part of the TFIIIB fraction. Cell. 1992 Dec 11;71(6):1029–1040. doi: 10.1016/0092-8674(92)90397-u. [DOI] [PubMed] [Google Scholar]
  25. Meissner W., Holland R., Waldschmidt R., Seifart K. H. Transcription factor IIA stimulates the expression of classical polIII-genes. Nucleic Acids Res. 1993 Feb 25;21(4):1013–1018. doi: 10.1093/nar/21.4.1013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Minshull J., Pines J., Golsteyn R., Standart N., Mackie S., Colman A., Blow J., Ruderman J. V., Wu M., Hunt T. The role of cyclin synthesis, modification and destruction in the control of cell division. J Cell Sci Suppl. 1989;12:77–97. doi: 10.1242/jcs.1989.supplement_12.8. [DOI] [PubMed] [Google Scholar]
  27. Murray A. W., Kirschner M. W. Cyclin synthesis drives the early embryonic cell cycle. Nature. 1989 May 25;339(6222):275–280. doi: 10.1038/339275a0. [DOI] [PubMed] [Google Scholar]
  28. Murray A. W., Solomon M. J., Kirschner M. W. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature. 1989 May 25;339(6222):280–286. doi: 10.1038/339280a0. [DOI] [PubMed] [Google Scholar]
  29. PRESCOTT D. M., BENDER M. A. Synthesis of RNA and protein during mitosis in mammalian tissue culture cells. Exp Cell Res. 1962 Mar;26:260–268. doi: 10.1016/0014-4827(62)90176-3. [DOI] [PubMed] [Google Scholar]
  30. Partridge J. F., La Thangue N. B. A developmentally regulated and tissue-dependent transcription factor complexes with the retinoblastoma gene product. EMBO J. 1991 Dec;10(12):3819–3827. doi: 10.1002/j.1460-2075.1991.tb04951.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pruzan R., Chatterjee P. K., Flint S. J. Specific transcription from the adenovirus E2E promoter by RNA polymerase III requires a subpopulation of TFIID. Nucleic Acids Res. 1992 Nov 11;20(21):5705–5712. doi: 10.1093/nar/20.21.5705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pugh B. F., Tjian R. Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell. 1990 Jun 29;61(7):1187–1197. doi: 10.1016/0092-8674(90)90683-6. [DOI] [PubMed] [Google Scholar]
  33. Rigby P. W. Three in one and one in three: it all depends on TBP. Cell. 1993 Jan 15;72(1):7–10. doi: 10.1016/0092-8674(93)90042-o. [DOI] [PubMed] [Google Scholar]
  34. Roeder R. G. Multiple forms of deoxyribonucleic acid-dependent ribonucleic acid polymerase in Xenopus laevis. Isolation and partial characterization. J Biol Chem. 1974 Jan 10;249(1):241–248. [PubMed] [Google Scholar]
  35. Ruppert S., Wang E. H., Tjian R. Cloning and expression of human TAFII250: a TBP-associated factor implicated in cell-cycle regulation. Nature. 1993 Mar 11;362(6416):175–179. doi: 10.1038/362175a0. [DOI] [PubMed] [Google Scholar]
  36. Sahasrabuddhe C. G., Adlakha R. C., Rao P. N. Phosphorylation of non-histone proteins associated with mitosis in HeLa cells. Exp Cell Res. 1984 Aug;153(2):439–450. doi: 10.1016/0014-4827(84)90612-8. [DOI] [PubMed] [Google Scholar]
  37. Sakonju S., Bogenhagen D. F., Brown D. D. A control region in the center of the 5S RNA gene directs specific initiation of transcription: I. The 5' border of the region. Cell. 1980 Jan;19(1):13–25. doi: 10.1016/0092-8674(80)90384-0. [DOI] [PubMed] [Google Scholar]
  38. Schultz M. C., Reeder R. H., Hahn S. Variants of the TATA-binding protein can distinguish subsets of RNA polymerase I, II, and III promoters. Cell. 1992 May 15;69(4):697–702. doi: 10.1016/0092-8674(92)90233-3. [DOI] [PubMed] [Google Scholar]
  39. Segall J., Matsui T., Roeder R. G. Multiple factors are required for the accurate transcription of purified genes by RNA polymerase III. J Biol Chem. 1980 Dec 25;255(24):11986–11991. [PubMed] [Google Scholar]
  40. Sekiguchi T., Miyata T., Nishimoto T. Molecular cloning of the cDNA of human X chromosomal gene (CCG1) which complements the temperature-sensitive G1 mutants, tsBN462 and ts13, of the BHK cell line. EMBO J. 1988 Jun;7(6):1683–1687. doi: 10.1002/j.1460-2075.1988.tb02996.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sekiguchi T., Nohiro Y., Nakamura Y., Hisamoto N., Nishimoto T. The human CCG1 gene, essential for progression of the G1 phase, encodes a 210-kilodalton nuclear DNA-binding protein. Mol Cell Biol. 1991 Jun;11(6):3317–3325. doi: 10.1128/mcb.11.6.3317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Simmen K. A., Bernués J., Parry H. D., Stunnenberg H. G., Berkenstam A., Cavallini B., Egly J. M., Mattaj I. W. TFIID is required for in vitro transcription of the human U6 gene by RNA polymerase III. EMBO J. 1991 Jul;10(7):1853–1862. doi: 10.1002/j.1460-2075.1991.tb07711.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. TAYLOR J. H. Nucleic acid synthesis in relation to the cell division cycle. Ann N Y Acad Sci. 1960 Oct 7;90:409–421. doi: 10.1111/j.1749-6632.1960.tb23259.x. [DOI] [PubMed] [Google Scholar]
  44. TERASIMA T., TOLMACH L. J. Growth and nucleic acid synthesis in synchronously dividing populations of HeLa cells. Exp Cell Res. 1963 Apr;30:344–362. doi: 10.1016/0014-4827(63)90306-9. [DOI] [PubMed] [Google Scholar]
  45. Taggart A. K., Fisher T. S., Pugh B. F. The TATA-binding protein and associated factors are components of pol III transcription factor TFIIIB. Cell. 1992 Dec 11;71(6):1015–1028. doi: 10.1016/0092-8674(92)90396-t. [DOI] [PubMed] [Google Scholar]
  46. Tower J., Sollner-Webb B. Polymerase III transcription factor B activity is reduced in extracts of growth-restricted cells. Mol Cell Biol. 1988 Feb;8(2):1001–1005. doi: 10.1128/mcb.8.2.1001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Waldschmidt R., Seifart K. H. TFIIA is required for in vitro transcription of mammalian U6 genes by RNA polymerase III. J Biol Chem. 1992 Aug 15;267(23):16359–16364. [PubMed] [Google Scholar]
  48. Wang E. H., Tjian R. Promoter-selective transcriptional defect in cell cycle mutant ts13 rescued by hTAFII250. Science. 1994 Feb 11;263(5148):811–814. doi: 10.1126/science.8303298. [DOI] [PubMed] [Google Scholar]
  49. White R. J., Jackson S. P. Mechanism of TATA-binding protein recruitment to a TATA-less class III promoter. Cell. 1992 Dec 11;71(6):1041–1053. doi: 10.1016/0092-8674(92)90398-v. [DOI] [PubMed] [Google Scholar]
  50. White R. J., Jackson S. P., Rigby P. W. A role for the TATA-box-binding protein component of the transcription factor IID complex as a general RNA polymerase III transcription factor. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1949–1953. doi: 10.1073/pnas.89.5.1949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. White R. J., Jackson S. P. The TATA-binding protein: a central role in transcription by RNA polymerases I, II and III. Trends Genet. 1992 Aug;8(8):284–288. doi: 10.1016/0168-9525(92)90255-3. [DOI] [PubMed] [Google Scholar]
  52. White R. J., Khoo B. C., Inostroza J. A., Reinberg D., Jackson S. P. Differential regulation of RNA polymerases I, II, and III by the TBP-binding repressor Dr1. Science. 1994 Oct 21;266(5184):448–450. doi: 10.1126/science.7939686. [DOI] [PubMed] [Google Scholar]
  53. White R. J., Rigby P. W., Jackson S. P. The TATA-binding protein is a general transcription factor for RNA polymerase III. J Cell Sci Suppl. 1992;16:1–7. doi: 10.1242/jcs.1992.supplement_16.1. [DOI] [PubMed] [Google Scholar]
  54. White R. J., Stott D., Rigby P. W. Regulation of RNA polymerase III transcription in response to F9 embryonal carcinoma stem cell differentiation. Cell. 1989 Dec 22;59(6):1081–1092. doi: 10.1016/0092-8674(89)90764-2. [DOI] [PubMed] [Google Scholar]
  55. Willis I. M. RNA polymerase III. Genes, factors and transcriptional specificity. Eur J Biochem. 1993 Feb 15;212(1):1–11. doi: 10.1111/j.1432-1033.1993.tb17626.x. [DOI] [PubMed] [Google Scholar]
  56. Yoshinaga S., Dean N., Han M., Berk A. J. Adenovirus stimulation of transcription by RNA polymerase III: evidence for an E1A-dependent increase in transcription factor IIIC concentration. EMBO J. 1986 Feb;5(2):343–354. doi: 10.1002/j.1460-2075.1986.tb04218.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES