Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1995 Dec;15(12):6653–6662. doi: 10.1128/mcb.15.12.6653

Cell cycle regulation of RNA polymerase III transcription.

R J White 1, T M Gottlieb 1, C S Downes 1, S P Jackson 1
PMCID: PMC230918  PMID: 8524230

Abstract

Inactivation of the TATA-binding protein-containing complex TFIIIB contributes to the mitotic repression of RNA polymerase III transcription, both in frogs and in humans (J. M. Gottesfeld, V. J. Wolf, T. Dang, D. J. Forbes, and P. Hartl, Science 263:81-84, 1994; R. J. White, T. M. Gottlieb, C. S. Downes, and S. P. Jackson, Mol. Cell. Biol. 15:1983-1992, 1995). Using extracts of synchronized proliferating HeLa cells, we show that TFIIIB activity remains low during the early part of G1 phase and increases only gradually as cells approach S phase. As a result, the transcription of all class III genes tested is significantly less active in early G1 than it is in S or G2 phase, both in vitro and in vivo. The increased activity of TFIIIB as cells progress through interphase appears to be due to changes in the TATA-binding protein-associated components of this complex. The data suggest that TFIIIB is an important target for the cell cycle regulation of RNA polymerase III transcription during both mitosis and interphase of actively proliferating HeLa cells.

Full Text

The Full Text of this article is available as a PDF (501.8 KB).

Selected References

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

  1. Brinkley B. R., Rao P. N. Nitrous oxide: effects on the mitotic apparatus and chromosome movement in HeLa cells. J Cell Biol. 1973 Jul;58(1):96–106. doi: 10.1083/jcb.58.1.96. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Buratowski S., Zhou H. A suppressor of TBP mutations encodes an RNA polymerase III transcription factor with homology to TFIIB. Cell. 1992 Oct 16;71(2):221–230. doi: 10.1016/0092-8674(92)90351-c. [DOI] [PubMed] [Google Scholar]
  3. 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]
  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. 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]
  6. 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]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. Hoeffler W. K., Kovelman R., Roeder R. G. Activation of transcription factor IIIC by the adenovirus E1A protein. Cell. 1988 Jun 17;53(6):907–920. doi: 10.1016/s0092-8674(88)90409-6. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Ittmann M., Greco A., Basilico C. Isolation of the human gene that complements a temperature-sensitive cell cycle mutation in BHK cells. Mol Cell Biol. 1987 Oct;7(10):3386–3393. doi: 10.1128/mcb.7.10.3386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Johnston G. C., Singer R. A. RNA synthesis and control of cell division in the yeast S. cerevisiae. Cell. 1978 Aug;14(4):951–958. doi: 10.1016/0092-8674(78)90349-5. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Kunkel G. R., Maser R. L., Calvet J. P., Pederson T. U6 small nuclear RNA is transcribed by RNA polymerase III. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8575–8579. doi: 10.1073/pnas.83.22.8575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lania L., Pannuti A., La Mantia G., Basilico C. The transcription of B2 repeated sequences is regulated during the transition from quiescent to proliferative state in cultured rodent cells. FEBS Lett. 1987 Jul 27;219(2):400–404. doi: 10.1016/0014-5793(87)80260-0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Mann C., Micouin J. Y., Chiannilkulchai N., Treich I., Buhler J. M., Sentenac A. RPC53 encodes a subunit of Saccharomyces cerevisiae RNA polymerase C (III) whose inactivation leads to a predominantly G1 arrest. Mol Cell Biol. 1992 Oct;12(10):4314–4326. doi: 10.1128/mcb.12.10.4314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mauck J. C., Green H. Regulation of pre-transfer RNA synthesis during transition from resting to growing state. Cell. 1974 Oct;3(2):171–177. doi: 10.1016/0092-8674(74)90122-6. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Pardee A. B. G1 events and regulation of cell proliferation. Science. 1989 Nov 3;246(4930):603–608. doi: 10.1126/science.2683075. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. 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]
  28. Simmen K. A., Bernués J., Lewis J. D., Mattaj I. W. Cofractionation of the TATA-binding protein with the RNA polymerase III transcription factor TFIIIB. Nucleic Acids Res. 1992 Nov 25;20(22):5889–5898. doi: 10.1093/nar/20.22.5889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. 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]
  33. 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]
  34. 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]
  35. White R. J., Gottlieb T. M., Downes C. S., Jackson S. P. Mitotic regulation of a TATA-binding-protein-containing complex. Mol Cell Biol. 1995 Apr;15(4):1983–1992. doi: 10.1128/mcb.15.4.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. 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]
  39. 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]
  40. 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]
  41. 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]
  42. White R. J., Stott D., Rigby P. W. Regulation of RNA polymerase III transcription in response to Simian virus 40 transformation. EMBO J. 1990 Nov;9(11):3713–3721. doi: 10.1002/j.1460-2075.1990.tb07584.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Wright S., Lu X., Peterlin B. M. Human immunodeficiency virus type 1 tat directs transcription through attenuation sites within the mouse c-myc gene. J Mol Biol. 1994 Nov 4;243(4):568–573. doi: 10.1016/0022-2836(94)90031-0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES