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. 1987 Feb;7(2):614–621. doi: 10.1128/mcb.7.2.614

Role of transcriptional and posttranscriptional regulation in expression of histone genes in Saccharomyces cerevisiae.

D E Lycan, M A Osley, L M Hereford
PMCID: PMC365116  PMID: 3547077

Abstract

We analyzed the role of posttranscriptional mechanisms in the regulation of histone gene expression in Saccharomyces cerevisiae. The rapid drop in histone RNA levels associated with the inhibition of ongoing DNA replication was postulated to be due to posttranscriptional degradation of histone transcripts. However, in analyzing the sequences required for this response, we showed that the coupling of histone RNA levels to DNA replication was due mostly, if not entirely, to transcriptional regulatory mechanisms. Furthermore, deletions which removed the negative, cell cycle control sequences from the histone promoter also uncoupled histone transcription from DNA replication. We propose that the arrest of DNA synthesis prematurely activates the regulatory pathway used in the normal cell cycle to repress transcription. Although posttranscriptional regulation did not appear to play a significant role in coupling histone RNA levels to DNA replication, it did affect the levels of histone RNA in the cell cycle. Posttranscriptional regulation could apparently restore much of the periodicity of histone RNA accumulation in cells which constitutively transcribed the histone genes. Unlike transcriptional regulation, periodic posttranscriptional regulation appears to operate on a clock which is independent of events in the mitotic DNA cycle. Posttranscriptional recognition of histone RNA must require either sequences in the 3' end of the RNA or an intact three-dimensional structure since H2A- and H2B-lacZ fusion transcripts, containing only 5' histone sequences, were insensitive to posttranscriptional controls.

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Selected References

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

  1. Baumbach L. L., Marashi F., Plumb M., Stein G., Stein J. Inhibition of DNA replication coordinately reduces cellular levels of core and H1 histone mRNAs: requirement for protein synthesis. Biochemistry. 1984 Apr 10;23(8):1618–1625. doi: 10.1021/bi00303a006. [DOI] [PubMed] [Google Scholar]
  2. Berk A. J., Sharp P. A. Spliced early mRNAs of simian virus 40. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1274–1278. doi: 10.1073/pnas.75.3.1274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Borun T. W., Scharff M. D., Robbins E. Rapidly labeled, polyribosome-associated RNA having the properties of histone messenger. Proc Natl Acad Sci U S A. 1967 Nov;58(5):1977–1983. doi: 10.1073/pnas.58.5.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Fried H. M., Nam H. G., Loechel S., Teem J. Characterization of yeast strains with conditionally expressed variants of ribosomal protein genes tcm1 and cyh2. Mol Cell Biol. 1985 Jan;5(1):99–108. doi: 10.1128/mcb.5.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gallwitz D. Kinetics of inactivation of histone mRNA in the cytoplasm after inhibition of DNA replication in synchronised HeLa cells. Nature. 1975 Sep 18;257(5523):247–248. doi: 10.1038/257247a0. [DOI] [PubMed] [Google Scholar]
  6. Gallwitz D., Mueller G. C. Histone synthesis in vitro on HeLa cell microsomes. The nature of the coupling to deoxyribonucleic acid synthesis. J Biol Chem. 1969 Nov 10;244(21):5947–5952. [PubMed] [Google Scholar]
  7. Graves R. A., Marzluff W. F. Rapid reversible changes in the rate of histone gene transcription and histone mRNA levels in mouse myeloma cells. Mol Cell Biol. 1984 Feb;4(2):351–357. doi: 10.1128/mcb.4.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Guarente L., Mason T. Heme regulates transcription of the CYC1 gene of S. cerevisiae via an upstream activation site. Cell. 1983 Apr;32(4):1279–1286. doi: 10.1016/0092-8674(83)90309-4. [DOI] [PubMed] [Google Scholar]
  9. Guarente L., Ptashne M. Fusion of Escherichia coli lacZ to the cytochrome c gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2199–2203. doi: 10.1073/pnas.78.4.2199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Guarente L., Yocum R. R., Gifford P. A GAL10-CYC1 hybrid yeast promoter identifies the GAL4 regulatory region as an upstream site. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7410–7414. doi: 10.1073/pnas.79.23.7410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hartwell L. H. Genetic control of the cell division cycle in yeast. II. Genes controlling DNA replication and its initiation. J Mol Biol. 1971 Jul 14;59(1):183–194. doi: 10.1016/0022-2836(71)90420-7. [DOI] [PubMed] [Google Scholar]
  12. Hartwell L. H. Macromolecule synthesis in temperature-sensitive mutants of yeast. J Bacteriol. 1967 May;93(5):1662–1670. doi: 10.1128/jb.93.5.1662-1670.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hartwell L. H. Saccharomyces cerevisiae cell cycle. Bacteriol Rev. 1974 Jun;38(2):164–198. doi: 10.1128/br.38.2.164-198.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hartwell L. H. Sequential function of gene products relative to DNA synthesis in the yeast cell cycle. J Mol Biol. 1976 Jul 15;104(4):803–817. doi: 10.1016/0022-2836(76)90183-2. [DOI] [PubMed] [Google Scholar]
  15. Heintz N., Sive H. L., Roeder R. G. Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol Cell Biol. 1983 Apr;3(4):539–550. doi: 10.1128/mcb.3.4.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hereford L. M., Hartwell L. H. Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis. J Mol Biol. 1974 Apr 15;84(3):445–461. doi: 10.1016/0022-2836(74)90451-3. [DOI] [PubMed] [Google Scholar]
  17. Hereford L. M., Osley M. A., Ludwig T. R., 2nd, McLaughlin C. S. Cell-cycle regulation of yeast histone mRNA. Cell. 1981 May;24(2):367–375. doi: 10.1016/0092-8674(81)90326-3. [DOI] [PubMed] [Google Scholar]
  18. Hereford L., Bromley S., Osley M. A. Periodic transcription of yeast histone genes. Cell. 1982 Aug;30(1):305–310. doi: 10.1016/0092-8674(82)90036-8. [DOI] [PubMed] [Google Scholar]
  19. Hereford L., Fahrner K., Woolford J., Jr, Rosbash M., Kaback D. B. Isolation of yeast histone genes H2A and H2B. Cell. 1979 Dec;18(4):1261–1271. doi: 10.1016/0092-8674(79)90237-x. [DOI] [PubMed] [Google Scholar]
  20. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lüscher B., Stauber C., Schindler R., Schümperli D. Faithful cell-cycle regulation of a recombinant mouse histone H4 gene is controlled by sequences in the 3'-terminal part of the gene. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4389–4393. doi: 10.1073/pnas.82.13.4389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Meeks-Wagner D., Hartwell L. H. Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell. 1986 Jan 17;44(1):43–52. doi: 10.1016/0092-8674(86)90483-6. [DOI] [PubMed] [Google Scholar]
  23. Osley M. A., Gould J., Kim S., Kane M. Y., Hereford L. Identification of sequences in a yeast histone promoter involved in periodic transcription. Cell. 1986 May 23;45(4):537–544. doi: 10.1016/0092-8674(86)90285-0. [DOI] [PubMed] [Google Scholar]
  24. Osley M. A., Hereford L. M. Yeast histone genes show dosage compensation. Cell. 1981 May;24(2):377–384. doi: 10.1016/0092-8674(81)90327-5. [DOI] [PubMed] [Google Scholar]
  25. Osley M. A., Hereford L. Identification of a sequence responsible for periodic synthesis of yeast histone 2A mRNA. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7689–7693. doi: 10.1073/pnas.79.24.7689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Perry R. P., Kelley D. E. Messenger RNA turnover in mouse L cells. J Mol Biol. 1973 Oct 5;79(4):681–696. doi: 10.1016/0022-2836(73)90071-5. [DOI] [PubMed] [Google Scholar]
  27. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  28. Sittman D. B., Graves R. A., Marzluff W. F. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1849–1853. doi: 10.1073/pnas.80.7.1849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Teem J. L., Rosbash M. Expression of a beta-galactosidase gene containing the ribosomal protein 51 intron is sensitive to the rna2 mutation of yeast. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4403–4407. doi: 10.1073/pnas.80.14.4403. [DOI] [PMC free article] [PubMed] [Google Scholar]

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