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. 1998 Jul 1;26(13):3255–3262. doi: 10.1093/nar/26.13.3255

Multilevel regulation of histone gene expression during the cell cycle in tobacco cells.

J P Reichheld 1, C Gigot 1, N Chaubet-Gigot 1
PMCID: PMC147694  PMID: 9628927

Abstract

The respective involvement of transcriptional and post-transcriptional mechanisms in coupling H3 and H4 histone gene expression to the S phase of the cell cycle has been studied in synchronized tobacco cells. Induction of histone gene expression at the G1/S transition is shown to be essentially directed by an increase in the transcription rate in response to cellular signals occurring at the initiation step of DNA replication. Histone gene induction thus precedes the burst of DNA synthesis. However, when the elongation step of DNA replication is ineffective or artificially arrested, feedback mechanisms apparently act at the translation level to avoid overproduction of histone proteins from their mRNAs. At the end of S phase, post-transcriptional mechanisms ensure a rapid degradation of histone mRNAs. Transcription factors are bound to the cis -elements of histone promoters throughout the cell cycle, thus suggesting a post-translational modification of some of them to trigger promoter activation at the G1/S transition. Based on these results, a model is proposed for histone gene transcriptional induction in connection with the components of the cell cycle machinery.

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Selected References

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  1. Atanassova R., Chaubet N., Gigot C. A 126 bp fragment of a plant histone gene promoter confers preferential expression in meristems of transgenic Arabidopsis. Plant J. 1992 May;2(3):291–300. doi: 10.1111/j.1365-313x.1992.00291.x. [DOI] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  3. Brignon P., Chaubet N. Constitutive and cell-division-inducible protein-DNA interactions in two maize histone gene promoters. Plant J. 1993 Sep;4(3):445–457. doi: 10.1046/j.1365-313x.1993.04030445.x. [DOI] [PubMed] [Google Scholar]
  4. Brignon P., Lepetit M., Gigot C., Chaubet N. Nuclease sensitivity and functional analysis of a maize histone H3 gene promoter. Plant Mol Biol. 1993 Sep;22(6):1007–1015. doi: 10.1007/BF00028973. [DOI] [PubMed] [Google Scholar]
  5. Bénard M., Pierron G. Mapping of a Physarum chromosomal origin of replication tightly linked to a developmentally-regulated profilin gene. Nucleic Acids Res. 1992 Jul 11;20(13):3309–3315. doi: 10.1093/nar/20.13.3309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cardoso M. C., Leonhardt H., Nadal-Ginard B. Reversal of terminal differentiation and control of DNA replication: cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell. 1993 Sep 24;74(6):979–992. doi: 10.1016/0092-8674(93)90721-2. [DOI] [PubMed] [Google Scholar]
  7. Chaubet N., Clement B., Gigot C. Genes encoding a histone H3.3-like variant in Arabidopsis contain intervening sequences. J Mol Biol. 1992 May 20;225(2):569–574. doi: 10.1016/0022-2836(92)90943-e. [DOI] [PubMed] [Google Scholar]
  8. Chaubet N., Flénet M., Clément B., Brignon P., Gigot C. Identification of cis-elements regulating the expression of an Arabidopsis histone H4 gene. Plant J. 1996 Sep;10(3):425–435. doi: 10.1046/j.1365-313x.1996.10030425.x. [DOI] [PubMed] [Google Scholar]
  9. Curie C., Liboz T., Bardet C., Gander E., Médale C., Axelos M., Lescure B. Cis and trans-acting elements involved in the activation of Arabidopsis thaliana A1 gene encoding the translation elongation factor EF-1 alpha. Nucleic Acids Res. 1991 Mar 25;19(6):1305–1310. doi: 10.1093/nar/19.6.1305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Heintz N. The regulation of histone gene expression during the cell cycle. Biochim Biophys Acta. 1991 Mar 26;1088(3):327–339. doi: 10.1016/0167-4781(91)90122-3. [DOI] [PubMed] [Google Scholar]
  11. Hershkovitz M., Riggs A. D. Metaphase chromosome analysis by ligation-mediated PCR: heritable chromatin structure and a comparison of active and inactive X chromosomes. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2379–2383. doi: 10.1073/pnas.92.6.2379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hozák P., Cook P. R. Replication factories. Trends Cell Biol. 1994 Feb;4(2):48–52. doi: 10.1016/0962-8924(94)90009-4. [DOI] [PubMed] [Google Scholar]
  13. Huberman J. A. Prokaryotic and eukaryotic replicons. Cell. 1995 Aug 25;82(4):535–542. doi: 10.1016/0092-8674(95)90025-x. [DOI] [PubMed] [Google Scholar]
  14. Kapros T., Robertson A. J., Waterborg J. H. Histone H3 transcript stability in alfalfa. Plant Mol Biol. 1995 Aug;28(5):901–914. doi: 10.1007/BF00042074. [DOI] [PubMed] [Google Scholar]
  15. Kawata T., Nakayama T., Mikami K., Tabata T., Takase H., Iwabuchi M. DNA-binding protein(s) interacts with a conserved nonameric sequence in the upstream regions of wheat histone genes. FEBS Lett. 1988 Nov 7;239(2):319–323. doi: 10.1016/0014-5793(88)80943-8. [DOI] [PubMed] [Google Scholar]
  16. Laquel P., Litvak S., Castroviejo M. Mammalian proliferating cell nuclear antigen stimulates the processivity of two wheat embryo DNA polymerases. Plant Physiol. 1993 May;102(1):107–114. doi: 10.1104/pp.102.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Laquel P., Litvak S., Castroviejo M. Wheat DNA Primase (RNA Primer Synthesis in Vitro, Structural Studies by Photochemical Cross-Linking, and Modulation of Primase Activity by DNA Polymerases). Plant Physiol. 1994 May;105(1):69–79. doi: 10.1104/pp.105.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lepetit M., Ehling M., Chaubet N., Gigot C. A plant histone gene promoter can direct both replication-dependent and -independent gene expression in transgenic plants. Mol Gen Genet. 1992 Jan;231(2):276–285. doi: 10.1007/BF00279801. [DOI] [PubMed] [Google Scholar]
  19. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  20. Mosca P. J., Lin H. B., Hamlin J. L. Mimosine, a novel inhibitor of DNA replication, binds to a 50 kDa protein in Chinese hamster cells. Nucleic Acids Res. 1995 Jan 25;23(2):261–268. doi: 10.1093/nar/23.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mueller P. R., Wold B. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science. 1989 Nov 10;246(4931):780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]
  22. Ohtsubo N., Nakayama T., Terada R., Shimamoto K., Iwabuchi M. Proximal promoter region of the wheat histone H3 gene confers S phase-specific gene expression in transformed rice cells. Plant Mol Biol. 1993 Nov;23(3):553–565. doi: 10.1007/BF00019303. [DOI] [PubMed] [Google Scholar]
  23. Osley M. A. The regulation of histone synthesis in the cell cycle. Annu Rev Biochem. 1991;60:827–861. doi: 10.1146/annurev.bi.60.070191.004143. [DOI] [PubMed] [Google Scholar]
  24. Pedrali-Noy G., Spadari S., Miller-Faurès A., Miller A. O., Kruppa J., Koch G. Synchronization of HeLa cell cultures by inhibition of DNA polymerase alpha with aphidicolin. Nucleic Acids Res. 1980 Jan 25;8(2):377–387. doi: 10.1093/nar/8.2.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Regad F., Hervé C., Marinx O., Bergounioux C., Tremousaygue D., Lescure B. The tef1 box, a ubiquitous cis-acting element involved in the activation of plant genes that are highly expressed in cycling cells. Mol Gen Genet. 1995 Oct 25;248(6):703–711. doi: 10.1007/BF02191710. [DOI] [PubMed] [Google Scholar]
  26. Reichheld J. P., Chaubet N., Shen W. H., Renaudin J. P., Gigot C. Multiple A-type cyclins express sequentially during the cell cycle in Nicotiana tabacum BY2 cells. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13819–13824. doi: 10.1073/pnas.93.24.13819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schümperli D. Multilevel regulation of replication-dependent histone genes. Trends Genet. 1988 Jul;4(7):187–191. doi: 10.1016/0168-9525(88)90074-1. [DOI] [PubMed] [Google Scholar]
  28. Shen W. H., Gigot C. Protein complexes binding to cis elements of the plant histone gene promoters: multiplicity, phosphorylation and cell cycle alteration. Plant Mol Biol. 1997 Feb;33(3):367–379. doi: 10.1023/a:1005797104536. [DOI] [PubMed] [Google Scholar]
  29. Slater M. L. Effect of reversible inhibition of deoxyribonucleic acid synthesis on the yeast cell cycle. J Bacteriol. 1973 Jan;113(1):263–270. doi: 10.1128/jb.113.1.263-270.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Soni R., Carmichael J. P., Shah Z. H., Murray J. A. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell. 1995 Jan;7(1):85–103. doi: 10.1105/tpc.7.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tabata T., Nakayama T., Mikami K., Iwabuchi M. HBP-1a and HBP-1b: leucine zipper-type transcription factors of wheat. EMBO J. 1991 Jun;10(6):1459–1467. doi: 10.1002/j.1460-2075.1991.tb07666.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Terada R., Nakayama T., Iwabuchi M., Shimamoto K. A type I element composed of the hexamer (ACGTCA) and octamer (CGCGGATC) motifs plays a role(s) in meristematic expression of a wheat histone H3 gene in transgenic rice plants. Plant Mol Biol. 1995 Jan;27(1):17–26. doi: 10.1007/BF00019175. [DOI] [PubMed] [Google Scholar]
  33. Terada R., Nakayama T., Iwabuchi M., Shimamoto K. A wheat histone H3 promoter confers cell division-dependent and -independent expression of the gus A gene in transgenic rice plants. Plant J. 1993 Feb;3(2):241–252. doi: 10.1046/j.1365-313x.1993.t01-16-00999.x. [DOI] [PubMed] [Google Scholar]
  34. Waterborg J. H. Multiplicity of histone h3 variants in wheat, barley, rice, and maize. Plant Physiol. 1991 Jun;96(2):453–458. doi: 10.1104/pp.96.2.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. van Wijnen A. J., Aziz F., Graña X., De Luca A., Desai R. K., Jaarsveld K., Last T. J., Soprano K., Giordano A., Lian J. B. Transcription of histone H4, H3, and H1 cell cycle genes: promoter factor HiNF-D contains CDC2, cyclin A, and an RB-related protein. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12882–12886. doi: 10.1073/pnas.91.26.12882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. van Wijnen A. J., van Gurp M. F., de Ridder M. C., Tufarelli C., Last T. J., Birnbaum M., Vaughan P. S., Giordano A., Krek W., Neufeld E. J. CDP/cut is the DNA-binding subunit of histone gene transcription factor HiNF-D: a mechanism for gene regulation at the G1/S phase cell cycle transition point independent of transcription factor E2F. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11516–11521. doi: 10.1073/pnas.93.21.11516. [DOI] [PMC free article] [PubMed] [Google Scholar]

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