Abstract
The nucleotide sequences of two chicken histone genes encoding replacement variant H3.3 polypeptides are described. Unlike the replication variant genes of chickens (and almost all other organisms), these genes contain intervening sequences; introns are present in both genes in the 5' noncoding and coding sequences. Furthermore, the replacement variant histone mRNAs are post-transcriptionally polyadenylated. The locations, but not the sizes, of the two introns within the coding segments of the two genes have been exactly conserved, whereas the intron positions in their respective 5' flanking regions differ. Although both H3.3 genes predict the identical histone polypeptide sequence, they are as different from one another as each of them is from a more common replication variant H3.2 gene in silent base substitutions within the coding sequences. Thus, the H3.3 polypeptide sequence has been precisely maintained over a great evolutionary period, suggesting that this class of histones performs a strongly selected biological function. Although replacement variant histones can account for more than 50% of the total H3 protein in the nuclei of specific chicken tissues, the steady-state level of H3.3 mRNA is nearly the same (and is quite low) in all tissues and ages of animals examined. These properties suggest novel mechanisms for the control of the basal histone biosynthesis which takes place outside of the S phase of the cell cycle.
Full text
PDF










Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Benoist C., Chambon P. In vivo sequence requirements of the SV40 early promotor region. Nature. 1981 Mar 26;290(5804):304–310. doi: 10.1038/290304a0. [DOI] [PubMed] [Google Scholar]
- Borun T. W., Ajiro K., Zweidler A., Dolby T. W., Stephens R. E. Studies of human histone messenger RNA. II. The resolution of fractions containing individual human histone messenger RNA species. J Biol Chem. 1977 Jan 10;252(1):173–180. [PubMed] [Google Scholar]
- Brandt W. F., von Holt C. The determination of the primary structure of histone F3 from chicken erythrocytes by automatic Edman degradation. 2. Sequence analysis of histone F3. Eur J Biochem. 1974 Jul 15;46(2):419–429. doi: 10.1111/j.1432-1033.1974.tb03635.x. [DOI] [PubMed] [Google Scholar]
- Butler E. T., Chamberlin M. J. Bacteriophage SP6-specific RNA polymerase. I. Isolation and characterization of the enzyme. J Biol Chem. 1982 May 25;257(10):5772–5778. [PubMed] [Google Scholar]
- Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
- Dodgson J. B., Engel J. D. The nucleotide sequence of the adult chicken alpha-globin genes. J Biol Chem. 1983 Apr 10;258(7):4623–4629. [PubMed] [Google Scholar]
- Dodgson J. B., Stadt S. J., Choi O. R., Dolan M., Fischer H. D., Engel J. D. The nucleotide sequence of the embryonic chicken beta-type globin genes. J Biol Chem. 1983 Oct 25;258(20):12685–12692. [PubMed] [Google Scholar]
- Dodgson J. B., Strommer J., Engel J. D. Isolation of the chicken beta-globin gene and a linked embryonic beta-like globin gene from a chicken DNA recombinant library. Cell. 1979 Aug;17(4):879–887. doi: 10.1016/0092-8674(79)90328-3. [DOI] [PubMed] [Google Scholar]
- Dolan M., Dodgson J. B., Engel J. D. Analysis of the adult chicken beta-globin gene. Nucleotide sequence of the locus, microheterogeneity at the 5'-end of beta-globin mRNA, and aberrant nuclear RNA species. J Biol Chem. 1983 Mar 25;258(6):3983–3990. [PubMed] [Google Scholar]
- Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
- Engel J. D., Dodgson J. B. Analysis of the closely linked adult chicken alpha-globin genes in recombinant DNAs. Proc Natl Acad Sci U S A. 1980 May;77(5):2596–2600. doi: 10.1073/pnas.77.5.2596. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engel J. D., Dodgson J. B. Histone genes are clustered but not tandemly repeated in the chicken genome. Proc Natl Acad Sci U S A. 1981 May;78(5):2856–2860. doi: 10.1073/pnas.78.5.2856. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engel J. D., Rusling D. J., McCune K. C., Dodgson J. B. Unusual structure of the chicken embryonic alpha-globin gene, pi'. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1392–1396. doi: 10.1073/pnas.80.5.1392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engel J. D., Sugarman B. J., Dodgson J. B. A chicken histone H3 gene contains intervening sequences. Nature. 1982 Jun 3;297(5865):434–436. doi: 10.1038/297434a0. [DOI] [PubMed] [Google Scholar]
- Fischer H. D., Dodgson J. B., Hughes S., Engel J. D. An unusual 5' splice sequence is efficiently utilized in vivo. Proc Natl Acad Sci U S A. 1984 May;81(9):2733–2737. doi: 10.1073/pnas.81.9.2733. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fyrberg E. A., Kindle K. L., Davidson N., Kindle K. L. The actin genes of Drosophila: a dispersed multigene family. Cell. 1980 Feb;19(2):365–378. doi: 10.1016/0092-8674(80)90511-5. [DOI] [PubMed] [Google Scholar]
- Grandy D. K., Engel J. D., Dodgson J. B. Complete nucleotide sequence of a chicken H2b histone gene. J Biol Chem. 1982 Aug 10;257(15):8577–8580. [PubMed] [Google Scholar]
- Green M. R., Maniatis T., Melton D. A. Human beta-globin pre-mRNA synthesized in vitro is accurately spliced in Xenopus oocyte nuclei. Cell. 1983 Mar;32(3):681–694. doi: 10.1016/0092-8674(83)90054-5. [DOI] [PubMed] [Google Scholar]
- Harvey R. P., Whiting J. A., Coles L. S., Krieg P. A., Wells J. R. H2A.F: an extremely variant histone H2A sequence expressed in the chicken embryo. Proc Natl Acad Sci U S A. 1983 May;80(10):2819–2823. doi: 10.1073/pnas.80.10.2819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heintz N., Zernik M., Roeder R. G. The structure of the human histone genes: clustered but not tandemly repeated. Cell. 1981 Jun;24(3):661–668. doi: 10.1016/0092-8674(81)90092-1. [DOI] [PubMed] [Google Scholar]
- Hentschel C. C., Birnstiel M. L. The organization and expression of histone gene families. Cell. 1981 Aug;25(2):301–313. doi: 10.1016/0092-8674(81)90048-9. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Krieg P. A., Robins A. J., D'Andrea R., Wells J. R. The chicken H5 gene is unlinked to core and H1 histone genes. Nucleic Acids Res. 1983 Feb 11;11(3):619–627. doi: 10.1093/nar/11.3.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- McKnight S. L., Kingsbury R. Transcriptional control signals of a eukaryotic protein-coding gene. Science. 1982 Jul 23;217(4557):316–324. doi: 10.1126/science.6283634. [DOI] [PubMed] [Google Scholar]
- Molgaard H. V., Perucho M., Ruiz-Carrillo A. Histone H5 messenger RNA is polyadenylated. Nature. 1980 Jan 31;283(5746):502–504. doi: 10.1038/283502a0. [DOI] [PubMed] [Google Scholar]
- Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
- Reddy V. B., Ghosh P. K., Lebowitz P., Piatak M., Weissman S. M. Simian virus 40 early mRNA's. I. Genomic localization of 3' and 5' termini and two major splices in mRNA from transformed and lytically infected cells. J Virol. 1979 Apr;30(1):279–296. doi: 10.1128/jvi.30.1.279-296.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robbins E., Borun T. W. The cytoplasmic synthesis of histones in hela cells and its temporal relationship to DNA replication. Proc Natl Acad Sci U S A. 1967 Feb;57(2):409–416. doi: 10.1073/pnas.57.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruiz-Carrillo A., Affolter M., Renaud J. Genomic organization of the genes coding for the six main histones of the chicken: complete sequence of the H5 gene. J Mol Biol. 1983 Nov 15;170(4):843–859. doi: 10.1016/s0022-2836(83)80191-0. [DOI] [PubMed] [Google Scholar]
- Sittman D. B., Chiu I. M., Pan C. J., Cohn R. H., Kedes L. H., Marzluff W. F. Isolation of two clusters of mouse histone genes. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4078–4082. doi: 10.1073/pnas.78.7.4078. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Smith D. R., Calvo J. M. Nucleotide sequence of the E coli gene coding for dihydrofolate reductase. Nucleic Acids Res. 1980 May 24;8(10):2255–2274. doi: 10.1093/nar/8.10.2255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spalding J., Kajiwara K., Mueller G. C. The metabolism of basic proteins in HeLa cell nuclei. Proc Natl Acad Sci U S A. 1966 Nov;56(5):1535–1542. doi: 10.1073/pnas.56.5.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugarman B. J., Dodgson J. B., Engel J. D. Genomic organization, DNA sequence, and expression of chicken embryonic histone genes. J Biol Chem. 1983 Jul 25;258(14):9005–9016. [PubMed] [Google Scholar]
- Tsai Y. H., Hnilica L. S. Tissue-specific histones in the erythrocytes of chicken and turtle. Exp Cell Res. 1975 Mar 1;91(1):107–112. doi: 10.1016/0014-4827(75)90147-0. [DOI] [PubMed] [Google Scholar]
- Twigg A. J., Sherratt D. Trans-complementable copy-number mutants of plasmid ColE1. Nature. 1980 Jan 10;283(5743):216–218. doi: 10.1038/283216a0. [DOI] [PubMed] [Google Scholar]
- Urban M. K., Franklin S. G., Zweidler A. Isolation and characterization of the histone variants in chicken erythrocytes. Biochemistry. 1979 Sep 4;18(18):3952–3960. doi: 10.1021/bi00585a017. [DOI] [PubMed] [Google Scholar]
- Urban M. K., Zweidler A. Changes in nucleosomal core histone variants during chicken development and maturation. Dev Biol. 1983 Feb;95(2):421–428. doi: 10.1016/0012-1606(83)90043-x. [DOI] [PubMed] [Google Scholar]
- Woudt L. P., Pastink A., Kempers-Veenstra A. E., Jansen A. E., Mager W. H., Planta R. J. The genes coding for histone H3 and H4 in Neurospora crassa are unique and contain intervening sequences. Nucleic Acids Res. 1983 Aug 25;11(16):5347–5360. doi: 10.1093/nar/11.16.5347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wu R. S., Bonner W. M. Separation of basal histone synthesis from S-phase histone synthesis in dividing cells. Cell. 1981 Dec;27(2 Pt 1):321–330. doi: 10.1016/0092-8674(81)90415-3. [DOI] [PubMed] [Google Scholar]
- Wu R. S., Tsai S., Bonner W. M. Patterns of histone variant synthesis can distinguish G0 from G1 cells. Cell. 1982 Dec;31(2 Pt 1):367–374. doi: 10.1016/0092-8674(82)90130-1. [DOI] [PubMed] [Google Scholar]
- Zinn K., DiMaio D., Maniatis T. Identification of two distinct regulatory regions adjacent to the human beta-interferon gene. Cell. 1983 Oct;34(3):865–879. doi: 10.1016/0092-8674(83)90544-5. [DOI] [PubMed] [Google Scholar]