Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1988 Feb 15;250(1):233–240. doi: 10.1042/bj2500233

Histone acetylation in chicken erythrocytes. Rates of acetylation and evidence that histones in both active and potentially active chromatin are rapidly modified.

D E Zhang 1, D A Nelson 1
PMCID: PMC1148838  PMID: 2451508

Abstract

Of the modifiable histone lysine sites, 2-4% participate in dynamic acetylation in chicken erythrocytes, suggesting the involvement of no more than 1-2% of the total genome. The rates and chromatin locality of this dynamic acetylation were studied in both chicken mature and immature red blood cells. In mature erythrocytes, two rates of acetylation of radiolabelled, monoacetylated H4 are observed, with half-lives of approximately 12 and approximately 300 min. In contrast, only one rate with a half-life (t1/2) of 12 min is observed in immature cells, and further experiments rule out the possibility of a slow rate of acetylation (with a t1/2 of approximately 300 min) for any form of H4 in this cell type. The simplest interpretation of these quantitative results, taken together with the behaviour of H3, H2B and H4 observed on the fluorograms used for rate analysis, is that a portion of the rapidly acetylated histone is converted to a more slowly acetylated form during erythrocyte maturation. The transcriptionally active adult beta-globin and H5 nucleohistone, which are presumably converted to potentially active chromatin during the maturation process, remain of the rapidly acetylated form in the mature cell.

Full text

PDF
233

Images in this article

235Fig. 1.
on p.235
236Fig. 4.
on p.236
238Fig. 7.
on p.238

Selected References

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

  1. ALLFREY V. G., FAULKNER R., MIRSKY A. E. ACETYLATION AND METHYLATION OF HISTONES AND THEIR POSSIBLE ROLE IN THE REGULATION OF RNA SYNTHESIS. Proc Natl Acad Sci U S A. 1964 May;51:786–794. doi: 10.1073/pnas.51.5.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Affolter M., Ruiz-Carrillo A. Transcription unit of the chicken histone H5 gene and mapping of H5 pre-mRNA sequences. J Biol Chem. 1986 Sep 5;261(25):11496–11502. [PubMed] [Google Scholar]
  3. Appels R., Wells J. R. Synthesis and turnover of DNA-bound histone during maturation of avian red blood cells. J Mol Biol. 1972 Oct 14;70(3):425–434. doi: 10.1016/0022-2836(72)90550-5. [DOI] [PubMed] [Google Scholar]
  4. Belikoff E., Wong L. J., Alberts B. M. Extensive purification of histone acetylase A, the major histone N-acetyl transferase activity detected in mammalian cell nuclei. J Biol Chem. 1980 Dec 10;255(23):11448–11453. [PubMed] [Google Scholar]
  5. Brotherton T. W., Covault J., Shires A., Chalkley R. Only a small fraction of avian erythrocyte histone is involved in ongoing acetylation. Nucleic Acids Res. 1981 Oct 10;9(19):5061–5073. doi: 10.1093/nar/9.19.5061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Covault J., Chalkley R. The identification of distinct populations of acetylated histone. J Biol Chem. 1980 Oct 10;255(19):9110–9116. [PubMed] [Google Scholar]
  7. Doenecke D., Gallwitz D. Acetylation of histones in nucleosomes. Mol Cell Biochem. 1982 Apr 30;44(2):113–128. doi: 10.1007/BF00226895. [DOI] [PubMed] [Google Scholar]
  8. Ferenz C. R., Nelson D. A. N-Butyrate incubation of immature chicken erythrocytes preferentially enhances the solubility of beta A chromatin. Nucleic Acids Res. 1985 Mar 25;13(6):1977–1995. doi: 10.1093/nar/13.6.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Garcea R. L., Alberts B. M. Comparative studies of histone acetylation in nucleosomes, nuclei, and intact cells. Evidence for special factors which modify acetylase action. J Biol Chem. 1980 Dec 10;255(23):11454–11463. [PubMed] [Google Scholar]
  10. Hay C. W., Candido E. P. Histone deacetylase. Association with a nuclease resistant, high molecular weight fraction of HeLa cell chromatin. J Biol Chem. 1983 Mar 25;258(6):3726–3734. [PubMed] [Google Scholar]
  11. Kaneta H., Fujimoto D. A histone deacetylase capable of deacetylating chromatin-bound histone. J Biochem. 1974 Oct;76(4):905–907. [PubMed] [Google Scholar]
  12. 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]
  13. Loidl P., Gröbner P. Biosynthesis and posttranslational acetylation of histones during spherulation of Physarum polycephalum. Nucleic Acids Res. 1986 May 12;14(9):3745–3762. doi: 10.1093/nar/14.9.3745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Louie A. J., Dixon G. H. Synthesis, acetylation, and phosphorylation of histone IV and its binding to DNA during spermatogenesis in trout. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1975–1979. doi: 10.1073/pnas.69.7.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nelson D. A., Ferris R. C., Zhang D. E., Ferenz C. R. The beta-globin domain in immature chicken erythrocytes: enhanced solubility is coincident with histone hyperacetylation. Nucleic Acids Res. 1986 Feb 25;14(4):1667–1682. doi: 10.1093/nar/14.4.1667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nelson D. A. Histone acetylation in baker's yeast. Maintenance of the hyperacetylated configuration in log phase protoplasts. J Biol Chem. 1982 Feb 25;257(4):1565–1568. [PubMed] [Google Scholar]
  17. Nelson D. A., Perry M., Sealy L., Chalkley R. DNAse I preferentially digests chromatin containing hyperacetylated histones. Biochem Biophys Res Commun. 1978 Jun 29;82(4):1346–1353. doi: 10.1016/0006-291x(78)90337-6. [DOI] [PubMed] [Google Scholar]
  18. Nelson D., Covault J., Chalkley R. Segregation of rapidly acetylated histones into a chromatin fraction released from intact nuclei by the action of micrococcal nuclease. Nucleic Acids Res. 1980 Apr 25;8(8):1745–1763. doi: 10.1093/nar/8.8.1745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. PHILLIPS D. M. The presence of acetyl groups of histones. Biochem J. 1963 May;87:258–263. doi: 10.1042/bj0870258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Perry M., Chalkley R. Histone acetylation increases the solubility of chromatin and occurs sequentially over most of the chromatin. A novel model for the biological role of histone acetylation. J Biol Chem. 1982 Jul 10;257(13):7336–7347. [PubMed] [Google Scholar]
  21. Perry M., Chalkley R. The effect of histone hyperacetylation on the nuclease sensitivity and the solubility of chromatin. J Biol Chem. 1981 Apr 10;256(7):3313–3318. [PubMed] [Google Scholar]
  22. Riggs M. G., Whittaker R. G., Neumann J. R., Ingram V. M. n-Butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature. 1977 Aug 4;268(5619):462–464. doi: 10.1038/268462a0. [DOI] [PubMed] [Google Scholar]
  23. Ruiz-Carrillo A., Wangh L. J., Allfrey V. G. Selective synthesis and modification of nuclear proteins during maturation of avian erythroid cells. Arch Biochem Biophys. 1976 May;174(1):273–290. doi: 10.1016/0003-9861(76)90346-5. [DOI] [PubMed] [Google Scholar]
  24. Ruiz-Carrillo A., Wangh L. J., Littau V. C., Allfrey V. G. Changes in histone acetyl content and in nuclear non-histone protein composition of avian erythroid cells at different stages of maturation. J Biol Chem. 1974 Nov 25;249(22):7358–7368. [PubMed] [Google Scholar]
  25. Sanders L. A., Schechter N. M., McCarty K. S. A comparative study of histone acetylation, histone deacetylation, and ribonucleic acid synthesis in avian reticulocytes and erythrocytes. Biochemistry. 1973 Feb 27;12(5):783–791. doi: 10.1021/bi00729a001. [DOI] [PubMed] [Google Scholar]
  26. Simpson R. T. Structure of chromatin containing extensively acetylated H3 and H4. Cell. 1978 Apr;13(4):691–699. doi: 10.1016/0092-8674(78)90219-2. [DOI] [PubMed] [Google Scholar]
  27. Sippel A. E., Land H., Lindenmaier W., Nguyen-Huu M. C., Wurtz T., Timmis K. N., Giesecke K., Schütz G. Cloning of chicken lysozyme structural gene sequences synthesized in vitro. Nucleic Acids Res. 1978 Sep;5(9):3275–3294. doi: 10.1093/nar/5.9.3275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Vidali G., Boffa L. C., Bradbury E. M., Allfrey V. G. Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc Natl Acad Sci U S A. 1978 May;75(5):2239–2243. doi: 10.1073/pnas.75.5.2239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Weintraub H., Groudine M. Chromosomal subunits in active genes have an altered conformation. Science. 1976 Sep 3;193(4256):848–856. doi: 10.1126/science.948749. [DOI] [PubMed] [Google Scholar]
  31. Williams A. F. DNA synthesis in purified populations of avian erythroid cells. J Cell Sci. 1972 Jan;10(1):27–46. doi: 10.1242/jcs.10.1.27. [DOI] [PubMed] [Google Scholar]
  32. Wu R. S., Panusz H. T., Hatch C. L., Bonner W. M. Histones and their modifications. CRC Crit Rev Biochem. 1986;20(2):201–263. doi: 10.3109/10409238609083735. [DOI] [PubMed] [Google Scholar]
  33. Zhang D. E., Nelson D. A. Histone acetylation in chicken erythrocytes. Rates of deacetylation in immature and mature red blood cells. Biochem J. 1988 Feb 15;250(1):241–245. doi: 10.1042/bj2500241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zhang D., Nelson D. A. Histone acetylation in chicken erythrocytes. Estimation of the percentage of sites actively modified. Biochem J. 1986 Dec 15;240(3):857–862. doi: 10.1042/bj2400857. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES