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. 1971 Jul;123(3):465–469. doi: 10.1042/bj1230465

The synthesis and decay of histone fractions and of deoxyribonucleic acid in the developing avian brain

Stephen C Bondy 1
PMCID: PMC1176979  PMID: 5126095

Abstract

1. The turnover of cerebral histones and DNA after injection of [4,5-3H]leucine or [methyl-3-3H]thymidine, respectively, was studied in the developing chick. 2. Chromatin was prepared from chick nuclei that had been purified by centrifugation through 1.9m-sucrose. 3. Nuclear proteins were fractionated into three major histone classes, F1 (lysine-rich), F2(b) (slightly lysine-rich) and [F3+F2(a)] (arginine-rich), and a non-histone protein residue. 4. The proportions of the histone classes remained constant throughout the period of development studied. 5. All histone fractions decayed at a similar rate, initially with a half-life of around 5 days, later with a half-life of 19 days. 6. Non-histone proteins from chromatin decayed in a heterogeneous manner with a wide range of half-lives. 7. Short-term labelling studies showed that all histone fractions were synthesized at the same rate. 8. Some non-histone proteins were very rapidly synthesized relative to histones. 9. DNA had a longer half-life than any histone fraction studied. A biphasic exponential decay curve with half-lives of 23 and 50 days was found. 10. It was concluded that the turnover of histones can occur independently of that of DNA and that different histone classes have similar rates of synthesis and decay.

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Selected References

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

  1. Adams D. H. The relationship between cellular nucleic acids in the developing rat cerebral cortex. Biochem J. 1966 Feb;98(2):636–640. doi: 10.1042/bj0980636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Agrell I. P., Christensson E. G. Changes of histone composition in the developing chick embryo. Nature. 1965 Aug 7;207(997):638–640. doi: 10.1038/207638a0. [DOI] [PubMed] [Google Scholar]
  3. BURTON K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J. 1956 Feb;62(2):315–323. doi: 10.1042/bj0620315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bondy S. C., Roberts S. Developmental and regional variations in ribonucleic acid synthesis on cerebral chromatin. Biochem J. 1969 Nov;115(2):341–349. doi: 10.1042/bj1150341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burdman J. A., Haglid K., Dravid A. R. Protein synthesis in fractions from isolated brain cell nuclei. J Neurochem. 1970 May;17(5):669–676. doi: 10.1111/j.1471-4159.1970.tb00546.x. [DOI] [PubMed] [Google Scholar]
  6. Bustin M., Cole R. D. Species and organ specificity in very lysine-rich histones. J Biol Chem. 1968 Sep 10;243(17):4500–4505. [PubMed] [Google Scholar]
  7. Bustos-Valdes S. E., Deisseroth A., Dounce A. L. Metabolic studies of histones and residual protein of rat liver nuclei. Arch Biochem Biophys. 1968 Sep 10;126(3):848–855. doi: 10.1016/0003-9861(68)90478-5. [DOI] [PubMed] [Google Scholar]
  8. Byvoet P. Metabolic integrity of deoxyribonucleohistones. J Mol Biol. 1966 Jun;17(2):311–318. doi: 10.1016/s0022-2836(66)80143-2. [DOI] [PubMed] [Google Scholar]
  9. DINGMAN C. W., SPORN M. B. STUDIES ON CHROMATIN. I. ISOLATION AND CHARACTERIZATION OF NUCLEAR COMPLEXES OF DEOXYRIBONUCLEIC ACID, RIBONUCLEIC ACID, AND PROTEIN FROM EMBRYONIC AND ADULT TISSUES OF THE CHICKEN. J Biol Chem. 1964 Oct;239:3483–3492. [PubMed] [Google Scholar]
  10. DeLange R. J., Fambrough D. M., Smith E. L., Bonner J. Calf and pea histone IV. 3. Complete amino acid sequence of pea seedling histone IV; comparison with the homologous calf thymus histone. J Biol Chem. 1969 Oct 25;244(20):5669–5679. [PubMed] [Google Scholar]
  11. Dick C., Johns E. W. The biosynthesis of the five main histone fractions of rat thymus. Biochim Biophys Acta. 1969 Jan 21;174(1):380–386. doi: 10.1016/0005-2787(69)90263-9. [DOI] [PubMed] [Google Scholar]
  12. FLAMM W. G., BIRNSTIEL M. L. INHIBITION OF DNA REPLICATION AND ITS EFFECT ON HISTONE SYNTHESIS. Exp Cell Res. 1964 Feb;33:616–619. doi: 10.1016/0014-4827(64)90035-7. [DOI] [PubMed] [Google Scholar]
  13. Gaitonde M. K., Martenson R. E. Metabolism of highly basic proteins of rat brain during postnatal development. J Neurochem. 1970 Apr;17(4):551–563. doi: 10.1111/j.1471-4159.1970.tb00534.x. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Gilmour R. S., Paul J. RNA transcribed from reconstituted nucleoprotein is similar to natural RNA. J Mol Biol. 1969 Feb 28;40(1):137–139. doi: 10.1016/0022-2836(69)90301-5. [DOI] [PubMed] [Google Scholar]
  16. Gurley L. R., Hardin J. M. The metabolism of histone fractions. 3. Synthesis and turnover of histone f1. Arch Biochem Biophys. 1970 Feb;136(2):392–401. doi: 10.1016/0003-9861(70)90210-9. [DOI] [PubMed] [Google Scholar]
  17. Hancock R. Conservation of histones in chromatin during growth and mitosis in vitro. J Mol Biol. 1969 Mar 28;40(3):457–466. doi: 10.1016/0022-2836(69)90165-x. [DOI] [PubMed] [Google Scholar]
  18. JOHNS E. W., PHILLIPS D. M., SIMSON P., BUTLER J. A. Improved fractionations of arginine-rich histones from calf thymus. Biochem J. 1960 Dec;77:631–636. doi: 10.1042/bj0770631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Johns E. W. Studies on histones. 7. Preparative methods for histone fractions from calf thymus. Biochem J. 1964 Jul;92(1):55–59. doi: 10.1042/bj0920055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kinkade J. M., Jr Qualitative species differences and quantitative tissue differences in the distribution of lysine-rich histones. J Biol Chem. 1969 Jun 25;244(12):3375–3386. [PubMed] [Google Scholar]
  21. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  22. MCCARTHY B. J., HOYER B. H. IDENTITY OF DNA AND DIVERSITY OF MESSENGER RNA MOLECULES IN NORMAL MOUSE TISSUES. Proc Natl Acad Sci U S A. 1964 Oct;52:915–922. doi: 10.1073/pnas.52.4.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Margolis F. L. DNA and DNA-polymerase activity in chicken brain regions during ontogeny. J Neurochem. 1969 Mar;16(3):447–456. doi: 10.1111/j.1471-4159.1969.tb10385.x. [DOI] [PubMed] [Google Scholar]
  24. Mori K., Yamagami S., Kawakita Y. Thymidine metabolism and deoxyribonucleic acid synthesis in the developing rat brain. J Neurochem. 1970 Jul;17(7):835–843. doi: 10.1111/j.1471-4159.1970.tb02237.x. [DOI] [PubMed] [Google Scholar]
  25. Murray K., Vidali G., Neelin J. M. The stepwise removal of histones from chicken erythrocyte nucleoprotein. Biochem J. 1968 Mar;107(2):207–215. doi: 10.1042/bj1070207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Murthy L. D., Pradhan D. S., Sreenivasan A. Effects of hydrocortisone upon metabolism of histones in rat liver. Biochim Biophys Acta. 1970 Feb 18;199(2):500–510. doi: 10.1016/0005-2787(70)90092-4. [DOI] [PubMed] [Google Scholar]
  27. Panyim S., Chalkley R. The heterogeneity of histones. I. A quantitative analysis of calf histones in very long polyacrylamide gels. Biochemistry. 1969 Oct;8(10):3972–3979. doi: 10.1021/bi00838a013. [DOI] [PubMed] [Google Scholar]
  28. Paul J., Gilmour R. S. Organ-specific restriction of transcription in mammalian chromatin. J Mol Biol. 1968 Jul 14;34(2):305–316. doi: 10.1016/0022-2836(68)90255-6. [DOI] [PubMed] [Google Scholar]
  29. Piha R. S., Cuénod M., Waelsch H. Metabolism of histones of brain and liver. J Biol Chem. 1966 May 25;241(10):2397–2404. [PubMed] [Google Scholar]
  30. 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]
  31. Sadgopal A., Bonner J. The relationship between histone and DNA synthesis in HeLa cells. Biochim Biophys Acta. 1969 Aug 20;186(2):349–357. doi: 10.1016/0005-2787(69)90013-6. [DOI] [PubMed] [Google Scholar]
  32. Stellwagen R. H., Cole R. D. Histone biosynthesis in the mammary gland during development and lactation. J Biol Chem. 1969 Sep 25;244(18):4878–4887. [PubMed] [Google Scholar]

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