Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1986 Dec 20;5(13):3531–3537. doi: 10.1002/j.1460-2075.1986.tb04679.x

Selective radiolabelling and identification of a strong nucleosome binding site on the globular domain of histone H5.

J O Thomas, C M Wilson
PMCID: PMC1167390  PMID: 3104028

Abstract

We describe a chemical investigation of the nucleosome binding site(s) on histone H5. Selective radiolabelling by reductive methylation has led to the identification of lysine residues in H5 that are protected by its association with chromatin. The most strongly protected lysine is Lys-85 which occurs in the globular domain, in a region that is highly conserved between H5 and H1, and in H1 variants, and which probably constitutes a strong binding site for DNA where it enters and leaves the nucleosome. Lysines in the amino-terminal and lysine-rich carboxy-terminal tails are only weakly protected against chemical modification, suggesting a different mode of interaction with DNA.

Full text

PDF
3531

Images in this article

3532Fig. 1.
on p.3532
3532Fig. 2.
on p.3532
3532Fig. 3.
on p.3532
3533Fig. 4.
on p.3533
3534Fig. 6.
on p.3534

Selected References

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

  1. Allan J., Hartman P. G., Crane-Robinson C., Aviles F. X. The structure of histone H1 and its location in chromatin. Nature. 1980 Dec 25;288(5792):675–679. doi: 10.1038/288675a0. [DOI] [PubMed] [Google Scholar]
  2. Aviles F. J., Chapman G. E., Kneale G. G., Crane-Robinson C., Bradbury E. M. The conformation of histone H5. Isolation and characterisation of the globular segment. Eur J Biochem. 1978 Aug 1;88(2):363–371. doi: 10.1111/j.1432-1033.1978.tb12457.x. [DOI] [PubMed] [Google Scholar]
  3. Bates D. L., Butler P. J., Pearson E. C., Thomas J. O. Stability of the higher-order structure of chicken-erythrocyte chromatin in solution. Eur J Biochem. 1981 Oct;119(3):469–476. doi: 10.1111/j.1432-1033.1981.tb05631.x. [DOI] [PubMed] [Google Scholar]
  4. Bates D. L., Harrison R. A., Perham R. N. The stoichiometry of polypeptide chains in the pyruvate dehydrogenase multienzyme complex of E. coli determined by a simple novel method. FEBS Lett. 1975 Dec 15;60(2):427–430. doi: 10.1016/0014-5793(75)80764-2. [DOI] [PubMed] [Google Scholar]
  5. Belyavsky A. V., Bavykin S. G., Goguadze E. G., Mirzabekov A. D. Primary organization of nucleosomes containing all five histones and DNA 175 and 165 base-pairs long. J Mol Biol. 1980 May 25;139(3):519–536. doi: 10.1016/0022-2836(80)90144-8. [DOI] [PubMed] [Google Scholar]
  6. Briand G., Kmiecik D., Sautiere P., Wouters D., Borie-Loy O., Biserte G., Mazen A., Champagne M. Chicken erythrocyte histone H5. IV. Sequence of the carboxy-termined half of the molecule (96 residues) and complete sequence. FEBS Lett. 1980 Apr 7;112(2):147–151. doi: 10.1016/0014-5793(80)80167-0. [DOI] [PubMed] [Google Scholar]
  7. Camerini-Otero R. D., Sollner-Webb B., Felsenfeld G. The organization of histones and DNA in chromatin: evidence for an arginine-rich histone kernel. Cell. 1976 Jul;8(3):333–347. doi: 10.1016/0092-8674(76)90145-8. [DOI] [PubMed] [Google Scholar]
  8. Cary P. D., Hines M. L., Bradbury E. M., Smith B. J., Johns E. W. Conformation studies of histone H1(0) in comparison with histones H1 and H5. Eur J Biochem. 1981 Nov;120(2):371–377. doi: 10.1111/j.1432-1033.1981.tb05714.x. [DOI] [PubMed] [Google Scholar]
  9. Clark D. J., Thomas J. O. Salt-dependent co-operative interaction of histone H1 with linear DNA. J Mol Biol. 1986 Feb 20;187(4):569–580. doi: 10.1016/0022-2836(86)90335-9. [DOI] [PubMed] [Google Scholar]
  10. Cole K. D., York R. G., Kistler W. S. The amino acid sequence of boar H1t, a testis-specific H1 histone variant. J Biol Chem. 1984 Nov 25;259(22):13695–13702. [PubMed] [Google Scholar]
  11. Doenecke D., Tönjes R. Differential distribution of lysine and arginine residues in the closely related histones H1 and H5. Analysis of a human H1 gene. J Mol Biol. 1986 Feb 5;187(3):461–464. doi: 10.1016/0022-2836(86)90446-8. [DOI] [PubMed] [Google Scholar]
  12. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  13. Ichimura S., Mita K., Zama M. Essential role of arginine residues in the folding of deoxyribonucleic acid into nucleosome cores. Biochemistry. 1982 Oct 12;21(21):5329–5334. doi: 10.1021/bi00264a032. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Kmiecik D., Sellos D., Belaïche D., Sautiere P. Primary structure of the two variants of a sperm-specific histone H1 from the annelid Platynereis dumerilii. Eur J Biochem. 1985 Jul 15;150(2):359–370. doi: 10.1111/j.1432-1033.1985.tb09028.x. [DOI] [PubMed] [Google Scholar]
  16. Kumar N. M., Walker I. O. The binding of histones H1 and H5 to chromatin in chicken erythrocyte nuclei. Nucleic Acids Res. 1980 Aug 25;8(16):3535–3551. doi: 10.1093/nar/8.16.3535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lambert S. F., Thomas J. O. Lysine-containing DNA-binding regions on the surface of the histone octamer in the nucleosome core particle. Eur J Biochem. 1986 Oct 1;160(1):191–201. doi: 10.1111/j.1432-1033.1986.tb09957.x. [DOI] [PubMed] [Google Scholar]
  18. Laskey R. A., Mills A. D. Enhanced autoradiographic detection of 32P and 125I using intensifying screens and hypersensitized film. FEBS Lett. 1977 Oct 15;82(2):314–316. doi: 10.1016/0014-5793(77)80609-1. [DOI] [PubMed] [Google Scholar]
  19. Levy S., Sures I., Kedes L. The nucleotide and amino acid coding sequence of a gene for H1 histone that interacts with euchromatin. The early embryonic H1 gene of the sea urchin Strongylocentrotus purpuratus. J Biol Chem. 1982 Aug 25;257(16):9438–9443. [PubMed] [Google Scholar]
  20. Macleod A. R., Wong N. C., Dixon G. H. The amino-acid sequence of trout-testis histone H1. Eur J Biochem. 1977 Aug 15;78(1):281–291. doi: 10.1111/j.1432-1033.1977.tb11739.x. [DOI] [PubMed] [Google Scholar]
  21. Manning G. S. The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Q Rev Biophys. 1978 May;11(2):179–246. doi: 10.1017/s0033583500002031. [DOI] [PubMed] [Google Scholar]
  22. Pabo C. O., Sauer R. T. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. doi: 10.1146/annurev.bi.53.070184.001453. [DOI] [PubMed] [Google Scholar]
  23. Prunell A., Kornberg R. D. Relation of nucleosomes to DNA sequences. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 1):103–108. doi: 10.1101/sqb.1978.042.01.011. [DOI] [PubMed] [Google Scholar]
  24. Renz M., Day L. A. Transition from noncooperative to cooperative and selective binding of histone H1 to DNA. Biochemistry. 1976 Jul 27;15(15):3220–3228. doi: 10.1021/bi00660a010. [DOI] [PubMed] [Google Scholar]
  25. Richmond T. J., Finch J. T., Rushton B., Rhodes D., Klug A. Structure of the nucleosome core particle at 7 A resolution. Nature. 1984 Oct 11;311(5986):532–537. doi: 10.1038/311532a0. [DOI] [PubMed] [Google Scholar]
  26. Seely J. H., Benoiton N. L. Effect of N-methylation and chain length on kinetic constants of trypsin substrates. Epsilon-N-methyllysine and homolysine derivatives as substrates. Can J Biochem. 1970 Oct;48(10):1122–1131. doi: 10.1139/o70-176. [DOI] [PubMed] [Google Scholar]
  27. Simpson R. T. Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. Biochemistry. 1978 Dec 12;17(25):5524–5531. doi: 10.1021/bi00618a030. [DOI] [PubMed] [Google Scholar]
  28. Strickland W. N., Strickland M., Brandt W. F., Von Holt C., Lehmann A., Wittmann-Liebold B. The primary structure of histone H1 from sperm of the sea urchin Parechinus angulosus. 2. Sequence of the C-terminal CNBr peptide and the entire primary structure. Eur J Biochem. 1980 Mar;104(2):567–578. doi: 10.1111/j.1432-1033.1980.tb04460.x. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Thoma F., Koller T., Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol. 1979 Nov;83(2 Pt 1):403–427. doi: 10.1083/jcb.83.2.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Thoma F., Losa R., Koller T. Involvement of the domains of histones H1 and H5 in the structural organization of soluble chromatin. J Mol Biol. 1983 Jul 5;167(3):619–640. doi: 10.1016/s0022-2836(83)80102-8. [DOI] [PubMed] [Google Scholar]
  32. Thomas J. O., Khabaza A. J. Cross-linking of histone H1 in chromatin. Eur J Biochem. 1980 Dec;112(3):501–511. doi: 10.1111/j.1432-1033.1980.tb06113.x. [DOI] [PubMed] [Google Scholar]
  33. Thomas J. O., Kornberg R. D. The study of histone--histone associations by chemical cross-linking. Methods Cell Biol. 1978;18:429–440. [PubMed] [Google Scholar]
  34. Thomas J. O., Rees C. Exchange of histones H1 and H5 between chromatin fragments. A preference of H5 for higher-order structures. Eur J Biochem. 1983 Jul 15;134(1):109–115. doi: 10.1111/j.1432-1033.1983.tb07538.x. [DOI] [PubMed] [Google Scholar]
  35. Turner P. C., Aldridge T. C., Woodland H. R., Old R. W. Nucleotide sequences of H1 histone genes from Xenopus laevis. A recently diverged pair of H1 genes and an unusual H1 pseudogene. Nucleic Acids Res. 1983 Jun 25;11(12):4093–4107. doi: 10.1093/nar/11.12.4093. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES