Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Nov 21;92(24):11170–11174. doi: 10.1073/pnas.92.24.11170

The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization.

G Arents 1, E N Moudrianakis 1
PMCID: PMC40593  PMID: 7479959

Abstract

The histones of all eukaryotes show only a low degree of primary structure homology, but our earlier crystallographic results defined a three-dimensional structural motif, the histone fold, common to all core histones. We now examine the specific architectural patterns within the fold and analyze the nature of the amino acid residues within its functional segments. The histone fold emerges as a fundamental protein dimerization motif while the differentiations of the tips of the histone dimers appear to provide the rules of core octamer assembly and the basis for nucleosome regulation. We present evidence for the occurrence of the fold from archaebacteria to mammals and propose the use of this structural motif to define a distinct family of proteins, the histone fold superfamily. It appears that evolution has conserved the conformation of the fold even through variations in primary structure and among proteins with various functional roles.

Full text

PDF
11170

Images in this article

11171Fig. 2
on p.11171
11172Fig. 3
on p.11172
11173Fig. 4
on p.11173
11173Fig. 5
on p.11173

Selected References

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

  1. Arents G., Burlingame R. W., Wang B. C., Love W. E., Moudrianakis E. N. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148–10152. doi: 10.1073/pnas.88.22.10148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arents G., Moudrianakis E. N. Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10489–10493. doi: 10.1073/pnas.90.22.10489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baxevanis A. D., Arents G., Moudrianakis E. N., Landsman D. A variety of DNA-binding and multimeric proteins contain the histone fold motif. Nucleic Acids Res. 1995 Jul 25;23(14):2685–2691. doi: 10.1093/nar/23.14.2685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baxevanis A. D., Godfrey J. E., Moudrianakis E. N. Associative behavior of the histone (H3-H4)2 tetramer: dependence on ionic environment. Biochemistry. 1991 Sep 10;30(36):8817–8823. doi: 10.1021/bi00100a013. [DOI] [PubMed] [Google Scholar]
  5. Bernstein F. C., Koetzle T. F., Williams G. J., Meyer E. F., Jr, Brice M. D., Rodgers J. R., Kennard O., Shimanouchi T., Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structures. J Mol Biol. 1977 May 25;112(3):535–542. doi: 10.1016/s0022-2836(77)80200-3. [DOI] [PubMed] [Google Scholar]
  6. Chothia C., Lesk A. M. The relation between the divergence of sequence and structure in proteins. EMBO J. 1986 Apr;5(4):823–826. doi: 10.1002/j.1460-2075.1986.tb04288.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. D'Anna J. A., Jr, Isenberg I. A histone cross-complexing pattern. Biochemistry. 1974 Nov 19;13(24):4992–4997. doi: 10.1021/bi00721a019. [DOI] [PubMed] [Google Scholar]
  8. Eickbush T. H., Moudrianakis E. N. The compaction of DNA helices into either continuous supercoils or folded-fiber rods and toroids. Cell. 1978 Feb;13(2):295–306. doi: 10.1016/0092-8674(78)90198-8. [DOI] [PubMed] [Google Scholar]
  9. Eickbush T. H., Moudrianakis E. N. The histone core complex: an octamer assembled by two sets of protein-protein interactions. Biochemistry. 1978 Nov 14;17(23):4955–4964. doi: 10.1021/bi00616a016. [DOI] [PubMed] [Google Scholar]
  10. Eisenberg D., McLachlan A. D. Solvation energy in protein folding and binding. Nature. 1986 Jan 16;319(6050):199–203. doi: 10.1038/319199a0. [DOI] [PubMed] [Google Scholar]
  11. Hosford D. A., Clark S., Cao Z., Wilson W. A., Jr, Lin F. H., Morrisett R. A., Huin A. The role of GABAB receptor activation in absence seizures of lethargic (lh/lh) mice. Science. 1992 Jul 17;257(5068):398–401. doi: 10.1126/science.1321503. [DOI] [PubMed] [Google Scholar]
  12. Kokubo T., Gong D. W., Wootton J. C., Horikoshi M., Roeder R. G., Nakatani Y. Molecular cloning of Drosophila TFIID subunits. Nature. 1994 Feb 3;367(6462):484–487. doi: 10.1038/367484a0. [DOI] [PubMed] [Google Scholar]
  13. Musgrave D. R., Sandman K. M., Reeve J. N. DNA binding by the archaeal histone HMf results in positive supercoiling. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10397–10401. doi: 10.1073/pnas.88.23.10397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Palmer D. K., O'Day K., Trong H. L., Charbonneau H., Margolis R. L. Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3734–3738. doi: 10.1073/pnas.88.9.3734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ramakrishnan V., Finch J. T., Graziano V., Lee P. L., Sweet R. M. Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature. 1993 Mar 18;362(6417):219–223. doi: 10.1038/362219a0. [DOI] [PubMed] [Google Scholar]
  16. Sperling R., Bustin M. Dynamic equilibrium in histone assembly: self-assembly of single histones and histone pairs. Biochemistry. 1975 Jul 29;14(15):3322–3331. doi: 10.1021/bi00686a006. [DOI] [PubMed] [Google Scholar]
  17. Sullivan K. F., Hechenberger M., Masri K. Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol. 1994 Nov;127(3):581–592. doi: 10.1083/jcb.127.3.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Tabassum R., Sandman K. M., Reeve J. N. HMt, a histone-related protein from Methanobacterium thermoautotrophicum delta H. J Bacteriol. 1992 Dec;174(24):7890–7895. doi: 10.1128/jb.174.24.7890-7895.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES