Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1989 Mar;8(3):797–804. doi: 10.1002/j.1460-2075.1989.tb03440.x

SPKK, a new nucleic acid-binding unit of protein found in histone.

M Suzuki 1
PMCID: PMC400876  PMID: 2470589

Abstract

A new DNA-binding unit of a protein different from the alpha-helix, the beta-sheet and the Zn-finger is proposed based on the analysis of the structure of the N-terminus of sea urchin spermatogenous histone H1. DNA-binding arms of the sea urchin spermatogenous histones, H1 and H2B, are composed of repeats of Ser-Pro-Lys(Arg)-Lys(Arg) (SPKK) residues. A six-times repeat of SPKK (S6 peptide) was isolated from H1 and the competition of S6 for DNA binding with a DNA-binding dye, Hoechst 33258, was analysed. The S6 peptide is shown to be a competitive inhibitor of Hoechst 33258, and it is concluded that the SPKK repeat binds to DNA in its minor groove with a binding constant, KS6 = 1.67 X 10(10) M-1. The circular dichroism (CD) spectrum of a synthetic peptide, SPRKSPRK (S2 peptide), is quite different from those of both the alpha-helix and the beta-sheet and resembles that of a random coil. From statistical consideration of protein structures it is proposed that SPKK forms a compact beta-turn stabilized by an additional hydrogen bond. Since a repeated chain of such turn of SPKK offers a repeat of amides of Ser residues at a distance similar to that of DNA-binding amides of the drugs, Hoechst 33258 and netropsin, and since the amides of these drugs bind to DNA replacing the spine of hydration in a minor groove, it is proposed that a repeat of SPKK binds to DNA in the minor groove using similar hydrogen bonds.

Full text

PDF
797

Images in this article

801Image
on p.801
802Image
on p.802

Selected References

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

  1. Alber T., Sun D. P., Wilson K., Wozniak J. A., Cook S. P., Matthews B. W. Contributions of hydrogen bonds of Thr 157 to the thermodynamic stability of phage T4 lysozyme. Nature. 1987 Nov 5;330(6143):41–46. doi: 10.1038/330041a0. [DOI] [PubMed] [Google Scholar]
  2. Baker E. N., Hubbard R. E. Hydrogen bonding in globular proteins. Prog Biophys Mol Biol. 1984;44(2):97–179. doi: 10.1016/0079-6107(84)90007-5. [DOI] [PubMed] [Google Scholar]
  3. Bontemps J., Houssier C., Fredericq E. Physico-chemical study of the complexes of "33258 Hoechst" with DNA and nucleohistone. Nucleic Acids Res. 1975 Jun;2(6):971–984. doi: 10.1093/nar/2.6.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brayer G. D., McPherson A. Refined structure of the gene 5 DNA binding protein from bacteriophage fd. J Mol Biol. 1983 Sep 15;169(2):565–596. doi: 10.1016/s0022-2836(83)80065-5. [DOI] [PubMed] [Google Scholar]
  5. Burlingame R. W., Love W. E., Wang B. C., Hamlin R., Nguyen H. X., Moudrianakis E. N. Crystallographic structure of the octameric histone core of the nucleosome at a resolution of 3.3 A. Science. 1985 May 3;228(4699):546–553. doi: 10.1126/science.3983639. [DOI] [PubMed] [Google Scholar]
  6. Busslinger M., Barberis A. Synthesis of sperm and late histone cDNAs of the sea urchin with a primer complementary to the conserved 3' terminal palindrome: evidence for tissue-specific and more general histone gene variants. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5676–5680. doi: 10.1073/pnas.82.17.5676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen Y. H., Yang J. T., Martinez H. M. Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion. Biochemistry. 1972 Oct 24;11(22):4120–4131. doi: 10.1021/bi00772a015. [DOI] [PubMed] [Google Scholar]
  8. Chou P. Y., Fasman G. D. Prediction of protein conformation. Biochemistry. 1974 Jan 15;13(2):222–245. doi: 10.1021/bi00699a002. [DOI] [PubMed] [Google Scholar]
  9. FEUGHELMAN M., LANGRIDGE R., SEEDS W. E., STOKES A. R., WILSON H. R., HOOPER C. W., WILKINS M. H., BARCLAY R. K., HAMILTON L. D. Molecular structure of deoxyribose nucleic acid and nucleoprotein. Nature. 1955 May 14;175(4463):834–838. [PubMed] [Google Scholar]
  10. Godowski P. J., Rusconi S., Miesfeld R., Yamamoto K. R. Glucocorticoid receptor mutants that are constitutive activators of transcriptional enhancement. Nature. 1987 Jan 22;325(6102):365–368. doi: 10.1038/325365a0. [DOI] [PubMed] [Google Scholar]
  11. Green S., Chambon P. Oestradiol induction of a glucocorticoid-responsive gene by a chimaeric receptor. Nature. 1987 Jan 1;325(6099):75–78. doi: 10.1038/325075a0. [DOI] [PubMed] [Google Scholar]
  12. Green S., Walter P., Kumar V., Krust A., Bornert J. M., Argos P., Chambon P. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature. 1986 Mar 13;320(6058):134–139. doi: 10.1038/320134a0. [DOI] [PubMed] [Google Scholar]
  13. Hartman P. G., Chapman G. E., Moss T., Bradbury E. M. Studies on the role and mode of operation of the very-lysine-rich histone H1 in eukaryote chromatin. The three structural regions of the histone H1 molecule. Eur J Biochem. 1977 Jul 1;77(1):45–51. doi: 10.1111/j.1432-1033.1977.tb11639.x. [DOI] [PubMed] [Google Scholar]
  14. Hartshorne T. A., Blumberg H., Young E. T. Sequence homology of the yeast regulatory protein ADR1 with Xenopus transcription factor TFIIIA. Nature. 1986 Mar 20;320(6059):283–287. doi: 10.1038/320283a0. [DOI] [PubMed] [Google Scholar]
  15. Klug A., Rhodes D., Smith J., Finch J. T., Thomas J. O. A low resolution structure for the histone core of the nucleosome. Nature. 1980 Oct 9;287(5782):509–516. doi: 10.1038/287509a0. [DOI] [PubMed] [Google Scholar]
  16. Kopka M. L., Fratini A. V., Drew H. R., Dickerson R. E. Ordered water structure around a B-DNA dodecamer. A quantitative study. J Mol Biol. 1983 Jan 5;163(1):129–146. doi: 10.1016/0022-2836(83)90033-5. [DOI] [PubMed] [Google Scholar]
  17. Lai Z. C., Childs G. Isolation and characterization of the gene encoding the testis specific histone protein H2B-2 from the sea urchin Lytechinus pictus. Nucleic Acids Res. 1986 Sep 11;14(17):6845–6856. doi: 10.1093/nar/14.17.6845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Laughon A., Scott M. P. Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins. Nature. 1984 Jul 5;310(5972):25–31. doi: 10.1038/310025a0. [DOI] [PubMed] [Google Scholar]
  19. Lewis P. N., Momany F. A., Scheraga H. A. Chain reversals in proteins. Biochim Biophys Acta. 1973 Apr 20;303(2):211–229. doi: 10.1016/0005-2795(73)90350-4. [DOI] [PubMed] [Google Scholar]
  20. McGhee J. D., Nickol J. M., Felsenfeld G., Rau D. C. Higher order structure of chromatin: orientation of nucleosomes within the 30 nm chromatin solenoid is independent of species and spacer length. Cell. 1983 Jul;33(3):831–841. doi: 10.1016/0092-8674(83)90025-9. [DOI] [PubMed] [Google Scholar]
  21. McKay D. B., Steitz T. A. Structure of catabolite gene activator protein at 2.9 A resolution suggests binding to left-handed B-DNA. Nature. 1981 Apr 30;290(5809):744–749. doi: 10.1038/290744a0. [DOI] [PubMed] [Google Scholar]
  22. Miller J., McLachlan A. D., Klug A. Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 1985 Jun;4(6):1609–1614. doi: 10.1002/j.1460-2075.1985.tb03825.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rees D. C., Lewis M., Lipscomb W. N. Refined crystal structure of carboxypeptidase A at 1.54 A resolution. J Mol Biol. 1983 Aug 5;168(2):367–387. doi: 10.1016/s0022-2836(83)80024-2. [DOI] [PubMed] [Google Scholar]
  24. Rhodes D. Structural analysis of a triple complex between the histone octamer, a Xenopus gene for 5S RNA and transcription factor IIIA. EMBO J. 1985 Dec 16;4(13A):3473–3482. doi: 10.1002/j.1460-2075.1985.tb04106.x. [DOI] [PMC free article] [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. Sap J., Muñoz A., Damm K., Goldberg Y., Ghysdael J., Leutz A., Beug H., Vennström B. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature. 1986 Dec 18;324(6098):635–640. doi: 10.1038/324635a0. [DOI] [PubMed] [Google Scholar]
  27. Takeda Y., Ohlendorf D. H., Anderson W. F., Matthews B. W. DNA-binding proteins. Science. 1983 Sep 9;221(4615):1020–1026. doi: 10.1126/science.6308768. [DOI] [PubMed] [Google Scholar]
  28. Tanaka I., Appelt K., Dijk J., White S. W., Wilson K. S. 3-A resolution structure of a protein with histone-like properties in prokaryotes. Nature. 1984 Aug 2;310(5976):376–381. doi: 10.1038/310376a0. [DOI] [PubMed] [Google Scholar]
  29. Tullius T. D., Dombroski B. A., Churchill M. E., Kam L. Hydroxyl radical footprinting: a high-resolution method for mapping protein-DNA contacts. Methods Enzymol. 1987;155:537–558. doi: 10.1016/0076-6879(87)55035-2. [DOI] [PubMed] [Google Scholar]
  30. Zalenskaya I. A., Pospelov V. A., Zalensky A. O., Vorob'ev V. I. Nucleosomal structure of sea urchin and starfish sperm chromatin. Histone H2B is possibly involved in determining the length of linker DNA. Nucleic Acids Res. 1981 Feb 11;9(3):473–487. doi: 10.1093/nar/9.3.473. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES