Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1975 Aug;2(8):1275–1289. doi: 10.1093/nar/2.8.1275

A model for chromatin structure.

H J Li
PMCID: PMC344381  PMID: 1101222

Abstract

A model for chromatin structure is presented. (a) Each of four histone species, H2A (IIbl or f2a2), H2B (IIb2 or f2b), H3 (III or f3) and H4 (IV or f2al) can form a parallel dimer. (b) These dimers can form two tetramers, (H2A)2(H2b)2 and (H3)2(H4)2. (C) These two tetramers bind a segment of DNA and condense it into a "C" segments. (d) The adjacent segments, termed extended or "E" segments, are bound by histone H1 (I or fl) for the major fraction of chromatin; the other "E" regions can be either bound by non-histone proteins or free of protein binding. (e) The binding of histones causes a structural distortion of the DNA which, depending upon the external conditions, may generate the formation of either an open structure with a heterogeneous and non-uniform supercoil or a compact structure with a string of beads. The model is supported by experimental data on histone-histone interaction, histone-DNA interaction and histone subunit-DNA interaction.

Full text

PDF
1275

Selected References

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

  1. Ansevin A. T., Brown B. W. Specificity in the association of histones with deoxyribonucleic acid. Evidence from derivative thermal denaturation profiles. Biochemistry. 1971 Mar 30;10(7):1133–1142. doi: 10.1021/bi00783a006. [DOI] [PubMed] [Google Scholar]
  2. Ansevin A. T., Hnilica L. S., Spelsberg T. C., Kehm S. L. Structure studies on chromatin and nucleohistones. Thermal denaturation profiles recorded in the presence of urea. Biochemistry. 1971 Dec 7;10(25):4793–4803. doi: 10.1021/bi00801a030. [DOI] [PubMed] [Google Scholar]
  3. Baldwin J. P., Boseley P. G., Bradbury E. M., Ibel K. The subunit structure of the eukaryotic chromosome. Nature. 1975 Jan 24;253(5489):245–249. doi: 10.1038/253245a0. [DOI] [PubMed] [Google Scholar]
  4. Bartley J., Chalkley R. An approach to the structure of native nucleohistone. Biochemistry. 1973 Jan 30;12(3):468–474. doi: 10.1021/bi00727a017. [DOI] [PubMed] [Google Scholar]
  5. Bonner J., Dahmus M. E., Fambrough D., Huang R. C., Marushige K., Tuan D. Y. The Biology of Isolated Chromatin: Chromosomes, biologically active in the test tube, provide a powerful tool for the study of gene action. Science. 1968 Jan 5;159(3810):47–56. doi: 10.1126/science.159.3810.47. [DOI] [PubMed] [Google Scholar]
  6. Boublík M., Bradbury E. M., Crane-Robinson C. An investigation of the conformational changes in histones F1 and F2a1 by proton magnetic resonance spectroscopy. Eur J Biochem. 1970 Jul;14(3):486–497. doi: 10.1111/j.1432-1033.1970.tb00315.x. [DOI] [PubMed] [Google Scholar]
  7. Boublík M., Bradbury E. M., Crane-Robinson C., Johns E. W. An investigation of the conformational changes of histone F2b by high resolution nuclear magnetic resonance. Eur J Biochem. 1970 Nov;17(1):151–159. doi: 10.1111/j.1432-1033.1970.tb01147.x. [DOI] [PubMed] [Google Scholar]
  8. CHIH R., HUANG C., BONNER J., MURRAY K. PHYSICAL AND BIOLOGICAL PROPERTIES OF SOLUBLE NUCLEOHISTONES. J Mol Biol. 1964 Jan;8:54–64. doi: 10.1016/s0022-2836(64)80148-0. [DOI] [PubMed] [Google Scholar]
  9. Chang C., Li H. J. Urea perturbation and the reversibility of nucleohistone conformation. Nucleic Acids Res. 1974 Aug;1(8):945–958. doi: 10.1093/nar/1.8.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Clark R. J., Felsenfeld G. Structure of chromatin. Nat New Biol. 1971 Jan 27;229(4):101–106. doi: 10.1038/newbio229101a0. [DOI] [PubMed] [Google Scholar]
  11. Crick F. General model for the chromosomes of higher organisms. Nature. 1971 Nov 5;234(5323):25–27. doi: 10.1038/234025a0. [DOI] [PubMed] [Google Scholar]
  12. D'Anna J. A., Jr, Isenberg I. A complex of histones IIb2 and IV. Biochemistry. 1973 Mar 13;12(6):1035–1043. doi: 10.1021/bi00730a003. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. D'Anna J. A., Jr, Isenberg I. Conformational changes of histone ARE(F3, III). Biochemistry. 1974 Nov 19;13(24):4987–4992. doi: 10.1021/bi00721a018. [DOI] [PubMed] [Google Scholar]
  15. D'Anna J. A., Jr, Isenberg I. Conformational changes of histone LAK (f2a2). Biochemistry. 1974 May 7;13(10):2093–2098. doi: 10.1021/bi00707a015. [DOI] [PubMed] [Google Scholar]
  16. D'Anna J. A., Jr, Isenberg I. Fluorescence anisotropy and circular dichroism study of conformational changes in histone IIb2. Biochemistry. 1972 Oct 24;11(22):4017–4025. doi: 10.1021/bi00772a002. [DOI] [PubMed] [Google Scholar]
  17. D'Anna J. A., Jr, Isenberg I. Interaction of renatured histones f3 and f2al. Biochem Biophys Res Commun. 1974 Nov 6;61(1):343–347. doi: 10.1016/0006-291x(74)90572-5. [DOI] [PubMed] [Google Scholar]
  18. D'Anna J. A., Jr, Isenberg I. Interactions of histone LAK (f2a2) with histones KAS (f2b) and GRK (f2a1). Biochemistry. 1974 May 7;13(10):2098–2104. doi: 10.1021/bi00707a016. [DOI] [PubMed] [Google Scholar]
  19. DeLange R. J., Fambrough D. M., Smith E. L., Bonner J. Calf and pea histone IV. II. The complete amino acid sequence of calf thymus histone IV; presence of epsilon-N-acetyllysine. J Biol Chem. 1969 Jan 25;244(2):319–334. [PubMed] [Google Scholar]
  20. DeLange R. J., Hooper J. A., Smith E. L. Histone 3. 3. Sequence studies on the cyanogen bromide peptides; complete amino acid sequence of calf thymus histone 3. J Biol Chem. 1973 May 10;248(9):3261–3274. [PubMed] [Google Scholar]
  21. Hanlon S., Johnson R. S., Chan A. Relationship between protein and DNA structure in calf thymus chromatin. I. Compositional aspects. Biochemistry. 1974 Sep 10;13(19):3963–3971. doi: 10.1021/bi00716a023. [DOI] [PubMed] [Google Scholar]
  22. Hjelm R. P., Jr, Huang R. C. The role of histones in the conformation of DNA in chromatin as studied by circular dichroism. Biochemistry. 1974 Dec 17;13(26):5275–5283. doi: 10.1021/bi00723a004. [DOI] [PubMed] [Google Scholar]
  23. Hwan J. C., Leffak I. M., Li H. J., Huang P. C., Mura C. Studies on interaction between histone V (f2c) and deoxyribonucleic acids. Biochemistry. 1975 Apr 8;14(7):1390–1396. doi: 10.1021/bi00678a008. [DOI] [PubMed] [Google Scholar]
  24. Johnson R. S., Chan A., Hanlon S. Mixed conformations of deoxyribonucleic acid in intact chromatin isolated by various preparative methods. Biochemistry. 1972 Nov 7;11(23):4347–4358. doi: 10.1021/bi00773a023. [DOI] [PubMed] [Google Scholar]
  25. Kornberg R. D. Chromatin structure: a repeating unit of histones and DNA. Science. 1974 May 24;184(4139):868–871. doi: 10.1126/science.184.4139.868. [DOI] [PubMed] [Google Scholar]
  26. Kornberg R. D., Thomas J. O. Chromatin structure; oligomers of the histones. Science. 1974 May 24;184(4139):865–868. doi: 10.1126/science.184.4139.865. [DOI] [PubMed] [Google Scholar]
  27. Leffak I. M., Hwan J. C., Li H. J., Shih T. Y. Circular dichroism and thermal denaturation studies of nucleohistone IIb2. Biochemistry. 1974 Mar 12;13(6):1116–1121. doi: 10.1021/bi00703a010. [DOI] [PubMed] [Google Scholar]
  28. Li H. J., Bonner J. Interaction of histone half-molecules with deoxyribonucleic acid. Biochemistry. 1971 Apr 13;10(8):1461–1470. doi: 10.1021/bi00784a030. [DOI] [PubMed] [Google Scholar]
  29. Li H. J., Chang C., Evagelinou Z., Weiskopf M. Circular dichroism of histone-bound regions in chromatin. Biopolymers. 1975 Jan;14(1):211–226. doi: 10.1002/bip.1975.360140115. [DOI] [PubMed] [Google Scholar]
  30. Li H. J., Chang C., Weiskopf M., Brand B., Rotter A. Helix-coil transition in nucleoprotein: renaturation of polylysine-DNA and polylysine-nucleohistone complexes. Biopolymers. 1974 Apr;13(4):649–667. doi: 10.1002/bip.1974.360130402. [DOI] [PubMed] [Google Scholar]
  31. Li H. J., Chang C., Weiskopf M. Helix-coil transition in nucleoprotein-chromatin structure. Biochemistry. 1973 Apr 24;12(9):1763–1772. doi: 10.1021/bi00733a016. [DOI] [PubMed] [Google Scholar]
  32. Li H. J., Isenberg I. The effect of urea on salt-induced changes in histone IV. Biochim Biophys Acta. 1972 Dec 28;285(2):467–472. doi: 10.1016/0005-2795(72)90334-0. [DOI] [PubMed] [Google Scholar]
  33. Li H. J. Thermal denaturation of nucleohistones--effects of formaldehyde reaction. Biopolymers. 1972;11(4):835–847. doi: 10.1002/bip.1972.360110408. [DOI] [PubMed] [Google Scholar]
  34. Li H. J., Wickett R., Craig A. M., Isenberg I. Conformational changes in histone IV. Biopolymers. 1972 Feb;11(2):375–397. doi: 10.1002/bip.1972.360110206. [DOI] [PubMed] [Google Scholar]
  35. Martinson H. G., McCarthy B. J. Histone-histone associations within chromatin. Cross-linking studies using tetranitromethane. Biochemistry. 1975 Mar 11;14(5):1073–1078. doi: 10.1021/bi00676a030. [DOI] [PubMed] [Google Scholar]
  36. Mirzabekov A. D., Melnikova A. F. Localization of chromatin proteins within DNA grooves by methylation of chromatin with dimethyl sulphate. Mol Biol Rep. 1974 Sep;1(7):379–384. doi: 10.1007/BF00385669. [DOI] [PubMed] [Google Scholar]
  37. Ogawa Y., Quagliarotti G., Jordan J., Taylor C. W., Starbuck W. C., Busch H. Structural analysis of the glycine-rich, arginine-rich histone. 3. Sequence of the amino-terminal half of the molecule containing the modified lysine residues and the total sequence. J Biol Chem. 1969 Aug 25;244(16):4387–4392. [PubMed] [Google Scholar]
  38. Ohlenbusch H. H., Olivera B. M., Tuan D., Davidson N. Selective dissociation of histones from calf thymus nucleoprotein. J Mol Biol. 1967 Apr 28;25(2):299–315. doi: 10.1016/0022-2836(67)90143-x. [DOI] [PubMed] [Google Scholar]
  39. Olins A. L., Olins D. E. Spheroid chromatin units (v bodies). Science. 1974 Jan 25;183(4122):330–332. doi: 10.1126/science.183.4122.330. [DOI] [PubMed] [Google Scholar]
  40. Pardon J. F., Wilkins M. H., Richards B. M. Super-helical model for nucleohistone. Nature. 1967 Jul 29;215(5100):508–509. doi: 10.1038/215508a0. [DOI] [PubMed] [Google Scholar]
  41. Paul J. General theory of chromosome structure and gene activation in eukaryotes. Nature. 1972 Aug 25;238(5365):444–446. doi: 10.1038/238444a0. [DOI] [PubMed] [Google Scholar]
  42. Pekary A. E., Chan S. I., Hsu C. J., Wagner T. E. Nuclear magnetic resonance studies on the solution conformation of histone IV fragments obtained by cyanogen bromide cleavage. Biochemistry. 1975 Mar 25;14(6):1184–1189. doi: 10.1021/bi00677a013. [DOI] [PubMed] [Google Scholar]
  43. Pekary A. E., Li H. J., Chan S. I., Hsu C. J., Wagner T. E. Nuclear magnetic resonance studies of histone IV solution conformation. Biochemistry. 1975 Mar 25;14(6):1177–1184. doi: 10.1021/bi00677a012. [DOI] [PubMed] [Google Scholar]
  44. Permogorov V. I., Debabov V. G., Sladkova I. A., Rebentish B. A. Structure of DNA and histones in the nucleohistone. Biochim Biophys Acta. 1970 Feb 18;199(2):556–558. doi: 10.1016/0005-2787(70)90107-3. [DOI] [PubMed] [Google Scholar]
  45. Pooley A. S., Pardon J. F., Richards B. M. The relation between the unit thread of chromosomes and isolated nucleohistone. J Mol Biol. 1974 Jan 5;85(4):533–549. doi: 10.1016/0022-2836(74)90314-3. [DOI] [PubMed] [Google Scholar]
  46. Rall S. C., Cole R. D. Amino acid sequence and sequence variability of the amino-terminal regions of lysine-rich histones. J Biol Chem. 1971 Dec 10;246(23):7175–7190. [PubMed] [Google Scholar]
  47. Roark D. E., Geoghegan T. E., Keller G. H. A two-subunit histone complex from calf thymus. Biochem Biophys Res Commun. 1974 Jul 24;59(2):542–547. doi: 10.1016/s0006-291x(74)80014-8. [DOI] [PubMed] [Google Scholar]
  48. Sautiére P., Tyrou D., Laine B., Mizon J., Lambelin-Breynaert M. D., Ruffin P., Biserte G. Structure primaire de l'histone riche en arginine et en lysine du thymus de veau. C R Acad Sci Hebd Seances Acad Sci D. 1972 Feb 28;274(9):1422–1425. [PubMed] [Google Scholar]
  49. Shih T. Y., Fasman G. D. Conformation of deoxyribonucleic acid in chromatin: a circular dichroism study. J Mol Biol. 1970 Aug 28;52(1):125–129. doi: 10.1016/0022-2836(70)90182-8. [DOI] [PubMed] [Google Scholar]
  50. Shih T. Y., Lake R. S. Studies on the structure of metaphase and interphase chromatin of Chinese hamster cells by circular dichroism and thermal denaturation. Biochemistry. 1972 Dec 5;11(25):4811–4817. doi: 10.1021/bi00775a026. [DOI] [PubMed] [Google Scholar]
  51. Simpson R. T. Interaction of a repotter molecule with chromatin. Evidence suggesting that the proteins of chromatin do not occupy the minor groove of deoxyribonucleic acid. Biochemistry. 1970 Nov 24;9(24):4814–4819. doi: 10.1021/bi00826a028. [DOI] [PubMed] [Google Scholar]
  52. Simpson R. T., Sober H. A. Circular dichroism of calf liver nucleohistone. Biochemistry. 1970 Aug 4;9(16):3103–3109. doi: 10.1021/bi00818a001. [DOI] [PubMed] [Google Scholar]
  53. Sperling R., Bustin M. Self assembly of histone F2a1. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4625–4629. doi: 10.1073/pnas.71.11.4625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Tsuboi M., Matsuo K., Ts'o P. O. Interaction of poly-L-lysine and nucleic acids. J Mol Biol. 1966 Jan;15(1):256–267. doi: 10.1016/s0022-2836(66)80225-5. [DOI] [PubMed] [Google Scholar]
  55. Van Holde K. E., Sahasrabuddhe C. G., Shaw B. R. A model for particulate structure in chromatin. Nucleic Acids Res. 1974 Nov;1(11):1579–1586. doi: 10.1093/nar/1.11.1579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Wickett R. R., Li H. J., Isenberg I. Salt effects on histone IV conformation. Biochemistry. 1972 Aug 1;11(16):2952–2957. doi: 10.1021/bi00766a005. [DOI] [PubMed] [Google Scholar]
  57. Wilhelm F. X., de Murcia G. M., Champagne M. H., Daune M. P. Conformational changes of histones and DNA during the thermal denaturation of nucleoprotein. Eur J Biochem. 1974 Jun 15;45(2):431–443. doi: 10.1111/j.1432-1033.1974.tb03567.x. [DOI] [PubMed] [Google Scholar]
  58. Yeoman L. C., Olson M. O., Sugano N., Jordan J. J., Taylor D. W., Starbuck W. C., Busch H. Amino acid sequence of the center of the arginine-lysine-rich histone from calf thymus. The total sequence. J Biol Chem. 1972 Oct 10;247(19):6018–6023. [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES