Skip to main content
Log in

The role of histones and their modifications in the informative content of chromatin

  • Reviews
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

It is traditionally accepted that the DNA sequence cannot by itself explain all the mechanisms necessary for the development of living beings, especially in eukaryotes. Indeed part of the information used in these processes is stored in other ways, generally called ‘epigenetic’, whose molecular mechanisms are mostly unknown. The ultimate explanation for them might reside in the non-DNA moiety of chromatin which may play an active role in heredity (‘chromatin information’). Histones are the universal structural component of chromatin. However, recent studies strongly suggest that histones, and their modifications — especially the reversible acetylation of lysines — may act as a recognition signal for regulatory proteins and they may participate, for this reason, in gene regulation. This type of information could be maintained through its replication and, ultimately, it could form the molecular basis of certain processes related to the development of the eukaryotic organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Alberts, B., and Sternglanz, R., Chromatin contract to silence. Nature334 (1990) 193–194.

    Article  Google Scholar 

  2. Allfrey, V. G., Faulkner, R., and Mirsky, A. E., Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis.Proc. natl Acad. Sci. USA 51 (1964) 786–794.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Alonso, W. R., and Nelson, D. A., A novel yeast histone deacetylase: partial characterization and development of an activity assay. Biochim. biophys. Acta866 (1986) 161–169.

    Article  CAS  PubMed  Google Scholar 

  4. Ausió, J., Structure and dynamics of transcriptionally active chromatin. J. Cell Sci.102 (1992) 1–5.

    Article  PubMed  Google Scholar 

  5. Ausió, J., Dong, F., and van Holde, K. E., Use of selectively trypsinized nucleosome core particle to analyze the role of the histone “tails” in the stabilization of the nucleosome. J. molec. Biol.206 (1989) 451–463.

    Article  PubMed  Google Scholar 

  6. Beato, M., Transcriptional control by nuclear receptors. FASEB J.5 (1991) 2044–2051.

    Article  CAS  PubMed  Google Scholar 

  7. Bonne-Andrea, C., Wong, M. L., and Alberts, B. M.,in vitro replication through nucleosomes without histone displacement. Nature343 (1990) 719–726.

    Article  CAS  PubMed  Google Scholar 

  8. Bradbury, E. M., Reversible histone modifications and the chromosome cell cycle. Bioessays14 (1992) 9–16.

    Article  CAS  PubMed  Google Scholar 

  9. Chicoine, L. G., Schulman, I. G., Richman, R., Cook, R. G., and Allis, C. D., Nonrandom utilization of acetylation sites in histones isolated fromTetrahymena. Evidence for functionally distinct H4 acetylation sites. J. biol. Chem.261 (1986) 1071–1076.

    Article  CAS  PubMed  Google Scholar 

  10. Couppez, M., Martin-Ponthieu, A., and Sautière, P., Histone H4 from cuttlefish testis is sequentially acetylated. Comparison with acetylation of calf thymus histone H4. J. biol. Chem.262 (1987) 2854–2860.

    Article  CAS  PubMed  Google Scholar 

  11. Csordas, A., On the biological role of histone acetylation, Biochem. J.265 (1990) 23–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Durrin, L. K., Mann, R. K., Kayne, P. S., and Grunstein, M., Yeast histone H4 N-terminal sequence is required for promoter activationin vivo. Cell65 (1991) 1023–1031.

    Article  CAS  PubMed  Google Scholar 

  13. Eissenberg, J. C., Position effect veriegation inDrosphilia: towards a genetics of chromatin assembly. Bioessays11 (1989) 14–17.

    Article  CAS  PubMed  Google Scholar 

  14. Eissenberg, J. C., and Elgin, S. C. R., Boundary functions in the control of gene expression. Trends Genet.7 (1991) 335–340.

    Article  CAS  PubMed  Google Scholar 

  15. Eissenberg, J. C., James, T. C., Foster-Hartnett, D. M., Hartnett, T., Ngan, V., and Elgin, S. C. R., Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation inDrosophilia melanogaster. Proc. natl Acad. Sci. USA,87 (1990) 9923–9927.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Fairman, M. P., Nucleosome segregation-divided opinions. Bioessays12 (1990) 237–239.

    Article  CAS  PubMed  Google Scholar 

  17. Fascher, K.-D., Schnitz, J., and Hörz, W., Role of trans-activating proteins in the generation of active chromatin at thePHO5 promoter inS. cerevsiae. EMBO J.9 (1990) 2523–2528.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Garcea, R. L., and Alberts, B. M., Comparative studies of histone acetylation in nucleosomes, nuclei, and intact cells. Evidence for special factors which modify acetylase action. J. biol. Chem.255 (1980) 11454–11463.

    Article  CAS  PubMed  Google Scholar 

  19. Gottschling, D. E., Aparicio, O. M., Billington, B. L., and Zakian, V. A., Position effect atS. cerevisiae telomers: reversible repression of pol II transcription. Cell63 (1990) 751–762.

    Article  CAS  PubMed  Google Scholar 

  20. Grunstein, M., Histone function in transcription. A. Rev. Cell Biol.6 (1990) 643–678.

    Article  CAS  Google Scholar 

  21. Grunstein, M., Nucleosomes: regulators of transcription. Trends Genet.6 (1990) 395–400.

    Article  CAS  PubMed  Google Scholar 

  22. Gruss, C., and Sogo, J. M., Chromatin replication. Bioessays14 (1992) 1–8.

    Article  CAS  PubMed  Google Scholar 

  23. Henikoff, S., Position-effect variegation after 60 years. Trends Genet.6 (1990) 422–426.

    Article  CAS  PubMed  Google Scholar 

  24. Isenberg, I., Histones. A. Rev. Biochem.48 (1979) 159–191.

    Article  CAS  Google Scholar 

  25. Johnson, L. M., Kayne, P. S., Kahn, E. S., and Grunstein, M., Genetic evidence for an interaction between SIR3 and histone H4 in the repression of the silent mating loci inSaccharomyces cerevisiae. Proc. natl Acad. Sci. USA87 (1990) 6286–6290.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kayne, P. S., Kim, U.-J., Han, M., Muller, L. R., Yoshizaki, F., and Grunstein, M., Extremely conserved histone H4 N-terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. Cell55 (1988) 27–39.

    Article  CAS  PubMed  Google Scholar 

  27. Kelner, D. N., and McCarty, K. S., Porcine liver nuclear histone acetyltransferase. Partial purification and basic properties. J. biol. Chem.259 (1984) 3413–3419.

    Article  CAS  PubMed  Google Scholar 

  28. Libby, P. R., Rat liver nuclear N-acetyltransferases: separation of two enzymes with both histone and spermidine acetyltransferase activity. Archs Biochem. Biophys.203 (1980) 384–389.

    Article  CAS  Google Scholar 

  29. Libertini, L. J., Ausió, J., van Holde, K. E., and Small, E. W., Histone hyperacetylation. Its effects on nucleosome core particle transitions. Biophys. J.53 (1988) 477–487.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Loidl, P., Towards an understanding of the biological function of histone acetylation. FEBS lett.227 (1988) 91–95.

    Article  CAS  PubMed  Google Scholar 

  31. Loidl, P., and Gröbner, P., Postsynthetic acetylation of histones during the cell cycle: a general function for the displacement of histones during chromatin rearrangements. Nucleic Acids Res.15 (1987) 8351–8366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. López-Rodas, G., Brosch, G., Georgieva, E. I., Sendra, R., Franco, L., and Loidl, P., Histone deacetylase. A key enzyme for the binding of regulatory proteins to chromatin. FEBS lett.317 (1993) 175–180.

    Article  PubMed  Google Scholar 

  33. López-Rodas, G., Tordera, V., Sánchez del Pino, M. M., and Franco, L., Yeast contains multiple forms of histone acetyltransferase. J. biol. Chem.264 (1989) 19028–19033.

    Article  PubMed  Google Scholar 

  34. López-Rodas, G., Tordera, V., Sánchez del Pino, M. M., and Franco, L., Subcellular localization and nucleosome specificity of yeast histone acetyltransferase. Biochemistry30 (1991) 3728–3732.

    Article  PubMed  Google Scholar 

  35. Mann, R. K., and Grunstein, M., Histone H3 N-terminal mutations allow hyperactivation of the yeastGAL1 genein vivo. EMBO J.11 (1992) 3297–3306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Megee, P. C., Morgan, B. A., Mittman, B. A., and Smith, M. M., Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science247 (1990) 841–845.

    Article  CAS  PubMed  Google Scholar 

  37. Mingarro, I., Sendra, R., Salvador, M. L., and Franco, L., Site-specificity of pea histone acetyltransferase Bin vitro. J. biol. Chem.268 (1993) 13248–13252.

    Article  CAS  PubMed  Google Scholar 

  38. Moore, G. D., Sinclair, D. A., and Grigliatti, T. A., Histone gene multiplicity and position effect variegation inDrosophilia melanogaster. Genetics105 (1983) 327–344.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mottus, R., Reeves, R., and Grigliatti, T. A., Butyrate suppression of position-effect variegation inDrosphila melanogaster. Molec gen. Genet.178 (1980) 465–469.

    Article  CAS  PubMed  Google Scholar 

  40. Park, E.-C., and Szostak, J. W., Point mutations in the yeast histone H4 gene prevent silencing of the silent mating type locusHML. Molec. cell. Biol.10 (1990) 4932–4934.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Paro, R., Imprinting a determined state into the chromatin ofDrosophilia. Trends Genet.6 (1990) 416–421.

    Article  CAS  PubMed  Google Scholar 

  42. Pesis, K. H., and Matthews, H. R., Histone acetylation in replication and transcription: turnover at specific acetylation sites in histone H4 fromPhysarum polycephalum. Arch. Biochem. Biophys.251 (1986) 665–673.

    Article  CAS  PubMed  Google Scholar 

  43. Pillus, L., Any which way but loose — determining a transcription state in yeast. Bioessays13 (1991) 303–304.

    Article  Google Scholar 

  44. Reuter, G., Giarre, M., Farah, J., Gausz, J., Spierer, A., and Spierer, P., Dependence of position-effect variegation inDrosophilia on a dose of a gene encoding an unusual zinc-finger protein. Nature344 (1990) 219–223.

    Article  CAS  PubMed  Google Scholar 

  45. Reuter, G., and Spierer, P., Position effect variegation and chromatin proteins. Bioessays14 (1992) 605–612.

    Article  CAS  PubMed  Google Scholar 

  46. Riggs, A. D., and Pfeifer, G. P., X-Chromosome inactivation and cell memory. Trends Genet.8 (1992) 169–174.

    Article  CAS  PubMed  Google Scholar 

  47. Sendra, R., Rodrigo, I., Salvador, M. L., and Franco, L., Characterization of pea histone deacetylases. Plant molec. Biol.11 (1988) 857–866.

    Article  CAS  Google Scholar 

  48. Sendra, R., Salvador, M. L., López-Rodas, G., Tordera, V., and Franco, L., A plant histone acetyltransferase specific for H3 in nucleosomes. Plant Sci.46 (1986) 189–194.

    Article  CAS  Google Scholar 

  49. Solter, D., Differential imprinting and expression of maternal and paternal genomes. A. Rev. Genet.22 (1988) 127–146.

    Article  CAS  Google Scholar 

  50. Sures, I., and Gallwitz, D., Histone-specific acetyltransferases from calf thymus. Isolation, properties and substrate specificity of three different enzymes. Biochemistry19 (1980) 943–951.

    Article  CAS  PubMed  Google Scholar 

  51. Turner, B. M., Histone acetylation and control of gene expression. J. Cell Sci.99 (1991) 13–20.

    Article  CAS  PubMed  Google Scholar 

  52. Turner, B. M., Birley, A. J., and Lavender, J., Histone H4 isomorfs acetylated at specific lysine residues define individual chromosomes and chromatin domains inDrosophila polytene nuclei. Cell69 (1992) 375–384.

    Article  CAS  PubMed  Google Scholar 

  53. van Holde, K. E., Chromatin. Springer-Verlag, New York (1988).

    Google Scholar 

  54. Vidali, G., Boffa, L. C., and Allfrey V. G., Properties of an acidic histone-binding protein fraction from cell nuclei. Selective precipitation and deacetylation of histone f2a1 and f3. J. biol. Chem.247 (1972) 7365–7373.

    Article  CAS  PubMed  Google Scholar 

  55. Wilson, C., Bellen, H. J., and Gehring, W. J., Position effects on eukaryotic gene expression. A. Rev. Cell Biol.6 (1990) 679–714.

    Article  CAS  Google Scholar 

  56. Yamasu, K., and Senshu, T., Conservative segregation of tetrameric units of H3 and H4 histones during nucleosome replication. J. Biochem.107 (1990) 15–20.

    Article  CAS  PubMed  Google Scholar 

  57. Yukioka, M., Sasaki, S., QI, S.-L., and Inoue, A., Two species of histone aceyltransferase of rat liver nuclei. J. biol. Chem.259 (1984) 8372–8377.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tordera, V., Sendra, R. & Pérez-Ortín, J.E. The role of histones and their modifications in the informative content of chromatin. Experientia 49, 780–788 (1993). https://doi.org/10.1007/BF01923548

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01923548

Key words

Navigation