Abstract
Thirty years ago, our conception of chromatin structure underwent a total metamorphosis as the nucleosome era began. In Kurosawa's classic movie 'Rashomon' (1951), each participant had a different perspective of the same pivotal event. This review outlines our perception of history.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
References
Flemming, W. Zellsubstanz, Kern und Zelltheilung (F.C.W. Vogel, Leipzig, 1882).
Paweletz, N. Walther Flemming: pioneer of mitosis research. Nature Rev. Mol. Cell Biol. 2, 72–75 (2001).
Hughes, A. A History of Cytology 100–101 (Abelard–Schuman, London, 1959).
Bradbury, S. Landmarks in biological light microscopy. J. Microsc. 155, 281–305 (1989).
Bracegirdle, B. The development of biological preparative techniques for light microscopy, 1839–1989. J. Microsc. 155, 307–318 (1989).
Luck, J. M. The Nucleohistones 3–11 (Holden–Day, Inc., San Francisco, 1964).
van Holde, K. E. Chromatin (Springer–Verlag, New York, 1989).
Miescher, F. Ueber die chemische Zusammensetzung der Eiterzellen. Hoppe-Seyler, med. chem. Unters. 4, 441–460 (1871).
Kossel, A. Ueber die chemische Beschaffenheit des Zellkerns. Munchen Med. Wochenschrift. 58, 65–69 (1911).
Avery, O., MacLeod, C. & McCarty, M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. J. Exp. Med. 79, 137–158 (1944).
Felix, K. & Harteneck, A. Ueber den Aufbau des Histons der Thymusdruse. Z. Physiol. Chem. 165, 103–120 (1927).
Mazia, D. Enzyme studies of chromosomes. Cold Spring Harb. Symp. Quant. Biol. IX, 40–46 (1941).
Schultz, J. The evidence of the nucleoprotein nature of the gene. Cold Spring Harb. Symp. Quant. Biol. IX, 55–65 (1941).
Pauling, L., Corey, R. B. & Branson, H. R. The structure of proteins: two hydrogen-bonded helical configurations of the polypeptide chain. Proc. Natl Acad. Sci. USA 27, 205–211 (1951).
Watson, J. D. & Crick, F. H. C. Molecular structure of nucleic acids. A structure for deoxyribose nucleic acid. Nature 171, 737–738 (1953).
Wilkins, M. H. F., Stokes, A. R. & Wilson, H. R. Molecular structure of deoxypentose nucleic acids. Nature 171, 738–740 (1953).
Franklin, R. & Gosling, R. G. Molecular configuration in sodium thymonucleate. Nature 171, 740–741 (1953).
Gall, J. G. Kinetics of deoxyribonuclease action on chromosomes. Nature 198, 36–38 (1963).
Johns, E. W. The Histones, Their Interactions with DNA and Some Aspects of Gene Control. 128 (Churchill, London, 1969).
Allfrey, V. G., Faulkner, R. & Mirsky, A. E. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl Acad. Sci. USA 51, 786–794 (1964).
Zubay, G. & Doty, P. The isolation and properties of deoxyribonucleoprotein particles. J. Mol. Biol. 1, 1–20 (1959).
Pardon, J. F., Richards, B. M. & Cotter, R. I. X-ray diffraction studies on oriented nucleohistone gels. Cold Spring Harb. Symp. Quant. Biol. 38, 75–81 (1973).
Everid, A. C., Small, J. V. & Davies, H. G. Electron-microscope observations on the structure of condensed chromatin: evidence for orderly arrays of unit threads on the surface of chicken erythrocyte nuclei. J. Cell Sci. 7, 35–48 (1970).
Swift, H. The organization of genetic material in eukaryotes: progress and prospects. Cold Spring Harb. Symp. Quant. Biol. 38, 963–979 (1974).
Olins, D. E. & Olins, A. L. Physical studies of isolated eucaryotic nuclei. J. Cell Biol. 53, 715–736 (1972).
Clark, R. J. & Felsenfeld, G. Structure of chromatin. Nature New Biol. 229, 101–106 (1971).
Itzhaki, R. F. Studies on the accessibility of deoxyribonucleic acid in deoxyribonucleoprotein to cationic molecules. Biochem. J. 122, 583–592 (1971).
Mirsky, A. E. The structure of chromatin. Proc. Natl Acad. Sci. USA 68, 2945–2948 (1971).
Olins, A. L. & Olins, D. E. Spheroid chromatin units (ν bodies). Science 183, 330–332 (1974).
Olins, A. L. & Olins, D. E. Spheroid chromatin units (ν bodies). J. Cell Biol. 59, A252 (1973).
Woodcock, C. L. F. Ultrastructure of inactive chromatin. J. Cell Biol. 59, A368 (1973).
Woodcock, C. L., Safer, J. P. & Stanchfield, J. E. Structural repeating units in chromatin. I. Evidence for their general occurrence. Exp. Cell Res. 97, 101–110 (1976).
D'Anna, J. A. J. & Isenberg, I. A histone cross-complexing pattern. Biochemistry 13, 4992–4997 (1974).
Roark, D. E., Geoghegan, T. E. & Keller, G. H. A two-subunit histone complex from calf thymus. Biochem. Biophys. Res. Comm. 59, 542–547 (1974).
Sahasrabuddhe, C. G. & Van Holde, K. E. The effect of trypsin on nuclease-resistant chromatin fragments. J. Biol. Chem. 249, 152–156 (1974).
Kornberg, R. Chromatin structure: a repeating unit of histones and DNA. Science 184, 868–871 (1974).
Kornberg, R. D. & Thomas, J. O. Chromatin structure; oligomers of the histones. Science 184, 865–868 (1974).
Hewish, D. R. & Burgoyne, L. A. Chromatin substructure. The digestion of chromatin at regularly spaced sites by a nuclear deoxyribonuclease. Biochem. Biophys. Res. Comm. 52, 504–510 (1973).
Oudet, P., Gross-Bellard, M. & Chambon, P. Electron microscopic and biochemical evidence that chromatin structure is a repeating unit. Cell 4, 281–300 (1975).
Wolffe, A. Chromatin Structure and Function (Academic Press, San Diego, 1998).
Kornberg, R. & Lorch, Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryotic chromosome. Cell 98, 285–294 (1999).
Thomas, G. J., Prescott, B. & Olins, D. E. Secondary structure of histones and DNA in chromatin. Science 197, 385–388 (1977).
Mardian, J. K., Paton, A. E., Bunick, G. J. & Olins, D. E. Nucleosome cores have two specific binding sites for nonhistone chromosomal proteins HMG 14 and HMG 17. Science 209, 1534–1536 (1980).
Sandeen, G., Wood, W. I. & Felsenfeld, G. The interaction of high mobility proteins HMG14 and 17 with nucleosomes. Nucl. Acids Res. 8, 3757–3778 (1980).
Olins, D. E. et al. Electron microscope tomography: transcription in three dimensions. Science 220, 498–500 (1983).
Olins, A. L., Olins, D. E. & Bazett-Jones, D. P. Balbiani ring hnRNP substructure visualized by selective staining and electron spectroscopic imaging. J. Cell Biol. 117, 483–491 (1992).
Olins, D. E. & Olins, A. L. The replication band of ciliated protozoa. Int. Rev. Cytol. 153, 137–170 (1994).
Richmond, T. J., Finch, J. T., Rushton, B., Rhodes, D. & Klug, A. Structure of the nucleosome core particle at 7 Å resolution. Nature 311, 532–537 (1984).
Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251–260 (1997).
Uberbacher, E. C. & Bunick, G. J. X-ray structure of the nucleosome core particle. J. Biomol. Struct. Dyn. 2, 1033–1055 (1985).
Harp, J. M., Hanson, B. L., Tim, D. E. & Bunick, G. J. Asymmetries in the nucleosome core particle at 2.5 Å resolution. Acta Crystallogr. (Section D Biol. Crystallogr.) 56, 1513–1534 (2000).
Harp, J. M., Hanson, B. L. & Bunick, G. J. The Structure of the Nucleosome Core Particle (Elsevier Science B. V., Amsterdam) (in the press).
Arents, G., Burlingame, R. W., Wang, B. C., Love, W. E. & Moudrianakis, E. N. The nucleosomal core histone octamer at 3.1 Å resolution: a tripartite protein assembly and a left-handed superhelix. Proc. Natl Acad. Sci. USA 88, 10148–10152 (1991).
Richmond, T. J. & Davey, C. A. The structure of DNA in the nucleosome core. Nature 423, 145–150 (2003).
Woodcock, C. L. F. & Dimitrov, S. Higher-order structure of chromatin and chromosomes. Curr. Opin. Genet. Dev. 11, 130–135 (2001).
Horn, P. J. & Peterson, C. L. Chromatin higher order folding: wrapping up transcription. Science 297, 1824–1827 (2002).
de la Serna, I. L. & Imbalzano, A. N. Unfolding heterochromatin for replication. Nature Genet. 32, 560–562 (2002).
Turner, B. M. Decoding the nucleosome. Cell 75, 5–8 (1993).
Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074–1080 (2001).
Fry, C. J. & Peterson, C. L. Unlocking the gates to gene expression. Science 295, 1847–1848 (2002).
Heun, P., Laroche, T., Shimada, K., Furrer, P. & Gasser, S. M. Chromosome dynamics in the yeast interphase nucleus. Science 294, 2181–2186 (2001).
Hutchinson, C. Lamins: building blocks or regulators of gene expression. Nature Rev. Mol. Cell Biol. 3, 848–858 (2002).
Burke, B. & Stewart, C. L. Life at the edge: the nuclear envelope and human disease. Nature Rev. Mol. Cell Biol. 3, 575–585 (2002).
Hoffmann, K. et al. Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger–Huët anomaly). Nature Genet. 31, 410–414 (2002).
Shultz, L. D. et al. Mutations at the mouse ichthyosis locus are within the lamin B receptor gene: a single gene model for human Pelger–Huët anomaly. Hum. Mol. Genet. 12, 61–69 (2003).
Waterham, H. R. et al. Autosomal recessive HEM/Greenberg skeletal dysplasia is caused by 3β-hydroxysterol Δ14-reductase deficiency due to mutations in the lamin B receptor gene. Am. J. Hum. Genet. 72, 1013–1017 (2003).
Grandville, J. J. Un Autre Monde (H. Fournier, Paris, 1844).
DuPraw, E. J. Quantitative constraints in the arrangement of human DNA. Cold Spring Harb. Symp. Quant. Biol. 38, 87–98 (1974).
Acknowledgements
The authors express their gratitude to Bowdoin College and to the German Cancer Research Center (Heidelberg) for providing stimulating intellectual and scientific environments. H. Herrmann and P. Lichter, our generous hosts at the German Cancer Research Center, supplied helpful comments on the manuscript. Several anonymous referees made significant contributions towards the improvement of this essay. The authors dedicate this review to the memory of H. G. Davis (formerly at the Department of Biophysics, King's College, London), an excellent microscopist and our good friend.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Olins, D., Olins, A. Chromatin history: our view from the bridge. Nat Rev Mol Cell Biol 4, 809–814 (2003). https://doi.org/10.1038/nrm1225
Issue Date:
DOI: https://doi.org/10.1038/nrm1225
This article is cited by
-
Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
BMC Biology (2022)
-
Epithelial cells-enriched lncRNA SNHG8 regulates chromatin condensation by binding to Histone H1s
Cell Death & Differentiation (2022)
-
Analysis of three-dimensional chromatin packing domains by chromatin scanning transmission electron microscopy (ChromSTEM)
Scientific Reports (2022)
-
Interphase epichromatin: last refuge for the 30-nm chromatin fiber?
Chromosoma (2021)
-
Linker histone epitopes are hidden by in situ higher-order chromatin structure
Epigenetics & Chromatin (2020)