Skip to main content
SpringerLink
Log in

The superstructure of chromatin and its condensation mechanism

V. Effect of linker length, condensation by multivalent cations, solubility and electric dichroism properties

  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

Comparison between the internucleosomal distance found by X-ray solution scattering for chicken erythrocyte (23 nm) and sea urchin (30 nm) chromatin indicates that this distance is proportional to the linker length. The diameter of the condensed sea urchin chromatin fibers is about 45 nm which is significantly larger than in chicken erythrocyte chromatin (35 nm). Trivalent cations (Gd, Tb, Cr) and the polyamines spermine and spermidine were found to induce compaction at much lower concentrations than the divalent cations but Gd, Tb and Cr induce aggregation before full compaction of the fibers. The influence of hydrogen bonding is illustrated by comparison of the effects of NaCl, ammonium chloride and alkylammonium chlorides on condensation. Solubility experiments indicate that there is a nearly linear dependence of the Mg-- concentration at which precipitation occures on chromatin concentration and confirm the differences between cations observed by X-ray scattering.

The chicken erythrocyte chromatin samples were further characterized by their reduced electric dichroism. The values found are consistent with the model derived from X-ray scattering and are compared with those reported in the literature.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allan J, Rau DC, Harborne N, Gould H (1984) Higher order structure in short repeat length chromatin. J Cell Biol 98:1320–1327

    Google Scholar 

  • Ausio J, Borochov N, Seger D, Eisenberg H (1984) Interaction of chromatin with NaCl and MgCl2: Solubility and binding studies, Transition to and characterization of the higher order structure. J Mol Biol 177:373–398

    Google Scholar 

  • Bordas J, Perez-Grau L, Koch MHJ, Nave C, Vega MC (1986a) The superstructure of chromatin and its condensation mechanism. I: Synchrotron radiation X-ray scattering results. Eur Biophys J 13:157–174

    Google Scholar 

  • Bordas J, Perez-Grau L, Koch MHJ, Nave C, Vega MC (1986b) The superstructure of chromatin and its condensation mechanism. II: Theoretical analysis of the X-ray scattering patterns and model calculations. Eur Biophys J 13:175–186

    Google Scholar 

  • Borochov N, Ausio J, Eisenberg H (1984) Interaction and conformational changes of chromatin with divalent ions. Nucleic Acid Res 12:3089–3096

    Google Scholar 

  • Boulin C, Kempf R, Koch MHJ, McLaughlin SM (1986) Data appraisal, evaluation and display for synchrotron radiation experiments: hardware and software. Nucl Instrum Methods A249:399–407

    Google Scholar 

  • Dimitrov SI, Smirnov IV, Makarov VL (1988) Optical anisotropy of chromatin: Flow linear dichroism and electric dichroism studies. J Biomol Struct Dyn 5:1135–1148

    Google Scholar 

  • Drinkwater RD, Wilson PR, Skinner JD, Burgoyne LA (1987) Chromatin structures: dissecting their patterns in nuclear digests. Nucl Acids Res 15:8087–8103

    Google Scholar 

  • Finch JT, Klug A (1976) Solenoidal model for superstructure in chromatin. Proc Natl Acad Sci USA 73:1897–1901

    Google Scholar 

  • Gerchman SE, Ramakrishnan V (1987) Chromatin higher order structure studied by neutron scattering and scanning transmission electron microscopy. Proc Natl Acad Sci USA 84: 7802–7806

    Google Scholar 

  • Greulich KO, Wachtel E, Ausio J, Seger D, Eisenberg H (1987) Transition of chromatin from the “10 nm” lower order structure, to the “30 nm” higher order structure, as followed by small angle X-ray scattering. J Mol Biol 193:709–721

    Google Scholar 

  • Harrington RE (1985) Optical model studies of the salt induced 10–30 nm fiber transition in chromatin. Biochemistry 24: 2011–2021

    Google Scholar 

  • Kellenberger E (1987) The compactness of cellular plasmas; in particular chromatin compactness in relation to function. TIBS 12:105–107

    Google Scholar 

  • Koch MHJ, Bordas J (1983) X-ray diffraction and scattering on disordered systems using synchrotron radiation. Nucl Instrum Methods 208:461–469

    Google Scholar 

  • Koch MHJ, Vega MC, Sayers Z, Michon AM (1987a) The superstructure of chromatin and its condensation mechanism. III: Effect of monovalent and divalent cations X-ray solution scattering and hydrodynamic studies. Eur Biophys J 14: 307–319

    Google Scholar 

  • Koch MHJ, Sayers Z, Vega MC, Michon AM (1987b) The superstructure of chromatin and its condensation mechanism. IV: Enzymatic digestion, thermal denaturation, effect of netropsin and distamycin. Eur Biophys J 15:133–140

    Google Scholar 

  • Kubista M, Hard T, Nielsen PE, Norden B (1985) Structural transitions of chromatin at low salt concentrations: A flow linear dichroism study. Biochemistry 24:6336–6342

    Google Scholar 

  • Langmore JP, Paulson JR (1983) Low angle X-ray diffraction studies of chromatin structure in vivo and in isolated cell nuclei and metaphase chromosomes. J Cell Biol 96:1120–1131

    Google Scholar 

  • Makarov V, Dimitrov S, Smirnov V, Pashev I (1985) A triple helix for the structure of chromatin fiber. FEBS Lett 181: 357–361

    Google Scholar 

  • Manning GS (1978) The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Qu Rev Biophys 11:179–246

    Google Scholar 

  • Marion C, Martinage A, Tirard A, Roux B, Daune M, Mazen A (1985) Histone phosphorylation in native chromatin induces local structural changes as probed by electric birefringence. J Mol Biol 186:367–379

    Google Scholar 

  • Marquet R, Colson P, Matton AM, Houssier C, Thiry M, Goessens G (1988) Comparative study of the condensation of chicken erythrocyte and calf thymus chromatins by di- and multivalent cations. J Biol Struct Dyn 5:839–857

    Google Scholar 

  • McGhee JD, Rau DC, Charney E, Felsenfeld G (1980) Orientation of the nucleosome within the higher order structure of chromatin. Cell 22:87–96

    Google Scholar 

  • Lee KS, Mandelkern M, Crothers DM (1981) Solution structural studies of chromatin fibers. Biochemistry 20:1438–1445

    Google Scholar 

  • Notbohm H (1986) Small angle scattering of cell nuclei. Eur Biophys J 13:367–372

    Google Scholar 

  • Perez-Grau L, Bordas J, Koch MHJ (1984) Synchrotron radiation X-ray scattering study on solutions and gels. Nucleic Acids Res 12:2987–2995

    Google Scholar 

  • Ramsay-Shaw B, Schmitz KS (1976) Quasielastic light scattering by biopolymers. Conformation of chromatin multimers. Biochem Biophys Res Commun 73:224–232

    Google Scholar 

  • Sayers Z (1988) Synchrotron X-ray scattering studies of the chromatin fiber structure. In: Mandelkow E (ed) Synchrotron radiation in chemistry and biology, I. Springer, Berlin heidelberg New York (Topics in current chemistry, vol 145, pp 203–232)

    Google Scholar 

  • Sen D, Crothers DM (1986) Condensation of Chromatin: Role of Multivalent Cations. Biochemistry 25:1495–1503

    Google Scholar 

  • Staynov DZ (1983) Possible nucleosome arrangements in the higher order structure of chromatin. Int J Biol Macromol 5:3–9

    Google Scholar 

  • Subirana JA, Munoz-Guerra S, Aymami J, Radermacher M, Frank J (1985) The layered organization of nucleosomes in 30 nm fibers. Chromosoma 91:377–390

    Google Scholar 

  • Tam SC, Williams RJP (1985) Electrostatics and biological systems. Struct Bonding 63:103–151

    Google Scholar 

  • Thoma F, Koller T, Klug A (1979) Involvement of histone H1 in the organization of the nucleosome and of the salt dependent superstructures of chromatin. J Cell Biol 83:403–407

    Google Scholar 

  • Walker PR, Sikorska M (1987) Chromatin structure: Evidence that the 30 nm fiber is a helical coil with 12 nucleosomes/turn. J Biol Chem 262:12223–12227

    Google Scholar 

  • Wedrychowski A, Ward WS, Schmidt WN, Hnilica LS (1985) Chromium-induced cross-linking of nuclear proteins and DNA. J Biol Chem 260:7150–7155

    Google Scholar 

  • Widom J (1986) Physicochemical studies of the folding of the 100 Å nucleosome filament into the 300 Å filament. J Mol Biol 190:411–424

    Google Scholar 

  • Widom J, Klug A (1985) Structure of the 300 A filament: X-ray diffraction from oriented samples. Cell 43:207–213

    Google Scholar 

  • Widom J, Finch JT, Thomas JO (1985) Higher order structure of long repeat chromatin. EMBO J 4:3189–3194

    Google Scholar 

  • Williams SP, Athey BD, Muglia LJ, Schappe R, Gough AJ, Langmore JP (1986) Chromatin fibers are left-handed double helices with diameter and mass per unit length that depend on linker length. Biophys J 49:233–250

    Google Scholar 

  • Yabuki H, Dattagupta N, Crothers DM (1982) Orientation of nucleosomes in the thirty-nanometer chromatin fiber. Biochemistry 21:5015–5020

    Google Scholar 

  • Zentgraf H, Franke WW (1984) Differences of supranucleosomal organization in different kinds of chromatin: Cell type-specific globular subunits containign different numbers of nucleosomes. J Cell Biol 99:272–286

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. European Molecular Biology Laboratory, c/o DESY, Notkestrasse 85, D-2000, Hamburg 52, Federal Republic of Germany

    M. H. J. Koch, Z. Sayers & A. M. Michon

  2. Laboratoire de Chimie Macromoleculaire et Chimie Physique, Sart Tilman (B6), Université de Liège, B-4000, Liège, Belgium

    R. Marquet & C. Houssier

  3. Biologische Anstalt Helgoland, Notkestrasse 31, D-2000, Hamburg 52, Federal Republic of Germany

    J. Willführ

Authors
  1. M. H. J. Koch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Z. Sayers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. M. Michon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Marquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Houssier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. Willführ
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koch, M.H.J., Sayers, Z., Michon, A.M. et al. The superstructure of chromatin and its condensation mechanism. Eur Biophys J 16, 177–185 (1988). https://doi.org/10.1007/BF00261903

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00261903

Key words

Search

Navigation