An estimate of the extent of folding of nucleosomal DNA by laterally asymmetric neutralization of phosphate groups.

We attempt quantitative implementation of a previous suggestion that asymmetric charge neutralization of DNA phosphate groups may provide part of the driving force for nucleosome folding. Polyelectrolyte theory can be used to estimate the effective compressive force acting along the length of one side of the DNA surface when a fraction of the phosphate groups are neutralized by histones bound to that side. A standard engineering formula then relates the force to the bending amplitude caused by it. Calculated bending amplitudes are consistent with the curvature of nucleosomal DNA and the overall extent of charge neutralization by the histones. The relation of the model to various aspects of nucleosome folding, including the detailed path of core-particle DNA, is discussed. Several other DNA-protein complexes are listed as examples of possible asymmetric charge-induced bending.

[1]  D. Wemmer,et al.  Nuclear magnetic resonance studies of polyamine binding to a defined DNA sequence. , 1985, Journal of molecular biology.

[2]  F. Richards,et al.  Electrostatic field of the large fragment of Escherichia coli DNA polymerase I. , 1985, Journal of molecular biology.

[3]  A. Klug,et al.  Structure of the nucleosome core particle at 7 Å resolution , 1984, Nature.

[4]  E. Bradbury,et al.  Hyperacetylation of core histones does not cause unfolding of nucleosomes. Neutron scatter data accords with disc shape of the nucleosome. , 1986, The Journal of biological chemistry.

[5]  Gerald S. Manning,et al.  Counterion binding in polyelectrolyte theory , 1979 .

[6]  R. Simpson,et al.  Cromatin and core particles formed from the inner histones and synthetic polydeoxyribonucleotides of defined sequence. , 1979, Nucleic acids research.

[7]  D. Crothers,et al.  The DNA binding domain and bending angle of E. coli CAP protein , 1986, Cell.

[8]  G. S. Manning,et al.  Polyelectrolyte effects on site‐binding equilibria with application to the intercalation of drugs into DNA , 1984, Biopolymers.

[9]  G. Felsenfeld,et al.  Supercoiling energy and nucleosome formation: the role of the arginine-rich histone kernel. , 1977, Nucleic acids research.

[10]  A. Klug,et al.  Location of the primary sites of micrococcal nuclease cleavage on the nucleosome core. , 1983, Journal of molecular biology.

[11]  S. Harrison,et al.  Effect of non-contacted bases on the affinity of 434 operator for 434 repressor and Cro , 1987, Nature.

[12]  R. M. Smith,et al.  Natural abundance carbon-13 nuclear magnetic resonance studies of histone and DNA dynamics in nucleosome cores. , 1986, The Journal of biological chemistry.

[13]  G. S. Manning The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides , 1978, Quarterly Reviews of Biophysics.

[14]  S. Harrison,et al.  Structure of the represser–operator complex of bacteriophage 434 , 1987, Nature.

[15]  A. Rich,et al.  Asymmetric lateral distribution of unshielded phosphate groups in nucleosomal DNA and its role in DNA bending. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[16]  J M Rosenberg,et al.  Structure of the DNA-Eco RI endonuclease recognition complex at 3 A resolution. , 1986, Science.

[17]  A. Belyavsky,et al.  Primary organization of nucleosome core particle of chromatin: sequence of histone arrangement along DNA. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[18]  C. F. Anderson,et al.  Competitive interactions of cobalt(3+)hexamine and sodium with helical B-DNA probed by cobalt-59 and sodium-23 NMR , 1987 .

[19]  J. Méry,et al.  A chromatin core particle obtained by selective cleavage of histones by clostripain. , 1986, The EMBO journal.

[20]  Andrew Travers,et al.  DNA bending and nucleosome positioning , 1987 .

[21]  T. Steitz,et al.  Structure of a complex of catabolite gene activator protein and cyclic AMP refined at 2.5 A resolution. , 1987, Journal of molecular biology.

[22]  T. Steitz,et al.  Model of specific complex between catabolite gene activator protein and B-DNA suggested by electrostatic complementarity. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Mirzabekov,et al.  A highly basic histone H4 domain bound to the sharply bent region of nucleosomal DNA , 1988, Nature.

[24]  Robert H. Austin,et al.  Evidence for kinks in DNA folding in the nucleosome , 1987, Nature.

[25]  G. Felsenfeld,et al.  The number of charge-charge interactions stabilizing the ends of nucleosome DNA. , 1980, Nucleic acids research.

[26]  T. Richmond,et al.  Crystals of a nucleosome core particle containing defined sequence DNA. , 1988, Journal of molecular biology.

[27]  E. Uberbacher,et al.  X-ray structure of the nucleosome core particle. , 1985, Journal of biomolecular structure & dynamics.

[28]  A. Mirzabekov,et al.  One‐domain interaction of histone H4 with nucleosomal core DNA is restricted to a narrow DNA segment , 1986, FEBS letters.

[29]  A. Belyavsky,et al.  Primary organization of the nucleosome core particles. Sequential arrangement of histones along DNA. , 1980, Journal of molecular biology.