Abstract
We review and deepen a theory of elastic bending of DNA on a persistence length scale. In a regime of extensive charge neutralization the axis of the double helix is elastically unstable when straight. Its stable bent conformation allows nucleation of DNA toruses and in principle could direct the supercoiled (solenoid) form of a polynucleosome. The Euler theory of elastic instability of macroscopic rods gives a partial description of the intrinsic ability of DNA to form locally stable bends. A different, quasi-Eulerian theory can be based on what is probably the dominant bending mechanism of DNA in solution—flexible kinking at the sites of open base pairs. This predictive theory is in quantitative agreement with the observed value (about 16 nm) for the minimum radius of torus holes. Stability of the inner torus ring is achieved when DNA phosphate groups are about 90% neutralized by trivalent cations, another prediction that is consistent with the observed formation of toruses in these conditions. The predicted stable radius of curvature of charge-neutralized DNA is also equal to the radial dimension of a maximally contracted polynucleosome supercoil as measured by neutron scattering (17 nm), but further experimental investigation of the geometrical disposition of the spacer DNA regions in the solenoid will be necessary to rule out the possibility of accidental agreement for this complex system. We stress again the experimental reality and probable importance of open base pairs in the equilibrium solution conformation of DNA.
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References
Kleinschmidt, A. K., Lang, D., Jacherts, D., and Zahn, R. K. (1962),Biochim. Biophys. Acta 61, 857.
Riemer, S. C., and Bloomfield, V. A. (1978),Biopolymers 17, 785.
Shore, D., Langowski, J., and Baldwin, R. L. (1981),Proc. Natl. Acad. Sci. USA 78, 4833.
McGhee, J. D., and Felsenfeld, G. (1980),Ann. Rev. Biochem. 49, 1115.
Manning, G. S. (1978),Quart. Revs. Biophys. 11, 179.
Manning, G. S. (1979),Biopolymers 18, 2929.
Manning, G. S. (1980),Biopolymers 19, 37.
Manning, G. S. (1981),Biopolymers 20, 1261.
Manning, G. S. (1981),Biopolymers 20, 1751.
Manning, G. S. (1981),Biopolymers 20, 2337.
Manning, G. S. (1982),Comments Mol. Cell. Biophys. 1, 311.
Manning, G. S. (1983),Biopolymers 22, 689.
Manning, G. S., inStructure and Dynamics: Nucleic Acids and Proteins, Clementi, E., and Sarma, R. H., eds., Adenine Press, NY, 1983.
Bloomfield, V. A., Crothers, D. M., and Tinoco, Jr., I.,Physical Chemistry of Nucleic Acids, Harper & Row, New York, 1974.
Landau, L. D., and Lifshitz, E. M.,Theory of Elasticity, Pergamon Press, Oxford, 1970.
Love, A. E. H.,A Treatise on the Mathematical Theory of Elasticity, Dover, New York, 1944.
Shore, D., and Baldwin, R. L. (1983),J. Mol. Biol. 170, 957.
Shore, D., and Baldwin, R. L. (1983),J. Mol. Biol. 170, 983.
Horowitz, D. S., and Wang, J. C. (1984),J. Mol. Biol. 173, 75.
Post, C. B. (1983),Biopolymers 76, 1087.
Le Bret, M. (1982),J. Chem. Phys. 76, 6243.
Fixman, M. (1982),J. Chem. Phys. 76, 6346.
Manning, G. S. (1969),J. Chem. Phys. 51, 3249.
Landau, L. D., and Lifshitz, E. M.,Statistical Physics, Pergamon Press, London, 1958.
Frontali, C., Dore, F., Ferrauto, A., Gratton, E., Bettini, A., Pozzan, M. R., and Valdevit, E. (1979),Biopolymers 18, 1353.
Pfeuty, P., Velasco, R. M., and de Gennes, P. G. (1977),J. Phys. (Paris) Lett. 38, 5.
Englander, S. W., and Kallenbach, N. R. (1984),Quart, Revs. Biophys. 17, 1.
Wing, R., Drew, H., Takano, T., Broka, C., Tanaka, S., Itakura, K., and Dickerson, R. E. (1980),Nature 287, 755.
Gosule, L. C., and Schellman, J. A. (1978),J. Mol. Biol. 121, 311.
Thomas, T. J., and Bloomfield, V. A. (1983),Biopolymers 22, 1097.
Yen, W. S., Rhee, K. W., and Ware, B. R. (1983),J. Phys. Chem. 87, 2148.
Widom, J., and Baldwin, R. L. (1980),J. Mol. Biol. 144, 431.
Widom, J., and Baldwin, R. L. (1983),Biopolymers 22, 1595.
Benbasat, J. A.,Biochemistry.
Chattoraj, D. K., Gosule, L. C., and Schellman, J. A. (1978),J. Mol. Biol. 121, 327.
Ruben, G. C., Marx, K. A., and Reynolds, T. C.,39th Ann. Proc. Electron Microscopy Soc. Amer., Atlanta, Georgia, 1981, G. W. Bailey, ed.
Marx, K. A., and Ruben, G. C. (1983),Nucleic Acids Res. 11, 1839.
Marx, K. A., and Ruben, G. C., inThe Molecular Basis of Cancer (Rein, R. R., ed.), Liss, New York, in press.
Castleman, H., and Erlanger, B. F. (1983),Cold Spring Harbor Symp. Quant. Biol. 47, 133.
Marx, K. A., and Reynolds, T. C. (1982),Proc. Natl. Acad. Sci. USA 79, 6484.
Marx, K. A., and Reynolds, T. C. (1983),Biochim. Biophys. Acta 741, 279:
Grosberg, A. Yu. (1979),Biofizica 24, 32.
Bina, M., Sturtevant, J. M., and Stein, A. (1980),Proc. Natl. Acad. Sci. USA 77, 4044.
McGhee, J. D., and Felsenfeld, G. (1979),Proc. Natl. Acad. Sci. USA 76, 2133.
McGhee, J. D., and Felsenfeld, G. (1982),J. Mol. Biol. 158, 685.
McGhee, J. D., and Felsenfeld, G. (1980),Nucleic Acids Res. 8, 2751.
Simpson, R. T. (1978),Biochemistry 17, 5524.
Suau, P., Bradbury, E. M., and Baldwin, J. P. (1979),Eur. J. Biochem. 97, 593.
Renz, M., Nehls, P., and Hozier, J. (1977),Cold Spring Harbor Symp. Quant. Riol. 42, 245.
Renz, M., and Day, L. A. (1976),Biochemistry 15, 3220.
Thomas, J. D., and Butler, P. J. G. (1980),J. Mol. Biol. 144, 89.
Butler, P. J. G., and Thomas, J. D. (1980),J. Mol. Biol. 140, 505.
Belmont, A., and Nicolini, C. (1981),J. Theoret. Biol. 90, 169.
Thoma, F., Losa, R., and Koller, T. (1983),J. Mol. Biol. 167, 619.
Cole, R. D., Lawson, G. M., and Hsiang, M. W. (1977),Cold Spring Harbor Symp. Quant. Biol. 42, 253.
Finch, J. T., and Klug, A. (1976),Proc. Natl. Acad. Sci. USA 73, 1897.
Sperling, L., and Klug, A. (1977),J. Mol. Biol. 112, 253.
Schurr, J. M. (1984),Biopolymers 23, 191.
References
Richmond, T. J., Finch, J. T., Rushton, B., Rhodes, D., and Klug, A. (1984),Nature 311, 532.
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An erratum to this article is available at http://dx.doi.org/10.1007/BF02788462.
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Manning, G.S. Packaged DNA. Cell Biophysics 7, 57–89 (1985). https://doi.org/10.1007/BF02788639
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DOI: https://doi.org/10.1007/BF02788639