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The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides

Published online by Cambridge University Press:  17 March 2009

Gerald S. Manning
Affiliation:
Wright and Rieman Chemistry Laboratories, Rutgers, The State University of New Jersey, New Brunswick, New Jersey 08903

Extract

Although the importance of the polyelectrolyte character of DNA has been recognized for some time (Felsenfeld & Miles 1967), few of the implications have been explored, primarily because of a lag in translating the breakthroughs in polyelectrolyte theory of the last decade into a form that is well adapted to the analysis of the specialized problems of biophysical chemistry. Perhaps an analogous situation existed in the field of protein chemistry during the period after the formulation and confirmation of the Debye—Hückel theory of ionic solutions but before Scatchard's incorporation of the theory into his analysis of the binding properties of proteins. An achievement for polynucleotide solutions parallel to Scatchard's was recently presented by Record, Lohman, & de Haseth (1976) and further developed and reviewed by Record, Anderson & Lohman (1978).

Type
Research Article
Copyright
Copyright © Cambridge University Press 1978

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References

REFERENCES

Abramson, H. S.Moyer, L. S. & Gorin, M. H. (1942). Electrophoresis of Proteins. New York: Reinhold.Google Scholar
Anderson, C. F.Record, M. T. Jr & Hart, P. A. (1978). Sodium-23 NMR studies of cation—DNA interactions. Biophys. Chem. 7, 301316.CrossRefGoogle ScholarPubMed
Archer, B. C.Craney, C. L. & Krakauer, H. (1972). The interaction of Na ions with synthetic polynucleotides. Biopolymers II, 781809.CrossRefGoogle Scholar
Bailey, J. M. (1973). A comparison of two cluster expansion approaches to polyelectrolyte theory. Biopolymers 12, 17051708.CrossRefGoogle Scholar
Bhat, K. R. (1974). Physicochemical investigations of magnesium—DNA— proflavine system. Ph.D. thesis, Rutgers University (dir., U. P. Strauss).Google Scholar
Bloomfield, V. A.Crothers, D. M. & Tinoco, I. Jr (1974). Physical Chemistry of Nucleic Acids. New York: Harper and Row.Google Scholar
Bourgeois, S. & Pfahl, M. (1976). Repressors. Adv. Protein Chem. 30, 199.CrossRefGoogle ScholarPubMed
Boyd, G. E.Wilson, D. P. & Manning, G. S. (1976). Enthalpies of mixing of polyelectrolytes with simple aqueous electrolyte solutions. J. Phys. Chem. 80, 808810.CrossRefGoogle Scholar
Brun, F.Toulmé, J. & Héléne, C. (1975). Interactions of aromatic residues of proteins with nucleic acids. Fluorescence studies of the binding of oligopeptides containing tryptophan and tyrosine residues to polynucleotides. Biochemistry, N.Y. 14, 558563.CrossRefGoogle ScholarPubMed
Camerman, N.Fawcett, J. K. & Camerman, A. (1976). Molecular structure of a deoxyribose-dinucleotide, sodium thymidylyl-(5' → 3')-thymidylate- (5') hydrate (pTpT), and a possible structural model for polythymidylate. J. molec Biol. 107, 601621.CrossRefGoogle Scholar
Clarke, H. B.Cusworth, D.C. & Datta, S. P. (1954). Thermodynamic quantities for the dissociation equilibria of biologically important compounds. 3. The dissociations of the magnesium salts of phosphoric acid, glucose i-phosphoric acid and glycerol 2-phosphoric acid. Biochem. J. 146154.Google Scholar
Clement, R. M.Sturm, J. & Daune, M. P. (1973). Interaction of metallic cations with DNA. VI. Specific binding of Mg++ and Mn++. Biopolymers 12, 405421.CrossRefGoogle Scholar
Daune, M. (1970). Binding of divalent cations to DNA. Stud. Biophys. 24/25, 287297.Google Scholar
deHaseth, P. L.Lohman, T. M. & Record, M. T. Jr (1977). The nonspecific interaction of lac repressor with DNA: an association reaction driven by counterion release. Biochemistry, N. Y. 16, 47834790.CrossRefGoogle ScholarPubMed
De, Marky N. & Manning, G. S. (1975). On the application of polyelectrolyte limiting laws to the helix-coil transition of DNA. III. Dependence of helix stability on excess univalent salt and on polynucleotide phosphate concentration for variable equivalent ratios of divalent metal ion to phosphate. Biopolymers 14, 14071422.Google Scholar
Devore, D. I. & Manning, S. (1974). Application of polyelectrolyte limiting laws to virial and asymptotic expansions for the Donnan equilibrium. Biophys. Chem. 2, 4248.CrossRefGoogle ScholarPubMed
Dove, W. F. & Davidson, N. (1962). Cation effects on the denaturation of DNA. J. molec. Biol. 5, 467478.CrossRefGoogle Scholar
Eigen, M. (1963). Fast elementary steps in chemical reaction mechanisms. Pure appl. Chem. 6, 97115.CrossRefGoogle Scholar
Felsenfeld, G. & Miles, H. T. (1967). The physical and chemical properties of nucleic acids. A. Rev. Biochem. 36, 407448.CrossRefGoogle ScholarPubMed
Felsenfeld, G. & Rich, A. (1957). Studies on the formation of two- and three-stranded polyribonucleotides. Biochim. biophys. Acta 26, 457468.CrossRefGoogle ScholarPubMed
Gilbert, W.Maxam, A. & Mirzabekov, A. (1975). In Control of Ribosome Synthesis. Alfred Benson Symposium IX, Copenhagen.Google Scholar
Gosule, L. C. & Schellman, J. A. (1976). Compact form of DNA induced by spermidine. Nature, Lond. 259, 333335.CrossRefGoogle ScholarPubMed
Greenwald, I.Redish, J. & Kibrick, A. C. (1940). The dissociation of calcium and magnesium phosphates. J. biol. Chem. 135, 6576.CrossRefGoogle Scholar
Gulick, A.Inoue, H. & Luzzati, V. (1970). Conformation of single-stranded polynucleotides: small-angle X-ray scattering and spectroscopic study of polyribocytidylic acid in water and in water-alcohol solutions. J. molec. Biol. 53, 221238.CrossRefGoogle Scholar
Gruenwedel, D. W.Hsu, C. H. & Lu, D. S. (1971). The effects of aqueous neutral-salt solutions on the melting temperatures of deoxyribonucleic acids. Biopolymers 10, 4768.CrossRefGoogle ScholarPubMed
Harrington, R. E. (1978). The optico-hydrodynamic properties of high molecular weight DNA. III. The effects of NaCl concentration. Biopolymers 17, 919936,CrossRefGoogle Scholar
Hen, J. & Strauss, U. P. (1974). Studies of counterion binding by poly (vinylsulfonate). J. Phys. Chem. 78, 10131017.CrossRefGoogle Scholar
Hirsch, J. & Schleif, R. (1976). High resolution electron microscopic studies of genetic regulation. J. molec. Biol. 108, 471490.CrossRefGoogle Scholar
Iwasa, K. (1977). An examination of the limiting laws of polyelectrolytes and counterion condensation. J. Phys. Chem. 81, 18291833.CrossRefGoogle Scholar
Kielman, H. S.Van, Der Hoeven J. M. A. M. & Leyte, J. C. (1976). Nuclear magnetic relaxation of 23Na and 7Li ions in polyphosphate solutions. Biophys. Chem. 4, 103111.CrossRefGoogle ScholarPubMed
Kirkwood, J. G. & Oppenheim, I. (1961). Chemical Thermodynamics. New York: McGraw-Hill.Google Scholar
Kolchinsky, A. M.Mirzaeekov, A. D.Gilbert, W. & Li, L. (1976). Preferential protection of the minor groove of non-operator DNA by lac repressor against methylation by dimethyl sulphate. Nucl. Acids Res. 3, 1118.CrossRefGoogle ScholarPubMed
Krakauer, H. (1974). A thermodynamic analysis of the influence of simple mono- and divalent cations on the conformational transitions of polynucleotide complexes. Biochemistry, N.Y. 13, 25792589.CrossRefGoogle ScholarPubMed
Krakauer, H. & Sturtevant, J. M. (1968). Heats of the helix-coil transitions of the polyA-polyU complexes. Biopolymers 6, 491512.CrossRefGoogle Scholar
Kwak, J. C. T.O'Brien, M. C. & MacLean, D. A. (1975). Mean activity coefficients for the simple electrolyte in aqueous mixtures of polyelectrolyte and simple electrolyte. The systems potassium chloridepotassium poly(styrenesulfonate), magnesium chloride-magnesium poly (styrenesulfonate), and calcium chloride-calcium poly(styrenesulfonate). J. Phys. Chem. 79, 23812386.CrossRefGoogle Scholar
Latt, S. & Sober, H. (1967). Protein—nucleic acid interactions. II. Oligopeptide-polyribonucleotide binding studies. Biochemistry, N. Y. 6, 32933306.CrossRefGoogle ScholarPubMed
Leng, M. & Felsenfeld, G. (1966). The preferential interactions of poly lysine and polyarginine with specific base sequences in DNA. Proc. natn. Acad. Sci. USA 56, 13251332.CrossRefGoogle Scholar
Lin, S. Y. & Riggs, A. D. (1972). Lac repressor binding to non-operator DNA: detailed studies and a comparison of equilibrium and rate competition methods. J. molec. Biol. 72, 671690.CrossRefGoogle Scholar
Lyons, J. W. & Kotin, L. (1965). Ion-binding in polyelectrolyte systems with or without added salt. J. Amer. chein. Soc. 87, 16701678.CrossRefGoogle Scholar
Manning, G. S. (1969). Limiting laws and counterion condensation in polyelectrolyte solutions. I. Colligative properties. J. chem. Phys. 51, 924933.CrossRefGoogle Scholar
Manning, G. S. (1972 a). Polyelectrolytes. A. Rev. phys. Chem. 23, 117140.CrossRefGoogle Scholar
Manning, G. S. (1972 b). On the application of polyelectrolyte limiting laws to the helix-coil transition of DNA. I. Excess univalent cations. Biopolymers II, 937949.CrossRefGoogle Scholar
Manning, G. S. (1972c). On the application of polyelectrolyte limiting laws to the helix-coil transition of DNA. II. The effect of Mg+ counterions. Biopolymers II, 951955.CrossRefGoogle Scholar
Manning, G. S. (1974). Limiting laws for equilibrium and transport properties and polyelectrolyte solutions. In Polyelectrolytes (ed. Selegny, E.), Dordrecht, Holland: Reidel.Google Scholar
Manning, G. S. (1975). Remarks on the paper ‘Nucleic magnetic relaxation of 23Na in polyelectrolyte solutions’ by van der Klink, Zuiderweg, and Leyte. J. chem. Phys. 62, 748749.CrossRefGoogle Scholar
Manning, G. S. (1976 a). The application of polyelectrolyte limiting laws to the helix-coil transition of DNA. VI. The numerical value of the axial phosphate spacing for the coil form. Biopolymers 15, 23852390.CrossRefGoogle Scholar
Manning, G. S. (1976 b). On the application of polyelectrolyte limiting laws to the helix-coil transition of DNA. V. Ionic effects on renaturation kinetics. Biopolymers 15, 13331343.CrossRefGoogle Scholar
Manning, G. S. (1977 a). Limiting laws and counterion condensation in polyelectrolyte solutions. IV. The approach to the limit and the extraordinary stability of the charge fraction. Biophys. Chem. 7, 95102.CrossRefGoogle Scholar
Manning, G. S. (1977 b). Theory of the delocalized binding of Mg(II) to DNA: preliminary analysis for low binding levels. Biophys. Chem. 7, 141145.CrossRefGoogle ScholarPubMed
Manning, G. S. (1977 c). A field-dissociation relation for polyelectrolytes with an application to field-induced conformational changes of poiynucleotides. Biophys. Chem. 7, 189192.CrossRefGoogle Scholar
Manning, G. S. (1978). Limiting laws and counterion condensation in polyelectrolyte solutions. V. Further development of the chemical model. Biophys. Chem. (in the Press).CrossRefGoogle Scholar
Manning, G. S. & Zimm, B. H. (1965). Cluster theory of polyelectrolyte solutions. I. Activity coefficients of the mobile ions. J. chem. Phys. 43, 42504259.CrossRefGoogle Scholar
Melchior, W. B. Jr & Von, Hippel P. H. (1973). Alteration of the relative stability of dA·dT and dG·dC base pairs in DNA. Proc. natn Acad. Sci. U.S.A. 70, 298302.CrossRefGoogle ScholarPubMed
Mirzabekov, A. D. & Melnikova, A. F. (1974). Localization of chromatin proteins within DNA grooves by methylation of chromatin with di- methyl sulphate. Mol. Biol. Reports I, 379384.CrossRefGoogle Scholar
Olson, W. K. (1975). Configuration-dependent properties of randomly coiling polynucleotide chains. I. A comparison of theoretical energy estimates. Biopolymers 14, 17751795.CrossRefGoogle Scholar
Olson, W. K. & Manning, G. S. (1976). A configurational interpretation of the axial phosphate spacing in polynucleotide helices and random coils. Biopolymers 15, 23912405.CrossRefGoogle ScholarPubMed
Onsager, L. (1934). Deviations from Ohm's law in weak electrolytes. J. chem. Phys. 2, 599615.CrossRefGoogle Scholar
Onsager, L. & Liu, C. T. (1965). Zur Theorie des Wienseffekts in schwachen Elektrolyten. Z. phys. Chem. 228, 428432.CrossRefGoogle Scholar
Pless, R. C. & Ts'o, P. O. P. (1977). Duplex formation of a nonionic oligo (deoxythymidylate) analogue [heptadeoxythymidylyl-(3'-5')-deoxythy- midine heptaethyl ester (d-[Tp(Et)]7T)] with poly (deoxyadenylate). Evaluation of the electrostatic interaction. Biochemistry, N.Y. 16, 12391250.CrossRefGoogle Scholar
Pörschke, D. (1976a). Thermodynamic and kinetic parameters of ion condensation to polynucleotides. Outer sphere complex formed by Mg++ ions. Biophys. Chem. 4, 383394.CrossRefGoogle ScholarPubMed
Pörschke, D. (1976 b). Threshold effects observed in conformation changes induced by electric fields. Biopolymers 15, 19171928.CrossRefGoogle ScholarPubMed
Record, M. T. Jr (1975). Effects of Na+ and Mg++ ions on the helix-coil transition of DNA. Biopolymers 14, 21372158.CrossRefGoogle Scholar
Record, M. T. JrAnderson, C. F., & Lohman, T. M. (1978). Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening, and ion effects on water activity. Q. Rev. Biophys. 00, 000–000.Google Scholar
Record, M. T. JrdeHaseth, P. L. & Lohman, T. M. (1977). Interpretation of monovalent and divalent ion effects on the lac repressor-operator interaction. Biochemistry, N. Y. 16, 47914796.CrossRefGoogle ScholarPubMed
Record, M. T. JrLohman, T. M. & De, Haseth P. L. (1976). Ion effects on ligand-nucleic acid interactions. J. molec. Biol. 107, 145158.CrossRefGoogle ScholarPubMed
Record, M. T. JrWoodbury, C. P. & Lohman, T. M. (1976). Na+ effects on transitions of DNA and polynucleotides of variable linear charge density. Biopolymers 15, 893915.CrossRefGoogle ScholarPubMed
Reuben, J.Shporer, M. & Gabbay, E. J. (1975). The alkali-ion-DNA interaction as reflected in the nuclear relaxation rates of 23Na and 87Rb. Proc. natn Acad. Sci. U.S.A. 72, 245247.CrossRefGoogle Scholar
Revzin, A. & Neumann, E. (1974) Conformation changes in rRNA induced by electric impulses. Biophys. Chem. 2, 144150.CrossRefGoogle ScholarPubMed
Revzin, A. & Von, Hippel P. H. (1977). Direct measurements of association constants for the binding of Escherichia coli lac repressor to non-operator DNA. Biochemistry, N. Y. 16, 47694776.CrossRefGoogle ScholarPubMed
Richmond, T. J. & Steitz, T. A. (1976). Protein-DNA interaction investigated by binding Escherichia coli lac repressor protein to poiy [d(A. U-HgX)]. J. molec. Biol. 103, 2538.CrossRefGoogle Scholar
Riemer, S. C. & Bloomfield, V. A. (1978). Packaging of DNA in bacteriophage heads; some considerations on energetics. Biopolymers 17, 785794.CrossRefGoogle ScholarPubMed
Riggs, A. D.Bourgeois, S. & Cohn, M. (1970). The lac repressor-operator interaction. III. Kinetic studies. J. molec. Biol. 53, 401417.CrossRefGoogle Scholar
Robinson, B. A. & Stokes, R. H. (1959). Electrolyte Solutions. London: Butterworths.Google Scholar
Ross, P. D. & Scruggs, R. L. (1964). Electrophoresis of DNA. III. The effect of several univalent electrolytes on the mobility of DNA. Biopolymers 2, 231236.CrossRefGoogle Scholar
Ross, P. D. & Shapiro, J. T. (1974). Heat of interaction of DNA with polylysine, spermine, and Mg++. Biopolymers 13, 415416.CrossRefGoogle ScholarPubMed
Ross, P. D. & Sturtevant, J. M. (1960). The kinetics of double helix formation from polyriboadenylic acid and polyribouridylic acid. Proc. natn Acad. Sci. U.S.A. 46, 13601365.CrossRefGoogle ScholarPubMed
Schildkraut, C. & Lifson, S. (1965). Dependence of the melting temperature of DNA on salt concentration. Biopolymers 3, 195208.CrossRefGoogle ScholarPubMed
Seeman, N. C.Rosenberg, J. M.Suddath, F. L.Kim, J. J. P. & Rich, A. (1976). RNA double-helical fragments at atomic resolution: I. The crystal and molecular structure of sodium adenylyl-3',5'-uridine hexahydrate. J. molec. Biol. 104, 109144.CrossRefGoogle ScholarPubMed
Shapiro, J. T.Leng, M. & Felsenfeld, G. (1969 a). Deoxyribonucleic acid—polylysine complexes. Structure and nucleotide specificity. Biochemistry, N. Y. 8, 32193232.CrossRefGoogle ScholarPubMed
Shapiro, J. T.Stannard, B. S. & Felsenfeld, G. (1969b). The binding of small cations to deoxyribonucleic acid. Nucleotide specificity. Biochemistry, N. Y. 8, 32333241.CrossRefGoogle ScholarPubMed
Skerjanc, J. & Strauss, U. P. (1968). Interactions of polyelectrolytes with simple electrolytes. III. The binding of magnesium ion by deoxyribonucleic acid. J. Am. Chem. Soc. 90, 30813085.CrossRefGoogle Scholar
Spegt, P. & Weill, G. (1976). Magnetic resonance distinction between site bound and atmospherically bound paramagnetic counter-ions in polyelectrolyte solutions. Biophys. Chem. 4, 143149.CrossRefGoogle Scholar
Stannard, B. S. & Felsenfeld, G. (1975). The conformation of polyriboadenylic acid at low temperature and neutral pH. A single-stranded rodlike structure. Biopolymers 14, 299307.CrossRefGoogle Scholar
Strauss, U. P. (1974). Short-range interactions between polyions and small ions. In Polyeiectrolytes (ed. Selegny, E.), Dordrecht-Holland: Reidel.Google Scholar
Strauss, U. P. & Siegel, A. (1963). Counterion binding by polyelectrolytes VI. The binding of magnesium ion by polyphosphates in aqueous solutions. J. Phys. Chem. 67, 26832687.CrossRefGoogle Scholar
Studier, F. W. (1969). Effects of the conformation of single-stranded DNA on renaturation and aggregation. J. molec. Biol. 41, 199209.CrossRefGoogle ScholarPubMed
Tunis, M. J. B. & Hearst, J. E. (1968). On the hydration of DNA. II. Base composition dependence of the net hydration of DNA. Biopolymers 6, 13451353.CrossRefGoogle Scholar
Weintraub, H.Palter, K. & Van, Lente F. (1975). Histones H2a, H2b, H3, and H4 form a tetrameric complex in solutions of high salt. Cell 6, 85110.CrossRefGoogle Scholar
Wetmur, J. G. (1976). Hybridization and renaturation kinetics of nucleic acids. A. Rev. Biophys. Bioeng. 5, 337361.CrossRefGoogle ScholarPubMed
Wetmur, J. G. & Davidson, N. (1968). Kinetics of renaturation of DNA. J. molec. Biol. 31, 349370.CrossRefGoogle ScholarPubMed
Zana, R.Tondre, C.Rinaudo, M. & Milas, M. (1971). Étude ultrasonore de la fixation sur site des ions alcalins sur des carboxymethylcelluloses de densité de charge variable. J. Chim. phys. Physicochim. Biol. 68, 12581266.CrossRefGoogle Scholar
Zubay, G. & Doty, P. (1958). Nucleic acid interactions with metal ions and amino acids. Biochim. biophys. Acta 29, 4758.CrossRefGoogle ScholarPubMed