Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1992 Jun;61(6):1443–1453. doi: 10.1016/S0006-3495(92)81950-1

Determination of electrostatic potentials at biological interfaces using electron-electron double resonance.

Y K Shin 1, W L Hubbell 1
PMCID: PMC1260440  PMID: 1319760

Abstract

A new general method for the determination of electrostatic potentials at biological surfaces is presented. The approach is based on measurement of the collision frequency of a charged nitroxide in solution with a nitroxide fixed to the surface at the point of interest. The collision frequency is determined with 14N:15N double label electron-electron double resonance (ELDOR). As a test, the method is shown to give values for phospholipid bilayer surface potentials consistent with the Gouy-Chapman theory, a simple model shown by many independent tests to accurately describe charged, planar surfaces. In addition, the method is applied to determine the electrostatic potential near the surface of DNA. The results indicate that the potential is significantly smaller than that predicted from Poisson-Boltzmann analysis, but is in qualitative agreement with that predicted by Manning's theory of counter ion condensation. The method is readily extended to measurement of surface potentials of proteins.

Full text

PDF
1443

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abraham Z. H., Agbandje M., Neidle S., Acheson R. M. Experimental DNA-binding and computer modelling studies on an analogue of the anti-tumor drug amsacrine. J Biomol Struct Dyn. 1988 Dec;6(3):471–488. doi: 10.1080/07391102.1988.10506501. [DOI] [PubMed] [Google Scholar]
  2. Altenbach C., Flitsch S. L., Khorana H. G., Hubbell W. L. Structural studies on transmembrane proteins. 2. Spin labeling of bacteriorhodopsin mutants at unique cysteines. Biochemistry. 1989 Sep 19;28(19):7806–7812. doi: 10.1021/bi00445a042. [DOI] [PubMed] [Google Scholar]
  3. Anderson C. F., Record M. T., Jr, Hart P. A. Sodium-23 NMR studies of cation-DNA interactions. Biophys Chem. 1978 Jan;7(4):301–316. doi: 10.1016/0301-4622(78)85007-8. [DOI] [PubMed] [Google Scholar]
  4. Armstrong R. W., Kurucsev T., Strauss U. P. The interaction between acridine dyes and deoxyribonucleic acid. J Am Chem Soc. 1970 May 20;92(10):3174–3181. doi: 10.1021/ja00713a041. [DOI] [PubMed] [Google Scholar]
  5. Cafiso D. S., Hubbell W. L. Estimation of transmembrane potentials from phase equilibria of hydrophobic paramagnetic ions. Biochemistry. 1978 Jan 10;17(1):187–195. doi: 10.1021/bi00594a028. [DOI] [PubMed] [Google Scholar]
  6. Castle J. D., Hubbell W. L. Estimation of membrane surface potential and charge density from the phase equilibrium of a paramagnetic amphiphile. Biochemistry. 1976 Nov 2;15(22):4818–4831. doi: 10.1021/bi00667a011. [DOI] [PubMed] [Google Scholar]
  7. Denny W. A., Atwell G. J., Baguley B. C. Potential antitumor agents. 39. Anilino ring geometry of amsacrine and derivatives: relationship to DNA binding and antitumor activity. J Med Chem. 1983 Nov;26(11):1625–1630. doi: 10.1021/jm00365a014. [DOI] [PubMed] [Google Scholar]
  8. Eisenberg M., Gresalfi T., Riccio T., McLaughlin S. Adsorption of monovalent cations to bilayer membranes containing negative phospholipids. Biochemistry. 1979 Nov 13;18(23):5213–5223. doi: 10.1021/bi00590a028. [DOI] [PubMed] [Google Scholar]
  9. Hubbell W. L. Transbilayer coupling mechanism for the formation of lipid asymmetry in biological membranes. Application to the photoreceptor disc membrane. Biophys J. 1990 Jan;57(1):99–108. doi: 10.1016/S0006-3495(90)82510-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jayaram B., Sharp K. A., Honig B. The electrostatic potential of B-DNA. Biopolymers. 1989 May;28(5):975–993. doi: 10.1002/bip.360280506. [DOI] [PubMed] [Google Scholar]
  11. Klement R., Soumpasis D. M., Jovin T. M. Computation of ionic distributions around charged biomolecular structures: results for right-handed and left-handed DNA. Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4631–4635. doi: 10.1073/pnas.88.11.4631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kornberg R. D., McConnell H. M. Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry. 1971 Mar 30;10(7):1111–1120. doi: 10.1021/bi00783a003. [DOI] [PubMed] [Google Scholar]
  13. Manning G. S. The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Q Rev Biophys. 1978 May;11(2):179–246. doi: 10.1017/s0033583500002031. [DOI] [PubMed] [Google Scholar]
  14. McLaughlin S., Harary H. The hydrophobic adsorption of charged molecules to bilayer membranes: a test of the applicability of the stern equation. Biochemistry. 1976 May 4;15(9):1941–1948. doi: 10.1021/bi00654a023. [DOI] [PubMed] [Google Scholar]
  15. McLaughlin S. The electrostatic properties of membranes. Annu Rev Biophys Biophys Chem. 1989;18:113–136. doi: 10.1146/annurev.bb.18.060189.000553. [DOI] [PubMed] [Google Scholar]
  16. Northrup S. H., Wensel T. G., Meares C. F., Wendoloski J. J., Matthew J. B. Electrostatic field around cytochrome c: theory and energy transfer experiment. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9503–9507. doi: 10.1073/pnas.87.23.9503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Popp C. A., Hyde J. S. Electron-electron double resonance and saturation-recovery studies of nitroxide electron and nuclear spin-lattice relaxation times and Heisenberg exchange rates: lateral diffusion in dimyristoyl phosphatidylcholine. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2559–2563. doi: 10.1073/pnas.79.8.2559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rodgers K. K., Pochapsky T. C., Sligar S. G. Probing the mechanisms of macromolecular recognition: the cytochrome b5-cytochrome c complex. Science. 1988 Jun 17;240(4859):1657–1659. doi: 10.1126/science.2837825. [DOI] [PubMed] [Google Scholar]
  19. Sakore T. D., Jain S. C., Tsai C. C., Sobell H. M. Mutagen-nucleic acid intercalative binding: structure of a 9-aminoacridine: 5-iodocytidylyl(3'-5')guanosine crystalline complex. Proc Natl Acad Sci U S A. 1977 Jan;74(1):188–192. doi: 10.1073/pnas.74.1.188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Salemme F. R. An hypothetical structure for an intermolecular electron transfer complex of cytochromes c and b5. J Mol Biol. 1976 Apr 15;102(3):563–568. doi: 10.1016/0022-2836(76)90334-x. [DOI] [PubMed] [Google Scholar]
  21. Sharp K., Fine R., Honig B. Computer simulations of the diffusion of a substrate to an active site of an enzyme. Science. 1987 Jun 12;236(4807):1460–1463. doi: 10.1126/science.3589666. [DOI] [PubMed] [Google Scholar]
  22. Sinha B. K., Chignell C. F. Acridine spin labels as probes for nucleic acids. Life Sci. 1975 Dec 15;17(12):1829–1836. doi: 10.1016/0024-3205(75)90466-x. [DOI] [PubMed] [Google Scholar]
  23. Sinha B. K., Cysyk R. L., Millar D. B., Chignell C. F. Synthesis and biological properties of some spin-labeled 9-aminoacridines. J Med Chem. 1976 Aug;19(8):994–998. doi: 10.1021/jm00230a002. [DOI] [PubMed] [Google Scholar]
  24. Sundberg S. A., Hubbell W. L. Investigation of surface potential asymmetry in phospholipid vesicles by a spin label relaxation method. Biophys J. 1986 Feb;49(2):553–562. doi: 10.1016/S0006-3495(86)83665-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tanious F. A., Yen S. F., Wilson W. D. Kinetic and equilibrium analysis of a threading intercalation mode: DNA sequence and ion effects. Biochemistry. 1991 Feb 19;30(7):1813–1819. doi: 10.1021/bi00221a013. [DOI] [PubMed] [Google Scholar]
  26. Todd A. P., Cong J., Levinthal F., Levinthal C., Hubbell W. L. Site-directed mutagenesis of colicin E1 provides specific attachment sites for spin labels whose spectra are sensitive to local conformation. Proteins. 1989;6(3):294–305. doi: 10.1002/prot.340060312. [DOI] [PubMed] [Google Scholar]
  27. Wensel T. G., Chang C. H., Meares C. F. Diffusion-enhanced lanthanide energy-transfer study of DNA-bound cobalt(III) bleomycins: comparisons of accessibility and electrostatic potential with DNA complexes of ethidium and acridine orange. Biochemistry. 1985 Jun 4;24(12):3060–3069. doi: 10.1021/bi00333a039. [DOI] [PubMed] [Google Scholar]
  28. Wilson W. D., Krishnamoorthy C. R., Wang Y. H., Smith J. C. Mechanism of intercalation: ion effects on the equilibrium and kinetic constants for the interaction of propidium and ethidium with DNA. Biopolymers. 1985 Oct;24(10):1941–1961. doi: 10.1002/bip.360241008. [DOI] [PubMed] [Google Scholar]
  29. Winiski A. P., Eisenberg M., Langner M., McLaughlin S. Fluorescent probes of electrostatic potential 1 nm from the membrane surface. Biochemistry. 1988 Jan 12;27(1):386–392. doi: 10.1021/bi00401a058. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES