Electrostatic binding of proteins to membranes. Theoretical predictions and experimental results with charybdotoxin and phospholipid vesicles

Biophysical Journal

Volumn 73, Issue 4, 1997, Pages 1717-1727

  Ben Tal, Nir ^a   Honig, Barry ^a   Miller, Christopher ^b   McLaughlin, Stuart ^c  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHARYBDOTOXIN; IBERIOTOXIN; MEMBRANE PROTEIN; PHOSPHOLIPID; SODIUM CHLORIDE;

ARTICLE; ELECTRICITY; IONIC STRENGTH; MEMBRANE BINDING; PH; PHOSPHOLIPID BILAYER; PHOSPHOLIPID VESICLE; PREDICTION; PROTEIN BINDING; PROTEIN STRUCTURE; THEORY;

EID: 0030754783     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78203-1     Document Type: Article

References (71)

1. Aderem, A. 1992. The MARCKS brothers: a family of protein kinase c substrates. Cell. 71:713-716.
2. Andersen, O. S. 1978. Membrane Transport in Biology, Vol. 1, Chap. 11. G. Giebisch, D. C. Tosteson, and H. H. Ussing, editors. Springer-Verlag, New York.
3. + channels. Effects of channel gating, voltage, and ionic strength. J. Gen. Physiol. 91:317-333.
4. Ben-Tal, N. 1995. The energetics of colloids; do oppositely charged particles necessarily attract each other? J. Phys. Chem. 99:9642-9645.
5. Ben-Tal, N., B. Honig, R. M. Peitzsch, G. Denisov, and S. McLaughlin. 1996. Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results. Biophys. J. 71: 561-575.
6. Blackshear, P. J. 1993. The MARCKS family of cellular protein kinase c substrates. J. Biol. Chem. 268:1501-1504.
7. Bockris, J. O'M., and S. U. M. Khan. 1993. Surface Electrochemistry. Plenum and Rosetta edition, New York, 63-64.
8. Bontems, F., B. Gilquin, C. Roumestand, A. Menez, and F. Toma. 1992. Analysis of side-chain organization on a refined model of charybdotoxin: structural and functional implications. Biochemistry. 31: 7756-7764.
9. Bontems, F., C. Roumestand, P. Boyot, B. Gilquin, Y. Doljansky, A. Menez, and F. Toma. 1991a. Eur. J. Biochem. 196:19-28.
10. Bontems, F., C. Roumestand, B. Gilquin, A. Menez, and F. Toma. 1991b. Refined structure of charybdotoxin: common motifs in scorpion toxins and insect defensins. Science. 254:1521-1523.
11. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
12. Buser, C. A., and S. McLaughlin. 1997. Ultacentrifugation technique for measuring the binding of peptides and proteins to sucrose-loaded phospholipid vesicles. Methods Mol. Biol. (In the press).
13. Buser, C. A., C. T. Sigal, M. D. Resh, and S. McLaughlin. 1994. Membrane binding of myristoylated peptides corresponding to the NH2 terminus of Src. Biochemistry. 33:13093-13101.
14. Cadwallader, K. A., H. Paterson, S. G. Macdonald, and J. F. Hancock. 1994. N-terminally myristoylated Ras proteins require palmitoylation or a polybasic domain for plasma membrane localization. Mol. Cell. Biol. 14:4722-4730.
15. Chothia, C. 1976. The nature of the accessible and buried surface in proteins. J. Mol. Biol. 105:1-14.
16. Damodaran, K. V., and K. M. Merz, Jr. 1996. Bilayer-peptide interactions. In Biological Membranes. K. Merz, Jr., and B. Roux, editors. Birkhauser, Boston.
17. Froloff, N., A. Windemuth, and B. Honig. 1997. On the calculation of binding free energies using continuum methods: Application to MHC class I protein-peptide interactions. Protein Sci. (in press.)
18. Ganz, T., and R. I. Lehrer. 1995. Defensins. Pharmacol. & Ther. 66: 191-205.
19. + channel. Biophys. J. 65:1613-1619.
20. Hancock, J. F., H. Paterson, and C. J. Marshall. 1990. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell. 63:133-139.
21. Heimburg, T., and D. Marsh. 1995. Protein surface-distribution and protein-protein interactions in the binding of peripheral proteins to charged lipid membranes. Biophys. J. 68:536-546.
22. Heimburg, T., and D. Marsh. 1996. Thermodynamics of the interation of proteins with lipid membranes. In Biological Membranes. K. Merz, Jr., and B. Roux, editors. Birkhauser, Boston.
23. Hermann, R. B. 1972. Theory of hydrophobic binding. II. The correlation of hydrocarbon solubility in water with solvent cavity area. J. Phys. Chem. 76:2754-2759.
24. Hill, C. P., D. P. Bancroft, A. M. Christensen, and W. I. Sundquist. 1996. Crystal structures of the trimeric human immunodeficiency virus type I matrix protein: implications for membrane binding and assembly. Proc. Natl. Acad. Sci. USA. 93:3099-3104.
25. Honig, B., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
26. Honig, B., K. Sharp, and A.-S. Yang. 1993. Macroscopic models of aqueous solutions: biological and chemical applications. J. Phys. Chem. 97:1101-1109.
27. Hope, M. J., M. B. Bally, G. Webb, and P. R. Cullis. 1985. Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume, and ability to maintain a membrane potential. Biochim. Biophys. Acta. 812:55-65.
28. 1H-nuclear magnetic resonance spectroscopy. Biochemistry. 31:8151-8159.
29. Kim, J., M. Mosior, L. A. Chung, H. Wu, and S. McLaughlin. 1991. Binding of peptides with basic residues to membranes containing acidic phospholipids. Biophys. J. 60:135-148.
30. Li, M., N. Unwin, K. A. Stauffer, Y. N. Jan, and L. Y. Jan. 1994. Images of purified Shaker potassium channels. Curr. Biol. 4:110-115.
31. MacNaughtan, W., K. A. Snook, E. Caspi, and N. P. Franks. 1985. An x-ray diffraction analysis of oriented lipid multilayers containing basic proteins. Biochim. Biophys. Acta. 818:132-148.
32. Massiah, M. A., M. R. Starich, C. Paschall, M. F. Summers, A. M. Christensen, and W. I. Sundquist. 1994. Three-dimensional structure of the human immunodeficiency virus type 1 matrix protein. J. Mol. Biol. 244:198-223.
33. McLaughlin, S. 1989. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18:113-136.
34. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. TIBS. 20: 272-276.
35. + channel receptor. Biochemistry. 29:5320-5325.
36. + channel-blocking peptides. Neuron. 15:5-10.
37. Mui, B. L.-S., P. R. Cullis, E. A. Evans, and T. D. Madden. 1993. Osmotic properties of large unilamellar vesicles prepared by extrusion. Biophys. J. 64:443-453.
38. Newton, A. C. 1995. Protein kinase C: structure, function, and regulation. J. Biol. Chem. 270:28495-28498.
39. Nicholls, A., K. A. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 11:281-296.
40. Nozaki, Y., and C. H. Tanford. 1971. The solubility of amino acids and two glycine peptides in aqueous ethanol and dioxane solutions. Establishment of a hydrophobicity scale. J. Biol. Chem. 246:2211-2217.
41. + channels. Proc. Natl. Acad. Sci. USA. 88:2046-2050.
42. Parsegian, A. 1969. Energy of ion crossing a low dielectric membrane: solution to four relevant electrostatic problems. Nature. 221:844-846.
43. Pastor, R. W. 1994. Molecular dynamics and monte carlo simulations of lipid bilayers. Curr. Opin. Struct. Biol. 4:486-492.
44. Peitzsch, R. M., M. Eisenberg, K. A. Sharp, and S. McLaughlin. 1995. Calculations of the electrostatic potential adjacent to model phospholipid bilayers. Biophys. J. 68:729-738.
45. Peitzsch, R. M., and S. McLaughlin. 1993. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry. 32:10436-10443.
46. Pinheiro, T. J. 1994. The interaction of horse heart cytochrome c with phospholipid bilayers. Structural and dynamic effects. Biochimie. 76: 489-500.
47. 31P-NMR. Biochemistry. 33:2451-2458.
48. Pinheiro, T. J., and A. Watts. 1994b. Resolution of individual lipids in mixed phospholipid membranes and specific lipid-cytochrome c interactions by magic-angle spinning solid-state phosphorus-31 NMR. Biochemistry. 33:2459-2467.
49. Rebecchi, M. J., A. A. Peterson, and S. McLaughlin. 1992. Phosphoinositide-specific phospholipase C-delta 1 binds with high affinity to phospholipid vesicles containing phosphatidylinositol 4,5-bisphosphate. Biochemistry. 31:12742-12747.
50. Resh, M. D. 1993. Interaction of tyrosine kinase oncoproteins with cellular membranes. Biochim. Biophys. Acta. 1155:307-322.
51. Resh, M. D. 1994. Myristylation and palmitylation of Src family members: the fats of the matter. Cell. 76:411-413.
52. Roberts, M. F. 1996. Phospholipases: structural and functional motifs for working at an interface. FASEB J. 10:1159-1172.
53. Roth, C. M., and A. M. Lenhoff. 1993. Electrostatic and van der Waals contributions to protein adsorption: computation of equilibrium constants. Langmuir. 9:962-972.
54. Roush, D. J., D. S. Gill, and R. C. Willson. 1994. Electrostatic potentials and electrostatic interaction energies of rat cytochrome b5 and a simulated anion-exchange adsorbent surface. Biophys. J. 66:1290-1300.
55. Shimony, E., T. Sun, L. Kolmakova-Partensy, and C. Miller. 1994. Engineering a uniquely reactive thiol into a cysteine-rich peptide. Protein Eng. 7:503-507.
56. Shrake, A., and J. A. Rupley. 1973. Solvent accessible surface area calculation. J. Mol. Biol. 79:351-371.
57. Sigal, C. T., W. Zhou, C. A. Buser, S. McLaughlin, and M. D. Resh. 1994. Amino-terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Proc. Natl. Acad. Sci. USA. 91:12253-12257.
58. Sitkoff, D., N. Ben-Tal, and B. Honig. 1996. Calculation of alkane to water solvation free energies using continuum solvent models. J. Phys. Chem. 100:2744-2752.
59. Sitkoff, D., K. Sharp, and B. Honig. 1994. Accurate calculations of hydration free energies using macroscopic solvent models. J. Phys. Chem. 98:1978-1988.
60. Sridharan, S., A. Nicholls, and B. Honig. 1992. A new vertex algorithm to calculate solvent accessible surface areas. Biophys. J. 61:174a. (Abstr.).
61. Stams, T., S. K. Nair, T. Okuyama, A. Waheed, W. S. Sly, and D. W. Christianson. 1996. Crystal structure of the secretory form of membrane-associated human carbonic anhydrase IV at 2.8-Å resolution. Proc. Natl. Acad. Sci. USA. 93:13589-13594.
62. Thorgeirsson, T. E., C. J. Russell, D. S. King, and Y. K. Shin. 1996. Direct determination of the membrane affinities of individual amino acids. Biochemistry. 35:1803-1809.
63. Torrie, G. M., J. P. Valleau, and G. N. Patey. 1982. Electrical double layer. II. Monte Carlo and HNC studies of image effects. J. Chem. Phys. 76:4615-4622.
64. White, S. H., W. C. Wimley, and A. S. Ladokhin. 1997. Protein folding in membranes: determining the energetics of peptide-bilayer interactions. Methods in Enzymology. M. L. Johnson and G. K. Ackers, editors. (in press).
65. White, S. H., W. C. Wimley, and M. E. Selsted. 1995. Structure, function, and membrane integration of defensins. Curr. Opin. Struct. Biol. 5:521-527.
66. Wimley, W. C., M. E. Selsted, and S. H. White. 1994. Interactions between human defensins and lipid bilayers: evidence for formation of multimeric pores. Protein Sci. 3:1362-1373.
67. Wimley, W. C., and S. H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Struct. Biol. 3:842-848.
68. Woolf, T. B., and B. Roux. 1996. Structure, energetics, and dynamics of lipid-protein interactions: a molecular dynamics study of the gramicidin A channel in a DMPC bilayer. Proteins. 24:92-114.
69. Yoon, B. J., and A. M. Lenhoff. 1992. Computation of the electrostatic interaction energy between a protein and a charged surface. J. Phys. Chem. 96:3130-3134.
70. Zhou, W., L. J. Parent, J. W. Wills, and M. D. Resh. 1994. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J. Virol. 68:2556-2569.
71. Zhou, F., and K. Schulten. 1995. Molecular dynamics study of a membrane-water interface. J. Phys. Chem. 99:2195-2207.