Binding of small basic peptides to membranes containing acidic lipids: Theoretical models and experimental results

Biophysical Journal

Volumn 71, Issue 2, 1996, Pages 561-575

  Ben Tal, Nir ^a   Honig, Barry ^a   Peitzsch, Robert M ^b   Denisov, Gennady ^b,c   McLaughlin, Stuart ^b  

^a Columbia University ^*  (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c INSTITUTE OF MATHEMATICAL PROBLEMS OF BIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCEROPHOSPHOLIPID; LYSINE; MEMBRANE LIPID; PEPTIDE; PHOSPHOLIPID; PHOSPHOLIPID DERIVATIVE; PHOSPHORYLCHOLINE;

AQUEOUS SOLUTION; ARTICLE; DIELECTRIC CONSTANT; HYDROPHILICITY; IONIC STRENGTH; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE MODEL; MEMBRANE VESICLE; PH; PROTEIN LIPID INTERACTION;

EID: 0029757155     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(96)79280-9     Document Type: Article

References (94)

1. Aderem, A. 1992. The MARCKS brothers: a family of protein kinase c substrates. Cell. 71:713-716.
2. Akutsu, H., and T. Nagamori. 1991. Conformational analysis of the polar head group in phosphatidylcholine bilayer: a structural change induced by cations. Biochemistry, 30:4510-4516.
3. Andersen, O. S. 1978. Permeability properties of unmodified lipid bilayer membranes. In Membrane Transport in Biology, Vol. 1. G. Giebisch, D. C. Tosteson, and H. H. Ussing, editors. Springer, New York. 371-446.
4. Ashcroft, R. G., H. G. L. Coster, and J. R. Smith. 1981. The molecular organization of biomolecular lipid membranes. The dielectric structure of the hydrophilic/hydrophobic interface. Biochim. Biophys. Acta. 643: 191-204.
5. Aveyard, R., and D. A. Haydon. 1973. Introduction to the Principles of Surface Chemistry. Cambridge: Cambridge University Press.
6. Ben-Tal, N. 1995. The energetics of colloids: do oppositely charged particles necessary attract each other? J. Phys. Chem. 99:9642-9645.
7. Ben-Tal, N., and R. D. Coalson. 1994. Dielectric constant effects on the energetics of oppositely charged colloids: a lattice field theory study. J. Chem. Phys. 101:5148-5166.
8. Blackshear, P. J. 1993. The MARCKS family of cellular protein kinase c substrates. J. Biol. Chem. 268:1501-1504.
9. Bockris, J. O'M., and S. U. M. Khan. 1993. Surface Electrochemistry. Plenum, New York, and Rosetta edition. 63-64.
10. 1. Biochemistry. 33:3032-3037.
11. 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.
12. 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.
13. Büldt, G., H. U. Gaily, A. Seelig, and G. Zaccai. 1979. Neutron diffraction studies on phosphatidylcholine model membrane. I. Head group conformation. J. Mol. Biol. 134:673-691.
14. Buser, C. A., J. Kim, S. McLaughlin, and R. M. Peitzsch. 1995. Does the binding of clusters of basic residues to acidic lipids induce domain formation in membranes? Mol. Membr. Biol. 12:69-75.
15. 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.
16. 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.
17. Chiu, S.-W., M. Clark, V. Balaji, S. Subramaniam, H. L. Scott, and E. Jakobsson. 1995. Incorporation of surface tension into molecular dynamics simulations of an interface: a fluid phase lipid bilayer membrane. Biophys. J. 69:1230-1245.
18. Chothia, C. 1976. The nature of the accessible and buried surface in proteins. J. Mol. Biol. 105:1-14.
19. Davis, M. E., and J. A. McCammon. 1990. Electrostatics in biomolecular structure and dynamics. Chem. Rev. 90:509-521.
20. de Kroon, A. I., J. A. Killian, J. de Gier, and B. de Kruijf. 1991. The membrane interaction of amphiphilic model peptides affects phosphatidylserine headgroup and acyl chain order and dynamics. Application of the "phospholipid headgroup electrometer" concept to phosphatidylserine. Biochemistry. 30:1155-1162.
21. de Kroon, A. I., M. W. Soekarjo, J. de Gier, and B. de Kruijff. 1990. The role of charge and hydrophobicity in peptide-lipid interaction: a comparative study based on tryptophan fluorescence measurements combined with the use of aqueous and Hydrophobic quenchers. Biochemistry. 29:8229-8240.
22. de Kruijff, B., A. Rietveld, N. Telders, and B. Vaandrager. 1985. Molecular aspects of the bilayer stabilization induced by poly(L-lysines) of varying size in cardiolipin liposomes. Biochim. Biophys. Acta, 820: 295-304.
23. Denisov, G., S. Wanaski, L. Peng, M. Glaser, and S. McLaughlin. 1996. Domain formation induced by binding of basic ligands to membranes containing acidic lipids: an electrostatic mechanism. Biophys. J. 70: A223.
24. Dufourcq, J., J. F. Faucon, R. Maget-Dana, M. P. Pileni, and C. Hélène. 1981. A fluorescence study of the binding of oligopeptides containing aromatic and basic residues to phospholipids vesicles. Biochim. Biophys. Acta. 649:67-75.
25. Essmann, U., L. Perera, and M. L. Berkowitz. 1995. On the origin of the hydration interaction of lipid bilayers from MD simulation of DPPC membranes in gel and liquid crystalline phases. Langmuir. 11: 4519-4534.
26. Fromherz, P. 1975. Instrumentation for handling monomolecular films at an air-water interface. Rev. Sci. Instrum. 46:1380-1385.
27. Gilson, M., K. A. Sharp, and B. Honig. 1988. Calculating the electrostatic potential of molecules in solution: method and error assessment. J. Comp. Chem. 9:327-335.
28. Hagler, A. T., E. Huler, and S. Lifson. 1974. Energy functions for peptides and proteins. I. Derivation of a consistent force field including the hydrogen bond from amide crystals. J. Am. Chem. Soc. 96:5319-5327.
29. 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.
30. Hauser, H., I. Pascher, R. H. Pearson, and S. Sundell. 1981. Preferred conformation and molecular packing of phosphatidylethanolamine and phosphatidylcholine. Biochim. Biophys. Acta. 650:21-51.
31. 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. 68:5436-5546.
32. Hendsch, Z. S., and B. Tidor. 1994. Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3:211-226.
33. Hermann, R. B. 1972. Theory of hydrophobic bonding. II. The correlation of hydrocarbon solubility in water with solvent cavity area. J. Phys. Chem. 76:2754-2759.
34. Holst, M. 1993. Numerical solutions to the finite difference Poisson-Boltzmann equation. PhD thesis. University of Illinois, Urbana, IL.
35. Hoist, M., and F. Saied. 1993. Numerical solutions of the Poisson-Boltzmann equation. J. Comp. Chem. 14:105-113.
36. Honig, B. H., and W. L. Hubbell. 1984. Stability of "salt bridges" in membrane proteins. Proc. Natl. Acad. Sci. USA. 81:5412-5416.
37. Honig, B., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
38. Honig, B., K. Sharp, and A.-S. Yang. 1993. Macroscopic models of aqueous solutions: biological and chemical applications. J. Phys. Chem. 97:1101-1109.
39. 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.
40. Israelachvili, J. N. 1992. Intermolecular and Surface Forces. Academic, New York.
41. Israelachvili, J. N., and H. Wennerström. 1996. Role of hydration and water structure in biological and colloidal interactions. Nature. 379: 219-225.
42. Kim, J., P. J. Blackshear, J. D. Johnson, and S. McLaughlin. 1994. Phosphorylation reverses the membrane association of peptides that correspond to the basic domains of MARCKS and neuromodulin. Biophys. J. 67:227-237.
43. 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.
44. Klapper, I., R. Hagstrom, R. Fine, K. Sharp, and B. Honig. 1986. Focusing of electrostatic fields in the active site of Cu-Zn Superoxide dismutase: effects of ionic strength and amino-acid modification. Proteins. 1:47-59.
45. 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.
46. Mclntoch, T. J., and S. A. Simon. 1994. Hydration and steric pressures between phospholipid bilayers. Annu. Rev. Biophys. Biomol. Struct. 23:27-51.
47. McLaughlin, S. 1989. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18:113-136.
48. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20:272-276.
49. Misra, V. K., J. L. Hecht, K. A. Sharp, R. A. Friedman, and B. Honig. 1994a. Salt effect on protein-DNA interactions: the λcl repressor and EcoRI endonuclease. J. Mol. Biol. 238:264-280.
50. Misra, V. K., K. A. Sharp, R. A. Friedman, and B. Honig. 1994b. Salt effect on ligand-DNA binding: minor groove binding antibiotics. J. Mol. Biol. 238:245-263.
51. Montich, G., S. Scarlata, S. McLaughlin, R. Lehrmann, and J. Seelig. 1993. Thermodynamic characterization of the association of small basic peptides with membranes containing acidic lipids. Biochim. Biophys. Acta. 1146:17-24.
52. Mosior, M., and S. McLaughlin. 1992a. Binding of basic peptides to acidic lipids in membranes: effects of inserting alanine(s) between the basic residues. Biochemistry. 31:1767-1773.
53. Mosior, M., and S. McLaughlin. 1992b. Electrostatics and reduction of dimensionality produce apparent cooperativity when peptides bind to acidic lipids in membranes. Biochim. Biophys. Acta. 1105:185-187.
54. 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.
55. Newton, A. C. 1995. Seeing two domains. Curr. Biol. 5:973-976.
56. Novotny, J., and K. Sharp. 1992. Electrostatic fields in antibodies and antibody/antigen complexes. Prog. Biophys. Mol. Biol. 58:203-224.
57. 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.
58. Parsegian, A. 1969. Energy of ion crossing a low dielectric membrane: solution to four relevant electrostatic problems. Nature. 221:844-846.
59. Pastor, R. W. 1994. Molecular dynamics and monte carlo simulations of lipid bilayers. Curr. Opin. Struct. Biol. 4:486-492.
60. Pearson, R. H., and I. Pascher. 1979. The molecular structure of lecithin dihydrate. Nature. 281:499-501.
61. 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.
62. 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.
63. 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.
64. Resh, M. D. 1993. Interaction of tyrosine kinase oncoproteins with cellular membranes. Biochim. Biophys. Acta. 1155:307-322.
65. Resh, M. D. 1994. Myristylation and palmitylation of Src family members: the fats of the matter. Cell. 76:411-413.
66. Rosen, A., K. F. Keenan, M. Thelen, A. C. Nairn, and A. Aderem. 1990. Activation of protein kinase C results in the displacement of its myristoylated, alanine-rich substrate from punctate structures in macrophage filopodia. J. Exp. Med. 172:1211-1215.
67. 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.
68. 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.
69. 31P NMR study of pentalysine interaction with headgroup deuterated phosphatidylcholine and phosphatidylserine. Eur. Biophys. J. 16:267-273.
70. Scherer, P. G., and J. Seelig. 1987. Structure and dynamics of the phosphatidylcholine and the phosphatidylethanoamine head group in L-M fibroblasts as studied by deuterium nuclear magnetic resonance. EMBO J. 6:2915-2922.
71. Seelig, A. 1987. Local anesthetics and pressure: a comparison of dibucaine binding to lipid monolayers and bilayers. Biochim. Biophys. Acta. 899: 196-204.
72. Seelig, A. 1992. Interaction of a substance P agonist and of substance P antagonists with lipid membranes. A thermodynamic analysis. Biochemistry. 31:2897-2904.
73. Seelig, J., P. M. Macdonald, and P. G. Scherer. 1987. Phospholipid head groups as sensors of electrostatic charge in membranes. Biochemistry. 26:7535-7541.
74. Sharp, K. A. 1994. Electrostatic interactions in macromolecules. Curr. Opin. Struct. Biol. 4:234-239.
75. Sharp, K. A., and B. Honig. 1990. Calculating total electrostatic energies with the nonlinear Poisson-Boltzmann equation. J. Phys. Chem. 94: 7684-7692.
76. 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.
77. 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.
78. Sitkoff, D., K. Sharp, and B. Honig. 1994. Accurate calculations of hydralion free energies using macroscopic solvent models. J. Phys. Chem. 98:1978-1988.
79. Smith, S. O., I. Kustanovich, S. Bhamidipati, A. Salmon, and J. A. Hamilton. 1992. Interfacial conformation of dipalmitoylglycerol and dipalmitoylphosphatidylcholine in phospholipid bilayers. Biochemistry. 31:11660-11664.
80. Slouch, T. R. 1993. Lipid membrane structure and dynamics studies by all-atom molecular dynamics simulations of hydrated phospholipid bilayers. J. Mol. Simulations. 10:335-362.
81. Sütton, R. B., B. A. Davletov, A. M. Berghuis, T. C. Sudof, and S. R. Sprang. 1995. Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold. Cell. 80:929-938.
82. Tachiya, M. 1994. Energetics of electron transfer reaction in polar solvents. Chem. Phys. Lett. 230:491-494.
83. Tamm, L. K. 1991. Membrane insertion and lateral mobility of synthetic amphiphilic signal peptides in lipid model membranes. Biochim. Biophys. Acta. 1071:123-148.
84. Thorgeirsson, T. E., Y. G. Yu, and Y.-K. Shin. 1995. A limiting law for the electrostatics of the binding of polypeptides to phospholipid bilayers. Biochemistry. 34:5518-5522.
85. 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.
86. Warshel, A. 1981. Electrostatic basis of structure-function correlation in proteins. Ace. Chem. Res. 14:284-290.
87. Warshel, A., and S. T. Russell. 1984. Calculations of electrostatic interactions in biological systems and in solutions. Q. Rev. Biophys. 17:283-422.
88. Warshel, A., and D. W. Schlosser. 1981. Electrostatic control of the efficiency of light-induced electron transfer across membranes. Proc. Natl. Acad. Sci. USA. 78:5564-5568.
89. Wiener, M. C., and S. H. White. 1992. Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure. Biophys. J. 61:434-447.
90. Yang, L., and M. Glaser. 1995. Membrane domains containing phosphatidylserine and substrate can be important for the activation of protein kinase C. Biochemistry. 34:1500-1506.
91. 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.
92. Zacharias, M., B. A. Luty, M. E. Davis, and J. A. McCammon. 1992. Poisson-Boltzmann analysis of the lambda repressor-operator interaction. Biophys. J. 63:1280-1285.
93. Zhou, F., and K. Schulten. 1995. Molecular dynamics study of a membrane-water interface. J. Phys. Chem. 99:2195-2207.
94. 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.