Electrostatic properties of membranes containing acidic lipids and adsorbed basic peptides: Theory and experiment

Biophysical Journal

Volumn 77, Issue 6, 1999, Pages 3176-3188

  Murray, Diana ^a,c   Arbuzova, Anna ^a   Hangyás Mihályné, Gyöngyi ^a   Gambhir, Alok ^a   Ben Tal, Nir ^b   Honig, Barry ^c   McLaughlin, Stuart ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

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

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE DERIVATIVE; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE;

ADSORPTION; ARTICLE; ELECTRIC POTENTIAL; MEMBRANE BINDING; PROTEIN LIPID INTERACTION; SURFACE CHARGE;

EID: 0032763121     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77148-1     Document Type: Article

References (69)

1. Akashi, K., H. Miyata, H. Itoh, and K. Kinosita, Jr. 1996. Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope. Biophys. J. 71:3242-3250.
2. Allen, L. A., and A. Aderem. 1995. A role for MARCKS, the α isozyme of protein kinase C and myosin I in zymosan phagocytosis by macrophages. J. Exp. Med. 182:829-840.
3. Allen, L. A., and A. Aderem. 1996. Mechanisms of phagocytosis. Curr. Opin. Immunol. 8:36-40.
4. Bangham, A. D., M. W. Hill, and N. G. A. Miller. 1974. Preparation and use of liposomes: models of biological membranes. Methods Membr. Biol. 1:1-68.
5. Barlow, C. A., and J. R. MacDonald. 1967. Theory of discreteness of charge effects in the electrolyte compact double layer. Adv. Electrochem. Electrochem. Eng. 6:1-194.
6. Ben-Tal, N., B. Honig, C. Miller, and S. McLaughlin. 1997. Electrostatic binding of proteins to membranes: theoretical prediction and experimental results with charybdotoxin and phospholipid vesicles. Biophys. J. 73:1717-1727.
7. 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.
8. Bhatnagar, R. S., and J. I. Gordon. 1997. Understanding covalent modifications of proteins by lipids: where cell biology and biophysics mingle. Trends Cell Biol. 7:14-21.
9. 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. Comp. Chem. 4:187-217.
10. 2-terminus of Src. Biochemistry. 33:13093-13101.
11. Cafiso, D., A. McLaughlin, S. McLaughlin, and A. Winiski. 1989. Measuring electrostatic potentials adjacent to membranes. Methods Enzymol. 171:342-364.
12. Chatelier, R. C., and A. P. Minton. 1996. Adsorption of globular proteins on locally planar surfaces: models for the effect of excluded area and aggregation of adsorbed protein on adsorption equilibria. Biophys. J. 71:2367-2374.
13. Dell'Acqua, M. L., M. C. Faux, J. Thorburn, A. Thorburn, and J. D. Scott. 1998. Membrane-targeting sequences on AKAP79 bind phosphatidyl-4,5-bisphosphate. EMBO J. 17:2246-2260.
14. Denisov, G., S. Wanaski, P. Luan, M. Glaser, and S. McLaughlin. 1997. Binding of basic peptides to membranes produces lateral domains enriched in the acidic lipids phosphatidylserine and phosphatidylinositol 4,5-bisphosphate: an electrostatic model and experimental results. Biophys. J. 74:731-744.
15. Epand, R. M., C. Stevenson, R. Bruins, V. Schram, and M. Glaser. 1998. The chirality of phosphatidylserine and the activation of protein kinase C. Biochemistry. 37:12068-12073.
16. Garnier, L., B. Bowzard, and J. W. Wills. 1998. Recent advances and remaining problems in HIV assembly. AIDS. 12:S5-S16.
17. Ghomashchi, F., X. Zhang, L. Liu, and M. H. Gelb. 1995. Binding of prenylated and polybasic peptides to membranes: affinities and intervesicle exchange. Biochemistry. 34:11910-11918.
18. Glaser, M., S. Wanaski, C. A. Buser, V. Boguslavsky, W. Rashidzada, A. Morris, M. Rebecchi, S. F. Scarlata, L. W. Runnels, G. D. Prestwich, J. Chen, A. Aderem, J. Ahn, and S. McLaughlin. 1996. MARCKS produces reversible inhibition of phospholipase C by sequestering phosphatidylinositol 4,5-bisphosphate in lateral domains. J. Biol. Chem. 271:26187-26193.
19. Grahame, D. C. 1958. Discreteness-of-charge-effects in the inner region of the electrical double layer. Z. Elektrochem. 62:264-274.
20. Hartsel, S. C., and D. S. Cafiso. 1986. A test of the discreteness-of-charge effects in phospholipid vesicles. Biochemistry. 25:8214-8219.
21. Heimburg, T., B. Angerstein, and D. Marsh. 1999. Binding of peripheral proteins to mixed lipid membranes: effect of lipid demixing upon binding. Biophys. J. 76:2575-2586.
22. 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.
23. Holst, M. 1993. Numerical solutions to the finite-difference Poisson-Boltzmann equation. Ph.D. thesis, University of Illinois.
24. Holst, M., and F. Saied. 1993. Multigrid solution of the Poisson-Boltzmann equation. J. Comp. Chem. 14:105-113.
25. Honig, B. H., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
26. 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.
27. Hunter, R. J. 1981. Zeta Potential in Colloid Science. Academic Press, New York.
28. Kaplan, J. M., H. E. Varmus, and J. M. Bishop. 1990. The src protein contains multiple domains for specific attachment to membranes. Mol. Cell. Biol. 10:1000-1009.
29. Keller, S. L., W. H. Pitcher, III, W. H. Huestis, and H. M. McConnell. 1998. Red blood cell lipids form immiscible liquids. Phys. Rev. Lett. 81:5019-5022.
30. 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.
31. 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.
32. Kleinschmidt, J. H., and D. Marsh. 1997. Spin-label electron spin resonance studies on the interactions of lysine peptides with phospholipid membranes. Biophys. J. 73:2546-2555.
33. Knoblich, J. A., L. Y. Jan, and Y. N. Jan. 1997. The N terminus of the Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization. Proc. Natl. Acad. Sci. USA. 94: 13005-13010.
34. Kwok, R., and E. Evans. 1981. Thermoelasticity of large lecithin bilayer vesicles. Biophys. J. 35:637-652.
35. Leventis, R., and J. R. Silvius. 1998. Lipid-binding characteristics of the polybasic carboxy-terminal sequence of K-ras4B. Biochemistry. 37: 7640-7648.
36. Levine, S., J. Mingins, and G. M. Bell. 1967. The discrete ion-effect in ionic double-layer theory. J. Electroanal. Chem. 13:280-329.
37. Liu, J., P. Oh, T. Horner, R. A. Rogers, and J. E. Schnitzer. 1997. Organized endothelial cell surface signal transduction in caveołae distinct from glycosylphosphatidylinositol-anchored protein microdomains. J. Biol. Chem. 272:7211-7222.
38. Liu, Y., L. Casey, and L. J. Pike. 1998. Compartmentalization of phosphatidlyinositol 4,5-bisphosphate in low-density membrane domains in the absence of caveolin. Biochem. Biophys. Res. Commun. 245: 684-690.
39. Maier, B., and J. O. Rädler. 1999. Conformation and self-diffusion of single DNA molecules confined to two dimensions. Phys. Rev. Lett. 82:1911-1914.
40. Martin, T. F. J. 1998. Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu. Rev. Cell Dev. Biol. 14:231-264.
41. McConnell, H. M. 1991. Structures and transitions in lipid monolayers at the air-water interface. Annu. Rev. Phys. Chem. 42:171-195.
42. McIlroy, B. K., J. D. Walters, and J. D. Johnson. 1991. A continuous fluorescence assay for protein kinase C. Anal. Biochem. 195:148-152.
43. McLaughlin, S. 1989. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18:113-136.
44. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20:272-276.
45. McLaughlin, S., N. Mulrine, T. Gresalfi, G. Vaio, and A. McLaughlin. 1981. Adsorption of divalent cations to bilayer membranes containing phosphatidylserine. J. Gen. Physiol. 77:445-473.
46. Möhwald, H. 1990. Phospholipid and phospholipid-protein monolayers and the air/water interface. Annu. Rev. Phys. Chem. 41:441-476.
47. Mosior, M., and S. McLaughlin. 1991. Peptides that mimic the pseudosubstrate region of protein kinase C bind to acidic lipids in membranes. Biophys. J. 60:149-159.
48. Mosior, M., and S. McLaughlin. 1992. Binding of basic peptides to acidic lipids in membranes: effects of inserting alanine(s) between the basic residues. Biochemistry. 31:1767-1773.
49. Mouritsen, O. G., and K. Jørgensen. 1997. Small-scale lipid-membrane structure: simulation versus experiment. Curr. Opin. Struct. Biol. 7:518-527.
50. Murray, D., N. Ben-Tal, B. Honig, and S. McLaughlin. 1997. Electrostatic interaction of myristoylated proteins with membranes: simple physics, complicated biology. Structure. 5:985-989.
51. Murray, D., L. Hermida-Matsumoto, C. A. Buser, J. Tsang, C. Sigal, N. Ben-Tal, B. Honig, M. D. Resh, and S. McLaughlin. 1998. Electrostatics and the membrane association of Src: theory and experiment. Biochemistry. 37:2145-2159.
52. Needham, D. 1993. Measurement of interbilayer adhesion energies. Methods Enzymol. 220:111-129.
53. Newton, A. C., and J. E. Johnson. 1998. Protein kinase C: a paradigm for regulation of protein function by two membrane-targeting modules. Biochim. Biophys. Acta. 1376:155-172.
54. 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.
55. Pitcher, J. A., N. J. Freedman, and R. J. Lefkowitz. 1998. G protein-coupled receptor kinases. Annu. Rev. Biochem. 67:653-692.
56. Prendergast, F. G., M. Meyer, G. L. Carlson, S. Iida, and J. D. Potter. 1983. Synthesis, spectral properties, and use of 6-acryloyl-2-dimethyIaminonaphthalene (acrylodan). J. Biol. Chem. 258:7541-7544.
57. Resh, M. D. 1996. Regulation of cellular signalling by fatty acid acylation and prenylation of signal transduction proteins. Cell. Signal. 8:403-412.
58. 2+-binding domain. J. Biol. Chem. 273:15879-15882.
59. Roa, V. D., S. Misra, I. V. Boronenkov, R. A. Anderson, and J. H. Hurley. 1998. Structure of type IIβ phosphatidylinositol phosphate kinase: a protein kinase fold flattened for interfacial phosphorylation. Cell. 94: 829-839.
60. 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.
61. Seykora, J. T., M. M. Myat, L. A. Allen, J. V. Ravetch, and A. Aderem. 1996. Molecular determinants of the myristoyl-electrostatic switch of MARCKS. J. Biol. Chem. 271:18797-18802.
62. Sigal, C. T., W. Zhou, C. A. Buser, S. McLaughlin, and M. D. Resh. 1994. The amino terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Proc. Natl. Acad. Sci. USA. 91:12253-12257.
63. Sutton, R. B., D. Fasshauer, R. Jahn, and A. T. Brunger. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature. 395:347-353.
64. Swierczynski, S. L., and P. J. Blackshear. 1996. Myristoylation-dependent and electrostatic interactions exert independent effects on the membrane association of the myristoylated alanine-rich C-kinase substrate. J. Biol. Chem. 271:23424-23430.
65. Toner, M., G. Vaio, A. McLaughlin, and S. McLaughlin. 1988. Adsorption of cations to phosphatidylinositol 4,5-bisphosphate. Biochemistry. 27: 7435-7443.
66. Winiski, A. P., A. C. McLaughlin, R. V. McDaniel, M. Eisenberg, and S. McLaughlin. 1986. An experimental test of the discreteness-of-charge effect in positive and negative lipid bilayers. Biochemistry. 25: 8206-8214.
67. 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.
68. Yang, L., and M. Glaser. 1996. Formation of membrane domains during the activation of protein kinase C. Biochemistry. 35:13966-13974.
69. 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.