Lipid membrane domain formation and alamethicin aggregation studied by calorimetry, sound velocity measurements, and atomic force microscopy

Biophysical Chemistry

Volumn 134, Issue 3, 2008, Pages 168-177

  Oliynyk, Vitaliy ^a,b   Jäger, Markus ^a   Heimburg, Thomas ^b   Buckin, Vitaly ^c   Kaatze, Udo ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Alamethicin; Atomic force microscopy; Differential scanning calorimetry; Lipid membranes; Peptide pores; Sound velocity

Indexed keywords

ALAMETHICIN; PHOSPHORYLCHOLINE;

ARTICLE; ATOMIC FORCE MICROSCOPY; DIFFERENTIAL SCANNING CALORIMETRY; LIPID BILAYER; LIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; SOUND INTENSITY; TITRIMETRY; VELOCITY;

ALAMETHICIN; CALORIMETRY; HEAT; MEMBRANE LIPIDS; MICROSCOPY, ATOMIC FORCE; SOLUTIONS; TITRIMETRY;

EID: 41549149911     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2008.02.004     Document Type: Article

References (69)

1. Gennis R.B. Biomembranes: Molecular Structure and Function (1989)
2. Lipowsky R., and Sackmann E. Structure and Dynamics of Membranes vol. 1A (1995)
3. Zhang R., Sun W., Tristram-Nagle S., Headrick R.L., Suter R.M., and Nagle J.F. Critical fluctuations in membranes. Phys. Rev. Lett. 74 (1995) 2832
4. Mouritsen O.G., and Jorgensen K. Micro-, nano- and meso-scale heterogeneity of lipid bilayers and its influence on macroscopic membrane properties. Mol. Membr. Biol. 12 (1995) 15-20
5. Veatch S.L., Soubias O., Keller S.L., and Gawrisch K. Critical fluctuations in domain-forming lipid mixtures. PNAS 104 (2007) 17650-176505
6. Mouritsen O.G., and Jorgensen K. Small-scale lipid-membrane structure: simulation versus experiment. Curr. Opin. Struct. Biol. 7 (1997) 518-527
7. Heimburg T. A model for the lipid pretransition: coupling of ripple formation with the chain-melting transition. Biophys. J. 78 (2000) 1154-1165
8. Mouritsen O.G., and Jorgensen K. Dynamical order and disorder in lipid bilayers. Chem. Phys. Lipids 73 (1994) 3-25
9. Halstenberg S., Schrader W., Das P., Bhattacharjee J.K., and Kaatze U. Critical fluctuations in the domain structure of lipid membranes. J. Chem. Phys. 118 (2003) 5683-5691
10. Schrader W., Halstenberg S., Behrends R., and Kaatze U. Critical slowing in lipid bilayers. J. Phys. Chem. B 107 (2003) 14457-14463
11. Kadanoff L.P., and Swift J. Transport coefficients near the liquid-gas critical point. Phys. Rev. 166 (1968) 89-101
12. Halperin B.I., and Hohenberg P.C. Scaling laws for dynamic critical phenomena. Phys. Rev. 177 (1969) 952-971
13. Ferrell R.A. Decoupled-mode dynamical scaling theory of the binary-liquid phase transition. Phys. Rev. Lett. 24 (1970) 1169-1172
14. Grabitz P., Ivanova V.P., and Heimburg T. Relaxation kinetics of lipid membranes and its relation to the heat capacity. Biophys. J. 82 (2002) 299-309
15. Seeger H.M., Gudmundsson M.L., and Heimburg T. How anesthetics, neurotransmitters, and antibiotics influence the relaxation processes in lipid membranes. J. Phys. Chem. B 111 (2007) 13858-13866
16. Cafiso D.S. Alamethicin: a peptide model for voltage gating and protein-membrane interactions. Annu. Rev. Biophys. Biomol. Struct. 23 (1994) 141-165
17. Salditt T., Li C., and Spaar A. Structure of antimicrobial peptides and lipid membranes probed by interface-sensitive X-ray scattering. Biochim. Biophys. Acta 1758 (2006) 1483-1498
18. Fox R.O., and Richards F.M. A voltage gated ion channel inferred from the crystal structure of alamethicin at 1.5 Å resolution. Nature 300 (1982) 325-330
19. Boheim G. Statistical analysis of alamethicin channels in black lipid membranes. J. Membr. Biol. 19 (1974) 277-303
20. Hall J.E. Voltage-dependent lipid flip-flop induced by alamethicin. Biophys. J. 33 (1981) 373-381
21. Schwarz G., and Savko P. Structural and dipolar properties of the voltage-dependent pore former alamethicin in octanol/dioxane. Biophys. J. 39 (1982) 211-219
22. Vodyanoy I., Hall J.E., and Balasubramanian T.M. Alamethicin-induced current-voltage curve asymmetry in lipid bilayers. Biophys. J. 42 (1983) 71-82
23. Aguilella V.M., and Bezrukov S.M. Alamethicin channel conductance modified by lipid charge. Eur Biophys J 30 (2001) 233-241
24. Eisenberg M., Hal J., and Mead C. The nature of the voltage-dependent conductance induced by alamethicin in black lipid membranes. J. Membr. Biol. 14 (1973) 143-176
25. Hanke W., and Boheim G. The lowest conductance state of the alamethicin pore. Biochim. Biophys. Acta 596 (1980) 456-462
26. Keller S.L., Bezrukov S.M., Gruner S.M., Tate M.W., Vodyanoy I., and Parsegian V.A. Probability of alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids. Biophys. J. 65 (1993) 23-27
27. He K., Ludtke S., Worcester D., and Huang H. Neutron scattering in the plane of membranes: structure of alamethicin pores. Biophys. J. 70 (1996) 2659-2666
28. Cantor R. Size distribution of barrel-stave aggregates of membrane peptides: influence of the bilayer lateral pressure profile. Biophys. J. 82 (2002) 2520-2525
29. Zhang Y.P., Lewis R.N., Hodges R.S., and McElhaney R.N. Peptide models of helical hydrophobic transmembrane segments of membrane proteins. 2. Differential scanning calorimetric and FTIR spectroscopic studies of the interaction of ac-k2-(la)12-k2-amide with phosphatidylcholine bilayers. Biochemistry 34 (1995) 2362-2371
30. Mouritsen O.G., and Bloom M. Models of lipid-protein interactions in membranes. Annu. Rev. Biophys. Biomol. Struct. 22 (1993) 145-171
31. Jensen M.Ø., and Mouritsen O.G. Lipids do influence protein function - the hydrophobic matching hypothesis revisited. Biochim. Biophys. Acta 1666 (2004) 205-226
32. MacDonald R.C., MacDonald R.I., Menco B.P.M., Takeshita K., Subbarao N.K., and Hu L. Small-volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim. Biophys. Acta 1061 (1991) 297-303
33. Bilaniuk N., and Wong G.S.K. Speed of sound in pure water as a function of temperature. J. Acoust. Soc. Am. 93 (1993) 1609-1612
34. Lautscham K., Wente F., Schrader W., and Kaatze U. High resolution and small volume automatic ultrasonic velocimeter for liquids. Meas. Sci. Technol. 11 (2000) 1432-1439
35. Buckin V., and Smyth C. High-resolution ultrasonic resonator measurements for analysis of liquids. Seminars in food analysis 4 (1999) 113-130
36. Dwyer C., Donnelly L., and Buckin V. Ultrasonic analysis of rennet-induced pre-gelation and gelation processes in milk. J. Dairy Res. 72 (2005) 303-310
37. 3 Probenvolumen. Z. angew. Physik 27 (1969) 273-277
38. Tamm L.K., and McConnell H.M. Supported phospholipid bilayers. Biophys. J. 47 (1985) 105-113
39. Mou J., Yang J., and Shao Z. Tris(hydroxymethyl)aminomethane (c4h11no3) induced a ripple phase in supported unilamellar phospholipid bilayers. Biochemistry 33 (1994) 4439-4443
40. Nagle J.F. Theory of the main lipid bilayer phase transition. Ann. Rev. Phys. Chem. 31 (1980) 157-195
41. Makowski L., and Li J. Topics in Molecular and Structural Biology: Biomembrane Structure and Function (1984) 43-166
42. Sarvazyan A.P., and Chalikian T.V. Theoretical analysis of an ultrasonic interferometer for precise measurements at high pressures. Ultrasonics 29 (1991) 119-124
43. Halstenberg S., Heimburg T., Hianik T., Kaatze U., and Krivanek R. Cholesterol-induced variations in the volume and enthalpy fluctuations of lipid bilayers. Biophys. J. 75 (1998) 264-271
44. Taulier N., and Chalikian T.V. Compressibility of protein transitions. Biochim. Biophys. Acta 1595 (2002) 48-70
45. Heimburg T. Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry. Biochim. Biophys. Acta 1415 (1998) 147-162
46. Anthony F.H., Biltonen R.L., and Freire E. Modification of a vibrating-tube density meter for precise temperature scanning. Anal. Biochem. 116 (1981) 161-167
47. Ebel H., Grabitz P., and Heimburg T. Enthalpy and volume changes in lipid membranes. I. The proportionality of heat and volume changes in the lipid melting transition and its implication for the elastic constants. J. Phys. Chem. B 105 (2001) 7353-7360
48. Osdol W.W.V., Biltonen R.L., and Johnson M.L. Measuring the kinetics of membrane phase transitions. J. Biochem. Biophys. Methods 20 (1989) 1-46
49. van Osdol W.W., Johnson M.L., Ye Q., and Biltonen R. Relaxation dynamics of the gel to liquid-crystalline transition of phosphatidylcholine bilayers. Effects of chainlength and vesicle size. Biophys. J. 59 (1991) 775-785
50. Schrader W., Ebel H., Grabitz P., Hanke E., Heimburg T., Hoeckel M., Kahle M., Wente F., and Kaatze U. Compressibility of lipid mixtures studied by calorimetry and ultrasonic velocity measurements. J. Phys. Chem. B 106 (2002) 6581-6586
51. Seeger H., Fidorra M., and Heimburg T. Domain size and fluctuations at domain interfaces in lipid mixtures. Macromol. Symp. 219 (2005) 85-96
52. Oliynyk V., Kaatze U., and Heimburg T. Defect formation of lytic peptides in lipid membranes and their influence on the thermodynamic properties of the pore environment. Biochim. Biophys. Acta 1768 (2007) 236-245
53. Schneider M.F., Marsh D., Jahn W., Kloesgen B., and Heimburg T. Network formation of lipid membranes: triggering structural transitions by chain melting. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 14312-14317
54. Ivanova V.P., Makarov I.M., Schäffer T.E., and Heimburg T. Analyzing heat capacity profiles of peptide-containing membranes: cluster formation of gramicidin A. Biophys. J. 84 (2003) 2427-2439
55. He K., Ludtke S., Heller W., and Huang H. Mechanism of alamethicin insertion into lipid bilayers. Biophys. J. 71 (1996) 2669-2679
56. Tieleman D.P., Berendsen H.J., and Sansom M.S. Surface binding of alamethicin stabilizes its helical structure: molecular dynamics simulations. Biophys. J. 76 (1999) 3186-3191
57. Zuckermann M.J., and Heimburg T. Insertion and pore formation driven by adsorption of proteins onto lipid bilayer membrane-water interfaces. Biophys. J. 81 (2001) 2458-2472
58. Chen F.-Y., Lee M.-T., and Huang H.W. Evidence for membrane thinning effect as the mechanism for peptide-induced pore formation. Biophys. J. 84 (2003) 3751-3758
59. Heller W.T., He K., Ludtke S.J., Harroun T.A., and Huang H.W. Effect of changing the size of lipid headgroup on peptide insertion into membranes. Biophys. J. 73 (1997) 239-244
60. Isambert H. Understanding the electroporation of cells and artificial bilayer membranes. Phys. Rev. Lett. 80 (1998) 3404
61. Sens P., and Isambert H. Undulation instability of lipid membranes under an electric field. Phys. Rev. Lett. 88 (2002) 128102
62. Chen F.-Y., Lee M.-T., and Huang H.W. Sigmoidal concentration dependence of antimicrobial peptide activities: a case study on alamethicin. Biophys. J. 82 (2002) 908-914
63. Huang H.W. Elasticity of lipid bilayer interacting with amphiphilic helical peptides. J. Phys. II France 5 (1995) 1427-1431
64. Heimburg T., and Jackson A.D. On soliton propagation in biomembranes and nerves. Proc. Natl. Acad. Sci. USA 102 (2005) 9790-9795
65. Bhattacharjee J.K., and Ferrell R.A. Dynamic scaling theory for the critical ultrasonic attenuation in a binary liquid. Phys. Rev. A 24 (1981) 1643-1646
66. Ferrell R.A., and Bhattacharjee J.K. Dynamic scaling theory of the critical attenuation and dispersion of sound in a classical fluid: The binary liquid. Phys. Rev. A 31 (1985) 1788-1809
67. Bhattacharjee J.K., and Ferrell R.A. Scaling theory of critical ultrasonics near the isotropic-to-nematic transition. Phys. Rev. E 56 (1997) 5549-5552
68. M. Höckel, Experimentelle Untersuchungen wässriger Lipid-Suspensionen mittels Ultraschallabsorptionsspektroskopie, Kalorimetrie und Densitometrie, Diploma thesis (1999).
69. W. Schrader, Schallgeschwindigkeitsmessungen, Kalorimetrie sowie dielektrische und akustische Spektroskopie an wässrigen Phospholipidsuspensionen, Ph.D. thesis (2001).