Pore formation in a lipid bilayer under a tension ramp: Modeling the distribution of rupture tensions

Biophysical Journal

Volumn 92, Issue 12, 2007, Pages 4344-4355

  Boucher, Pierre Alexandre ^a   Joós, Béla ^a   Zuckermann, Martin J ^b,c   Fournier, Luc ^d  

^a UNIVERSITY OF OTTAWA   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c SIMON FRASER UNIVERSITY   (Canada)

^d Département de Physique du Cégep de l'Outaouais   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE;

ANALYTIC METHOD; ARTICLE; CHANNEL GATING; HYDROPHOBICITY; KINETICS; LIPID BILAYER; MEMBRANE VESICLE; TENSION;

EID: 34250333878     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.092023     Document Type: Article

References (55)

1. Wortis, M., and E. Evans. 1997. Membrane self-assembly: mechanical properties and vesicle shapes. Phys. Can. 53:281-288.
2. Dimitrov, D., and R. Jain. 1984. Membrane stability. Biochim. Biophys. Acta. 779:437-468.
3. Berk, D., and E. Evans. 1991. Detachment of agglutinin-bonded red blood cells. III. Mechanical analysis for large contact areas. Biophys. J. 59:861-872.
4. Bier, M., T. Gowrishankar, W. Chen, and R. Lee. 2004. Electroporation of a lipid bilayer as a chemical reaction. Bioelectromagnetics. 25:634-637.
5. Hunter, D., and B. Frisken. 1998. Effect of extrusion pressure and lipid properties on the size and polydispersity of lipid vesicles. Biophys. J. 74:2996-3002.
6. Patty, P., and B. Frisken. 2003. The pressure-dependence of the size of extruded vesicles. Biophys. J. 85:996-1004.
7. Karatekin, E., O. Sandre, H. Guitouni, N. Borghi, P. Puech, and F. Brochard-Wyart. 2003. Cascades of transient pores in giant vesicles: line tension and transport. Biophys. J. 84:1734-1749.
8. Ertel, A., A. Marangoni, J. Marsh, F. Hallett, and J. Wood. 1993. Mechanical properties of vesicles. I. Coordinated analysis of osmotic swelling and lysis. Biophys. J. 64:426-434.
9. Zhou, Z., and B. Joós. 1997. Mechanisms of membrane rupture: from cracks to pores. Phys. Rev. B. 56:2997-3009.
10. Zemel, A., A. Ben-Shaul, and S. May. 2005. Perturbation of a lipid membrane by amphipathic peptides and its role in pore formation. Eur. Biophys. J. 34:230-242.
11. Bechinger, B. 1999. The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta. 1462:157-183.
12. Sengupta, D., L. Meinhold, D. Langosch, G. Ullmann, and J. Smith. 2005. Understanding the energetics of helical peptide orientation in membranes. Proteins Struct. Funct. Bioinform. 58:913-922.
13. Lin, J., and A. Baumgaertner. 2000. Stability of a melittin pore in a lipid bilayer: a molecular dynamics study. Biophys. J. 78:1714-1724.
14. Hristova, K., C. Dempsey, and S. White. 2001. Structure, location, and lipid perturbations of melittin at the membrane interface. Biophys. J. 80:801-811.
15. Huang, H., F. Chen, and M. Lee. 2004. Molecular mechanism of peptide-induced pores in membranes. Phys. Rev. Lett. 92:198304.
16. Prenner, E. J., R. N. Lewis, and R. N. McElhaney. 1999. Biophysical studies of the interaction of the antimicrobial peptide gramicidin S with lipid bilayer model and biological membranes. Biochim. Biophys. Acta. 1462:201-221.
17. Prenner, E. J., R. N. Lewis, and R. N. McElhaney. 2004. Biophysical studies of the interaction of the antimicrobial peptide gramicidin S with lipid bilayer and biological membranes. Phys. Can. 60:121-129.
18. Evans, E., V. Heinrich, and W. Rawicz. 2004. Using dynamic tension spectroscopy to explore destabilization of membranes by antimicrobial peptides. Biophys. J. 86:330A.
19. Oren, Z., and Y. Shai. 1998. Mode of action of linear amphipathichelical antimicrobial peptides. Biopolymers (Pept. Sci.). 47:451-463.
20. Rapaport, D., R. Peled, S. Nir, and Y. Shai. 1996. Reversible surface aggregation in pore formation by pardaxin. Biophys. J. 70:2502-2512.
21. Schwarz, G., S. Stankowski, and V. Rizzo. 1986. Thermodynamic analysis of incorporation and aggregation in a membrane: application to the pore-forming peptide alamethicin. Biochim. Biophys. Acta. 861:141-151.
22. Rapaport, D., and Y. Shai. 1991. Interaction of fluorescently labeled pardaxin and its analogues with lipid bilayers. J. Biol. Chem. 266:23769-23775.
23. Rapaport, D., and Y. Shai. 1992. Aggregation and organization of pardaxin in phospholipid membranes. a fluorescence energy transfer study. J. Biol. Chem. 267:6502-6509.
24. Huang, H., and Y. Wu. 1991. Lipid-alamethicin interactions influence alamethicin orientation. Biophys. J. 60:1079-1087.
25. Yang, L., T. Harroun, T. Weiss, L. Ding, and H. Huang. 2001. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81:1475-1485.
26. Wolfe, J., M. Dowgert, and P. Steponkus. 1985. Dynamics of membrane exchange of the plasma membrane and the lysis of isolated protoplasts during rapid expansions in area. J. Membr. Biol. 86:127-138.
27. Evans, E., and D. Needham. 1987. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion and colloidal interactions. J. Phys. Chem. 91:4219-4228.
28. Needham, D., and R. Hochmuth. 1989. Electro-mechanical permeabilization of lipid vesicles. Role of membrane tension and compressibility. Biophys. J. 55:1001-1009.
29. Rawicz, W., K. Olbrich, T. McIntosh, D. Needham, and E. Evans. 2000. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79:328-339.
30. Olbrich, K., W. Rawicz, D. Needham, and E. Evans. 2000. Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys. J. 79:321-327.
31. Evans, E., V. Heinrich, F. Ludwig, and W. Rawicz. 2003. Dynamic tension spectroscopy and strength of biomembranes. Biophys. J. 85:2342-2350.
32. Fournier, L., and B. Joós. 2003. Lattice model for the kinetics of rupture of fluid bilayer membranes. Phys. Rev. E. 67:51908.
33. Shillcock, J., and D. Boal. 1996. Entropy-driven instability and rupture of fluid membranes. Biophys. J. 71:317-326.
34. Netz, R., and M. Schick. 1996. Pore formation and rupture in fluid bilayers. Phys. Rev. E. 53:3875-3885.
35. Leontiadou, H., A. Mark, and S. Marrink. 2004. Molecular dynamics simulations of hydrophilic pores in lipid bilayers. Biophys. J. 86:2156-2164.
36. Tieleman, D., H. Leontiadou, A. Mark, and S. Marrink. 2003. Simulation of pore formation in lipid bilayers by mechanical stress and electric fields. J. Am. Chem. Soc. 125:6382-6383.
37. Berneche, S., M. Nina, and B. Roux. 1998. Molecular dynamics simulation of melittin in a dimyristoylphosphatidylcholine bilayer membrane. Biophys. J. 75:1603-1618.
38. Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature. 415:389-395.
39. Zahn, D., and J. Brickmann. 2002. Molecular dynamics study of water pores in a phospholipid bilayer. Chem. Phys. Lett. 352:441-446.
40. Tolpekina, T., W. den Otter, and W. Briels. 2004. Simulations of stable pores in membranes: system size dependence and line tension. J. Chem. Phys. 121:8014-8020.
41. Tolpekina, T., W. den Otter, and W. Briels. 2004. Nucleation free energy of pore formation in an amphiphilic bilayer studied by molecular dynamics simulations. J. Chem. Phys. 121:12060-12066.
42. Farago, O., and C. Santangelo. 2005. Pore formation in fluctuating membranes. J. Chem. Phys. 122:44901.
43. Wang, Z., and D. Frenkel. 2005. Pore nucleation in mechanically stretched bilayer membranes. J. Chem. Phys. 123:1547011.
44. Wohlert, J., W. den Otter, O. Edholm, and W. Briels. 2006. Free energy of a trans-membrane pore calculated from atomistic molecular dynamics simulations. J. Chem. Phys. 124:154905.
45. Bermudez, H., A. K. Brannan, D. A. Hammer, F. S. Bates, and D. Discher. 2002. Molecular weight dependence of polymersome membrane structure, elasticity, and stability. Macromolecules. 35:8203-8208.
46. Taupin, C., M. Dvolaitzky, and C. Sauterey. 1975. Osmotic pressure-induced pores in phospholipid vesicles. Biochemistry. 14:4771-4775.
47. Boal, D. 2001. Mechanics of the Cell. Cambridge University Press, New York.
48. Feller, S., K. Gawrisch, and A. MacKerell, Jr. 2002. Polyunsaturated fatty acids in lipid bilayers: intrinsic and environmental contributions to their unique physical properties. J. Am. Chem. Soc. 124:318-326.
49. Israelachvili, J. 1985. Intermolecular and Surface Forces: With Applications to Colloidal and Biological Systems. Academic Press, London and Orlando.
50. Frenkel, D., and B. Smit. 2001. Understanding Molecular Simulation: From Algorithms to Applications. Academic Press, New York.
51. Benachir, T., and M. Lafleur. 1995. Study of vesicle leakage induced by melittin. Biochim. Biophys. Acta. 1235:452-460.
52. Mouritsen, O. G., and M. Bloom. 1984. Mattress model of lipid-protein interactions in membranes. Biophys. J. 46:141-153.
53. Ludtke, S., K. He, and H. Huang. 1995. Membrane thinning caused by magainin 2. Biochemistry. 34:16764-16769.
54. Chen, F., M. Lee, and H. Huang. 2003. Evidence for membrane thinning effect as the mechanism for peptide-induced pore formation. Biophys. J. 84:3751-3758.
55. Nagle, J., and S. Tristram-Nagle. 2000. Structure of lipid bilayers. Biochim. Biophys. Acta. 1469:159-195.