All-or-none versus graded: Single-vesicle analysis reveals lipid composition effects on membrane permeabilization

Biophysical Journal

Volumn 99, Issue 11, 2010, Pages 3619-3628

  Apellániz, Beatriz ^a,b   Nieva, José L ^a,b   Schwille, Petra ^c   García Sáez, Ana J ^d,e  

^a CSIC UPV Unidad de Biofisica UBF   (Spain)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78649761049     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.09.027     Document Type: Article

References (53)

1. Mulkidjanian, A. Y., M. Y. Galperin, and E. V. Koonin. 2009. Co-evolution of primordial membranes and membrane proteins. Trends Biochem. Sci. 34:206-215.
2. Malsam, J., S. Kreye, and T. H. Söllner. 2008. Membrane fusion: SNAREs and regulation. Cell. Mol. Life Sci. 65:2814-2832.
3. Antignani, A., and R. J. Youle. 2006. How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr. Opin. Cell Biol. 18:685-689.
4. Anderluh, G., and J. H. Lakey. 2008. Disparate proteins use similar architectures to damage membranes. Trends Biochem. Sci. 33:482-490.
5. Mathew, M., and R. S. Verma. 2009. Humanized immunotoxins: a new generation of immunotoxins for targeted cancer therapy. Cancer Sci. 100:1359-1365.
6. Pálffy, R., R. Gardlík, P. Celec. 2009. On the physiology and pathophysiology of antimicrobial peptides. Mol. Med. 15:51-59.
7. Almeida, P. F., and A. Pokorny. 2009. Mechanisms of antimicrobial, cytolytic, and cell-penetrating peptides: from kinetics to thermodynamics. Biochemistry. 48:8083-8093.
8. Huang, H. W. 2006. Molecular mechanism of antimicrobial peptides: the origin of cooperativity. Biochim. Biophys. Acta. 1758:1292-1302.
9. Huang, H. W., F. Y. Chen, and M. T. Lee. 2004. Molecular mechanism of peptide-induced pores in membranes. Phys. Rev. Lett. 92:198304.
10. Gregory, S. M., A. Pokorny, and P. F. Almeida. 2009. Magainin 2 revisited: a test of the quantitative model for the all-or-none permeabilization of phospholipid vesicles. Biophys. J. 96:116-131.
11. Gregory, S. M., A. Cavenaugh, P. F. Almeida. 2008. A quantitative model for the all-or-none permeabilization of phospholipid vesicles by the antimicrobial peptide cecropin A. Biophys. J. 94:1667-1680.
12. Huang, H. W. 2009. Free energies of molecular bound states in lipid bilayers: lethal concentrations of antimicrobial peptides. Biophys. J. 96:3263-3272.
13. Melo, M. N., R. Ferre, and M. A. Castanho. 2009. Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations. Nat. Rev. Microbiol. 7:245-250.
14. 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.
15. García-Sáez, A. J., M. Coraiola, J. Salgado. 2006. Peptides corresponding to helices 5 and 6 of Bax can independently form large lipid pores. FEBS J. 273:971-981.
16. Fuertes, G., A. J. García-Sáez, J. Salgado. 2010. Pores formed by Baxα5 relax to a smaller size and keep at equilibrium. Biophys. J. 99:2917-2925.
17. Pokorny, A., and P. F. F. Almeida. 2004. Kinetics of dye efflux and lipid flip-flop induced by δ-lysin in phosphatidylcholine vesicles and the mechanism of graded release by amphipathic, α-helical peptides. Biochemistry. 43:8846-8857.
18. Ladokhin, A. S., W. C. Wimley, S. H. White. 1997. Mechanism of leakage of contents of membrane vesicles determined by fluorescence requenching. Methods Enzymol. 278:474-486.
19. Ladokhin, A. S., W. C. Wimley, and S. H. White. 1995. Leakage of membrane vesicle contents: determination of mechanism using fluorescence requenching. Biophys. J. 69:1964-1971.
20. Fiser, R., and I. Konopásek. 2009. Different modes of membrane permeabilization by two RTX toxins: HlyA from Escherichia coli and CyaA from Bordetella pertussis. Biochim. Biophys. Acta. 1788: 1249-1254.
21. Apelláiniz, B., S. Nir, and J. L. Nieva. 2009. Distinct mechanisms of lipid bilayer perturbation induced by peptides derived from the membrane-proximal external region of HIV-1 gp41. Biochemistry. 48:5320-5331.
22. Patel, H., C. Tscheka, and H. Heerklotz. 2009. Characterizing vesicle leakage by fluorescence lifetime measurements. Soft Matter 5:2849-2851.
23. Garćia-Sáez, A. J., J. Ries, P. Schwille. 2009. Membrane promotes tBID interaction with BCL(XL). Nat. Struct. Mol. Biol. 16:1178-1185.
24. Schön, P., A. J. Garcia-Saez, P. Schwille. 2008. Equinatoxin II permeabilizing activity depends on the presence of sphingomyelin and lipid phase coexistence. Biophys. J. 95:691-698.
25. Tamba, Y., and M. Yamazaki. 2005. Single giant unilamellar vesicle method reveals effect of antimicrobial peptide magainin 2 on membrane permeability. Biochemistry. 44:15823-15833.
26. Sun, Y., W. C. Hung, H. W. Huang. 2009. Interaction of tea catechin ( - )-epigallocatechin gallate with lipid bilayers. Biophys. J. 96:1026-1035.
27. Ambroggio, E. E., F. Separovic, L. A. Bagatolli. 2005. Direct visualization of membrane leakage induced by the antibiotic peptides: maculatin, citropin, and aurein. Biophys. J. 89:1874-1881.
28. Montero, M., N. E. van Houten, J. K. Scott. 2008. The membraneproximal external region of the human immunodeficiency virus type 1 envelope: dominant site of antibody neutralization and target for vaccine design. Microbiol. Mol. Biol. Rev. 72:54-84. (table of contents.).
29. Lorizate, M., N. Huarte, J. L. Nieva. 2008. Interfacial pre-trans-membrane domains in viral proteins promoting membrane fusion and fission. Biochim. Biophys. Acta. 1778:1624-1639.
30. Vishwanathan, S. A., and E. Hunter. 2008. Importance of the membrane-perturbing properties of the membrane-proximal external region of human immunodeficiency virus type 1 gp41 to viral fusion. J. Virol. 82:5118-5126.
31. Huarte, N., M. Lorizate, J. L. Nieva. 2008. The broadly neutralizing anti-human immunodeficiency virus type 1 4E10 monoclonal antibody is better adapted to membrane-bound epitope recognition and blocking than 2F5. J. Virol. 82:8986-8996.
32. Lorizate, M., A. Cruz, J. L. Nieva. 2006. Recognition and blocking of HIV-1 gp41 pre-transmembrane sequence by monoclonal 4E10 antibody in a Raft-like membrane environment. J. Biol. Chem. 281:39598-39606.
33. Rausch, J. M., J. R. Marks, W. C. Wimley. 2007. β-Sheet poreforming peptides selected from a rational combinatorial library: mechanism of pore formation in lipid vesicles and activity in biological membranes. Biochemistry. 46:12124-12139.
34. Aloia, R. C., H. Tian, and F. C. Jensen. 1993. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc. Natl. Acad. Sci. USA. 90:5181-5185.
35. Allende, D., S. A. Simon, and T. J. McIntosh. 2005. Melittin-induced bilayer leakage depends on lipid material properties: evidence for toroidal pores. Biophys. J. 88:1828-1837.
36. Tamba, Y., and M. Yamazaki. 2009. Magainin 2-induced pore formation in the lipid membranes depends on its concentration in the membrane interface. J. Phys. Chem. B. 113:4846-4852.
37. Huang, H. W. 2000. Action of antimicrobial peptides: two-state model. Biochemistry. 39:8347-8352.
38. Matsuzaki, K., O. Murase, K. Miyajima. 1995. Translocation of a channel-forming antimicrobial peptide, magainin 2, across lipid bilayers by forming a pore. Biochemistry. 34:6521-6526.
39. Rathinakumar, R., and W. C. Wimley. 2008. Biomolecular engineering by combinatorial design and high-throughput screening: small, soluble peptides that permeabilize membranes. J. Am. Chem. Soc. 130:9849-9858.
40. Rex, S., and G. Schwarz. 1998. Quantitative studies on the melittininduced leakage mechanism of lipid vesicles. Biochemistry. 37: 2336-2345.
41. Matsuzaki, K., O. Murase, K. Miyajima. 1996. An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry. 35:11361-11368.
42. Sengupta, D., H. Leontiadou, S. J. Marrink. 2008. Toroidal pores formed by antimicrobial peptides show significant disorder. Biochim. Biophys. Acta. 1778:2308-2317.
43. Lee, M. T., W. C. Hung, H. W. Huang. 2008. Mechanism and kinetics of pore formation in membranes by water-soluble amphipathic peptides. Proc. Natl. Acad. Sci. USA. 105:5087-5092.
44. Leontiadou, H., A. E. Mark, and S. J. Marrink. 2006. Antimicrobial peptides in action. J. Am. Chem. Soc. 128:12156-12161.
45. Ludtke, S. J., K. He, H. W. Huang. 1996. Membrane pores induced by magainin. Biochemistry. 35:13723-13728.
46. Fuertes, G., D. Gimeinez, J. Salgado. 2010. Role ofmembranelipids for the activity of pore forming peptides and proteins. In Proteins: Membrane Binding and Pore Formation. G. Anderluh, and J. Lakey, editors. Landes Bioscience and Springer Bioscience+Business Media.
47. Graham, D. R., E. Chertova, J. E. Hildreth. 2003. Cholesterol depletion of human immunodeficiency virus type 1 and simian immunodeficiency virus with β-cyclodextrin inactivates and permeabilizes the virions: evidence for virion-associated lipid rafts. J. Virol. 77: 8237-8248.
48. Epand, R. F., A. Thomas, R. M. Epand. 2006. Juxtamembrane protein segments that contribute to recruitment of cholesterol into domains. Biochemistry. 45:6105-6114.
49. Epand, R. F., B. G. Sayer, and R. M. Epand. 2005. The tryptophan-rich region of HIV gp41 and the promotion of cholesterol-rich domains. Biochemistry. 44:5525-5531.
50. Chernomordik, L. V., and J. Zimmerberg. 1995. Bending membranes to the task: structural intermediates in bilayer fusion. Curr. Opin. Struct. Biol. 5:541-547.
51. Epand, R. M., A. Thomas, R. F. Epand. 2010. Cholesterol interaction with proteins that partition into membrane domains: an overview. Subcell. Biochem. 51:253-278.
52. Chernomordik, L. V., and M. M. Kozlov. 2008. Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15:675-683.
53. Müller, M., K. Katsov, and M. Schick. 2003. A new mechanism of model membrane fusion determined from Monte Carlo simulation. Biophys. J. 85:1611-1623.