The single-giant unilamellar vesicle method reveals lysenin-induced pore formation in lipid membranes containing sphingomyelin

Biochemistry

Volumn 51, Issue 25, 2012, Pages 5160-5172

  Alam, Jahangir Md ^a   Kobayashi, Toshihide ^b   Yamazaki, Masahito ^a  

^a SHIZUOKA UNIVERSITY   (Japan)

^b RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCEIN; DIOLEOYLPHOSPHATIDYLCHOLINE; ELEMENTARY PROCESS; FLUORESCENT PROBES; LIPID MEMBRANES; LIQUID-ORDERED PHASE; LOW CONCENTRATIONS; MEMBRANE PERMEATION; PORE FORMATION; PORE FORMING TOXINS; SODIUM DODECYL SULFATE; SPHINGOMYELIN; UNILAMELLAR VESICLE;

MEMBRANES; OLIGOMERS; PHOSPHOLIPIDS; PORE SIZE; SODIUM; SODIUM SULFATE;

PERMEATION;

CALCEIN; CHOLESTEROL; DIOLEOYLPHOSPHATIDYLCHOLINE; DODECYL SULFATE SODIUM; FLUORESCENT DYE; LYSENIN; OLIGOMER; SPHINGOMYELIN; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; CHANNEL GATING; CONCENTRATION RESPONSE; CORRELATION ANALYSIS; DIFFUSION COEFFICIENT; GIANT UNILAMELLAR VESICLE; HEMOLYSIS; LIPID COMPOSITION; LIPID MEMBRANE; MEMBRANE PERMEABILITY; MEMBRANE VESICLE; MOLECULAR INTERACTION; OLIGOMERIZATION; PRIORITY JOURNAL; PROCEDURES; SINGLE GIANT UNILAMELLAR VESICLE METHOD;

ANIMALS; FLUORESCENT DYES; MEMBRANE LIPIDS; OLIGOCHAETA; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN BINDING; SPHINGOMYELINS; TOXINS, BIOLOGICAL; UNILAMELLAR LIPOSOMES;

EID: 84862837463     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300448g     Document Type: Article

References (52)

1. Heuck, A. P., Tweten, R. K., and Johnson, A. E. (2001) β-Barrel pore-forming toxins: Intriguing dimorphic proteins Biochemistry 40, 9065-9073 (Pubitemid 32734170)
2. Parker, M. W. (2003) Cryptic clues as to how water-soluble protein toxins form pores in membranes Toxicon 42, 1-6 (Pubitemid 37297553)
3. Parker, M. W. and Feil, S. C. (2005) Pore-forming protein toxins: From structure to function Prog. Biophys. Mol. Biol. 88, 91-142 (Pubitemid 39547775)
4. Anderluh, G. and Lakey, J. (2010) Proteins: Membrane binding and pore formation, Springer-Verlag, Berlin.
5. Tomita, T., Watanabe, M., and Yasuda, T. (1992) Influence of membrane fluidity on assembly of Staphylococcus aureus α-toxin, a channel-forming protein, in liposome membrane J. Biol. Chem. 267, 13391-13397
6. Tilley, S. J., Oriova, E. V., Gilbert, R. J. C., Andrew, P. W., and Saibll, H. R. (2005) Structural basis of pore formation by the bacterial toxin pneumolysin Cell 121, 247-256 (Pubitemid 40546392)
7. Kristant, K., Podlesek, Z., Hojink, V., Gutierrez-Anderluh, I., Guncar, G., Turk, D., Gonzalez-Manas, J. M., Lakey, J. H., Macek, P., and Anderluh, G. (2004) Pore formation by equinatoxin, a eukaryotic pore-forming toxin, requires a flexible N-terminal region and a stable β-sandwich J. Biol. Chem. 279, 46509-46517 (Pubitemid 39518294)
8. Yamaji, A., Sekizawa, Y., Emoto, K., Sakurabe, H., Inoue, K., Kobayashi, H., and Umeda, M. (1998) Lysenin, a novel sphingomyelin-specific binding protein J. Biol. Chem. 273, 5300-5306 (Pubitemid 28108696)
9. Yamaji-Hasegawa, A., Makino, A., Baba, T., Senoh, Y., Kimura, H., Sato, S. B., Terada, N., Ohno, S., Kiyokawa, E., Umeda, M., and Kobayashi, T. (2003) Oligomerization and pore formation of a sphingomyelin-specific toxin, lysenin J. Biol. Chem. 278, 22762-22770 (Pubitemid 36830337)
10. Ishitsuka, R., Yamaji-Hasegawa, A., Hirabayashi, A. Y., and Kobayashi, T. (2004) A lipid-specific toxin reveals heterogeneity of sphingomyelin-containing membranes Biophys. J. 86, 296-300
11. Ishitsuka, R. and Kobayashi, T. (2007) Cholesterol and lipid/protein ratio control the oligomerization of a sphingomyelin-specific toxin, lysenin Biochemistry 46, 1495-1502
12. Kulma, M., Herec, M., Grudzinski, W., Anderluh, G., Gruszecki, W. I., Kwiatkowska, K., and Sobota, A. (2010) Sphingomyelin-rich domains are sites of lysenin oligomerization: Implications for raft studies Biochim. Biophys. Acta 1798, 471-481
13. Evans, E. and Rawicz, E. (1990) Entropy-driven tension and bending elasticity in condensed-fluid membranes Phys. Rev. Lett. 64, 2094-2097
14. Farge, E. and Devaux, P. F. (1992) Shape changes of giant liposomes induced by an asymmetric transmembrane distribution of phospholipids Biophys. J. 61, 347-357
15. Saitoh, A., Takiguchi, K., Tanaka, Y., and Hotani, H. (1998) Opening-up of liposomal membranes by talin Proc. Natl. Acad. Sci. U.S.A. 95, 1026-1031 (Pubitemid 28124906)
16. Zhao, H., Mattila, J.-P., Holopainen, J. M., and Kinnunen, P. K. J. (2001) Comparison of the membrane association of two antimicrobial peptides, magainin 2 and indolicidin Biophys. J. 81, 2979-2991 (Pubitemid 33020082)
17. Zhao, H., Rinaldi, A. C., Giulio, A. D., Simmaco, M., and Kinnunen, P. K. J. (2002) Interactions of the antimicrobial peptides temporins with model biomembranes. Comparison of temporins B and L Biochemistry 41, 4425-4436 (Pubitemid 34259887)
18. 3+ induce shape change of giant unilamellar vesicles of phosphatidylcholine Biochim. Biophys. Acta 1564, 173-182 (Pubitemid 34717883)
19. Yamashita, Y., Masum, S. M., Tanaka, T., and Yamazaki, M. (2002) Shape changes of giant unilamellar vesicles of phosphatidylcholine induced by a de novo designed peptide interacting with their membrane interface Langmuir 18, 9638-9641
20. Yamazaki, M. (2008) The single GUV method to reveal elementary processes of leakage of internal contents from liposomes induced by antimicrobial substances. In Advances in Planar Lipid Bilayers and Liposomes (Leitmannova, A. L., Ed.) Vol. 7, pp 121-142, Elsevier/Academic Press, London. (Pubitemid 351970337)
21. Tamba, Y., Ohba, S., Kubota, M., Yoshioka, H., Yoshioka, H., and Yamazaki, M. (2007) Single GUV method reveals interaction of tea catechin (-)-epigallocatechin gallate with lipid membranes Biophys. J. 92, 3178-3194 (Pubitemid 46684578)
22. 3+ Langmuir 20, 5160-5164
23. Tanaka, T., Sano, R., Yamashita, Y., and Yamazaki, M. (2004) Shape changes and vesicle fission of giant unilamellar vesicles of liquid-ordered phase membrane induced by lysophosphatidylcholine Langmuir 20, 9526-9534
24. Inaoka, Y. and Yamazaki, M. (2007) Vesicle fission of giant unilamellar vesicles of liquid-ordered phase-membranes induced by amphiphiles with a single long hydrocarbon chain Langmuir 23, 720-728 (Pubitemid 46226585)
25. Tamba, Y. and Yamazaki, M. (2005) Single giant unilamellar vesicle method reveals effect of antimicrobial peptide, magainin-2, on membrane permeability Biochemistry 44, 15823-15833 (Pubitemid 41746913)
26. Tamba, Y. and Yamazaki, M. (2009) Magainin 2-induce pore formation in the lipid membranes depends of its concentration in the membrane interface J. Phys. Chem. B 113, 4846-4852
27. Tamba, Y., Ariyama, H., Levadny, V., and Yamazaki, M. (2010) Kinetic pathway of antimicrobial peptide magainin 2-induced pore formation in lipid membranes J. Phys. Chem. B 114, 12018-12026
28. Tamba, Y., Tanaka, T., Yahagi, T., Yamashita, Y., and Yamazaki, M. (2004) Stability of giant unilamellar vesicles and large unilamellar vesicles of liquid-ordered phase membranes in the presence of Triton X-100 Biochim. Biophys. Acta 1667, 1-6 (Pubitemid 39463329)
29. Maeda, T. and Ohnishi, S. (1980) Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes FEBS Lett. 122, 283-287 (Pubitemid 11186279)
30. Yamazaki, M. and Ito, T. (1990) Deformation and instability in membrane structure of phospholipid vesicles caused by osmophobic association: Mechanical stress model for the mechanism of poly (ethylene glycol)-induced membrane fusion Biochemistry 29, 1309-1314 (Pubitemid 20053856)
31. Yamashita, Y., Oka, M., Tanaka, T., and Yamazaki, M. (2002) A mew method for preparation of giant liposomes in high salt concentrations and growth of protein microcrystals in them Biochim. Biophys. Acta 1561, 129-134 (Pubitemid 34454780)
32. Tamba, Y., Terashima, H., and Yamazaki, M. (2011) A membrane filtering method for the purification of giant unilamellar vesicles Chem. Phys. Lipids 164, 351-358
33. Yamazaki, M., Ohnihi, S., and Ito, T. (1989) Osmoelastic coupling in biological structures: Decrease in membrane fluidity and osmophobic association of phospholipid vesicles in response to osmotic stress Biochemistry 28, 3710-3715 (Pubitemid 19125412)
34. Rasband, W. S. (1997-2011) ImageJ, version 1.45s, National Institutes of Health, Bethesda, MD (http://imagej.nih.gov/ij/).
35. Yoshida, N., Tamura, M., and Kinjo, M. (2000) Fluorescence correlation spectroscopy: A new tool for probing the microenvironment of the internal space of organelles Single Mol. 1, 279-283
36. Gribbon, P. and Hardingham, T. E. (1998) Macromolecular diffusion of biological polymers measured by confocal fluorescence recovery after photobleaching Biophys. J. 75, 1032-1039 (Pubitemid 28357544)
37. Baumgard, T., Hess, S. T., and Webb, W. W. (2003) Imaging coexisting fluid domains in biomembranes models coupling curvature and line tension Nature 425, 821-824 (Pubitemid 37351463)
38. Kwiatkowska, K., Hordejuk, R., Szymczyk, P., Kulma, M., Abdel-Shakor, A., Plucienniczak, A., Dolowy, K., Szewczyk, A., and Sobota, A. (2007) Lysenin-His, a sphingomyelin-recognizing toxin, requires tryptophan 20 for cation-selective channel assembly but not membrane binding Mol. Membr. Biol. 24, 121-134 (Pubitemid 46633893)
39. Miller, C., Ed. (1986) Ion channel reconstitution, Plenum Press, New York.
40. Bayley, H., Jayasinghe, L., and Wallace, M. (2005) Prepore for a breakthrough Nat. Struct. Mol. Biol. 12, 385-386 (Pubitemid 43085893)
41. Lawrence, J. C., Saslowsky, D. E., Edwardson, J. M., and Henderson, R. M. (2003) Real-time analysis of the effects of cholesterol on lipid raft behavior using atomic force microscopy Biophys. J. 84, 1827-1832 (Pubitemid 36322944)
42. Aoki, T., Hirano, M., Takeuchi, Y., Kobayashi, T., Yanagida, T., and Ide, T. (2010) Single channel properties of lysenin measured in artificial lipid bilayers applications to biomolecule detection Proc. Jpn. Acad., Ser. B 86, 920-925
43. Doi, M. (1996) Introduction to Polymer Physics, Oxford University Press, Oxford, U.K.
44. Mabrey, S. and Sturtevant, J. M. (1976) Investigation of phase transitions of lipids and lipid mixtures by high sensitivity differential scanning calorimetry Proc. Natl. Acad. Sci. U.S.A. 73, 3862-3866
45. Veatch, S. L. and Keller, S. L. (2005) Seeing spots: Complex phase behavior in simple membranes Biochim. Biophys. Acta 1746, 172-185 (Pubitemid 41815014)
46. Döbereiner, H.-G., Käs, J., Noppl, D., Sprenger, I., and Sackmann, E. (2003) Budding and fission of vesicles Biophys. J. 65, 1396-1403
47. Marsh, D. (1996) Lateral pressure in membranes Biochim. Biophys. Acta 1286, 183-223 (Pubitemid 26426521)
48. Needham, D. and Nunn, R. S. (1990) Elastic deformation and failure of lipid bilayer membranes containing cholesterol Biophys. J. 58, 997-1009 (Pubitemid 20307868)
49. Simons, K. and Toomre, D. (2000) Lipid rafts and signal transduction Nat. Rev. Mol. Cell Biol. 1, 31-40
50. Schön, P., Garcia-Saez, A. J., Malovrh, P., Bacia, K., Anderluh, G., and Schwille, P. (2008) Equinatoxin II permeabilizing activity depends on the presence of sphingomyelin and lipid coexistence Biophys. J. 95, 691-698
51. Larsen, J., Hatzakis, N. S., and Stamou, D. (2011) Observation of inhomogeneity in the lipid composition of individual nanoscale liposomes J. Am. Chem. Soc. 133, 10685-10687
52. Landau, L. D. and Lifshitz, E. M. (1980) Statistical Physics, 3rd ed., Vol. 5, Part 1, Butterworth-Heinmann, Oxford, U.K.