Solubilization of binary lipid mixtures by the detergent triton X-100: The role of cholesterol

Langmuir

Volumn 31, Issue 1, 2015, Pages 378-386

  Mattei, Bruno ^a   Franča, Ana D C ^a   Riske, Karin A ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; FLUORESCENCE; FLUORESCENCE MICROSCOPY; HYDROPHOBICITY; LIGHT SCATTERING; LIPID BILAYERS; LIQUIDS; MIXTURES; OPTICAL DATA STORAGE; OPTICAL MICROSCOPY; PHASE SEPARATION; PHOSPHOLIPIDS; SOLUBILITY; SYNCHROTRONS;

BILAYER FRAGMENTS; BINARY LIPID MIXTURES; GIANT UNILAMELLAR VESICLES; LARGE UNILAMELLAR VESICLES; LIPID MIXTURES; MEMBRANE RESISTANCE; PHOSPHOLIPID BILAYER; SOLUBILIZATION OF LIPIDS;

BINARY MIXTURES;

CHOLESTEROL; LIPID; OCTOXINOL;

CHEMISTRY; CLASSIFICATION; FLUORESCENCE MICROSCOPY; SOLUBILITY;

CHOLESTEROL; LIPIDS; MICROSCOPY, FLUORESCENCE; OCTOXYNOL; SOLUBILITY;

EID: 84921414956     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la504004r     Document Type: Article

References (53)

1. Jones, M. N. Surfactants in membrane solubilisation Int. J. Pharm. 1999, 177, 137-159
2. Seddon, A. M.; Curnow, P.; Booth, P. J. Membrane proteins, lipids and detergents: not just a soap opera Biochim. Biophys. Acta 2004, 1666, 105-117
3. Heerklotz, H.; Seelig, J. Titration calorimetry of surfactant-membrane partitioning and membrane solubilization Biochim. Biophys. Acta 2000, 1508, 69-85
4. Lichtenberg, D.; Ahyaauch, H.; Goni, F. M. The mechanism of detergent solubilization of lipid bilayers Biophys. J. 2013, 105, 289-299
5. Helenius, A.; Simons, K. Solubilization of membranes by detergents Biochim. Biophys. Acta 1975, 415, 29-79
6. Schurtenberger, P.; Mazer, N.; Kaenzig, W. Micelle to vesicle transition in aqueous solutions of bile salt and lecithin J. Phys. Chem. 1985, 89, 1042-1049
7. Lichtenberg, D. Characterization of the solubilization of lipid bilayers by surfactants Biochim. Biophys. Acta 1985, 821, 470-478
8. Sáez-Cirion, A.; Alonso, A.; Goni, F. M.; McMullen, T. P. W.; McElhaney, R. N.; Rivas, E. A. Equilibrium and kinetic studies of the solubilization of phospholipid-cholesterol bilayers by C12E8. The influence of the lipid phase structure Langmuir 2000, 16, 1960-1968
9. Heerklotz, H.; Seelig, J. Correlation of membrane/water partition coefficients of detergents with the critical micelle concentration Biophys. J. 2000, 78, 2435-2440
10. Tsamaloukas, A.; Szadkowska, H.; Heerklotz, H. Nonideal mixing in multicomponent lipid/detergent systems J. Phys.: Condens. Matter 2006, 18, 1125-1138
11. Ahyayauch, H.; Collado, M.; Alonso, A.; Goni, F. M. Lipid bilayers in the gel phase become saturated by triton X-100 at lower surfactant concentrations than those in the fluid phase Biophys. J. 2012, 102, 2510-2516
12. Ahmed, S. N.; Brown, D. A.; London, E. On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes Biochemistry 1997, 36, 10944-10953
13. Sot, J.; Collado, M. I.; Arrondo, J. L. R.; Alonso, A.; Goni, F. M. Triton X-100-resistant bilayers: effect of lipid composition and relevance to the raft phenomenon Langmuir 2002, 18, 2828-2835
14. McMullen, T. P. W.; Lewis, R. N. A. H.; McElhaney, R. N. Cholesterol-phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes Curr. Opin. Colloid Interface Sci. 2004, 8, 459-468
15. Simons, K.; Ikonen, E. Functional rafts in cell membranes Nature 1997, 387, 569-572
16. Brown, D. A.; London, E. Functions of lipid rafts in biological membranes Annu. Rev. Cell Dev. Biol. 1998, 14, 111-136
17. Arnulphi, C.; Sot, J.; Garcia-Pacios, M.; Arrondo, J. L.; Alonso, A.; Goni, F. M. Triton X-100 partitioning into sphingomyelin bilayers at subsolubilizing detergent concentrations: effect of lipid phase and a comparison with dipalmitoylphosphatidylcholine Biophys. J. 2007, 93, 3504-3514
18. Patra, S. K.; Alonso, A.; Goni, F. M. Detergent solubilisation of phospholipid bilayers in the gel state: the role of polar and hydrophobic forces Biochim. Biophys. Acta 1998, 1373, 112-118
19. Ahyayauch, H.; Collado, M. I.; Goni, F. M.; Lichtenberg, D. Cholesterol reverts TX-100 preferential solubilization of sphingomyelin over phosphatidylcholine: A 31P-NMR study FEBS Lett. 2009, 583, 2859-2864
20. Li, X.; Momsen, M. M.; Smaby, J. M.; Brockman, H. L.; Brown, R. E. Cholesterol decreases the interfacial elasticity and detergent solubility of sphingomyelins Biochemistry 2001, 40, 5954-5963
21. Patra, S. K.; Alonso, A.; Arrondo, J. L. R.; Goni, F. M. Liposomes containing sphingomyelin and cholesterol: detergent solubilisation and infrared spectroscopic studies J. Liposome Res. 1999, 9, 247-260
22. Heerklotz, H. Triton promotes domain formation in lipid raft mixtures Biophys. J. 2002, 83, 2693-2701
23. El Kirat, K.; Morandat, S. Cholesterol modulation of membrane resistance to Triton X-100 explored by atomic force microscopy Biochim. Biophys. Acta 2007, 1768, 2300-2309
24. Garner, A. E.; Smith, D. A.; Hooper, N. M. Visualization of detergent solubilization of membranes: implications for the isolation of rafts Biophys. J. 2008, 94, 1326-1340
25. Casadei, B. R.; Domingues, C. C.; de Paula, E.; Riske, K. A. Direct visualization of the action of Triton X-100 on giant vesicles of erythrocyte membrane lipids Biophys. J. 2014, 106, 2417-2425
26. van Rheenen, J.; Achame, E. M.; Janssen, H.; Calafat, J.; Jalink, K. PIP2 signaling in lipid domains: a critical re-evaluation EMBO J. 2005, 24, 1664-1673
27. Ingelmo-Torres, M.; Gaus, K.; Herms, A.; González-Moreno, E.; Kassan, A.; Bosch, M.; Grewal, T.; Tebar, F.; Enrich, C.; Pol, A. Triton X-100 promotes a cholesterol-dependent condensation of the plasma membrane Biochem. J. 2009, 420, 373-381
28. Baumgart, T.; Hess, S. T.; Webb, W. W. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension Nature 2003, 425, 821-824
29. Veatch, S. L.; Keller, S. L. Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol Biophys. J. 2003, 85, 3074-3083
30. Dimova, R.; Aranda, S.; Bezlyepkina, N.; Nikolov, V.; Riske, K. A.; Lipowsky, R. A practical guide to giant vesicles. Probing the membrane nanoregime via optical microscopy J. Phys.: Condens. Matter 2006, 18, 1151-1176
31. Nomura, F.; Nagata, M.; Inaba, T.; Hiramatsu, H.; Hotani, H.; Takiguchi, K. Capabilities of liposomes for topological transformation Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 2340-2345
32. Sudbrack, T. P.; Archilha, N. L.; Itri, R.; Riske, K. A. Observing the solubilization of lipid bilayers by detergents with optical microscopy of GUVs J. Phys. Chem. B 2011, 115, 269-277
33. Schnitzer, E.; Kozlov, M. M.; Lichtenberg, D. The effect of cholesterol on the solubilization of phosphatidylcholine bilayers by the non-ionic surfactant Triton X-100 Chem. Phys. Lipids 2005, 135, 69-82
34. Angelova, M. I.; Dimitrov, D. S. Liposome electroformation Faraday Discuss. 1986, 81, 303-311
35. Rouser, G.; Fleischer, S.; Yamamoto, A. Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots Lipids 1970, 5, 494-496
36. Aranda, S.; Riske, K. A.; Lipowsky, R.; Dimova, R. Morphological transitions of vesicles induced by alternating electric fields Biophys. J. 2008, 95, L19-21
37. Riske, K. A.; Dimova, R. Electro-deformation and poration of giant vesicles viewed with high temporal resolution Biophys. J. 2005, 88, 1143-1155
38. Hägerstrand, H.; Isomaa, B. Vesiculation induced by amphiphiles in erythrocytes Biochim. Biophys. Acta 1989, 982, 179-186
39. Lichtenberg, D.; Ahyaauch, H.; Alonson, A.; Goni, F. M. Detergent solubilization of lipid bilayers: a balance of driving forces Trends Biochem. Sci. 2013, 38, 85-93
40. Nyholm, T.; Slotte, J. P. Comparison of Triton X-100 penetration into phosphatidylcholine and sphingomyelin mono- and bilayers Langmuir 2001, 17, 4724-4730
41. Riske, K. A.; Sudbrack, T. P.; Archilha, N. L.; Uchoa, A. F.; Schroder, A. P.; Marques, C.; Baptista, M. S.; Itri, R. Giant vesicles under oxidative stress induced by a membrane-anchored photosensitizer Biophys. J. 2009, 97, 1362-1370
42. Alonso, A.; Villena, A.; Goni, F. M. Lysis and reassembly of sonicated lecithin vesicles in the presence of Triton X-100 FEBS Lett. 1981, 123, 200-204
43. Funari, S. S.; Nuscher, B.; Rapp, G.; Beyer, K. Detergent-phospholipid mixed micelles with a crystalline phospholipid core Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 8938-8943
44. Keller, S.; Tsamaloukas, A.; Heerklotz, H. A quantitative model describing the selective solubilization of membrane domains J. Am. Chem. Soc. 2005, 127, 11469-11476
45. Pathak, P.; London, E. Measurement of lipid nanodomain (raft) formation and size in sphingomyelin/POPC/cholesterol vesicles shows TX-100 and transmembrane helices increase domain size by coalescing preexisting nanodomains but do not induce domain formation Biophys. J. 2011, 101, 2417-2425
46. Almeida, R. F. M.; Fedorov, A.; Prieto, M. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts Biophys. J. 2003, 85, 2406-2416
47. Kucerka, N.; Nieh, M.; Katsaras, J. Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature Biochim. Biophys. Acta 2011, 1808, 2761-2771
48. Kucerka, N.; Tristram-Nagle, S.; Nagle, J. F. Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains J. Membr. Biol. 2005, 208, 193-202
49. Hofsäszlig;, C.; Lindahl, E.; Edholm, O. Molecular dynamics simulations of phospholipid bilayers with cholesterol Biophys. J. 2003, 84, 2192-2206
50. Maulik, P. R.; Sripada, P. K.; Shipley, G. G. Structure and thermotropic properties of hydrated N-stearoyl sphingomyelin bilayer membranes Biochim. Biophys. Acta 1991, 1062, 211-219
51. de la Maza, A.; Parra, J. L. Vesicle-micelle structural transition of phosphatidylcholine bilayers and Triton X-100 Biochem. J. 1994, 303, 907-914
52. Partearroyo, M. A.; Alonso, A.; Goni, F. M.; Tribout, M.; Paredes, S. J. Solubilization of phospholipid bilayers by surfactants belonging to the triton X series: effect of polar group size J. Colloid Interface Sci. 1996, 178, 156-159
53. Heerklotz, H.; Szadkowska, H.; Anderson, T.; Seelig, J. The sensitivity of lipid domains to small perturbations demonstrated by the effect of Triton J. Mol. Biol. 2003, 329, 793-799