Nanoscale analysis of supported lipid bilayers using atomic force microscopy

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 4, 2010, Pages 750-765

  El Kirat, Karim ^a   Morandat, Sandrine ^a   Dufrêne, Yves F ^b  

^a UNIVERSITÉ DE TECHNOLOGIE DE COMPIÈGNE   (France)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Atomic force microscopy; Biomembranes; Nanoscale organization; Real time imaging; Supported lipid bilayers

Indexed keywords

AMYLOID PROTEIN; ANTIINFECTIVE AGENT; CHOLESTEROL; DENDRIMER; DETERGENT; MEMBRANE PROTEIN; NANOPARTICLE; PEPTIDE DERIVATIVE; PHOSPHOLIPID; PROTEIN DERIVATIVE; SOLVENT;

ATOMIC FORCE MICROSCOPY; CATALYSIS; CELL MEMBRANE; DRUG DELIVERY SYSTEM; HUMAN; HYDROPHILICITY; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE BIOLOGY; MEMBRANE MODEL; MEMBRANE STABILIZATION; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR PROBE; NANOANALYSIS; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; REVIEW; SOLUBILITY; SURFACE PROPERTY;

LIPID BILAYERS; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; NANOSTRUCTURES; NANOTECHNOLOGY; PROTEIN BINDING;

EID: 77449144707     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.07.026     Document Type: Review

References (220)

1. Sackmann E. Supported membranes: scientific and practical applications. Science 271 (1996) 43-48
2. Castellana E.T., and Cremer P.S. Solid supported lipid bilayers: from biophysical studies to sensor design. Surf. Sci. Rep. 61 (2006) 429-444
3. Schuster B., and Sleytr U.B. Biomimetic S-layer supported lipid membranes. Curr. Nanosci. 2 (2006) 143-152
4. Chan Y.H., and Boxer S.G. Model membrane systems and their applications. Curr. Opin. Chem. Biol. 11 (2007) 581-587
5. Reimhult E., and Kumar K. Membrane biosensor platforms using nano- and microporous supports. Trends Biotechnol. 26 (2008) 82-89
6. Peetla C., Stine A., and Labhasetwar V.D. Biophysical interactions with model lipid membranes: applications in drug discovery and drug delivery. Mol. Pharm. 6 5 (2009) 1264-1276
7. Ulman A. Ultrathin organic films (1991), Academic Press, San Diego
8. Vie V., Van Mau M., Lesniewska E., Goudonnet J.P., Heitz F., and Le Grimellec C. Distribution of ganglioside GM1 between two component, two-phase phosphatidylcholine monolayers. Langmuir 14 (1998) 4574-4583
9. Rinia H.A., Demel R.A., van der Eerden J.P., and de Kruijff B. Blistering of Langmuir-Blodgett bilayers containing anionic phospholipids as observed by atomic force microscopy. Biophys. J. 77 (1999) 1683-1693
10. Dufrene Y.F., Barger W.R., Green J.-B.D., and Lee G.U. Nanometer-scale surface properties of mixed phospholipid monolayers and bilayers. Langmuir 13 (1997) 4779-4784
11. Horn R.G. Direct measurement of the force between two lipid bilayers and observation of their fusion. Biochim. Biophys. Acta 778 (1984) 224-228
12. Brian A.A., and McConnell H.M. Allogeneic stimulation of cytotoxic T cells by supported planar membranes. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 6159-6163
13. Jass J., Tjarnhage T., and Puu G. From liposomes to supported, planar bilayer structures on hydrophilic and hydrophobic surfaces: an atomic force microscopy study. Biophys. J. 79 (2000) 3153-3163
14. Richter R.P., and Brisson A.R. Following the formation of supported lipid bilayers on mica: a study combining AFM, QCM-D, and ellipsometry. Biophys. J. 88 (2005) 3422-3433
15. Richter R., Mukhopadhyay A., and Brisson A. Pathways of lipid vesicle deposition on solid surfaces: a combined QCM-D and AFM study. Biophys. J. 85 (2003) 3035-3047
16. Richter R.P., Berat R., and Brisson A.R. Formation of solid-supported lipid bilayers: an integrated view. Langmuir 22 (2006) 3497-3505
17. Przybylo M., Sykora J., Humpolickova J., Benda A., Zan A., and Hof M. Lipid diffusion in giant unilamellar vesicles is more than 2 times faster than in supported phospholipid bilayers under identical conditions. Langmuir 22 (2006) 9096-9099
18. Mennicke U., and Salditt T. Preparation of solid-supported lipid bilayers by spin-coating. Langmuir 18 (2002) 8172-8177
19. Simonsen A.C., and Bagatolli L.A. Structure of spin-coated lipid films and domain formation in supported membranes formed by hydration. Langmuir 20 (2004) 9720-9728
20. Pompeo G., Girasole M., Cricenti A., Cattaruzza F., Flamini A., Prosperi T., Generosi J., and Castellano A.C. AFM characterization of solid-supported lipid multilayers prepared by spin-coating. Biochim. Biophys. Acta 1712 (2005) 29-36
21. Chiantia S., Kahya N., and Schwille P. Dehydration damage of domain-exhibiting supported bilayers: an AFM study on the protective effects of disaccharides and other stabilizing substances. Langmuir 21 (2005) 6317-6323
22. Bennun S.V., Faller R., and Longo M.L. Drying and rehydration of DLPC/DSPC symmetric and asymmetric supported lipid bilayers: a combined AFM and fluorescence microscopy study. Langmuir 24 (2008) 10371-10381
23. Slotte J.P. Direct observation of the action of cholesterol oxidase in monolayers. Biochim. Biophys. Acta 1259 (1995) 180-186
24. Honig D., and Mobius D. Direct visualization of monolayers at the air-water-interface by Brewster-angle microscopy. J. Phys. Chem. 95 (1991) 4590-4592
25. Kago K., Matsuoka H., Yoshitome R., Yamaoka H., Ijiro K., and Shimomura M. Direct in situ observation of a lipid monolayer-DNA complex at the air-water interface by X-ray reflectometry. Langmuir 15 (1999) 5193-5196
26. Möhwald H. Direct characterization of monolayers at the air-water interface. Thin Solid Films 159 (1988) 1-15
27. Reinl H., Brumm T., and Bayerl T.M. Changes of the physical properties of the liquid-ordered phase with temperature in binary mixtures of DPPC with cholesterol: a H-NMR, FT-IR, DSC, and neutron scattering study. Biophys. J. 61 (1992) 1025-1035
28. Grelard A., Couvreux A., Loudet C., and Dufourc E.J. Solution and solid-state NMR of lipids. Methods Mol. Biol. 462 (2009) 111-133
29. Bechinger B. The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta 1462 (1999) 157-183
30. Dufrene Y.F., Boland T., Schneider J.W., Barger W.R., and Lee G.U. Characterization of the physical properties of model biomembranes at the nanometer scale with the atomic force microscope. Faraday Discuss. 111 (1998) 79-94
31. Deleu M., Paquot M., Jacques P., Thonart P., Adriaensen Y., and Dufrene Y.F. Nanometer scale organization of mixed surfactin/phosphatidylcholine monolayers. Biophys. J. 77 (1999) 2304-2310
32. Schram V., Lin H.N., and Thompson T.E. Topology of gel-phase domains and lipid mixing properties in phase-separated two-component phosphatidylcholine bilayers. Biophys. J. 71 (1996) 1811-1822
33. Linton R., Guarisco V., Lee J.J., Hagenhoff B., and Benninghoven A. Analytical surface spectroscopy of phospholipid Langmuir-Blodgett-films. Thin Solid Films 210 (1992) 565-570
34. Binnig G., Quate C.F., and Gerber C. Atomic force microscope. Phys. Rev. Lett. 56 (1986) 930-933
35. Muller D.J., and Dufrene Y.F. Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nat. Nanotechnol. 3 (2008) 261-269
36. Dufrene Y.F. Towards nanomicrobiology using atomic force microscopy. Nat. Rev. Microbiol. 6 (2008) 674-680
37. Schneider J., Dufrene Y.F., Barger Jr. W.R., and Lee G.U. Atomic force microscope image contrast mechanisms on supported lipid bilayers. Biophys. J. 79 (2000) 1107-1118
38. Schneider J., Barger W., and Lee G.U. Nanometer scale surface properties of supported lipid bilayers measured with hydrophobic and hydrophilic atomic force microscope probes. Langmuir 19 (2003) 1899-1907
39. Kunneke S., Kruger D., and Janshoff A. Scrutiny of the failure of lipid membranes as a function of headgroups, chain length, and lamellarity measured by scanning force microscopy. Biophys. J. 86 (2004) 1545-1553
40. Garcia-Manyes S., Oncins G., and Sanz F. Effect of ion-binding and chemical phospholipid structure on the nanomechanics of lipid bilayers studied by force spectroscopy. Biophys. J. 89 (2005) 1812-1826
41. Abdulreda M.H., and Moy V.T. Atomic force microscope studies of the fusion of floating lipid bilayers. Biophys. J. 92 (2007) 4369-4378
42. Picas L., Montero M.T., Morros A., Cabanas M.E., Seantier B., Milhiet P.E., and Hernandez-Borrell J. Calcium-induced formation of subdomains in phosphatidylethanolamine-phosphatidylglycerol bilayers: a combined DSC, 31P NMR, and AFM study. J. Phys. Chem. B 113 (2009) 4648-4655
43. R.M. Sullan, J.K. Li, S. Zou, Direct correlation of structures and nanomechanical properties of multicomponent lipid bilayers, Langmuir 25 (2009) 7471-7477.
44. Weisenhorn A.L., Schmitt F.J., Knoll W., and Hansma P.K. Streptavidin binding observed with an atomic force microscope. Ultramicroscopy 42-44 Pt B (1992) 1125-1132
45. Giocondi M.-C., Vie V., Lesniewska E., Milhiet P.-E., Zinke-Allmang M., and Le Grimellec C. Phase topology and growth of single domains in lipid bilayers. Langmuir 17 (2001) 1653-1659
46. Giocondi M.C., Boichot S., Plenat T., and Le Grimellec C.C. Structural diversity of sphingomyelin microdomains. Ultramicroscopy 100 (2004) 135-143
47. Lin W.C., Blanchette C.D., Ratto T.V., and Longo M.L. Lipid asymmetry in DLPC/DSPC-supported lipid bilayers: a combined AFM and fluorescence microscopy study. Biophys. J. 90 (2006) 228-237
48. Johnston L.J. Nanoscale imaging of domains in supported lipid membranes. Langmuir 23 (2007) 5886-5895
49. Kaasgaard T., Leidy C., Crowe J.H., Mouritsen O.G., and Jorgensen K. Temperature-controlled structure and kinetics of ripple phases in one- and two-component supported lipid bilayers. Biophys. J. 85 (2003) 350-360
50. Leidy C., Kaasgaard T., Crowe J.H., Mouritsen O.G., and Jorgensen K. Ripples and the formation of anisotropic lipid domains: imaging two-component supported double bilayers by atomic force microscopy. Biophys. J. 83 (2002) 2625-2633
51. Giocondi M.C., Pacheco L., Milhiet P.E., and Le Grimellec C. Temperature dependence of the topology of supported dimirystoyl-distearoyl phosphatidylcholine bilayers. Ultramicroscopy 86 (2001) 151-157
52. Blanchette C.D., Lin W.C., Ratto T.V., and Longo M.L. Galactosylceramide domain microstructure: impact of cholesterol and nucleation/growth conditions. Biophys. J. 90 (2006) 4466-4478
53. Blanchette C.D., Orme C.A., Ratto T.V., and Longo M.L. Quantifying growth of symmetric and asymmetric lipid bilayer domains. Langmuir 24 (2008) 1219-1224
54. Goksu E.I., Vanegas J.M., Blanchette C.D., Lin W.C., and Longo M.L. AFM for structure and dynamics of biomembranes. Biochim. Biophys. Acta 1788 (2009) 254-266
55. Bernchou U., Ipsen J.H., and Simonsen A.C. Growth of solid domains in model membranes: quantitative image analysis reveals a strong correlation between domain shape and spatial position. J. Phys. Chem. B 113 (2009) 7170-7177
56. Choucair A., Chakrapani M., Chakravarthy B., Katsaras J., and Johnston L.J. Preferential accumulation of Abeta(1-42) on gel phase domains of lipid bilayers: an AFM and fluorescence study. Biochim. Biophys. Acta 1768 (2007) 146-154
57. Anderson R.G. The caveolae membrane system. Annu. Rev. Biochem. 67 (1998) 199-225
58. Harder T., and Simons K. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9 (1997) 534-542
59. McMullen T.P.W., Lewis R.N.A.H., and McElhaney R.N. Cholesterol-phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes. Curr. Opin. Colloid Interface Sci. 8 (2004) 459-468
60. Rinia H.A., Snel M.M., van der Eerden J.P., and de Kruijff B. Visualizing detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett. 501 (2001) 92-96
61. Saslowsky D.E., Lawrence J., Ren X., Brown D.A., Henderson R.M., and Edwardson J.M. Placental alkaline phosphatase is efficiently targeted to rafts in supported lipid bilayers. J. Biol. Chem. 277 (2002) 26966-26970
62. Lin W.C., Blanchette C.D., and Longo M.L. Fluid-phase chain unsaturation controlling domain microstructure and phase in ternary lipid bilayers containing GalCer and cholesterol. Biophys. J. 92 (2007) 2831-2841
63. Chiantia S., Kahya N., Ries J., and Schwille P. Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS. Biophys. J. 90 (2006) 4500-4508
64. Chiantia S., Kahya N., and Schwille P. Raft domain reorganization driven by short- and long-chain ceramide: a combined AFM and FCS study. Langmuir 23 (2007) 7659-7665
65. El Kirat K., and Morandat S. Cholesterol modulation of membrane resistance to Triton X-100 explored by atomic force microscopy. Biochim. Biophys. Acta 1768 (2007) 2300-2309
66. Milhiet P.E., Giocondi M.C., Baghdadi O., Ronzon F., Roux B., and Le Grimellec C. Spontaneous insertion and partitioning of alkaline phosphatase into model lipid rafts. EMBO Rep. 3 (2002) 485-490
67. Kolesnick R.N., Goni F.M., and Alonso A. Compartmentalization of ceramide signaling: physical foundations and biological effects. J. Cell Physiol. 184 (2000) 285-300
68. Bollinger C.R., Teichgraber V., and Gulbins E. Ceramide-enriched membrane domains. Biochim. Biophys. Acta 1746 (2005) 284-294
69. Hannun Y.A. Functions of ceramide in coordinating cellular responses to stress. Science 274 (1996) 1855-1859
70. Brown D.A., and Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68 (1992) 533-544
71. Domenech O., Redondo L., Montero M.T., and Hernandez-Borrell J. Specific adsorption of cytochrome C on cardiolipin-glycerophospholipid monolayers and bilayers. Langmuir 23 (2007) 5651-5656
72. Reviakine I., Simon A., and Brisson A. Effect of Ca2+ on the morphology of mixed DPPC-DOPS supported phospholipid bilayers. Langmuir 16 (2000) 1473-1477
73. Mou J., Yang J., Huang C., and Shao Z. Alcohol induces interdigitated domains in unilamellar phosphatidylcholine bilayers. Biochemistry 33 (1994) 9981-9985
74. Mcclain R.L., and Breen J.J. The image-based observation of the L beta I-to-L-beta′ phase transition in solid-supported lipid bilayers. Langmuir 17 (2001) 5121-5124
75. 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
76. Singer S.J., and Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 175 (1972) 720-731
77. Simons K., and van Meer G. Lipid sorting in epithelial cells. Biochemistry 27 (1988) 6197-6202
78. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
79. Cinek T., and Horejsi V. The nature of large noncovalent complexes containing glycosyl-phosphatidylinositol-anchored membrane glycoproteins and protein tyrosine kinases. J. Immunol. 149 (1992) 2262-2270
80. Brown D.A., and London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275 (2000) 17221-17224
81. Simons K., and Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1 (2000) 31-39
82. Lencer W.I., and Saslowsky D. Raft trafficking of AB5 subunit bacterial toxins. Biochim. Biophys. Acta 1746 (2005) 314-321
83. Taylor D.R., and Hooper N.M. The prion protein and lipid rafts. Mol. Membr. Biol. 23 (2006) 89-99
84. Schroeder R.J., London E., and Brown D.A. Insaturations between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behaviour. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 12130-12134
85. Pike L.J., Han X., Chung K.N., and Gross R.W. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry 41 (2002) 2075-2088
86. Bonnin S., El Kirat K., Becchi M., Dubois M., Grangeasse C., Giraud C., Prigent A.F., Lagarde M., Roux B., and Besson F. Protein and lipid analysis of detergent-resistant membranes isolated from bovine kidney. Biochimie 85 (2003) 1237-1244
87. Jackson M.L., Schmidt C.F., Lichtenberg D., Litman B.J., and Albert A.D. Solubilization of phosphatidylcholine bilayers by octyl glucoside. Biochemistry 21 (1982) 4576-4582
88. Rigaud J.L., Paternostre M.T., and Bluzat A. Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 2. Incorporation of the light-driven proton pump bacteriorhodopsin. Biochemistry 27 (1988) 2677-2688
89. Paternostre M.T., Roux M., and Rigaud J.L. Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 1. Solubilization of large unilamellar liposomes (prepared by reverse-phase evaporation) by Triton X-100, octyl glucoside, and sodium cholate. Biochemistry 27 (1988) 2668-2677
90. Morandat S., and El Kirat K. Membrane resistance to Triton X-100 explored by real-time atomic force microscopy. Langmuir 22 (2006) 5786-5791
91. Morandat S., and El Kirat K. Solubilization of supported lipid membranes by octyl glucoside observed by time-lapse atomic force microscopy. Colloids Surf. B 55 (2007) 179-184
92. Milhiet P.E., Gubellini F., Berquand A., Dosset P., Rigaud J.L., Le Grimellec C., and Levy D. High-resolution AFM of membrane proteins directly incorporated at high density in planar lipid bilayer. Biophys. J. 91 (2006) 3268-3275
93. Berquand A., Levy D., Gubellini F., Le Grimellec C., and Milhiet P.E. Influence of calcium on direct incorporation of membrane proteins into in-plane lipid bilayer. Ultramicroscopy 107 (2007) 928-933
94. El Kirat K., Pardo-Jacques A., and Morandat S. Interaction of non-ionic detergents with biomembranes at the nanoscale observed by atomic force microscopy. Int. J. Nanotechnol. 5 (2008) 769-783
95. Rinia H.A., Kik R.A., Demel R.A., Snel M.M., Killian J.A., van Der Eerden J.P., and de Kruijff B. Visualization of highly ordered striated domains induced by transmembrane peptides in supported phosphatidylcholine bilayers. Biochemistry 39 (2000) 5852-5858
96. Rinia H.A., Boots J.W., Rijkers D.T., Kik R.A., Snel M.M., Demel R.A., Killian J.A., van der Eerden J.P., and de Kruijff B. Domain formation in phosphatidylcholine bilayers containing transmembrane peptides: specific effects of flanking residues. Biochemistry 41 (2002) 2814-2824
97. Lins L., Decaffmeyer M., Thomas A., and Brasseur R. Relationships between the orientation and the structural properties of peptides and their membrane interactions. Biochim. Biophys. Acta 1778 (2008) 1537-1544
98. Epand R.M., and Vogel H.J. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462 (1999) 11-28
99. Pedersen T.B., Kaasgaard T., Jensen M.O., Frokjaer S., Mouritsen O.G., and Jorgensen K. Phase behavior and nanoscale structure of phospholipid membranes incorporated with acylated C14-peptides. Biophys. J. 89 (2005) 2494-2503
100. Mou J., Czajkowsky D.M., and Shao Z. Gramicidin A aggregation in supported gel state phosphatidylcholine bilayers. Biochemistry 35 (1996) 3222-3226
101. Steinem C., Galla H.J., and Janshoff A. Interaction of melittin with solid supported membranes. Phys. Chem. Chem. Phys. 2 (2000) 4580-4585
102. Mecke A., Lee D.K., Ramamoorthy A., Orr B.G., and Banaszak Holl M.M. Membrane thinning due to antimicrobial peptide binding: an atomic force microscopy study of MSI-78 in lipid bilayers. Biophys. J. 89 (2005) 4043-4050
103. Shaw J.E., Alattia J.R., Verity J.E., Prive G.G., and Yip C.M. Mechanisms of antimicrobial peptide action: studies of indolicidin assembly at model membrane interfaces by in situ atomic force microscopy. J. Struct. Biol. 154 (2006) 42-58
104. Epand R.F., Yip C.M., Chernomordik L.V., LeDuc D.L., Shin Y.K., and Epand R.M. Self-assembly of influenza hemagglutinin: studies of ectodomain aggregation by in situ atomic force microscopy. Biochim. Biophys. Acta 1513 (2001) 167-175
105. Brasseur R. Tilted peptides: a motif for membrane destabilization (hypothesis). Mol. Membr. Biol. 17 (2000) 31-40
106. Brasseur R., Pillot T., Lins L., Vandekerckhove J., and Rosseneu M. Peptides in membranes: tipping the balance of membrane stability. Trends Biochem. Sci. 22 (1997) 167-171
107. Lins L., Flore C., Chapelle L., Talmud P.J., Thomas A., and Brasseur R. Lipid-interacting properties of the N-terminal domain of human apolipoprotein C-III. Protein Eng. 15 (2002) 513-520
108. El Kirat K., Lins L., Brasseur R., and Dufrene Y.F. Fusogenic tilted peptides induce nanoscale holes in supported phosphatidylcholine bilayers. Langmuir 21 (2005) 3116-3121
109. Lev N., and Shai Y. Fatty acids can substitute the HIV fusion peptide in lipid merging and fusion: an analogy between viral and palmitoylated eukaryotic fusion proteins. J. Mol. Biol. 374 (2007) 220-230
110. Chernomordik L. Non-bilayer lipids and biological fusion intermediates. Chem. Phys. Lipids 81 (1996) 203-213
111. Haque M.E., and Lentz B.R. Roles of curvature and hydrophobic interstice energy in fusion: studies of lipid perturbant effects. Biochemistry 43 (2004) 3507-3517
112. El Kirat K., Dufrene Y.F., Lins L., and Brasseur R. The SIV tilted peptide induces cylindrical reverse micelles in supported lipid bilayers. Biochemistry 45 (2006) 9336-9341
113. Herbig M.E., Assi F., Textor M., and Merkle H.P. The cell penetrating peptides pVEC and W2-pVEC induce transformation of gel phase domains in phospholipid bilayers without affecting their integrity. Biochemistry 45 (2006) 3598-3609
114. Plenat T., Boichot S., Dosset P., Milhiet P.E., and Le Grimellec C. Coexistence of a two-states organization for a cell-penetrating peptide in lipid bilayer. Biophys. J. 89 (2005) 4300-4309
115. Sipe J.D., and Cohen A.S. Review: history of the amyloid fibril. J. Struct. Biol. 130 (2000) 88-98
116. Yip C.M., and McLaurin J. Amyloid-beta peptide assembly: a critical step in fibrillogenesis and membrane disruption. Biophys. J. 80 (2001) 1359-1371
117. Yip C.M., Darabie A.A., and McLaurin J. Abeta42-peptide assembly on lipid bilayers. J. Mol. Biol. 318 (2002) 97-107
118. Zhang L., Zhong J., Huang L., Wang L., Hong Y., and Sha Y. Parallel-oriented fibrogenesis of a beta-sheet forming peptide on supported lipid bilayers. J. Phys. Chem. B 112 (2008) 8950-8954
119. Zhong J., Zheng W., Huang L., Hong Y., Wang L., Qiu Y., and Sha Y. PrP106-126 amide causes the semi-penetrated poration in the supported lipid bilayers. Biochim. Biophys. Acta 1768 (2007) 1420-1429
120. Kakinuma A., Ouchida A., Shima T., Sugino H., Isono M., Tamura G., and Arima K. Confirmation of structure of surfactin by mass spectrometry. Agric. Biol. Chem. 33 (1969) 1669-1671
121. Brasseur R., Braun N., El Kirat K., Deleu M., Mingeot-Leclercq M.P., and Dufrene Y.F. The biologically important surfactin lipopeptide induces nanoripples in supported lipid bilayers. Langmuir 23 (2007) 9769-9772
122. Francius G., Dufour S., Deleu M., Paquot M., Mingeot-Leclercq M.P., and Dufrene Y.F. Nanoscale membrane activity of surfactins: influence of geometry, charge and hydrophobicity. Biochim. Biophys. Acta 1778 (2008) 2058-2068
123. Chen M., Li M., Brosseau C.L., and Lipkowski J. AFM studies of the effect of temperature and electric field on the structure of a DMPC-cholesterol bilayer supported on a Au(111) electrode surface. Langmuir 25 (2009) 1028-1037
124. Quist A.P., Chand A., Ramachandran S., Daraio C., Jin S., and Lal R. Atomic force microscopy imaging and electrical recording of lipid bilayers supported over microfabricated silicon chip nanopores: lab-on-a-chip system for lipid membranes and ion channels. Langmuir 23 (2007) 1375-1380
125. Goncalves R.P., Agnus G., Sens P., Houssin C., Bartenlian B., and Scheuring S. Two-chamber AFM: probing membrane proteins separating two aqueous compartments. Nat. Methods 3 (2006) 1007-1012
126. Dufrene Y.F. Atomic force microscopy of membrane proteins separating two aqueous compartments. Nat. Methods 3 (2006) 973-975
127. Marsh D. Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta 1778 (2008) 1545-1575
128. Giocondi M.C., Besson F., Dosset P., Milhiet P.E., and Le Grimellec C. Remodeling of ordered membrane domains by GPI-anchored intestinal alkaline phosphatase. Langmuir 23 (2007) 9358-9364
129. Giocondi M.C., Besson F., Dosset P., Milhiet P.E., and Le Grimellec C. Temperature-dependent localization of GPI-anchored intestinal alkaline phosphatase in model rafts. J. Mol. Recognit. 20 (2007) 531-537
130. Chiantia S., Ries J., Chwastek G., Carrer D., Li Z., Bittman R., and Schwille P. Role of ceramide in membrane protein organization investigated by combined AFM and FCS. Biochim. Biophys. Acta 1778 (2008) 1356-1364
131. Grandbois M., Clausen-Schaumann H., and Gaub H. Atomic force microscope imaging of phospholipid bilayer degradation by phospholipase A2. Biophys. J. 74 (1998) 2398-2404
132. Clausen-Schaumann H., Grandbois M., and Gaub H.E. Enzyme-assisted nanoscale lithography in lipid membranes. Adv. Mater. 10 (1998) 949-952
133. Nielsen L.K., Risbo J., Callisen T.H., and Bjornholm T. Lag-burst kinetics in phospholipase A(2) hydrolysis of DPPC bilayers visualized by atomic force microscopy. Biochim. Biophys. Acta 1420 (1999) 266-271
134. Nielsen L.K., Balashev K., Callisen T.H., and Bjornholm T. Influence of product phase separation on phospholipase A(2) hydrolysis of supported phospholipid bilayers studied by force microscopy. Biophys. J. 83 (2002) 2617-2624
135. Leidy C., Mouritsen O.G., Jorgensen K., and Peters G.H. Evolution of a rippled membrane during phospholipase A2 hydrolysis studied by time-resolved AFM. Biophys. J. 87 (2004) 408-418
136. El Kirat K., Dupres V., and Dufrene Y.F. Blistering of supported lipid membranes induced by Phospholipase D, as observed by real-time atomic force microscopy. Biochim. Biophys. Acta 1778 (2008) 276-282
137. Ira R., and Johnston L.J. Sphingomyelinase generation of ceramide promotes clustering of nanoscale domains in supported bilayer membranes. Biochim. Biophys. Acta 1778 (2008) 185-197
138. Ira, Zhou S., Ramirez D.M., Vanderlip S., Ogilvie W., Jakubek Z.J., and Johnston L.J. Enzymatic generation of ceramide induces membrane restructuring: correlated AFM and fluorescence imaging of supported bilayers. J. Struct. Biol. 168 1 (2009) 78-89
139. Alattia J.R., Shaw J.E., Yip C.M., and Prive G.G. Direct visualization of saposin remodelling of lipid bilayers. J. Mol. Biol. 362 (2006) 943-953
140. You H.X., Qi X., and Yu L. Direct AFM observation of saposin C-induced membrane domains in lipid bilayers: from simple to complex lipid mixtures. Chem. Phys. Lipids 132 (2004) 15-22
141. Alattia J.R., Shaw J.E., Yip C.M., and Prive G.G. Molecular imaging of membrane interfaces reveals mode of beta-glucosidase activation by saposin C. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 17394-17399
142. Cortese J.D., Voglino A.L., and Hackenbrock C.R. Multiple conformations of physiological membrane-bound cytochrome c. Biochemistry 37 (1998) 6402-6409
143. Choi E.J., and Dimitriadis E.K. Cytochrome c adsorption to supported, anionic lipid bilayers studied via atomic force microscopy. Biophys. J. 87 (2004) 3234-3241
144. Morandat S., and El Kirat K. Real-time atomic force microscopy reveals cytochrome c-induced alterations in neutral lipid bilayers. Langmuir 23 (2007) 10929-10932
145. Furuike S., Hirokawa J., Yamada S., and Yamazaki M. Atomic force microscopy studies of interaction of the 20S proteasome with supported lipid bilayers. Biochim. Biophys. Acta 1615 (2003) 1-6
146. Herrig A., Janke M., Austermann J., Gerke V., Janshoff A., and Steinem C. Cooperative adsorption of ezrin on PIP2-containing membranes. Biochemistry 45 (2006) 13025-13034
147. Zebrowska A., and Krysinski P. Incorporation of Na(+), K(+)-ATP-ase into the thiolipid biomimetic assemblies via the fusion of proteoliposomes. Langmuir 20 (2004) 11127-11133
148. Jeuken L.J., Connell S.D., Henderson P.J., Gennis R.B., Evans S.D., and Bushby R.J. Redox enzymes in tethered membranes. J. Am. Chem. Soc. 128 (2006) 1711-1716
149. Deniaud A., Rossi C., Berquand A., Homand J., Campagna S., Knoll W., Brenner C., and Chopineau J. Voltage-dependent anion channel transports calcium ions through biomimetic membranes. Langmuir 23 (2007) 3898-3905
150. Friedrich M.G., Kirste V.U., Zhu J., Gennis R.B., Knoll W., and Naumann R.L. Activity of membrane proteins immobilized on surfaces as a function of packing density. J. Phys. Chem. B 112 (2008) 3193-3201
151. Seydel J.K., and Wiese M. Drug-membrane interactions (2002), Wiley-VCH, Weinheim
152. Seydel J.K., Coats E.A., Cordes H.P., and Wiese M. Drug membrane interaction and the importance for drug transport, distribution, accumulation, efficacy and resistance. Arch. Pharm. 327 (1994) 601-610
153. Mouritsen O.G., and Jorgensen K. A new look at lipid-membrane structure in relation to drug research. Pharm. Res. 15 (1998) 1507-1519
154. Berquand A., Mingeot-Leclercq M.P., and Dufrene Y.F. Real-time imaging of drug-membrane interactions by atomic force microscopy. Biochim. Biophys. Acta 1664 (2004) 198-205
155. Bensikaddour H., Fa N., Burton I., Deleu M., Lins L., Schanck A., Brasseur R., Dufrene Y.F., Goormaghtigh E., and Mingeot-Leclercq M.P. Characterization of the interactions between fluoroquinolone antibiotics and lipids: a multitechnique approach. Biophys. J. 94 (2008) 3035-3046
156. Montero M.T., Pijoan M., Merino-Montero S., Vinuesa T., and Hernandez-Borrell J. Interfacial membrane effects of fluoroquinolones as revealed by a combination of fluorescence binding experiments and atomic force microscopy observations. Langmuir 22 (2006) 7574-7578
157. Santos N.C., Ter-Ovanesyan E., Zasadzinski J.A., Prieto M., and Castanho M.A. Filipin-induced lesions in planar phospholipid bilayers imaged by atomic force microscopy. Biophys. J. 75 (1998) 1869-1873
158. Lawrence J.C., Saslowsky D.E., Edwardson J.M., and Henderson R.M. Real-time analysis of the effects of cholesterol on lipid raft behavior using atomic force microscopy. Biophys. J. 84 (2003) 1827-1832
159. Leonenko Z., Finot E., and Cramb D. AFM study of interaction forces in supported planar DPPC bilayers in the presence of general anesthetic halothane. Biochim. Biophys. Acta 1758 (2006) 487-492
160. Lorite G.S., Nobre T.M., Zaniquelli M.E., de Paula E., and Cotta M.A. Dibucaine effects on structural and elastic properties of lipid bilayers. Biophys. Chem. 139 (2009) 75-83
161. R.M. Brechignac, J.K. Houdy, S. Lahmani, Nanomaterials and Nanochemistry, Springer-Verlag Berlin and Heidelberg GmbH & Co. K (2008).
162. Riehemann K., Schneider S.W., Luger T.A., Godin B., Ferrari M., and Fuchs H. Nanomedicine-challenge and perspectives. Angew. Chem. Int. Ed. Eng.l 48 (2009) 872-897
163. Popielarski S.R., Hu-Lieskovan S., French S.W., Triche T.J., and Davis M.E. A nanoparticle-based model delivery system to guide the rational design of gene delivery to the liver. 2. In vitro and in vivo uptake results. Bioconjug. Chem. 16 (2005) 1071-1080
164. Bielinska A.U., Yen A., Wu H.L., Zahos K.M., Sun R., Weiner N.D., Baker Jr. J.R., and Roessler B.J. Application of membrane-based dendrimer/DNA complexes for solid phase transfection in vitro and in vivo. Biomaterials 21 (2000) 877-887
165. Boas U., and Heegaard P.M. Dendrimers in drug research. Chem. Soc. Rev. 33 (2004) 43-63
166. Gillies E.R., and Frechet J.M. Dendrimers and dendritic polymers in drug delivery. Drug Discov. Today 10 (2005) 35-43
167. Manunta M., Tan P.H., Sagoo P., Kashefi K., and George A.J. Gene delivery by dendrimers operates via a cholesterol dependent pathway. Nucleic Acids Res. 32 (2004) 2730-2739
168. Mecke A., Uppuluri S., Sassanella T.M., Lee D.K., Ramamoorthy A., Baker Jr. J.R., Orr B.G., and Banaszak Holl M.M. Direct observation of lipid bilayer disruption by poly(amidoamine) dendrimers. Chem. Phys. Lipids 132 (2004) 3-14
169. Hong S., Bielinska A.U., Mecke A., Keszler B., Beals J.L., Shi X., Balogh L., Orr B.G., Baker Jr. J.R., and Banaszak Holl M.M. Interaction of poly(amidoamine) dendrimers with supported lipid bilayers and cells: hole formation and the relation to transport. Bioconjug. Chem. 15 (2004) 774-782
170. Mecke A., Majoros I.J., Patri A.K., Baker Jr. J.R., Holl M.M., and Orr B.G. Lipid bilayer disruption by polycationic polymers: the roles of size and chemical functional group. Langmuir 21 (2005) 10348-10354
171. Hong S., Hessler J.A., Banaszak Holl M.M., Leroueil P., Mecke A., and Orr B.G. Physical interactions of nanoparticles with biological membranes: the observation of nanoscale hole formation. J. Chem. Health Safety 13 (2006) 16-20
172. Leroueil P.R., Hong S., Mecke A., Baker Jr. J.R., Orr B.G., and Banaszak Holl M.M. Nanoparticle interaction with biological membranes: does nanotechnology present a Janus face?. Acc. Chem. Res. 40 (2007) 335-342
173. Leroueil P.R., Berry S.A., Duthie K., Han G., Rotello V.M., McNerny D.Q., Baker Jr. J.R., Orr B.G., and Holl M.M. Wide varieties of cationic nanoparticles induce defects in supported lipid bilayers. Nano Lett. 8 (2008) 420-424
174. Erickson B., DiMaggio S.C., Mullen D.G., Kelly C.V., Leroueil P.R., Berry S.A., Baker Jr. J.R., Orr B.G., and Banaszak Holl M.M. Interactions of poly(amidoamine) dendrimers with Survanta lung surfactant: the importance of lipid domains. Langmuir 24 (2008) 11003-11008
175. Parimi S., Barnes T.J., and Prestidge C.A. PAMAM dendrimer interactions with supported lipid bilayers: a kinetic and mechanistic investigation. Langmuir 24 (2008) 13532-13539
176. Spurlin T.A., and Gewirth A.A. Effect of C60 on solid supported lipid bilayers. Nano Lett. 7 (2007) 531-535
177. Moller C., Allen M., Elings V., Engel A., and Muller D.J. Tapping-mode atomic force microscopy produces faithful high-resolution images of protein surfaces. Biophys. J. 77 (1999) 1150-1158
178. Muller D.J., Sass H.J., Muller S.A., Buldt G., and Engel A. Surface structures of native bacteriorhodopsin depend on the molecular packing arrangement in the membrane. J. Mol. Biol. 285 (1999) 1903-1909
179. Persike N., Pfeiffer M., Guckenberger R., Radmacher M., and Fritz M. Direct observation of different surface structures on high-resolution images of native halorhodopsin. J. Mol. Biol. 310 (2001) 773-780
180. Cisneros D.A., Oesterhelt D., and Muller D.J. Probing origins of molecular interactions stabilizing the membrane proteins halorhodopsin and bacteriorhodopsin. Structure 13 (2005) 235-242
181. Buzhynskyy N., Girmens J.F., Faigle W., and Scheuring S. Human cataract lens membrane at subnanometer resolution. J. Mol. Biol. 374 (2007) 162-169
182. Scheuring S., Buzhynskyy N., Jaroslawski S., Goncalves R.P., Hite R.K., and Walz T. Structural models of the supramolecular organization of AQP0 and connexons in junctional microdomains. J. Struct. Biol. 160 (2007) 385-394
183. Goncalves R.P., Buzhynskyy N., Prima V., Sturgis J.N., and Scheuring S. Supramolecular assembly of VDAC in native mitochondrial outer membranes. J. Mol. Biol. 369 (2007) 413-418
184. John S.A., Saner D., Pitts J.D., Holzenburg A., Finbow M.E., and Lal R. Atomic force microscopy of arthropod gap junctions. J. Struct. Biol. 120 (1997) 22-31
185. Scheuring S., Seguin J., Marco S., Levy D., Robert B., and Rigaud J.L. Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 1690-1693
186. Scheuring S., Rigaud J.L., and Sturgis J.N. Variable LH2 stoichiometry and core clustering in native membranes of Rhodospirillum photometricum. EMBO J. 23 (2004) 4127-4133
187. Scheuring S., and Sturgis J.N. Chromatic adaptation of photosynthetic membranes. Science 309 (2005) 484-487
188. Bahatyrova S., Frese R.N., Siebert C.A., Olsen J.D., Van Der Werf K.O., Van Grondelle R., Niederman R.A., Bullough P.A., Otto C., and Hunter C.N. The native architecture of a photosynthetic membrane. Nature 430 (2004) 1058-1062
189. Scheuring S., Busselez J., and Levy D. Structure of the dimeric PufX-containing core complex of Rhodobacter blasticus by in situ atomic force microscopy. J. Biol. Chem. 280 (2005) 1426-1431
190. Scheuring S., Goncalves R.P., Prima V., and Sturgis J.N. The photosynthetic apparatus of Rhodopseudomonas palustris: structures and organization. J. Mol. Biol. 358 (2006) 83-96
191. Vie V., Van Mau N., Pomarede P., Dance C., Schwartz J.L., Laprade R., Frutos R., Rang C., Masson L., Heitz F., and Le Grimellec C. Lipid-induced pore formation of the Bacillus thuringiensis Cry1Aa insecticidal toxin. J. Membr. Biol. 180 (2001) 195-203
192. Mou J., Yang J., and Shao Z. Atomic force microscopy of cholera toxin B-oligomers bound to bilayers of biologically relevant lipids. J. Mol. Biol. 248 (1995) 507-512
193. Fang Y., Cheley S., Bayley H., and Yang J. The heptameric prepore of a staphylococcal alpha-hemolysin mutant in lipid bilayers imaged by atomic force microscopy. Biochemistry 36 (1997) 9518-9522
194. Malghani M.S., Fang Y., Cheley S., Bayley H., and Yang J. Heptameric structures of two alpha-hemolysin mutants imaged with in situ atomic force microscopy. Microsc. Res. Tech. 44 (1999) 353-356
195. Czajkowsky D.M., Hotze E.M., Shao Z., and Tweten R.K. Vertical collapse of a cytolysin prepore moves its transmembrane beta-hairpins to the membrane. EMBO J. 23 (2004) 3206-3215
196. Yang J., Mou J., and Shao Z. Structure and stability of pertussis toxin studied by in situ atomic force microscopy. FEBS Lett. 338 (1994) 89-92
197. Czajkowsky D.M., Iwamoto H., Cover T.L., and Shao Z. The vacuolating toxin from Helicobacter pylori forms hexameric pores in lipid bilayers at low pH. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 2001-2006
198. Reviakine I., and Brisson A. Streptavidin 2D crystals on supported phospholipid bilayers: toward constructing anchored phospholipid bilayers. Langmuir 17 (2001) 8293-8299
199. Reviakine I., Bergsma-Schutter W., and Brisson A. Growth of protein 2-D crystals on supported planar lipid bilayers imaged in situ by AFM. J. Struct. Biol. 121 (1998) 356-361
200. Reviakine I., Bergsma-Schutter W., Mazeres-Dubut C., Govorukhina N., and Brisson A. Surface topography of the p3 and p6 annexin V crystal forms determined by atomic force microscopy. J. Struct. Biol. 131 (2000) 234-239
201. Reviakine I., Bergsma-Schutter W., Morozov A.N., and Brisson A. Two-dimensional crystallization of annexin A5 on phospholipid bilayers and monolayers: a solid-solid phase transition between crystal forms. Langmuir 17 (2001) 1680-1686
202. Richter R.P., Him J.L., Tessier B., Tessier C., and Brisson A.R. On the kinetics of adsorption and two-dimensional self-assembly of annexin A5 on supported lipid bilayers. Biophys. J. 89 (2005) 3372-3385
203. Kim D.T., Blanch H.W., and Radke C.J. Imaging of reconstituted purple membranes by atomic force microscopy. Colloids Surf. B 41 (2005) 263-276
204. Klyszejko A.L., Shastri S., Mari S.A., Grubmuller H., Muller D.J., and Glaubitz C. Folding and assembly of proteorhodopsin. J. Mol. Biol. 376 (2008) 35-41
205. Jaroslawski S., Zadek B., Ashcroft F., Venien-Bryan C., and Scheuring S. Direct visualization of KirBac3.1 potassium channel gating by atomic force microscopy. J. Mol. Biol. 374 (2007) 500-505
206. Iwamoto H., Czajkowsky D.M., Cover T.L., Szabo G., and Shao Z. VacA from Helicobacter pylori: a hexameric chloride channel. FEBS Lett. 450 (1999) 101-104
207. Kedrov A., Ziegler C., Janovjak H., Kuhlbrandt W., and Muller D.J. Controlled unfolding and refolding of a single sodium-proton antiporter using atomic force microscopy. J. Mol. Biol. 340 (2004) 1143-1152
208. Muller D.J., and Engel A. Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy. J. Mol. Biol. 285 (1999) 1347-1351
209. Scheuring S., Ringler P., Borgnia M., Stahlberg H., Muller D.J., Agre P., and Engel A. High resolution AFM topographs of the Escherichia coli water channel aquaporin Z. EMBO J. 18 (1999) 4981-4987
210. Muller D.J., Dencher N.A., Meier T., Dimroth P., Suda K., Stahlberg H., Engel A., Seelert H., and Matthey U. ATP synthase: constrained stoichiometry of the transmembrane rotor. FEBS Lett. 504 (2001) 219-222
211. Seelert H., Dencher N.A., and Muller D.J. Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J. Mol. Biol. 333 (2003) 337-344
212. Arechaga I., and Fotiadis D. Reconstitution of mitochondrial ATP synthase into lipid bilayers for structural analysis. J. Struct. Biol. 160 (2007) 287-294
213. Hennesthal C., and Steinem C. Pore-spanning lipid bilayers visualized by scanning force microscopy. J. Am. Chem. Soc. 122 (2000) 8085-8086
214. Hennesthal C., Drexler J., and Steinem C. Membrane-suspended nanocompartments based on ordered pores in alumina. Chemphyschem 3 (2002) 885-889
215. Burns A.R. Domain structure in model membrane bilayers investigated by simultaneous atomic force microscopy and fluorescence imaging. Langmuir 19 (2003) 8358-8363
216. Burns A.R., Frankel D.J., and Buranda T. Local mobility in lipid domains of supported bilayers characterized by atomic force microscopy and fluorescence correlation spectroscopy. Biophys. J. 89 (2005) 1081-1093
217. Hell S.W. Far-field optical nanoscopy. Science 316 (2007) 1153-1158
218. Hell S.W. Microscopy and its focal switch. Nat. Methods 6 (2009) 24-32
219. Kraft M.L., Weber P.K., Longo M.L., Hutcheon I.D., and Boxer S.G. Phase separation of lipid membranes analyzed with high-resolution secondary ion mass spectrometry. Science 313 (2006) 1948-1951
220. McQuaw C.M., Zheng L., Ewing A.G., and Winograd N. Localization of sphingomyelin in cholesterol domains by imaging mass spectrometry. Langmuir 23 (2007) 5645-5650