Nanoscale mechanical properties of lipid bilayers and their relevance in biomembrane organization and function

Micron

Volumn 43, Issue 12, 2012, Pages 1212-1223

  Alessandrini, Andrea ^a,b   Facci, Paolo ^a  

^a CNR   (Italy)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

AFM; Force spectroscopy; Supported lipid bilayers

Indexed keywords

AFM; ATOMIC FORCE MICROSCOPE (AFM); BIOMEMBRANES; CHANGING ENVIRONMENT; DYNAMIC FORCE SPECTROSCOPY; FORCE SPECTROSCOPY; FUNCTIONAL ACTIVITIES; MEMBRANE PROTEINS; MEMBRANE RUPTURE; MESOSCOPICS; MICROPIPETTE ASPIRATION TECHNIQUES; NANO SCALE; NANOSCALE MECHANICAL PROPERTIES; SUPPORTED LIPID BILAYERS;

ATOMIC FORCE MICROSCOPY; CYTOLOGY; EXPERIMENTS; MECHANICAL PROPERTIES; PROBES; PROTEINS;

LIPID BILAYERS;

ARTICLE; ATOMIC FORCE MICROSCOPY; LIPID BILAYER; MECHANICS; MEMBRANE; METHODOLOGY; PHYSICAL CHEMISTRY; PHYSIOLOGY; ULTRASTRUCTURE;

LIPID BILAYERS; MECHANICAL PHENOMENA; MEMBRANES; MICROSCOPY, ATOMIC FORCE; PHYSICOCHEMICAL PHENOMENA;

EID: 84865864033     PISSN: 09684328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micron.2012.03.013     Document Type: Article

References (113)

1. Abdulreda M.H., Moy V.T. Atomic force microscope studies of the fusion of floating lipid bilayers. Biophys. J. 2007, 92:4369-4378.
2. Alessandrini A., Facci P. AFM: a versatile tool in biophysics. Meas. Sci. Technol. 2005, 16:R65-R92.
3. Alessandrini A., Facci P. Unraveling lipid/protein interaction in model lipid bilayers by atomic force microscopy. J. Mol. Recognit. 2011, 24:387-396.
4. + channel behavior induced by a lipid phase transition. Commun. Integr. Biol. 2011, 4:346-348.
5. Alessandrini A., Seeger H.M., Di Cerbo A., Caramaschi T., Facci P. What do we really measure in AFM punch-through experiments on supported lipid bilayers?. Soft Matter 2011, 7:7054-7064.
6. Alessandrini, A., Seeger, H.M., Caramaschi, T., Facci, P., submitted for publication.
7. Armond J.W., Macpherson J.V., Turner M.S. Pulling nanotubes from supported bilayers. Langmuir 2011, 27:8269-8274.
8. Bagatolli L.A., Ipsen J.H., Simonsen A.C., Mouritsen O.G. An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes. Prog. Lipid Res. 2010, 49:378-389.
9. Baldwin P.A., Hubbell W.L. Effects of lipid environment on the light-induced conformational changes of rhodopsin. 2. Roles of lipid chain length, unsaturation, and phase state. Biochemistry 1985, 24:2633-2639.
10. Beece D., Eisenstein L., Frauenfelder H., Good D., Marden M.C., Reinisch L., Reynolds A.H., Sorensen L.B., Yue K.T. Solvent viscosity and protein dynamics. Biochemistry 1980, 19:5147-5157.
11. Bell G.I. Models for the specific adhesion of cells to cells. Science 1978, 200:618-627.
12. Best R.B., Paci E., Hummer G., Dudko O.K. Pulling direction as a reaction coordinate for the mechanical unfolding of single molecules. J. Phys. Chem. B 2008, 112:5968-5976.
13. Bier M., Gowrishankar T.R., Chen W., Lee R.C. Electroporation of a lipid bilayer as a chemical reaction. Bioelectromagnetics 2004, 25:634-637.
14. Brian A.A., McConnell H.M. Allogeneic stimulation of cytotoxic T cells by supported planar membranes. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:6159-6163.
15. Butt H.J. Electrostatic interaction in atomic force microscopy. Biophys. J. 1991, 60:777-785.
16. Butt H.J. Measuring electrostatic, van der Waals, and hydration forces in electrolyte solutions with an atomic force microscope. Biophys. J. 1991, 60:1438-1444.
17. Butt H.J. Measuring local surface charge densities in electrolyte solutions with a scanning force microscope. Biophys. J. 1992, 63:578-582.
18. Butt H.J., Franz V. Rupture of molecular thin films observed in atomic force microscopy. I. Theory. Phys. Rev. E 2002, 66:031601.
19. Castellana E.T., Cremer P.S. Solid supported lipid bilayers: from biophysical studies to sensor design. Surf. Sci. Rep. 2006, 61:429-444.
20. Cevc G. Membrane electrostatics. Biochim. Biophys. Acta 1990, 1031:311-382.
21. Cevc G. Isothermal lipid phase transitions. Chem. Phys. Lipids 1991, 57:293-307.
22. Charrier A., Thibaudau F. Main phase transitions in supported lipid single-bilayer. Biophys. J. 2005, 89:1094-1101.
23. Collins M.D. Interleaflet coupling mechanisms in bilayers of lipids and cholesterol. Biophys. J. 2008, 94:L32-L34.
24. Collins M.D., Keller S.L. Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:124-128.
25. Crane J.M., Kiessling V., Tamm L.K. Measuring lipid asymmetry in planar supported bilayers by fluorescence interference contrast microscopy. Langmuir 2005, 21:1377-1388.
26. Das C., Sheikh K.H., Olmsted P.D., Connell S.D. Nanoscale mechanical probing of supported lipid bilayers with atomic force microscopy. Phys. Rev. E 2010, 82:041920.
27. Deserno M. Mesoscopic membrane physics: concepts, simulations, and selected applications. Macromol. Rapid Commun. 2009, 30:752-771.
28. Dieluweit S., Csiszár A., Rubner W., Fleischhauer J., Houben S., Merkel R. Mechanical properties of bare and protein-coated giant unilamellar phospholipid vesicles. A comparative study of micropipet aspiration and atomic force microscopy. Langmuir 2010, 26:11041-11049.
29. Dimitriadis E.K., Horkay F., Maresca J., Kachar B., Chadwick R.S. Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys. J. 2002, 82:2798-2810.
30. Domke J., Radmacher M. Measuring the elastic properties of thin polymer films with the atomic force microscope. Langmuir 1998, 14:3320-3325.
31. Dudko O.K., Filippov A.E., Klafter J., Urbakh M. Beyond the conventional description of dynamic force spectroscopy of adhesion bonds. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11378-11381.
32. Dudko O.K., Hummer G., Szabo A. Intrinsic rates and activation free energies from single-molecule pulling experiments. Phys. Rev. Lett. 2006, 96:108101.
33. Dufrêne Y.F., Barger W.R., Green J.B.D., Lee G.U. Nanometer-scale surface properties of mixed phospholipid monolayers and bilayers. Langmuir 1997, 13:4779-4784.
34. Dufrêne Y.F., Boland T., Schneider J.W., Barger W.R., Lee G.U. Characterization of the physical properties of model biomembranes at the anometer scale with the atomic force microscope. Faraday Discuss. 1998, 111:79-94.
35. Eggeling C., Ringemann C., Medda R., Schwarzmann G., Sandhoff K., Polyakova S., Belov V.N., Hein B., von Middendorff C., Schönle A., Hell S.W. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 2009, 457:1159-1162.
36. Evans E., Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys. J. 1997, 72:1541-1555.
37. Feng Z.V., Spurlin T.A., Gewirth A.A. Direct visualization of asymmetric behavior in supported lipid bilayers at the gel-fluid phase transition. Biophys. J. 2005, 88:2154-2164.
38. Ferber U., Kaggwa G., Jarvis S. Direct imaging of salt effects on lipid bilayer ordering at sub-molecular resolution. Eur. Biophys. J. 2011, 40:329-338.
39. Franz V., Loi S., Muller H., Bamberg E., Butt H.J. Tip penetration through lipid bilayers in atomic force microscopy. Colloids Surf. B Biointerfaces 2002, 23:191-2002.
40. Frauenfelder H., Chen G., Berendzen J., Fenimore P.W., Jansson H., McMahon B.H., Stroe I.R., Swenson J., Young R.D. A unified model of protein dynamics. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5129-5134.
41. Frauenfelder H. The Physics of Proteins: An Introduction to Biological Physics and Molecular Biophysics 2010, S.S. Chan, W.S. Chan (Eds.).
42. Garcia-Manyes S., Oncins G., Sanz F. Effect of temperature on the nanomechanics of lipid bilayers studied by force spectroscopy. Biophys. J. 2005, 89:4261-4274.
43. Garcia-Manyes S., Oncins G., Sanz F. Effect of ion-binding and chemical phospholipid structure on the nanomechanics of lipid bilayers studied by force spectroscopy. Biophys. J. 2005, 89:1812-1826.
44. Garcia-Manyes S., Gorostiza P., Sanz F. Titration force microscopy on supported lipid bilayers. Anal. Chem. 2006, 78:61-70.
45. Garcia-Manyes S., Sanz F. Nanomechanics of lipid bilayers by force spectroscopy with AFM: a perspective. Biochim. Biophys. Acta 2010, 1798:741-749.
46. Garcia-Manyes S., Redondo-Morata L., Oncins G., Sanz F. Nanomechanics of lipid bilayers: heads or tails?. J. Am. Chem. Soc. 2010, 132:12874-12886.
47. García-Sáez A.J., Chiantia S., Salgado J., Schwille P. Pore formation by a Bax-derived peptide: effect on the line tension of the membrane probed by AFM. Biophys. J. 2007, 93:103-112.
48. Glaser R.W., Leikin S.L., Chernomordik L.V., Pastushenko V.F., Sokirko A.I. Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. Biochim. Biophys. Acta 1988, 940:275-287.
49. Grant L.M., Tiberg F. Normal and lateral forces between lipid covered solids in solution: correlation with layer packing and structure. Biophys. J. 2002, 82:1373-1385.
50. Gurtovenko A.A., Vattulainen I. Effect of NaCl and KCl on phosphatidylcholine and phosphatidylethanolamine lipid membranes: insight from atomic-scale simulations for understanding salt-induced effects in the plasma membrane. J. Phys. Chem. B 2008, 112:1953-1962.
51. Heimburg T. Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry. Biochim. Biophys. Acta 1998, 1415:147-162.
52. Heimburg T. Lipid ion channels. Biophys. Chem. 2010, 150:2-22.
53. Helfrich W. Elastic properties of lipid bilayers-theory and possible experiments. Z. Naturforsch. C 1973, 28:693-703.
54. Henriksen R., Ipsen J.H. Measurement of membrane elasticity by micro-pipette aspiration. Eur. Phys. J. E 2004, 14:149-167.
55. Hertz H. über die Berührung fester, elastischer Körper. J. Reine Angew Math. 1882, 156-171.
56. Hetzer M., Heinz S., Grage S., Bayerl T.M. Asymmetric molecular friction in supported phospholipid bilayers revealed by NMR measurements of lipid diffusion. Langmuir 1998, 14:982-984.
57. Hoffman B.D., Crocker J.C. Cell mechanics: dissecting the physical responses of cells to force. Annu. Rev. Biomed. Eng. 2009, 11:259-288.
58. Hummer G., Szabo A. Kinetics from nonequilibrium single-molecule pulling experiments. Biophys. J. 2003, 85:5-15.
59. Israelachvili J. Intermolecular and Surface Forces 1992, Academic Press, New York.
60. Johnson S.J., Bayerl T.M., McDermott D.C., Adam G.W., Rennie A.R., Thomas R.K., Sackmann E. Structure of an adsorbed dimyristoylphosphatidylcholine bilayer measured with specular reflection of neutrons. Biophys. J. 1991, 59:289-294.
61. Kalani J.S., Pandeya A.P., Haquea F., Proctora E.A., Ribbea A.E., Hovis J.S. Effect of surface treatment on diffusion and domain formation in supported lipid bilayers. Biophys. J. 2007, 92:2445-2450.
62. Kasas S., Dietler G. Probing nanomechanical properties from biomolecules to living cells. Pflugers Arch. Eur. J. Physiol. 2008, 456:13-27.
63. Keller D., Larsen N.B., Moller I.M., Mouritsen O.G. Decoupled phase transitions and grain-boundary melting in supported phospholipid bilayers. Phys. Rev. Lett. 2005, 94:25701.
64. Kim J., Kim G., Cremer P.S. Investigations of water structure at the solid/liquid interface in the presence of supported lipid bilayers by vibrational sum frequency spectroscopy. Langmuir 2001, 17:7255-7260.
65. Koenig B.W., Kruger S., Orts W.J., Majkrzak C.F., Berk N.F., Silverton J.V., Gawrisch K. Neutron reflectivity and atomic force microscopy studies of a lipid bilayer in water adsorbed to the surface of a silicon single crystal. Langmuir 1996, 12:1343-1350.
66. Kunneke S., Kruger D., 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. 2004, 86:1545-1553.
67. Lee A.G. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 2004, 1666:62-87.
68. Lin W.-C., Blanchette C.D., Ratto T.V., Longo M.L. Lipid asymmetry in DLPC/DSPC-supported lipid bilayers: a combined AFM and fluorescence microscopy study. Biophys. J. 2006, 90:228-237.
69. Lingwood D., Simons K. Lipid rafts as a membrane-organizing principle. Science 2010, 327:46-50.
70. Loi S., Sun G., Franz V., Butt H.J. Rupture of molecular thin films observed in atomic force microscopy. II. Experiment. Phys. Rev. E 2002, 66:031602.
71. Lundbaek J.A. Lipid bilayer-mediated regulation of ion channel function by amphiphilic drugs. J. Gen. Physiol. 2008, 131:421-429.
72. Mall S., Broadbridge R., Sharma R.P., East J.M., Lee A.G. Self-association of model transmembrane alpha-helices is modulated by lipid structure. Biochemistry 2001, 40:12379-12386.
73. Marsh D. Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta 2008, 1778:1545-1575.
74. Martinac B., Buechner M., Delcour A.H., Adler J., Kung C. Pressure-sensitive ion channel in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:2297-2301.
75. McConnell H.M., Watts T.H., Weis R.M., Brian A.A. Supported planar membranes in studies of cell-cell recognition in the immune system. Biochim. Biophys. Acta 1986, 864:95-106.
76. McIntosh T.J., Simon S.A. Roles of bilayer material properties in function and distribution of membrane proteins. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:177-198.
77. Merkel R., Sackmann E., Evans E. Molecular friction and epitactic coupling between monolayers in supported bilayers. J. Phys. France 1989, 50:1535-1555.
78. Mey I., Stephan M., Schmitt E.K., Müller M.M., Ben Amar M., Steinem C., Janshoff A. Local membrane mechanics of pore-spanning bilayers. J. Am. Chem. Soc. 2009, 131:7031-7039.
79. Mora T., Bialek W. Are biological systems poised at criticality?. J. Stat. Phys. 2011, 144:268-302.
80. Morandat S., El Kirat K. Cytochrome c provokes the weakening of zwitterionic membranes as measured by force spectroscopy. Colloids Surf. B: Biointerfaces 2011, 82:111-117.
81. Morrisett J.D., Pownall H.J., Plumlee R.T., Smith L.C., Zehner Z.E. Multiple thermotropic phase transitions in Escherichia coli membranes and membrane lipids. A comparison of results obtained by nitroxyl stearate paramagnetic resonance, pyrene excimer fluorescence, and enzyme activity measurements. J. Biol. Chem. 1975, 250:6969-6976.
82. Neuman K.C., Nagy A. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 2008, 5:491-505.
83. Pabst G., Hodzic A., Strancar J., Danner S., Rappolt M., Laggner P. Rigidification of neutral lipid bilayers in the presence of salts. Biophys. J. 2007, 93:2688-2696.
84. Pelling A.E., Horton M.A. An historical perspective on cell mechanics. Pflugers Arch. 2008, 456:3-12.
85. Pera I., Stark R., Kappl M., Butt H.J., Benfenati F. Using the atomic force microscope to study the interaction between two solid supported lipid bilayers and the influence of synapsin I. Biophys. J. 2004, 87:2446-2455.
86. Petrov A.G., Usherwood P.N.R. Mechanosensitivity of cell membranes. Eur. Biophys. J. 1994, 23:1-19.
87. Phillips R., Ursell T., Wiggins P., Sens P. Emerging roles for lipids in shaping membrane-protein function. Nature 2009, 459:379-385.
88. Picas L., Montero M.T., Morros A., Oncins G., Hernández-Borrell J. Phase Changes in Supported Planar Bilayers of 1-Palmitoyl-2-oleoyl-sn-glycero-3-phosphoethanolamine. J. Phys. Chem. B 2008, 112:10181-10187.
89. Picas L., Suárez-Germà C., Teresa Montero M., Hernández-Borrell J. Force spectroscopy study of Langmuir-Blodgett asymmetric bilayers of phosphatidylethanolamine and phosphatidylglycerol. J. Phys. Chem. B 2010, 114:3543-3549.
90. Picas L., Rico F., Scheuring S. Direct measurement of the mechanical properties of lipid phases in supported bilayers. Biophys. J. 2012, 102:L01-L3.
91. Przybylo M., Sýkora J., Humpolí̂ková J., Benda A., Zan A., Hof M. The lipid diffusion in giant unilamellar vesicles is more than two times faster than in supported phospholipid bilayers under identical conditions. Langmuir 2006, 22:9096-9099.
92. Radmacher M., Fritz M., Kacher C.M., Cleveland J.P., Hansma P.K. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys. J. 1996, 70:556-567.
93. Rand R.P., Sengupta S. Cardiolipin forms hexagonal structures with divalent cations. Biochim. Biophys. Acta 1972, 255:484-492.
94. Rawicz W., Olbrich K.C., McIntosh T., Needham D., Evans E. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 2000, 79:328-339.
95. Rico F., Su C., Scheuring S. Mechanical mapping of single membrane proteins at submolecular resolution. Nano Lett. 2012, 11:3983-3986.
96. Sachs F. Stretch-activated ion channels: what are they?. Physiology 2010, 25:50-56.
97. Seeger H.M., Marino G., Alessandrini A., Facci P. Effect of physical parameters on the main phase transition of supported lipid bilayers. Biophys. J. 2009, 97:1067-1076.
98. Seeger H.M., Bortolotti C.A., Alessandrini A., Facci P. Phase-transition-induced protein redistribution in lipid bilayers. J. Phys. Chem. B 2009, 113:16654-16659.
99. Seeger H.M., Di Cerbo A., Alessandrini A., Facci P. Supported lipid bilayers on mica and silicon oxide: comparison of the main phase transition behavior. J. Phys. Chem. B 2010, 114:8926-8933.
100. + channel behavior induced by a lipid phase transition. Biophys. J. 2010, 99:3675-3683.
101. Shreve A.P., Howland M.C., Sapuri-Butti A.R., Allen T.W., Parikh A.N. Evidence for leaflet-dependent redistribution of charged molecules in fluid supported phospholipid bilayers. Langmuir 2008, 24:13250-13253.
102. Simons K., Ikonen E. Functional rafts in cell membranes. Nature 1997, 387:569-572.
103. Stottrup B., Veatch S., Keller S. Nonequilibrium behavior in supported lipid membranes containing cholesterol. Biophys. J. 2004, 86:2942-2950.
104. Sullan R.M., Li J.K., Zou S. Direct correlation of structures and nanomechanical properties of multicomponent lipid bilayers. Langmuir 2009, 25:7471-7477.
105. Sullan R.M., Li J.K., Hao C., Walker G.C., Zou S. Cholesterol-dependent nanomechanical stability of phase-segregated multicomponent lipid bilayers. Biophys. J. 2010, 99:507-516.
106. Thompson D.W. On Growth and Form 1917, Cambridge University Press, London.
107. Thormann E., Simonsen A.C., Nielsen L.K., Mouritsen O.G. Ligand-receptor interactions and membrane structure investigated by AFM and time-resolved fluorescence microscopy. J. Mol. Recognit. 2007, 20:554-560.
108. Tokumasu F., Jin A.J., Dvorak J.A. Lipid membrane phase behaviour elucidated in real time by controlled environment atomic force microscopy. J. Electron Microsc. 2002, 51:1-9.
109. Voïtchovsky K., Antoranz Contera S., Kamihira M., Watts A., Ryan J.F. Differential stiffness and lipid mobility in the leaflets of purple membranes. Biophys. J. 2006, 90:2075-2085.
110. Xing C., Faller R. Interactions of lipid bilayers with supports: a coarse-grained molecular simulation study. J. Phys. Chem. B 2008, 112:7086-7094.
111. Xing C., Faller R. Density imbalances and free energy of lipid transfer in supported lipid bilayers. J. Chem. Phys. 2009, 131:175104.
112. Yarrow F., Vlugt T.J.H., van der Eerden J.P.J.M., Snel M.M.E. Melting of a DPPC lipidbilayer observedwith atomic force microscopy andcomputer simulation. J. Cryst. Growth 2005, 275:e1417-e1421.
113. Zhang L., Granick S. Lipid diffusion compared in outer and inner leaflets of planar supported bilayers. J. Chem. Phys. 2005, 123:211104-211107.