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Structural and Mechanical Characterization of Supported Model Membranes by AFM

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Biomimetic Lipid Membranes: Fundamentals, Applications, and Commercialization

Abstract

Several cellular processes, including adhesion, signaling and transcription, endocytosis, and membrane resealing, among others, involve conformational changes such as bending, vesiculation, and tubulation. These mechanisms generally involve membrane separation from the cytoskeleton as well as strong bending, for which the membrane chemical composition and physicochemical properties, often highly localized and dynamic, are key players. The mechanical role of the lipid membrane in force triggered (or sensing) mechanisms in cells is important, and understanding the lipid bilayers’ physical and mechanical properties is essential to comprehend their contribution to the overall membrane. Atomic force microscopy (AFM)-based experimental approaches have been to date very valuable to deepen into these aspects. As a stand-alone, high-resolution imaging technique and force transducer with the possibility to operate in aqueous environment, it defies most other surface instrumentation in ease of use, sensitivity and versatility. In this chapter, we introduce the different AFM-based methods to assess topological and nanomechanical information on model membranes, specifically to supported lipid bilayers (SLBs), including several examples ranging from pure phospholipid homogeneous bilayers to multicomponent and phase-separated SLBs, increasing the bilayer complexity, in the direction of mimicking biological membranes.

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References

  1. G. van Meer, A.I.P.M. de Kroon, Lipid map of the mammalian cell. J. Cell Sci. 124, 5 (2011)

    Article  CAS  Google Scholar 

  2. D. Lingwood, K. Simons, Lipid rafts as a membrane-organizing principle. Science 327, 46–50 (2010)

    Article  CAS  Google Scholar 

  3. K. Simons, W.L.C. Vaz, Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. 33, 269–295 (2004)

    Article  CAS  Google Scholar 

  4. G. van Meer, D.R. Voelker, G.W. Feigenson, Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112–124 (2008)

    Article  CAS  Google Scholar 

  5. M.P. Sheetz, Cell control by membrane-cytoskeleton adhesion. Nat. Rev. Mol. Cell Biol. 2, 392 (2001)

    Article  CAS  Google Scholar 

  6. J.-Y. Shao, H.P. Ting-Beall, R.M. Hochmuth, Static and dynamic lengths of neutrophil microvilli. Proc. Natl. Acad. Sci. 95, 6797 (1998)

    Article  CAS  Google Scholar 

  7. D.W. Schmidtke, S.L. Diamond, Direct observation of membrane tethers formed during neutrophil attachment to platelets or P-selectin under physiological flow. J. Cell Biol. 149, 719 (2000)

    Article  CAS  Google Scholar 

  8. V. Vogel, Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. 35, 459–488 (2006)

    Article  CAS  Google Scholar 

  9. K. Bacia, P. Schwille, T. Kurzchalia, Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc. Natl. Acad. Sci. U. S. A. 102, 3272 (2005)

    Article  CAS  Google Scholar 

  10. E. Evans, V. Heinrich, F. Ludwig, W. Rawicz, Dynamic tension spectroscopy and strength of biomembranes. Biophys. J. 85, 2342–2350 (2003)

    Article  CAS  Google Scholar 

  11. N. Kahya, D. Scherfeld, K. Bacia, P. Schwille, Lipid domain formation and dynamics in giant unilamellar vesicles explored by fluorescence correlation spectroscopy. J. Struct. Biol. 147, 77–89 (2004)

    Article  CAS  Google Scholar 

  12. N. Kahya, Protein–protein and protein–lipid interactions in domain-assembly: lessons from giant unilamellar vesicles. Biochim. Biophys. Acta Biomembr. 2010(1798), 1392–1398 (2010)

    Article  CAS  Google Scholar 

  13. M.I. Angelova, I. Tsoneva, Interactions of DNA with giant liposomes. Chem. Phys. Lipids 101, 123–137 (1999)

    Article  CAS  Google Scholar 

  14. E. Sezgin, H.-J. Kaiser, T. Baumgart, P. Schwille, K. Simons, I. Levental, Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat. Protoc. 7, 1042 (2012)

    Article  CAS  Google Scholar 

  15. E. Sezgin, I. Levental, S. Mayor, C. Eggeling, The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat. Rev. Mol. Cell Biol. 18, 361 (2017)

    Article  CAS  Google Scholar 

  16. E.T. Castellana, P.S. Cremer, Solid supported lipid bilayers: from biophysical studies to sensor design. Surf. Sci. Rep. 61, 429–444 (2016)

    Article  CAS  Google Scholar 

  17. S. Garcia-Manyes, L. Redondo-Morata, G. Oncins, F. Sanz, Nanomechanics of lipid bilayers: heads or tails? J. Am. Chem. Soc. 132, 12874–12886 (2010)

    Article  CAS  Google Scholar 

  18. B. Gumí-Audenis, L. Costa, F. Carlà, F. Comin, F. Sanz, I.M. Giannotti, Structure and nanomechanics of model membranes by atomic force microscopy and spectroscopy: insights into the role of cholesterol and sphingolipids. Membranes 6, 58 (2016)

    Article  CAS  Google Scholar 

  19. M.-C. Giocondi, D. Yamamoto, E. Lesniewska, P.-E. Milhiet, T. Ando, C. Le Grimellec, Surface topography of membrane domains. Biochim. Biophys. Acta Biomembr. 1798, 703–718 (2010)

    Article  CAS  Google Scholar 

  20. A. Alessandrini, P. Facci, Unraveling lipid/protein interaction in model lipid bilayers by atomic force microscopy. J. Mol. Recognit. 24, 387–396 (2011)

    Article  CAS  Google Scholar 

  21. S. Morandat, K. El Kirat, Real-time atomic force microscopy reveals cytochrome c-induced alterations in neutral lipid bilayers. Langmuir 23, 10929–10932 (2007)

    Article  CAS  Google Scholar 

  22. R. Tero, K. Fukumoto, T. Motegi, M. Yoshida, M. Niwano, A. Hirano-Iwata, Formation of cell membrane component domains in artificial lipid bilayer. Sci. Rep. 7, 17905 (2017)

    Article  CAS  Google Scholar 

  23. S.J. Attwood, Y. Choi, Z. Leonenko, Preparation of DOPC and DPPC supported planar lipid bilayers for atomic force microscopy and atomic force spectroscopy. Int. J. Mol. Sci. 14, 3514–3539 (2013)

    Article  CAS  Google Scholar 

  24. L. Redondo-Morata, M.I. Giannotti, F. Sanz, AFM-based force-clamp monitors lipid bilayer failure kinetics. Langmuir 28, 6403–6410 (2012)

    Article  CAS  Google Scholar 

  25. L. Redondo-Morata, M.I. Giannotti, F. Sanz, Influence of cholesterol on the phase transition of lipid bilayers: a temperature-controlled force spectroscopy study. Langmuir 28, 12851–12860 (2012)

    Article  CAS  Google Scholar 

  26. H.M. Seeger, A.D. Cerbo, A. Alessandrini, P. Facci, Supported lipid bilayers on mica and silicon oxide: comparison of the main phase transition behavior. J. Phys. Chem. B 114, 8926–8933 (2010)

    Article  CAS  Google Scholar 

  27. T. Motegi, K. Yamazaki, T. Ogino, R. Tero, Substrate-induced structure and molecular dynamics in a lipid bilayer membrane. Langmuir 33, 14748–14755 (2017)

    Article  CAS  Google Scholar 

  28. B. Gumí-Audenis, L. Costa, L. Ferrer-Tasies, I. Ratera, N. Ventosa, F. Sanz, M.I. Giannotti, Pulling lipid tubes from supported bilayers unveils the underlying substrate contribution to the membrane mechanics. Nanoscale 10, 14763–14770 (2018)

    Article  Google Scholar 

  29. I. Mey, M. Stephan, E.K. Schmitt, M.M. Müller, M. Ben Amar, C. Steinem, A. Janshoff, Local membrane mechanics of pore-spanning bilayers. J. Am. Chem. Soc. 131, 7031–7039 (2009)

    Article  CAS  Google Scholar 

  30. H.L. Smith, M.S. Jablin, A. Vidyasagar, J. Saiz, E. Watkins, R. Toomey, A.J. Hurd, et al., Model lipid membranes on a tunable polymer cushion. Phys. Rev. Lett. 102, 228102 (2009)

    Article  CAS  Google Scholar 

  31. J. Relat-Goberna, E.M. Beedle Amy, S. Garcia-Manyes, The nanomechanics of lipid multibilayer stacks exhibits complex dynamics. Small 13, 1700147 (2017)

    Article  CAS  Google Scholar 

  32. X. Han, S. Achalkumar Ammathnadu, R. Cheetham Matthew, D.A. Connell Simon, R.G. Johnson Benjamin, J. Bushby Richard, D. Evans Stephen, A self-assembly route for double bilayer lipid membrane formation. ChemPhysChem 11, 569–574 (2010)

    Article  CAS  Google Scholar 

  33. S.R. Tabaei, P. Jönsson, M. Brändén, F. Höök, Self-assembly formation of multiple DNA-tethered lipid bilayers. J. Struct. Biol. 168, 200–206 (2009)

    Article  CAS  Google Scholar 

  34. R. Glazier, K. Salaita, Supported lipid bilayer platforms to probe cell mechanobiology. Biochim. Biophys. Acta Biomembr. 1859, 1465–1482 (2017)

    Article  CAS  Google Scholar 

  35. L.K. Tamm, H.M. McConnell, Supported phospholipid bilayers. Biophys. J. 47, 105–113 (1985)

    Article  CAS  Google Scholar 

  36. T.D. Osborn, P. Yager, Formation of planar solvent-free phospholipid bilayers by Langmuir-Blodgett transfer of monolayers to micromachined apertures in silicon. Langmuir 11, 8–12 (1995)

    Article  CAS  Google Scholar 

  37. H.R. Motschmann, T.L. Penner, N.J. Armstrong, M.C. Ezenyilimba, Additive second-order nonlinear susceptibilities in Langmuir-Blodgett multibilayers: testing the oriented gas model. J. Phys. Chem. 97, 3933–3936 (1993)

    Article  CAS  Google Scholar 

  38. L. Picas, C. Suárez-Germà, M. Teresa Montero, J. Hernández-Borrell, Force spectroscopy study of Langmuir−Blodgett asymmetric bilayers of phosphatidylethanolamine and phosphatidylglycerol. J. Phys. Chem. B 114, 3543–3549 (2010)

    Article  CAS  Google Scholar 

  39. U. Mennicke, T. Salditt, Preparation of solid-supported lipid bilayers by spin-coating. Langmuir 18, 8172–8177 (2012)

    Article  CAS  Google Scholar 

  40. M.P. Mingeot-Leclercq, M. Deleu, R. Brasseur, Y.F. Dufrene, Atomic force microscopy of supported lipid bilayers. Nat. Protoc. 3, 1654–1659 (2008)

    Article  Google Scholar 

  41. E. Reimhult, F. Hook, B. Kasemo, Intact vesicle adsorption and supported biomembrane formation from vesicles in solution: influence of surface chemistry, vesicle size, temperature, and osmotic pressure. Langmuir 19, 1681–1691 (2003)

    Article  CAS  Google Scholar 

  42. R.P. Richter, A.R. Brisson, Following the formation of supported lipid bilayers on mica: a study combining AFM, QCM-D, and ellipsometry. Biophys. J. 88, 3422–3433 (2005)

    Article  CAS  Google Scholar 

  43. B. Gumi-Audenis, L. Costa, L. Redondo-Morata, P.-E. Milhiet, F. Sanz, R. Felici, M.I. Giannotti, et al., In-plane molecular organization of hydrated single lipid bilayers: DPPC: cholesterol. Nanoscale 10, 87–92 (2018)

    Article  CAS  Google Scholar 

  44. S.-E. Choi, K. Greben, R. Wördenweber, A. Offenhäusser, Positively charged supported lipid bilayer formation on gold surfaces for neuronal cell culture. Biointerphases 11, 021003 (2016)

    Article  CAS  Google Scholar 

  45. G. Binnig, C.F. Quate, C. Gerber, Atomic force microscope. Phys. Rev. Lett. 56, 930–933 (1986)

    Article  CAS  Google Scholar 

  46. Y.F. Dufrêne, T. Ando, R. Garcia, D. Alsteens, D. Martinez-Martin, A. Engel, C. Gerber, et al., Imaging modes of atomic force microscopy for application in molecular and cell biology. Nat. Nanotechnol. 12, 295 (2017)

    Article  CAS  Google Scholar 

  47. P. Parot, Y.F. Dufrêne, P. Hinterdorfer, C. Le Grimellec, D. Navajas, J.L. Pellequer, S. Scheuring, Past, present and future of atomic force microscopy in life sciences and medicine. J. Mol. Recognit. 20, 418–431 (2007)

    Article  CAS  Google Scholar 

  48. L. Redondo-Morata, M.I. Giannotti, F. Sanz, Structural impact of cations on lipid bilayer models: nanomechanical properties by AFM-force spectroscopy. Mol. Membr. Biol. 31, 17–28 (2014)

    Article  CAS  Google Scholar 

  49. K. El Kirat, S. Morandat, Y.F. Dufrene, Nanoscale analysis of supported lipid bilayers using atomic force microscopy. BBA-Biomembranes 1798, 750–765 (2010)

    Article  CAS  Google Scholar 

  50. S. Morandat, S. Azouzi, E. Beauvais, A. Mastouri, K. El Kirat, Atomic force microscopy of model lipid membranes. Anal. Bioanal. Chem. 405, 1445–1461 (2013)

    Article  CAS  Google Scholar 

  51. B.E. Mierzwa, N. Chiaruttini, L. Redondo-Morata, J. Moser von Filseck, J. König, J. Larios, I. Poser, et al., Dynamic subunit turnover in ESCRT-III assemblies is regulated by Vps4 to mediate membrane remodelling during cytokinesis. Nat. Cell Biol. 19, 787 (2017)

    Article  CAS  Google Scholar 

  52. A. Toshio, High-speed atomic force microscopy coming of age. Nanotechnology 23, 062001 (2012)

    Article  Google Scholar 

  53. F. Eghiaian, F. Rico, A. Colom, I. Casuso, S. Scheuring, High-speed atomic force microscopy: imaging and force spectroscopy. FEBS Lett. 588, 3631–3638 (2014)

    Article  CAS  Google Scholar 

  54. T. Ando, N. Kodera, E. Takai, D. Maruyama, K. Saito, A. Toda, A high-speed atomic force microscope for studying biological macromolecules. Proc. Natl. Acad. Sci. 98, 12468 (2001)

    Article  CAS  Google Scholar 

  55. M.B. Viani, T.E. Schäffer, G.T. Paloczi, L.I. Pietrasanta, B.L. Smith, J.B. Thompson, M. Richter, et al., Fast imaging and fast force spectroscopy of single biopolymers with a new atomic force microscope designed for small cantilevers. Rev. Sci. Instrum. 70, 4300–4303 (1999)

    Article  CAS  Google Scholar 

  56. D.J. Müller, A. Engel, Atomic force microscopy and spectroscopy of native membrane proteins. Nat. Protoc. 2, 2191 (2007)

    Article  CAS  Google Scholar 

  57. S. Scheuring, Y.F. Dufrene, Atomic force microscopy: probing the spatial organization, interactions and elasticity of microbial cell envelopes at molecular resolution. Mol. Microbiol. 75, 1327–1336 (2010)

    Article  CAS  Google Scholar 

  58. D. Tranchida, S. Piccarolo, M. Soliman, Nanoscale mechanical characterization of polymers by AFM nanoindentations: critical approach to the elastic characterization. Macromolecules 39, 4547–4556 (2006)

    Article  CAS  Google Scholar 

  59. K. Sangwal, P. Gorostiza, J. Servat, F. Sanz, Atomic force microscopy study of nanoindentation deformation and indentation size effect in MgO crystals. J. Mater. Res. 14, 3973–3982 (1999)

    Article  CAS  Google Scholar 

  60. J. Fraxedas, S. Garcia-Manyes, P. Gorostiza, F. Sanz, Nanoindentation: toward the sensing of atomic interactions. Proc. Natl. Acad. Sci. U. S. A. 99, 5228–5232 (2002)

    Article  CAS  Google Scholar 

  61. M.E. Dokukin, I. Sokolov, Quantitative mapping of the elastic modulus of soft materials with harmonix and peakforce QNM AFM modes. Langmuir 28, 16060–16071 (2012)

    Article  CAS  Google Scholar 

  62. M.I. Giannotti, G.J. Vancso, Interrogation of single synthetic polymer chains and polysaccharides by AFM-based force spectroscopy. ChemPhysChem 8, 2290–2307 (2007)

    Article  CAS  Google Scholar 

  63. X. Zhang, C. Liu, Z. Wang, Force spectroscopy of polymers: studying on intramolecular and intermolecular interactions in single molecular level. Polymer 49, 3353–3361 (2008)

    Article  CAS  Google Scholar 

  64. M. Grandbois, M. Beyer, M. Rief, H. Clausen-Schaumann, H.E. Gaub, How strong is a covalent bond. Science 283, 1727 (1999)

    Article  CAS  Google Scholar 

  65. P.E. Marszalek, H. Li, J.M. Fernandez, Fingerprinting polysaccharides with single-molecule atomic force microscopy. Nat. Biotechnol. 19, 258–262 (2001)

    Article  CAS  Google Scholar 

  66. P.E. Marszalek, Y.F. Dufrêne, Stretching single polysaccharides and proteins using atomic force microscopy. Chem. Soc. Rev. 41, 3523–3534 (2012)

    Article  CAS  Google Scholar 

  67. T.E. Fisher, A.F. Oberhauser, M. Carrion-Vazquez, P.E. Marszalek, J.M. Fernandez, The study of protein mechanics with the atomic force microscope. Trends Biochem. Sci. 24, 379–384 (1999)

    Article  CAS  Google Scholar 

  68. F. Rico, L. Gonzalez, I. Casuso, M. Puig-Vidal, S. Scheuring, High-speed force spectroscopy unfolds titin at the velocity of molecular dynamics simulations. Science 342, 741 (2013)

    Article  CAS  Google Scholar 

  69. J.M. Fernandez, H.B. Li, Force-clamp spectroscopy monitors the folding trajectory of a single protein. Science 303, 1674–1678 (2004)

    Article  CAS  Google Scholar 

  70. G.U. Lee, L.A. Chrisey, R.J. Colton, Direct measurement of the forces between complementary strands of DN. Science 266, 771 (1994)

    Article  CAS  Google Scholar 

  71. Y.F. Dufrêne, G.U. Lee, Advances in the characterization of supported lipid films with the atomic force microscope. Biochim. Biophys. Acta Biomembr. 1509, 14–41 (2000)

    Article  Google Scholar 

  72. S. Garcia-Manyes, F. Sanz, Nanomechanics of lipid bilayers by force spectroscopy with AFM: a perspective. Biochim. Biophys. Acta Biomembr. 1798, 741–749 (2010)

    Article  CAS  Google Scholar 

  73. L. Picas, P.-E. Milhiet, J. Hernández-Borrell, Atomic force microscopy: a versatile tool to probe the physical and chemical properties of supported membranes at the nanoscale. Chem. Phys. Lipids 165, 845–860 (2012)

    Article  CAS  Google Scholar 

  74. Z. Leonenko, D. Cramb, M. Amrein, E. Finot, Atomic force microscopy: interaction forces measured in phospholipid monolayers, bilayers, and cell membranes, in Applied Scanning Probe Methods IX, ed. by M. Tomitori, B. Bhushan, H. Fuchs, (Springer, Berlin/Heidelberg, 2008), pp. 207–234

    Chapter  Google Scholar 

  75. L. Picas, F. Rico, S. Scheuring, Direct measurement of the mechanical properties of lipid phases in supported bilayers. Biophys. J. 102, L1–L3 (2012)

    Article  CAS  Google Scholar 

  76. S. Garcia-Manyes, G. Oncins, F. Sanz, Effect of ion-binding and chemical phospholipid structure on the nanomechanics of lipid bilayers studied by force spectroscopy. Biophys. J. 89, 1812–1826 (2005)

    Article  CAS  Google Scholar 

  77. S. Garcia-Manyes, G. Oncins, F. Sanz, Effect of temperature on the nanomechanics of lipid bilayers studied by force spectroscopy. Biophys. J. 89, 4261–4274 (2005)

    Article  CAS  Google Scholar 

  78. S. Garcia-Manyes, G. Oncins, F. Sanz, Effect of pH and ionic strength on phospholipid nanomechanics and on deposition process onto hydrophilic surfaces measured by AFM. Electrochim. Acta 51, 5029–5036 (2006)

    Article  CAS  Google Scholar 

  79. M.H. Abdulreda, V.T. Moy, Atomic force microscope studies of the fusion of floating lipid bilayers. Biophys. J. 92, 4369–4378 (2007)

    Article  CAS  Google Scholar 

  80. R.M.A. Sullan, J.K. Li, S. Zou, Direct correlation of structures and nanomechanical properties of multicomponent lipid bilayers. Langmuir 25, 7471–7477 (2009)

    Article  CAS  Google Scholar 

  81. J.K. Li, R.M.A. Sullan, S. Zou, Atomic force microscopy force mapping in the study of supported lipid bilayers. Langmuir 27, 1308–1313 (2011)

    Article  CAS  Google Scholar 

  82. E. Evans, Probing the relation between force – lifetime – and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. 30, 105–128 (2001)

    Article  CAS  Google Scholar 

  83. H.J. Butt, V. Franz, Rupture of molecular thin films observed in atomic force microscopy. I. Theory. Phys. Rev. E 66, 031601 (2002)

    Article  CAS  Google Scholar 

  84. B. Heymann, H. Grubmüller, Dynamic force spectroscopy of molecular adhesion bonds. Phys. Rev. Lett. 84, 6126–6129 (2000)

    Article  CAS  Google Scholar 

  85. D.F.J. Tees, R.E. Waugh, D.A. Hammer, A microcantilever device to assess the effect of force on the lifetime of selectin-carbohydrate bonds. Biophys. J. 80, 668–682 (2001)

    Article  CAS  Google Scholar 

  86. N.S. Zhurkov, Kinetic concept of the strength of solids. Int. J. Fract. 26, 295 (1984)

    Article  Google Scholar 

  87. S. Loi, G. Sun, V. Franz, H.J. Butt, Rupture of molecular thin films observed in atomic force microscopy. II. Experiment. Phys. Rev. E 66, 031602 (2002)

    Article  CAS  Google Scholar 

  88. A.F. Oberhauser, P.K. Hansma, M. Carrion-Vazquez, J.M. Fernandez, Stepwise unfolding of titin under force-clamp atomic force microscopy. Proc. Natl. Acad. Sci. U. S. A. 98, 468–472 (2001)

    Article  CAS  Google Scholar 

  89. P.E. Marszalek, H.B. Li, A.F. Oberhauser, J.M. Fernandez, Chair-boat transitions in single polysaccharide molecules observed with force-ramp AFM. Proc. Natl. Acad. Sci. U. S. A. 99, 4278–4283 (2002)

    Article  CAS  Google Scholar 

  90. W.D. Marcus, R.M. Hochmuth, Experimental studies of membrane tethers formed from human neutrophils. Ann. Biomed. Eng. 30, 1273–1280 (2002)

    Article  Google Scholar 

  91. F. Brochard-Wyart, N. Borghi, D. Cuvelier, P. Nassoy, Hydrodynamic narrowing of tubes extruded from cells. Proc. Natl. Acad. Sci. 103, 7660 (2006)

    Article  CAS  Google Scholar 

  92. S. Nawaz, P. Sánchez, S. Schmitt, N. Snaidero, M. Mitkovski, C. Velte, R. Brückner Bastian, et al., Actin filament turnover drives leading edge growth during myelin sheath formation in the central nervous system. Dev. Cell 34, 139–151 (2015)

    Article  CAS  Google Scholar 

  93. M. Sun, J.S. Graham, B. Hegedüs, F. Marga, Y. Zhang, G. Forgacs, M. Grandbois, Multiple membrane tethers probed by atomic force microscopy. Biophys. J. 89, 4320–4329 (2005)

    Article  CAS  Google Scholar 

  94. J. Friedrichs, K.R. Legate, R. Schubert, M. Bharadwaj, C. Werner, D.J. Müller, M. Benoit, A practical guide to quantify cell adhesion using single-cell force spectroscopy. Methods 60, 169–178 (2013)

    Article  CAS  Google Scholar 

  95. J.W. Armond, J.V. Macpherson, M.S. Turner, Pulling nanotubes from supported bilayers. Langmuir 27, 8269–8274 (2011)

    Article  CAS  Google Scholar 

  96. N. Maeda, T.J. Senden, J.-M. di Meglio, Micromanipulation of phospholipid bilayers by atomic force microscopy. Biochim. Biophys. Acta Biomembr. 1564, 165–172 (2002)

    Article  CAS  Google Scholar 

  97. J. Dai, M.P. Sheetz, Membrane tether formation from blebbing cells. Biophys. J. 77, 3363–3370 (1999)

    Article  CAS  Google Scholar 

  98. P.B. Canham, The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. J. Theor. Biol. 26, 61–81 (1970)

    Article  CAS  Google Scholar 

  99. J. Daillant, E. Bellet-Amalric, A. Braslau, T. Charitat, G. Fragneto, F. Graner, S. Mora, et al., Structure and fluctuations of a single floating lipid bilayer. Proc. Natl. Acad. Sci. U. S. A. 102, 11639 (2005)

    Article  CAS  Google Scholar 

  100. F.M. Hochmuth, J.Y. Shao, J. Dai, M.P. Sheetz, Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys. J. 70, 358–369 (1996)

    Article  CAS  Google Scholar 

  101. A. Roux, The physics of membrane tubes: soft templates for studying cellular membranes. Soft Matter 9, 6726–6736 (2013)

    Article  CAS  Google Scholar 

  102. E. Evans, A. Yeung, Hidden dynamics in rapid changes of bilayer shape. Chem. Phys. Lipids 73, 39–56 (1994)

    Article  CAS  Google Scholar 

  103. A. Martín-Molina, C. Rodríguez-Beas, J. Faraudo, Effect of calcium and magnesium on phosphatidylserine membranes: experiments and all-atomic simulations. Biophys. J. 102, 2095–2103 (2012)

    Article  CAS  Google Scholar 

  104. L. Redondo-Morata, G. Oncins, F. Sanz, Force spectroscopy reveals the effect of different ions in the nanomechanical behavior of phospholipid model membranes: the case of potassium cation. Biophys. J. 102, 66–74 (2012)

    Article  CAS  Google Scholar 

  105. J. Kwik, S. Boyle, D. Fooksman, L. Margolis, M.P. Sheetz, M. Edidin, Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc. Natl. Acad. Sci. 100, 13964 (2003)

    Article  CAS  Google Scholar 

  106. P. Jedlovszky, M. Mezei, Effect of cholesterol on the properties of phospholipid membranes. 2. Free energy profile of small molecules. J. Phys. Chem. B 107, 5322–5332 (2003)

    Article  CAS  Google Scholar 

  107. R.A. Cooper, Influence of increased membrane cholesterol on membrane fluidity and cell function in human red blood cells. J. Supramol. Struct. Cell 8, 413–430 (1978)

    Article  CAS  Google Scholar 

  108. J. Pan, T.T. Mills, S. Tristram-Nagle, J.F. Nagle, Cholesterol perturbs lipid bilayers nonuniversally. Phys. Rev. Lett. 100, 198103 (2008)

    Article  CAS  Google Scholar 

  109. T. Rog, M. Pasenkiewicz-Gierula, I. Vattulainen, M. Karttunen, Ordering effects of cholesterol and its analogues. Biochim. Biophys. Acta Biomembr. 1788, 97–121 (2009)

    Article  CAS  Google Scholar 

  110. W.-C. Hung, M.-T. Lee, F.-Y. Chen, H.W. Huang, The condensing effect of cholesterol in lipid bilayers. Biophys. J. 92, 3960–3967 (2007)

    Article  CAS  Google Scholar 

  111. Z. Leonenko, E. Finot, V. Vassiliev, M. Amrein, Effect of cholesterol on the physical properties of pulmonary surfactant films: atomic force measurements study. Ultramicroscopy 106, 687–694 (2006)

    Article  CAS  Google Scholar 

  112. T.P.W. McMullen, R.N. McElhaney, New aspects of the interaction of cholesterol with dipalmitoylphosphatidylcholine bilayers as revealed by high-sensitivity differential scanning calorimetry. Biochim. Biophys. Acta Biomembr. 1234, 90–98 (1995)

    Article  Google Scholar 

  113. S. Karmakar, V.A. Raghunathan, S. Mayor, Phase behaviour of dipalmitoyl phosphatidylcholine (DPPC)-cholesterol membranes. J. Phys. Condens. Matter 17, S1177–S1182 (2005)

    Article  CAS  Google Scholar 

  114. Y.-W. Chiang, A.J. Costa, J.H. Freed, Dynamic molecular structure and phase diagram of DPPC-cholesterol binary mixtures: a 2D-ELDOR study. J. Phys. Chem. B 111, 11260–11270 (2007)

    Article  CAS  Google Scholar 

  115. D. Marsh, Liquid-ordered phases induced by cholesterol: a compendium of binary phase diagrams. Biochim. Biophys. Acta Biomembr. 1798, 688–699 (2010)

    Article  CAS  Google Scholar 

  116. P.F. Almeida, A simple thermodynamic model of the liquid-ordered state and the interactions between phospholipids and cholesterol. Biophys. J. 100, 420–429 (2011)

    Article  CAS  Google Scholar 

  117. D. Marquardt, F.A. Heberle, J.D. Nickels, G. Pabst, J. Katsaras, On scattered waves and lipid domains: detecting membrane rafts with X-rays and neutrons. Soft Matter 11, 9055–9072 (2015)

    Article  CAS  Google Scholar 

  118. R.M.A. Sullan, J.K. Li, C.C. Hao, G.C. Walker, S. Zou, Cholesterol-dependent nanomechanical stability of phase-segregated multicomponent lipid bilayers. Biophys. J. 99, 507–516 (2010)

    Article  CAS  Google Scholar 

  119. L.M. Lima, M.I. Giannotti, L. Redondo-Morata, M.L. Vale, E.F. Marques, F. Sanz, Morphological and nanomechanical behavior of supported lipid bilayers on addition of cationic surfactants. Langmuir 29, 9352–9361 (2013)

    Article  CAS  Google Scholar 

  120. B. Gumi-Audenis, F. Sanz, M.I. Giannotti, Impact of galactosylceramides on the nanomechanical properties of lipid bilayer models: an AFM-force spectroscopy study. Soft Matter 11, 5447–5454 (2015)

    Article  CAS  Google Scholar 

  121. P.M. Winkler, R. Regmi, V. Flauraud, J. Brugger, H. Rigneault, J. Wenger, M.F. García-Parajo, Transient nanoscopic phase separation in biological lipid membranes resolved by planar plasmonic antennas. ACS Nano 11, 7241–7250 (2017)

    Article  CAS  Google Scholar 

  122. M. Javanainen, H. Martinez-Seara, I. Vattulainen, Nanoscale membrane domain formation driven by cholesterol. Sci. Rep. 7, 1143 (2017)

    Article  CAS  Google Scholar 

  123. R. Ziblat, K. Kjaer, L. Leiserowitz, L. Addadi, Structure of cholesterol/lipid ordered domains in monolayers and single hydrated bilayers. Angew. Chem. Int. Ed. 48, 8958–8961 (2009)

    Article  CAS  Google Scholar 

  124. C.E. Miller, J. Majewski, E.B. Watkins, D.J. Mulder, T. Gog, T.L. Kuhl, Probing the local order of single phospholipid membranes using grazing incidence X-ray diffraction. Phys. Rev. Lett. 100, 058103 (2008)

    Article  CAS  Google Scholar 

  125. K. Zhou, T. Blom, Trafficking and functions of bioactive sphingolipids: lessons from cells and model membranes. Lipid Insights 8, 11–20 (2015)

    Google Scholar 

  126. F.M. Goñi, A. Alonso, Biophysics of sphingolipids I. Membrane properties of sphingosine, ceramides and other simple sphingolipids. Biochim. Biophys. Acta Biomembr. 1758, 1902–1921 (2006)

    Article  CAS  Google Scholar 

  127. C.R. Bollinger, V. Teichgräber, E. Gulbins, Ceramide-enriched membrane domains. Biochim. Biophys. Acta, Mol. Cell Res. 1746, 284–294 (2005)

    Article  CAS  Google Scholar 

  128. X. Han, H. Cheng, Characterization and direct quantitation of cerebroside molecular species from lipid extracts by shotgun lipidomics. J. Lipid Res. 46, 163–175 (2005)

    Article  CAS  Google Scholar 

  129. W. Curatolo, The physical properties of glycolipids. Biochim. Biophys. Acta Rev. Biomembr. 906, 111–136 (1987)

    Article  CAS  Google Scholar 

  130. S. Chiantia, J. Ries, N. Kahya, P. Schwille, Combined AFM and two-focus SFCS study of raft-exhibiting model membranes. ChemPhysChem 7, 2409–2418 (2006)

    Article  CAS  Google Scholar 

  131. F. Guyomarc’h, S. Zou, M. Chen, P.-E. Milhiet, C. Godefroy, V. Vié, C. Lopez, Milk sphingomyelin domains in biomimetic membranes and the role of cholesterol: morphology and nanomechanical properties investigated using AFM and force spectroscopy. Langmuir 30, 6516–6524 (2014)

    Article  CAS  Google Scholar 

  132. A.V.R. Murthy, F. Guyomarc'h, C. Lopez, The temperature-dependent physical state of polar lipids and their miscibility impact the topography and mechanical properties of bilayer models of the milk fat globule membrane. Biochim. Biophys. Acta Biomembr. 1858, 2181–2190 (2016)

    Article  CAS  Google Scholar 

  133. A.V.R. Murthy, F. Guyomarc’h, C. Lopez, Cholesterol decreases the size and the mechanical resistance to rupture of sphingomyelin rich domains, in lipid bilayers studied as a model of the milk fat globule membrane. Langmuir 32, 6757–6765 (2016)

    Article  CAS  Google Scholar 

  134. A.V.R. Murthy, F. Guyomarc'h, C. Lopez, Palmitoyl ceramide promotes milk sphingomyelin gel phase domains formation and affects the mechanical properties of the fluid phase in milk-SM/DOPC supported membranes. Biochim. Biophys. Acta Biomembr. 1860, 635–644 (2018)

    Article  CAS  Google Scholar 

  135. S. Chiantia, N. Kahya, J. Ries, P. Schwille, Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS. Biophys. J. 90, 4500–4508 (2006)

    Article  CAS  Google Scholar 

  136. S. Zou, L.J. Johnston, Ceramide-enriched microdomains in planar membranes. Curr. Opin. Colloid Interface Sci. 15, 489–498 (2010)

    Article  CAS  Google Scholar 

  137. R.M.A. Sullan, J.K. Li, S. Zou, Quantification of the nanomechanical stability of ceramide-enriched domains. Langmuir 25, 12874–12877 (2009)

    Article  CAS  Google Scholar 

  138. L.E. Megha, Ceramide selectively displaces cholesterol from ordered lipid domains (rafts): implications for lipid raft structure and function. J. Biol. Chem. 279, 9997–10004 (2004)

    Article  CAS  Google Scholar 

  139. S. Chiantia, N. Kahya, P. Schwille, Raft domain reorganization driven by short- and long-chain ceramide: a combined AFM and FCS study. Langmuir 23, 7659–7665 (2007)

    Article  CAS  Google Scholar 

  140. M.R. Ali, K.H. Cheng, J. Huang, Ceramide drives cholesterol out of the ordered lipid bilayer phase into the crystal phase in 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine/cholesterol/ceramide ternary mixtures. Biochemistry-US 45, 12629–12638 (2006)

    Article  CAS  Google Scholar 

  141. J. Huang, G.W. Feigenson, A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys. J. 76, 2142–2157 (1999)

    Article  CAS  Google Scholar 

  142. M.L. Longo, C.D. Blanchette, Imaging cerebroside-rich domains for phase and shape characterization in binary and ternary mixtures. Biochim. Biophys. Acta Biomembr. 1798, 1357–1367 (2010)

    Article  CAS  Google Scholar 

  143. S.L. Veatch, S.L. Keller, Organization in Lipid Membranes Containing Cholesterol. Phys. Rev. Lett. 89, 268101 (2002)

    Article  CAS  Google Scholar 

  144. M. Fidorra, T. Heimburg, L.A. Bagatolli, Direct visualization of the lateral structure of porcine brain cerebrosides/POPC mixtures in presence and absence of cholesterol. Biophys. J. 97, 142–154 (2009)

    Article  CAS  Google Scholar 

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Gumí-Audenis, B., Giannotti, M.I. (2019). Structural and Mechanical Characterization of Supported Model Membranes by AFM. In: Kök, F., Arslan Yildiz, A., Inci, F. (eds) Biomimetic Lipid Membranes: Fundamentals, Applications, and Commercialization. Springer, Cham. https://doi.org/10.1007/978-3-030-11596-8_1

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