Skip to main content

Advertisement

Log in

Atomic force microscopy of model lipid membranes

  • Review
  • Published:
Analytical and Bioanalytical Chemistry Aims and scope Submit manuscript

Abstract

Supported lipid bilayers (SLBs) are biomimetic model systems that are now widely used to address the biophysical and biochemical properties of biological membranes. Two main methods are usually employed to form SLBs: the transfer of two successive monolayers by Langmuir–Blodgett or Langmuir–Schaefer techniques, and the fusion of preformed lipid vesicles. The transfer of lipid films on flat solid substrates offers the possibility to apply a wide range of surface analytical techniques that are very sensitive. Among them, atomic force microscopy (AFM) has opened new opportunities for determining the nanoscale organization of SLBs under physiological conditions. In this review, we first focus on the different protocols generally employed to prepare SLBs. Then, we describe AFM studies on the nanoscale lateral organization and mechanical properties of SLBs. Lastly, we survey recent developments in the AFM monitoring of bilayer alteration, remodeling, or digestion, by incubation with exogenous agents such as drugs, proteins, peptides, and nanoparticles.

The experimental atomic force microscopy (AFM) setup used to examine supported lipid bilayers (SLBs) under physiological conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Bagatolli LA, Ipsen JH, Simonsen AC, Mouritsen OG (2010) Prog Lipid Res 49:378–389

    Article  CAS  Google Scholar 

  2. Johnston LJ (2007) Langmuir 23:5886–5895

    Article  CAS  Google Scholar 

  3. Goksu EI, Vanegas JM, Blanchette CD, Lin WC, Longo ML (2009) Biochim Biophys Acta 1788:254–266

    Article  CAS  Google Scholar 

  4. El Kirat K, Morandat S, Dufrene YF (2010) Biochim Biophys Acta 1798:750–765

    Article  CAS  Google Scholar 

  5. Butt H.J. and Franz V. (2002) Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 66:031601

  6. Garcia-Manyes S, Redondo-Morata L, Oncins G, Sanz F (2010) J Am Chem Soc 132:12874–12886

    Article  CAS  Google Scholar 

  7. Garcia-Manyes S, Sanz F (2010) Biochim Biophys Acta 1798:741–749

    Article  CAS  Google Scholar 

  8. Muller DJ, Dufrene YF (2008) Nat Nanotechnol 3:261–269

    Article  CAS  Google Scholar 

  9. Horn RG (1984) Biochimica et Biophysica Acta Biomembranes 778:224–228

    Article  CAS  Google Scholar 

  10. Janshoff A, Steinem C (2006) Anal Bioanal Chem 385:433–451

    Article  CAS  Google Scholar 

  11. Brian AA, McConnell HM (1984) Proc Natl Acad Sci USA 81:6159–6163

    Article  CAS  Google Scholar 

  12. Jass J, Tjarnhage T, Puu G (2000) Biophys J 79:3153–3163

    Article  CAS  Google Scholar 

  13. Vie V, Van Mau M, Lesniewska E, Goudonnet JP, Heitz F, Le Grimellec C (1998) Langmuir 14:4574–4583

    Article  CAS  Google Scholar 

  14. Seantier B, Giocondi MC, Grimellec CL, Milhiet PE (2008) Curr Opin Colloid Interface Sci 13:326–337

    Article  CAS  Google Scholar 

  15. Rinia HA, Demel RA, van der Eerden JP, de Kruijff B (1999) Biophys J 77:1683–1693

    Article  CAS  Google Scholar 

  16. Simonsen AC, Bagatolli LA (2004) Langmuir 20:9720–9728

    Article  CAS  Google Scholar 

  17. Sackmann E (1996) Science 271:43–48

    Article  CAS  Google Scholar 

  18. Przybylo M, Sykora J, Humpolickova J, Benda A, Zan A, Hof M (2006) Langmuir 22:9096–9099

    Article  CAS  Google Scholar 

  19. Tanaka M, Sackmann E (2005) Nature 437:656–663

    Article  CAS  Google Scholar 

  20. Merzlyakov M, Li E, Gitsov I, Hristova K (2006) Langmuir 22:10145–10151

    Article  CAS  Google Scholar 

  21. Jeuken LJ, Connell SD, Henderson PJ, Gennis RB, Evans SD, Bushby RJ (2006) J Am Chem Soc 128:1711–1716

    Article  CAS  Google Scholar 

  22. Zebrowska A, Krysinski P (2004) Langmuir 20:11127–11133

    Article  CAS  Google Scholar 

  23. Friedrich MG, Kirste VU, Zhu J, Gennis RB, Knoll W, Naumann RL (2008) J Phys Chem B 112:3193–3201

    Article  CAS  Google Scholar 

  24. Largueze JB, El Kirat K, Morandat S (2010) Colloids Surf B Biointerfaces 79:33–40

    Google Scholar 

  25. Richter RP, Berat R, Brisson AR (2006) Langmuir 22:3497–3505

    Article  CAS  Google Scholar 

  26. Reviakine I, Brisson A (2000) Langmuir 16:1806–1815

    Article  CAS  Google Scholar 

  27. Richter RP, Brisson AR (2005) Biophys J 88:3422–3433

    Article  CAS  Google Scholar 

  28. Richter R, Mukhopadhyay A, Brisson A (2003) Biophys J 85:3035–3047

    Article  CAS  Google Scholar 

  29. Tokumasu F, Jin AJ, Feigenson GW, Dvorak JA (2003) Ultramicroscopy 97:217–227

    Article  CAS  Google Scholar 

  30. Leonenko ZV, Finot E, Ma H, Dahms TE, Cramb DT (2004) Biophys J 86:3783–3793

    Article  CAS  Google Scholar 

  31. Giocondi MC, Yamamoto D, Lesniewska E, Milhiet PE, Ando T, Le Grimellec C (2010) Biochim Biophys Acta 1798:703–718

    Article  CAS  Google Scholar 

  32. Suresh S, Edwardson JM (2010) Biochem Biophys Res Commun 399:571–574

    Article  CAS  Google Scholar 

  33. Seeger HM, Di Cerbo A, Alessandrini A, Facci P (2010) J Phys Chem B 114:8926–8933

    Article  CAS  Google Scholar 

  34. Giocondi M-C, Vie V, Lesniewska E, Milhiet P-E, Zinke-Allmang M, Le Grimellec C (2001) Langmuir 17:1653–1659

    Article  CAS  Google Scholar 

  35. Blanchette CD, Lin WC, Ratto TV, Longo ML (2006) Biophys J 90:4466–4478

    Article  CAS  Google Scholar 

  36. Lin WC, Blanchette CD, Ratto TV, Longo ML (2006) Biophys J 90:228–237

    Article  CAS  Google Scholar 

  37. Blanchette CD, Orme CA, Ratto TV, Longo ML (2008) Langmuir 24:1219–1224

    Article  CAS  Google Scholar 

  38. Bernchou U, Ipsen JH, Simonsen AC (2009) J Phys Chem B 113:7170–7177

    Article  CAS  Google Scholar 

  39. Choucair A, Chakrapani M, Chakravarthy B, Katsaras J, Johnston LJ (2007) Biochim Biophys Acta 1768:146–154

    Article  CAS  Google Scholar 

  40. Singer SJ, Nicolson GL (1972) Science 175:720–731

    Article  CAS  Google Scholar 

  41. Pike LJ (2006) J Lipid Res 47:1597–1598

    Article  CAS  Google Scholar 

  42. Simons K, Sampaio JL (2011) Cold Spring Harb Perspect Biol 3:a004697

    Article  CAS  Google Scholar 

  43. Anderson RG (1998) Annu Rev Biochem 67:199–225

    Article  CAS  Google Scholar 

  44. Levental I, Byfield FJ, Chowdhury P, Gai F, Baumgart T, Janmey PA (2009) Biochem J 424:163–167

    Article  CAS  Google Scholar 

  45. Harder T, Simons K (1997) Curr Opin Cell Biol 9:534–542

    Article  CAS  Google Scholar 

  46. McMullen TPW, Lewis RNAH, McElhaney RN (2004) Curr Opin Colloid Interface Sci 8:459–468

    Article  CAS  Google Scholar 

  47. Rinia HA, Snel MM, van der Eerden JP, de Kruijff B (2001) FEBS Lett 501:92–96

    Article  CAS  Google Scholar 

  48. Milhiet PE, Giocondi MC, Baghdadi O, Ronzon F, Roux B, Le Grimellec C (2002) EMBO Rep 3:485–490

    Article  CAS  Google Scholar 

  49. Epand RM, Vogel HJ (1999) Biochim Biophys Acta 1462:11–28

    Article  CAS  Google Scholar 

  50. Mou J, Czajkowsky DM, Shao Z (1996) Biochemistry 35:3222–3226

    Article  CAS  Google Scholar 

  51. Shaw JE, Alattia JR, Verity JE, Prive GG, Yip CM (2006) J Struct Biol 154:42–58

    Article  CAS  Google Scholar 

  52. Morgera F, Vaccari L, Antcheva N, Scaini D, Pacor S, Tossi A (2009) Biochem J 417:727–735

    Article  CAS  Google Scholar 

  53. Epand RF, Yip CM, Chernomordik LV, LeDuc DL, Shin YK, Epand RM (2001) Biochim Biophys Acta 1513:167–175

    Article  CAS  Google Scholar 

  54. Brasseur R (2000) Mol Membr Biol 17:31–40

    Article  CAS  Google Scholar 

  55. El Kirat K, Lins L, Brasseur R, Dufrene YF (2005) Langmuir 21:3116–3121

    Article  CAS  Google Scholar 

  56. Chernomordik L (1996) Chem Phys Lipids 81:203–213

    Article  CAS  Google Scholar 

  57. El Kirat K, Dufrene YF, Lins L, Brasseur R (2006) Biochemistry 45:9336–9341

    Article  CAS  Google Scholar 

  58. Sipe JD, Cohen AS (2000) J Struct Biol 130:88–98

    Article  CAS  Google Scholar 

  59. Yip CM, McLaurin J (2001) Biophys J 80:1359–1371

    Article  CAS  Google Scholar 

  60. Yip CM, Darabie AA, McLaurin J (2002) J Mol Biol 318:97–107

    Article  CAS  Google Scholar 

  61. Pifer PM, Yates EA, Legleiter J (2011) PLoS One 6:e16248

    Article  CAS  Google Scholar 

  62. Mao Y, Shang Z, Imai Y, Hoshino T, Tero R, Tanaka M, Yamamoto N, Yanagisawa K, Urisu T (2010) Biochim Biophys Acta 1798:1090–1099

    Article  CAS  Google Scholar 

  63. Zhong J, Zheng W, Huang L, Hong Y, Wang L, Qiu Y, Sha Y (2007) Biochim Biophys Acta 1768:1420–1429

    Article  CAS  Google Scholar 

  64. Marsh D (2008) Biochim Biophys Acta 1778:1545–1575

    Article  CAS  Google Scholar 

  65. Saslowsky DE, Lawrence J, Ren X, Brown DA, Henderson RM, Edwardson JM (2002) J Biol Chem 277:26966–26970

    Article  CAS  Google Scholar 

  66. Giocondi MC, Besson F, Dosset P, Milhiet PE, Le Grimellec C (2007) Langmuir 23:9358–9364

    Article  CAS  Google Scholar 

  67. Giocondi MC, Besson F, Dosset P, Milhiet PE, Le Grimellec C (2007) J Mol Recognit 20:531–537

    Article  CAS  Google Scholar 

  68. Grandbois M, Clausen-Schaumann H, Gaub H (1998) Biophys J 74:2398–2404

    Article  CAS  Google Scholar 

  69. Nielsen LK, Risbo J, Callisen TH, Bjornholm T (1999) Biochimica Et Biophysica Acta-Biomembranes 1420:266–271

    Article  CAS  Google Scholar 

  70. Nielsen LK, Balashev K, Callisen TH, Bjornholm T (2002) Biophys J 83:2617–2624

    Article  CAS  Google Scholar 

  71. Balashev K, Atanasov V, Mitewa M, Petrova S, Bjornholm T (2011) Biochim Biophys Acta 1808:191–198

    Article  CAS  Google Scholar 

  72. Leidy C, Mouritsen OG, Jorgensen K, Peters GH (2004) Biophys J 87:408–418

    Article  CAS  Google Scholar 

  73. Moraille P, Badia A (2005) J Am Chem Soc 127:6546–6547

    Article  CAS  Google Scholar 

  74. Nussio MR, Voelcker NH, Miners JO, Lewis BC, Sykes MJ, Shapter JG (2010) Chem Phys Lipids 163:182–189

    Article  CAS  Google Scholar 

  75. Kotova S, Vijayasarathy C, Dimitriadis EK, Ikonomou L, Jaffe H, Sieving PA (2010) Biochemistry 49:7023–7032

    Article  CAS  Google Scholar 

  76. Shahin V, Datta D, Hui E, Henderson RM, Chapman ER, Edwardson JM (2008) Biochemistry 47:2143–2152

    Article  CAS  Google Scholar 

  77. Milhiet PE, Gubellini F, Berquand A, Dosset P, Rigaud JL, Le Grimellec C, Levy D (2006) Biophys J 91:3268–3275

    Article  CAS  Google Scholar 

  78. Berquand A, Levy D, Gubellini F, Le Grimellec C, Milhiet PE (2007) Ultramicroscopy 107:928–933

    Article  CAS  Google Scholar 

  79. Picas L, Suarez-Germa C, Montero MT, Vazquez-Ibar JL, Hernandez-Borrell J, Prieto M, Loura LM (2010) Biochim Biophys Acta 1798:1707–1713

    Article  CAS  Google Scholar 

  80. Seydel J.K. and Wiese M. (2002) Wiley-VCH, Weinheim

  81. Seydel JK, Coats EA, Cordes HP, Wiese M (1994) Arch Pharm (Weinheim) 327:601–610

    Article  CAS  Google Scholar 

  82. Bensikaddour H, Fa N, Burton I, Deleu M, Lins L, Schanck A, Brasseur R, Dufrene YF, Goormaghtigh E, Mingeot-Leclercq MP (2008) Biophys J 94:3035–3046

    Article  CAS  Google Scholar 

  83. Leonenko Z, Finot E, Cramb D (2006) Biochim Biophys Acta 1758:487–492

    Article  CAS  Google Scholar 

  84. Lorite GS, Nobre TM, Zaniquelli ME, de Paula E, Cotta MA (2009) Biophys Chem 139:75–83

    Article  CAS  Google Scholar 

  85. Domenech O, Francius G, Tulkens PM, Van Bambeke F, Dufrene Y, Mingeot-Leclercq MP (2009) Biochim Biophys Acta 1788:1832–1840

    Article  CAS  Google Scholar 

  86. Domenech O, Dufrene YF, Van Bambeke F, Tukens PM, Mingeot-Leclercq MP (2010) Biochim Biophys Acta 1798:1876–1885

    Article  CAS  Google Scholar 

  87. Brechignac R.M., Houdy J.K., and Lahmani S. (2008) Springer-Verlag Berlin and Heidelberg GmbH & Co. K

  88. Riehemann K, Schneider SW, Luger TA, Godin B, Ferrari M, Fuchs H (2009) Angew Chem Int Ed Engl 48:872–897

    Article  CAS  Google Scholar 

  89. Nel AE, Madler L, Velegol D, Xia T, Hoek EM, Somasundaran P, Klaessig F, Castranova V, Thompson M (2009) Nat Mater 8:543–557

    Article  CAS  Google Scholar 

  90. Dawson KA, Salvati A, Lynch I (2009) Nat Nanotechnol 4:84–85

    Article  CAS  Google Scholar 

  91. Wang B, Zhang L, Bae SC, Granick S (2008) Proc Natl Acad Sci U S A 105:18171–18175

    Article  CAS  Google Scholar 

  92. Spurlin TA, Gewirth AA (2007) Nano Lett 7:531–535

    Article  CAS  Google Scholar 

  93. Leroueil PR, Berry SA, Duthie K, Han G, Rotello VM, McNerny DQ, Baker JR Jr, Orr BG, Holl MM (2008) Nano Lett 8:420–424

    Article  CAS  Google Scholar 

  94. Boas U, Heegaard PM (2004) Chem Soc Rev 33:43–63

    Article  CAS  Google Scholar 

  95. Gillies ER, Frechet JM (2005) Drug Discov Today 10:35–43

    Article  CAS  Google Scholar 

  96. Mecke A, Uppuluri S, Sassanella TM, Lee DK, Ramamoorthy A, Baker JR Jr, Orr BG, Banaszak Holl MM (2004) Chem Phys Lipids 132:3–14

    Article  CAS  Google Scholar 

  97. Parimi S, Barnes TJ, Prestidge CA (2008) Langmuir 24:13532–13539

    Article  CAS  Google Scholar 

  98. Dufrene YF, Barger WR, Green JBD, Lee GU (1997) Langmuir 13:4779–4784

    Article  CAS  Google Scholar 

  99. Schneider J, Barger W, Lee GU (2003) Langmuir 19:1899–1907

    Article  CAS  Google Scholar 

  100. Garcia-Manyes S, Oncins G, Sanz F (2006) Electrochim Acta 51:5029–5036

    Article  CAS  Google Scholar 

  101. Garcia-Manyes S, Oncins G, Sanz F (2005) Biophys J 89:1812–1826

    Article  CAS  Google Scholar 

  102. Garcia-Manyes S, Oncins G, Sanz F (2005) Biophys J 89:4261–4274

    Article  CAS  Google Scholar 

  103. Sullan RM, Li JK, Zou S (2009) Langmuir 25:7471–7477

    Article  CAS  Google Scholar 

  104. Canale C, Jacono M, Diaspro A, Dante S (2010) Microsc Res Tech 73:965–972

    Article  CAS  Google Scholar 

  105. Dante S, Hauss T, Steitz R, Canale C, Dencher NA (2011) Biochim Biophys Acta 1808:2646–2655

    Article  CAS  Google Scholar 

  106. Armond JW, Macpherson JV, Turner MS (2011) Langmuir 27:8269–8274

    Article  CAS  Google Scholar 

  107. Pera I, Stark R, Kappl M, Butt HJ, Benfenati F (2004) Biophys J 87:2446–2455

    Article  CAS  Google Scholar 

  108. Richter RP, Brisson A (2003) Langmuir 19:1632–1640

    Article  CAS  Google Scholar 

  109. Dufrene Y.F., Boland T., Schneider J.W., Barger W.R., and Lee G.U. (1998) Faraday Discuss. 79-94; discussion 137-57

  110. Choi EJ, Dimitriadis EK (2004) Biophys J 87:3234–3241

    Article  CAS  Google Scholar 

  111. Garcia-Saez AJ, Chiantia S, Salgado J, Schwille P (2007) Biophys J 93:103–112

    Article  CAS  Google Scholar 

  112. Abdulreda MH, Bhalla A, Chapman ER, Moy VT (2008) Biophys J 94:648–655

    Article  CAS  Google Scholar 

  113. Ando T, Kodera N, Takai E, Maruyama D, Saito K, Toda A (2001) Proc Natl Acad Sci U S A 98:12468–12472

    Article  CAS  Google Scholar 

  114. Casuso I, Sens P, Rico F, Scheuring S (2010) Biophys J 99:L47–L49

    Article  CAS  Google Scholar 

  115. Fantner GE, Barbero RJ, Gray DS, Belcher AM (2010) Nat Nanotechnol 5:280–285

    Article  CAS  Google Scholar 

  116. Burns AR (2003) Langmuir 19:8358–8363

    Article  CAS  Google Scholar 

  117. Ira, Zou S., Ramirez D.M., Vanderlip S., Ogilvie W., Jakubek Z.J., and Johnston L.J. (2009) J Struct Biol 168:78-89

    Google Scholar 

  118. Eggeling C, Ringemann C, Medda R, Schwarzmann G, Sandhoff K, Polyakova S, Belov VN, Hein B, von Middendorff C, Schonle A, Hell SW (2009) Nature 457:1159–1162

    Article  CAS  Google Scholar 

  119. Hell SW (2009) Nat Methods 6:24–32

    Article  CAS  Google Scholar 

  120. Hinterdorfer P, Dufrene YF (2006) Nat Methods 3:347–355

    Article  CAS  Google Scholar 

  121. Hinterdorfer P, Garcia-Parajo MF, Dufrene YF (2012) Acc Chem Res 45:327–336

    Article  CAS  Google Scholar 

  122. Burns AR, Frankel DJ, Buranda T (2005) Biophys J 89:1081–1093

    Article  CAS  Google Scholar 

  123. Chiantia S, Kahya N, Ries J, Schwille P (2006) Biophys J 90:4500–4508

    Article  CAS  Google Scholar 

  124. Chiantia S, Kahya N, Schwille P (2007) Langmuir 23:7659–7665

    Article  CAS  Google Scholar 

  125. Garcia-Saez AJ, Schwille P (2010) Biochim Biophys Acta 1798:766–776

    Article  CAS  Google Scholar 

  126. Anderson MS, Gaimari SD (2003) J Struct Biol 142:364–368

    Article  Google Scholar 

  127. Kraft ML, Weber PK, Longo ML, Hutcheon ID, Boxer SG (2006) Science 313:1948–1951

    Article  CAS  Google Scholar 

  128. Anderton CR, Lou K, Weber PK, Hutcheon ID, Kraft ML (2011) Biochim Biophys Acta 1808:307–315

    Article  CAS  Google Scholar 

  129. Hennesthal C, Drexler J, Steinem C (2002) Chemphyschem 3:885–889

    Article  CAS  Google Scholar 

  130. Goncalves RP, Agnus G, Sens P, Houssin C, Bartenlian B, Scheuring S (2006) Nat Methods 3:1007–1012

    Article  CAS  Google Scholar 

  131. Quist AP, Chand A, Ramachandran S, Daraio C, Jin S, Lal R (2007) Langmuir 23:1375–1380

    Article  CAS  Google Scholar 

  132. Sumino A, Dewa T, Takeuchi T, Sugiura R, Sasaki N, Misawa N, Tero R, Urisu T, Gardiner AT, Cogdell RJ, Hashimoto H, Nango M (2011) Biomacromolecules 12:2850–2858

    Article  CAS  Google Scholar 

  133. Nielsen CH (2009) Anal Bioanal Chem 395:697–718

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Yves Dufrene for the valuable suggestions and discussions. Financial support of the Centre National de la Recherche Scientifique (CNRS), of the French Research Ministry, of the Université de Technologie de Compiègne (UTC, Plan de Pluriformation “Assemblages Biomimétiques - PPF BIOMIM”), and of the Région Picardie (“Ce projet est cofinancé par l’Union Européenne. L’Europe s’engage en Picardie avec le Fonds Européen de Développement Régional”) is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karim El Kirat.

Additional information

Published in the topical collection Characterization of Thin Films and Membranes with guest editors Daniel Mandler and Pankaj Vadgama.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morandat, S., Azouzi, S., Beauvais, E. et al. Atomic force microscopy of model lipid membranes. Anal Bioanal Chem 405, 1445–1461 (2013). https://doi.org/10.1007/s00216-012-6383-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00216-012-6383-y

Keywords

Navigation