Observing the nanoscale organization of model biological membranes by atomic force microscopy

Life at the Nanoscale: Atomic Force Microscopy of Live Cells

Volumn , Issue , 2011, Pages 1-20

  Milhiet, Pierre Emmanuel ^a,b   Le Grimellec, Christian ^a,b  

^a INSERM   (France)

^b CENTRE DE BIOCHIMIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84860469646     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.4032/9789814267977     Document Type: Chapter

References (76)

1. Morrisset, J. D., Pownall, H. J., Plumlee, R. T., Smith, L. C., Zehner, Z. E., Esfahani, M., and Wakil, S. J. (1975) Multiple thermotropic phase transitions in Escherichia coli membranes and membrane lipids, J. Biol. Chem., 250, 6969-6976.
2. Jacobson, K., Mouritsen, O. G., and Anderson, R. G. (2007) Lipid rafts: at a crossroad between cell biology and physics, Nat. Cell Biol., 9, 7-14.
3. Johnston, L. J. (2007) Nanoscale imaging of domains in supported lipid membranes, Langmuir, 23, 5886-5895.
4. Sackmann, E. (1996) Supported membranes: scientific and practical applications, Science, 271, 43-48.
5. Kahya, N., Scherfeld, D., Bacia, K., and Schwille, P. (2004) Lipid domain formation and dynamics in giant unilamellar vesicles explored by fluorescence correlation spectroscopy, J. Struct. Biol., 147, 77-89.
6. El Kirat, K., Morandat, S., and Dufrene, Y. F. (2010) Nanoscale analysis of supported lipid bilayers using atomic force microscopy, Biochim. Biophys. Acta., 1798, 750-765.
7. Giocondi, M. C., Yamamoto, D., Lesniewska, E., Milhiet, P. E., Ando, T., and Le Grimellec, C. (2010) Surface topography of membrane domains, Biochim. Biophys. Acta, 1798, 703-718
8. Goksu, E. I., Vanegas, J. M., Blanchette, C. D., Lin, W. C., and Longo, M. L. (2009) AFM for structure and dynamics of biomembranes, Biochim. Biophys. Acta, 1788, 254-266.
9. Czajkowsky, D. M., Hotze, E. M., Shao, Z., and Tweten, R. K. (2004) Vertical collapse of a cytolysin prepore moves its transmembrane beta-hairpins to the membrane, Embo. J., 23, 3206-3215.
10. Milhiet, P. E., Gubellini, F., Berquand, A., Dosset, P., Rigaud, J. L., Le Grimellec, C., and Levy, D. (2006) High resolution AFM of membrane proteins directly incorporated at high density in planar lipid bilayer, Biophys. J., 91, 3268-3275.
11. Brian, A. A. and McConnell, H. M. (1984) Allogeneic stimulation of cytotoxic T cells by supported planar membranes, Proc. Natl. Acad. Sci. USA, 81, 6159-6163.
12. Picas, L., Montero, M. T., Morros, A., Cabanas, M. E., Seantier, B., Milhiet, P. E., and Hernandez-Borrell, J. (2009) Calcium-induced formation of subdomains in phosphatidylethanolamine-phosphatidylglycerol bilayers: a combined DSC, 31P NMR, and AFM study, J. Phys. Chem. B, 113, 4648-4655.
13. Richter, R. P., Berat, R., and Brisson, A. R. (2006) Formation of solid-supported lipid bilayers: an integrated view, Langmuir, 22, 3497-3505.
14. Berquand, A., Levy, D., Gubellini, F., Le Grimellec, C., and Milhiet, P. E. (2007) Influence of calcium on direct incorporation of membrane proteins into inplane lipid bilayer, Ultramicroscopy, 107, 928-933.
15. Garcia-Manyes, S., Oncins, G., and Sanz, F. (2005) Effect of ion-binding and chemical phospholipid structure on the nanomechanics of lipid bilayers studied by force spectroscopy, Biophys. J., 89, 1812-1826.
16. Seu, K. J., Pandey, A. P., Haque, F., Proctor, E. A., Ribbe, A. E., and Hovis, J. S. (2007) Effect of surface treatment on diffusion and domain formation in supported lipid bilayers, Biophys. J., 92, 2445-2450.
17. Seeger, H. M., Marino, G., Alessandrini, A., and Facci, P. (2009) Effect of physical parameters on the main phase transition of supported lipid bilayers, Biophys. J., 97, 1067-1076.
18. Leonenko, Z. V., Finot, E., Ma, H., Dahms, T. E., and Cramb, D. T. (2004) Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopy, Biophys. J., 86, 3783-3793.
19. Keller, D., Larsen, N. B., Moller, I. M., and Mouritsen, O. G. (2005) Decoupled phase transitions and grain-boundary melting in supported phospholipid bilayers, Phys. Rev. Lett., 9402, 186-189.
20. Charrier, A. and Thibaudau, F. (2005) Main phase transitions in supported lipid single-bilayer, Biophys. J., 89, 1094-1101.
21. Almeida, P. F., Vaz, W. L., and Thompson, T. E. (1992) Lateral diffusion and percolation in two-phase, two-component lipid bilayers. Topology of the solid-phase domains in-plane and across the lipid bilayer, Biochemistry, 31, 7198-7210.
22. Giocondi, M. C., Vie, V., Lesniewska, E., Milhiet, P. E., Zinke-Allmang, M., and Le Grimellec, C. (2001) Phase topology and growth of single domains in lipid bilayers., Langmuir, 17, 1653-1659.
23. Choucair, A., Chakrapani, M., Chakravarthy, B., Katsaras, J., and Johnston, L. J. (2007) Preferential accumulation of Abeta(1-42) on gel phase domains of lipid bilayers: an AFM and fluorescence study, Biochim. Biophys. Acta, 1768, 146-154.
24. Lin, W. C., Blanchette, C. D., Ratto, T. V., and Longo, M. L. (2006) Lipid asymmetry in DLPC/DSPC-supported lipid bilayers: a combined AFM and fluorescence microscopy study, Biophys. J., 90, 228-237.
25. Kiessling, V., Wan, C., and Tamm, L. K. (2009) Domain coupling in asymmetric lipid bilayers, Biochim. Biophys. Acta, 1788, 64-71.
26. Hollars, C. W. and Dunn, R. C. (1998) Submicron structure in L-alphadipalmitoylphosphatidylcholine monolayers and bilayers probed with confocal, atomic force, and near-field microscopy, Biophys. J., 75, 342-353.
27. Tanaka, M. and Sackmann, E. (2005) Polymer-supported membranes as models of cell surface, Nature, 437, 656-663.
28. Reimhult, E. and Kumar, K. (2008) Membrane biosensor platforms using nanoand microporous supports, Trends Biotechnol., 26, 82-89.
29. Kalb, E., Frey, S., and Tamm, L. K. (1992) Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers, Biochim. Biophys. Acta, 1103, 307-316.
30. Merzlyakov, M., Li, E., Gitsov, I., and Hristova, K. (2006) Surface-supported bilayers with transmembrane proteins: role of the polymer cushion revisited, Langmuir, 22, 10145-10151.
31. Israelachvili, J. (2002) Electrostatic forces between surfaces in liquids, in Intermolecular and Surface Forces, Academic Press, San Diego, pp. 213-259.
32. Muller, D. J., Amrein, M., and Engel, A. (1997) Adsorption of biological molecules to a solid support for scanning probe microscopy, J. Struct. Biol., 119, 172-188.
33. Frederix, P. L., Bosshart, P. D., and Engel, A. (2009) Atomic force microscopy of biological membranes, Biophys. J., 96, 329-338.
34. Preiner, J., Tang, J., Pastushenko, V., and Hinterdorfer, P. (2007) Higher harmonic atomic force microscopy: Imaging of biological membranes in a liquid, Phys. Rev. Lett., 99, 046102.
35. Sahin, O., Magonov, S., Su, C., Quate, C. F., and Solgaard, O. (2007) An atomic force microscope tip designed to measure time-varying nanomechanical forces, Nat. Nanotechnol., 2, 507-514.
36. London, E. (2005) How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells, Biochim. Biophys. Acta, 1746, 203-220.
37. Brown, D. A. and London, E. (1997) Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes? Biochem. Biophys. Res. Commun., 240, 1-7.
38. Giocondi, M. C., Boichot, S., Plenat, T., and Le Grimellec, C. C. (2004) Structural diversity of sphingomyelin microdomains, Ultramicroscopy, 100, 135-143.
39. Chiantia, S., Kahya, N., Ries, J., and Schwille, P. (2006) Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS, Biophys. J., 90, 4500-4508.
40. Johnston, I. and Johnston, L. J. (2006) Ceramide promotes restructuring of model raft membranes, Langmuir, 22, 11284-11289.
41. Fidorra, M., Duelund, L., Leidy, C., Simonsen, A. C., and Bagatolli, L. A. (2006) Absence of fluid-ordered/fluid-disordered phase coexistence in ceramide/POPC mixtures containing cholesterol, Biophys. J., 90, 4437-4451.
42. Johnston, L. J. (2008) Sphingomyelinase generation of ceramide promotes clustering of nanoscale domains in supported bilayer membranes, Biochim. Biophys. Acta, 1778, 185-197.
43. Contreras, F. X., Villar, A. V., Alonso, A., Kolesnick, R. N., and Goni, F. M. (2003) Sphingomyelinase activity causes transbilayer lipid translocation in model and cell membranes, J. Biol. Chem., 278, 37169-37174.
44. Giocondi, M. C., Seantier, B., Dosset, P., Milhiet, P. E., and Le Grimellec, C. (2008) Characterizing the interactions between GPI-anchored alkaline phosphatases and membrane domains by AFM, Pflugers Arch., 456, 179-188.
45. Milhiet, P., Giocondi, M., Baghdadi, O., Ronzon, F., Roux, B., and Le Grimellec, C. (2002) Spontaneous insertion and partitioning of alkaline phosphatase into model lipid rafts, EMBO Rep., 3, 485-490.
46. Saslowsky, D. E., Lawrence, J., Ren, X. Y., Brown, D. A., Henderson, R. M., and Edwardson, J. M. (2002) Placental alkaline phosphatase is efficiently targeted to rafts in supported lipid bilayers, J. Biol. Chem., 277, 26966-26970.
47. Chiantia, S., Ries, J., Kahya, N., and Schwille, P. (2006) Combined AFM and twofocus SFCS study of Raft-exhibiting model membranes, ChemPhysChem, 7, 2409-2418.
48. Giocondi, M. C., Besson, F., Dosset, P., Milhiet, P. E., and Le Grimellec, C. (2007) Remodelling of ordered membrane domains by gpi-anchored intestinal alkaline phosphatase, Langmuir, 23, 9358-9364.
49. Garner, A. E., Smith, D. A., and Hooper, N. M. (2007) Sphingomyelin chain length influences the distribution of GPI-anchored proteins in rafts in supported lipid bilayers, Mol. Membr. Biol., 24, 233-242.
50. Rigaud, J., Chami, M., Lambert, O., Levy, D., and Ranck, J. (2000) Use of detergents in two-dimensional crystallization of membrane proteins, Biochim. Biophys. Acta, 1508, 112-128.
51. Scheuring, S., Busselez, J., and Levy, D. (2005) Structure of the dimeric PufXcontaining core complex of Rhodobacter blasticus by in situ atomic force microscopy, J. Biol. Chem., 280, 1426-1431.
52. Conroy, M. J., Jamieson, S. J., Blakey, D., Kaufmann, T., Engel, A., Fotiadis, D., Merrick, M., and Bullough, P. A. (2004) Electron and atomic force microscopy of the trimeric ammonium transporter AmtB, EMBO Rep., 5, 1153-1158.
53. Fotiadis, D., Suda, K., Tittmann, P., Jeno, P., Philippsen, A., Muller, D. J., Gross, H., and Engel, A. (2002) Identification and structure of a putative Ca2+-binding domain at the C terminus of AQP1, J. Mol. Biol., 318, 1381-1394.
54. Rigaud, J. and Levy, D. (2003) Reconstitution of membrane proteins into liposomes, Methods Enzymol., 372, 65-86.
55. Naumann, C., Prucker, O., Lehmann T, Ruhe, J., Knoll, W., and Frank, C. W. (2002) The polymer-supported phospholipid bilayer: tethering as a new approach to substrate-membrane stabilization, Biomacromolecules, 3, 27-35.
56. Dorvel, B. R., Keiser, H. M., Fine, D., Vuorinen, J., Dodabalapur, A., and Duran, R. S. (2007) Formation of tethered bilayer lipid membranes on gold surfaces: QCM-Z and AFM study, Langmuir, 23, 7344-7355.
57. Jeuken, L. J., Connell, S. D., Henderson, P. J., Gennis, R. B., Evans, S. D., and Bushby, R. J. (2006) Redox enzymes in tethered membranes, J. Am. Chem. Soc., 128, 1711-1716.
58. Cunin, F., Milhiet, P. E., Anglin, E., Sailor, M. J., Espenel, C., Le Grimellec, C., Brunel, D., and Devoisselle, J. M. (2007) Continuous planar phospholipid bilayer supported on porous silicon thin film reflector, Ultramicroscopy, 107, 1048-1052.
59. Worsfold, O., Voelcker, N. H., and Nishiya, T. (2006) Biosensing using lipid bilayers suspended on porous silicon, Langmuir, 22, 7078-7083.
60. Janshoff, A. and Steinem, C. (2006) Transport across artificial membrane-an analytical perspective, Anal. Bioanal. Chem., 385, 433-451.
61. Schuster, B. and Sleytr, U. B. (2009) Composite S-layer lipid structures, J. Struct. Biol., 168, 207-216.
62. Kang, X. F., Cheley, S., Rice-Ficht, A. C., and Bayley, H. (2007) A storable encapsulated bilayer chip containing a single protein nanopore, J. Am. Chem. Soc., 129, 4701-4705.
63. Burns, A. R., Frankel, D. J., and Buranda, T. (2005) Local mobility in lipid domains of supported bilayers characterized by atomic force microscopy and fluorescence correlation spectroscopy, Biophys. J., 89, 1081-1093.
64. Hansma, P. K., Schitter, G., Fantner, G. E., and Prater, C. (2006) Applied physics. High-speed atomic force microscopy, Science, 314, 601-602.
65. Picco, L. M., Bozec, L., Ulcinas, A., Engledew, D. J., Antognozzi, M., Horton, M. A., and Miles, M. J. (2007) Breaking the speed limit with atomic force microscopy, Nanotechnology, 18, 044030.
66. Ando, T., Kodera, N., Uchihashi, T., Miyagi, A., Nakakita, R., Yamashita, H., and Matada, K. (2005) High-speed atomic force microscopy for capturing dynamic behavior of protein molecules at work, e-J. Surf. Sci. Nanotech., 3, 384-392.
67. Ando, T., Uchihashi, T., Kodera, N., Yamamoto, D., Miyagi, A., Taniguchi, M., and Yamashita, H. (2008) High-speed AFM and nano-visualization of biomolecular processes, Pflugers Arch., 456, 211-225.
68. Casuso, I., Kodera, N., Le Grimellec, C., Ando, T., and Scheuring, S. (2009) Contact-mode high-resolution high-speed atomic force microscopy movies of the purple membrane, Biophys. J., 97, 1354-1361.
69. Burns, A. R. (2003) Domain structure in model membrane bilayers investigated by simultaneous atomic force microscopy and fluorescence imaging, Langmuir, 19, 8358-8363.
70. Hell, S. W. (2007) Far-field optical nanoscopy, Science, 316, 1153-1158.
71. Shroff, H., Galbraith, C. G., Galbraith, J. A., and Betzig, E. (2008) Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics, Nat. Methods, 5, 417-423.
72. Hinterdorfer, P. and Dufrene, Y. F. (2006) Detection and localization of single molecular recognition events using atomic force microscopy, Nat. Methods, 3, 347-355.
73. McQuaw, C. M., Zheng, L., Ewing, A. G., and Winograd, N. (2007) Localization of sphingomyelin, in cholesterol domains by imaging mass spectrometry, Langmuir, 23, 5645-5650.
74. Oreopoulos, J. and Yip, C. M. (2009) Probing membrane order and topography in supported lipid bilayers by combined polarized total internal reflection fluorescence-atomic force microscopy, Biophys. J., 96, 1970-1984.
75. Fukuma, T., Higgins, M. J., and Jarvis, S. P. (2007) Direct imaging of lipid-ion network formation under physiological conditions by frequency modulation atomic force microscopy, Phys. Rev. Lett., 98, 106101, 106104 pp.
76. Hoogenboom, B. W., Frederix, P. L. T. M., Yang, J. L., Martin, S., Pellmont, Y., Steinacher, M., Zäch, S., Langenbach, E., Heimbeck, H.-J., Engel, A., and Hug, H. J. (2005) A Fabry-Perot interferometer for micrometer-sized cantilevers, Appl. Phys. Lett., 86, 074101-074103.