AFM: A nanotool in membrane biology

Biochemistry

Volumn 47, Issue 31, 2008, Pages 7986-7998

  Muller, Daniel J ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; CELL MEMBRANES; CELLS; CYTOLOGY; FLOW INTERACTIONS; MEDICAL IMAGING; MEMBRANES; MICROSCOPIC EXAMINATION; NEURAL NETWORKS; OPTICAL MICROSCOPY; PROTEIN FOLDING; PROTEINS; SCANNING PROBE MICROSCOPY; SIGNAL TO NOISE RATIO;

BIOLOGICAL SURFACES; BIOMOLECULAR REACTIONS; CELLULAR MEMBRANES; CELLULAR PROCESSES; CHEMICAL GROUPS; CYTOSKELETON; CYTOSOLIC COMPARTMENTS; ENERGY GRADIENTS; ENERGY LANDSCAPES; FOCAL ADHESIONS; FORCE SPECTROSCOPY; FUNCTIONAL STATES; IMAGING APPLICATIONS; LIVE CELLS; LOCAL ELASTICITY; MEMBRANE PROTEINS; MOLECULAR INTERACTIONS; MOLECULAR RESOLUTION; NANO TOOLS; OPTICAL-; REACTION PATHWAYS; RECEPTOR SITES; SINGLE CELLS; SPATIAL RESOLUTION SR); SUPRAMOLECULAR ASSEMBLIES;

IMAGING TECHNIQUES;

ENZYME; MEMBRANE PROTEIN; POLYPEPTIDE;

ATOMIC FORCE MICROSCOPY; CELL MEMBRANE; IMAGING; MEMBRANE BIOLOGY; MOLECULAR PROBE; NANOBIOTECHNOLOGY; PRIORITY JOURNAL; REVIEW;

CELL MEMBRANE; MEMBRANE PROTEINS; MICROSCOPY, ATOMIC FORCE; NANOTECHNOLOGY;

EID: 48649106769     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800753x     Document Type: Review

References (100)

1. Engelman, D. M. (2005) Membranes are more mosaic than fluid. Nature 438, 578-580.
2. Hell, S. W. (2007) Far-field optical nanoscopy. Science 316, 1153-1158.
3. Robinson, C. V., Sali, A., and Baumeister, W. (2007) The molecular sociology of the cell. Nature 450, 973-982.
4. Gerber, C., and Lang, H. P. (2007) How the doors to the nanoworld were opened. Nat. Nanotechnol. 1, 3-5.
5. Muller, D. J., and Dufrene, Y. (2008) Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nat. Nanotechnol. 3, 261-269.
6. Grandbois, M., Clausen-Schaumann, H., and Gaub, H. (1998) Atomic force microscope imaging of phospholipid bilayer degradation by phospholipase A2. Biophys. J. 74, 2398-2404.
7. Nielsen, L. K., Risbo, J., Callisen, T. H., and Bjornholm, T. (1999) Lag-burst kinetics in phospholipase A(2) hydrolysis of DPPC bilayers visualized by atomic force microscopy. Biochim. Biophys. Acta 1420, 266-271.
8. El Kirat, K., Dupres, V., and Dufrene, Y. F. (2008) Blistering of supported lipid membranes induced by phospholipase D, as observed by real-time atomic force microscopy. Biochim. Biophys. Acta 1778, 276-282.
9. Rigby-Singleton, S. M., Davies, M. C., Harris, H., O'Shea, P., and Allen, S. (2006) Visualizing the solubilization of supported lipid bilayers by an amphiphilic peptide. Langmuir 22, 6273-6279.
10. Pedersen, T. B., Kaasgaard, T., Jensen, M. O., Frokjaer, S., Mouritsen, O. G., and Jorgensen, K. (2005) Phase behavior and nanoscale structure of phospholipid membranes incorporated with acylated C14-peptides. Biophys. J. 89, 2494-2503.
11. Alattia, J. R., Shaw, J. E., Yip, C. M., and Prive, G. G. (2007) Molecular imaging of membrane interfaces reveals mode of β-glucosidase activation by saposin C. Proc. Natl. Acad. Sci. U.S.A. 104, 17394-17399.
12. 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. (2002) Domain formation in phosphatidylcholine bilayers containing transmembrane peptides: Specific effects of flanking residues. Biochemistry 41, 2814-2824.
13. Chiantia, S., Kahya, N., and Schwille, P. (2007) Raft domain reorganization driven by short- and long-chain ceramide: A combined AFM and FCS study. Langmuir 23, 7659-7665.
14. Giocondi, M. C., Besson, F., Dosset, P., Milhiet, P. E., and Le Grimellec, C. (2007) Remodeling of ordered membrane domains by GPI-anchoired intestinal alkaline phosphatase. Langmuir 23, 9358-9364.
15. Czajkowsky, D. M., and Shao, Z. (2002) Supported lipid bilayers as effective substrates for atomic force microscopy. Methods Cell Biol. 68, 231-241.
16. Muller, D. J., Engel, A. (2008) Strategies to prepare and characterize native membrane proteins and protein membranes by AFM. Curr. Opin. Colloid Interface Sci. (in press)
17. Muller, D. J., and Engel, A. (2007) Atomic force microscopy and spectroscopy of native membrane proteins. Nat. Protoc. 2, 2191-2197.
18. Muller, D. J., Schoenenberger, C. A., Büldt, G., and Engel, A. (1996) Immuno-atomic force microscopy of purple membrane. Biophys. J. 70, 1796-1802.
19. Scheuring, S., Ringler, P., Borgina, M., Stahlberg, H., Muller, D. J., Agre, P., and Engel, A. (1999) High resolution topographs of the Escherichia coli waterchannel aquaporin Z. EMBO J. 18, 4981-4987.
20. 2+-binding domain at the C terminus of AQP1. J. Mol. Biol. 318, 1381-1394.
21. Heymann, J. B., Pfeiffer, M., Hildebrandt, V., Fotiadis, D., de Groot, B., Kabak, R., Engel, A., Oesterhelt, D., and Muller, D. J. (2000) Conformations of the rhodopsin third cytoplasmic loop grafted onto bacteriorhodopsin. Structure 8, 643-644.
22. Engel, A., and Muller, D. J. (2000) Observing single biomolecules at work with the atomic force microscope. Nat. Struct. Biol. 7, 715-718.
23. Butt, H.-J., Jaschke, M., and Ducker, W. (1995) Measuring surface forces in aqueous solution with the atomic force microscope. Bioelectrochem. Bioenerg. 38, 191-201.
24. Muller, D. J., and Engel, A. (1997) The height of biomolecules measured with the atomic force microscope depends on electrostatic interactions. Biophys. J. 73, 1633-1644.
25. Muller, D. J., Sapra, K. T., Scheuring, S., Kedrov, A., Frederix, P. L., Fotiadis, D., and Engel, A. (2006) Single-molecule studies of membrane proteins. Curr. Opin. Struct. Biol. 16, 489-495.
26. Scheuring, S., Muller, D. J., Stahlberg, H., Engel, H. A., and Engel, A. (2002) Sampling the conformational space of membrane protein surfaces with the AFM. Eur. Biophys. J. 31, 172-178.
27. Muller, D. J., Hand, G. M., Engel, A., and Sosinsky, G. (2002) Conformational changes in surface structures of isolated Connexin26 gap junctions. EMBO J. 21, 3598-3607.
28. Muller, D. J., Sass, H.-J., Muller, S., Büldt, G., and Engel, A. (1999) Surface structures of native bacteriorhodopsin depend on the molecular packing arrangement in the membrane. J. Mol. Biol. 285, 1903-1909.
29. White, S. H., and Wimley, W. C. (1999) Membrane protein folding and stability: Physical principles. Annu. Rev. Biophys. Biomol. Struct. 28, 319-365.
30. Sapra, K. T., Park, P. S., Palczewski, K., and Muller, D. J. (2008) Mechanical properties of bovine rhodopsin and bacteriorhodopsin: Possible roles in folding and function. Langmuir 24, 1330-1337.
31. Hoh, J. H., Lal, R., John, S. A., Revel, J.-P., and Arnsdorf, M. F. (1991) Atomic force microscopy and dissection of gap junctions. Science 253, 1405-1408.
32. Fotiadis, D., Hasler, L., Muller, D. J., Stahlberg, H., Kistler, J., and Engel, A. (2000) Surface tongue-and-groove contours on lens MIP facilitate cell-to-cell adherence. J. Mol. Biol. 300, 779-789.
33. Fotiadis, D., Muller, D. J., Tsiotis, G., Hasler, L., Tittmann, P., Mini, T., Jenö, P., Gross, H., and Engel, A. (1998) Surface analysis of the photosystem I complex by electron and atomic force microscopy. J. Mol. Biol. 283, 83-94.
34. Scheuring, S., Seguin, J., Marco, S., Levy, D., Robert, B., and Rigaud, J. L. (2003) 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, 1690-1693.
35. Czajkowsky, D. M., Sheng, S., and Shao, Z. (1998) Staphylococcal α-hemolysin can form hexamers in phospholipid bilayers. J. Mol. Biol. 276, 325-330.
36. Mou, J. X., Yang, J., and Shao, Z. F. (1995) Atomic force microscopy of cholera toxin B-oligomers bound to bilayers of biologically relevant lipids. J. Mol. Biol. 248, 507-512.
37. Seelert, H., Poetsch, A., Dencher, N. A., Engel, A., Stahlberg, H., and Muller, D. J. (2000) Proton powered turbine of a plant motor. Nature 405, 418-419.
38. Stahlberg, H., Muller, D. J., Suda, K., Fotiadis, D., Engel, A., Matthey, U., Meier, T., and Dimroth, P. (2001) Bacterial ATP synthase has an undecameric rotor. EMBO Rep. 21, 1-5.
39. Pogoryelov, D., Yu, J., Meier, T., Vonck, J., Dimroth, P., and Muller, D. J. (2005) The c15 ring of the Spirulina platensis F-ATP synthase: F1/F0 symmetry mismatch is not obligatory. EMBO Rep. 6, 1040-1044.
40. Fotiadis, D., Liang, Y., Filipek, S., Saperstein, D. A., Engel, A., and Palczewski, K. (2003) Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature 421, 127-128.
41. Fotiadis, D., Jastrzebska, B., Philippsen, A., Muller, D. J., Palczewski, K., and Engel, A. (2006) Structure of the rhodopsin dimer: A working model for G-protein-coupled receptors. Curr. Opin. Struct. Biol. 16, 252-259.
42. Cisneros, D. A., Oesterhelt, D., and Muller, D. J. (2005) Probing origins of molecular interactions stabilizing the membrane proteins halorhodopsin and bacteriorhodopsin. Structure 13, 235-242.
43. Klyszejko, A. L., Shastri, S., Mari, S. A., Grubmuller, H., Muller, D. J., and Glaubitz, C. (2008) Folding and assembly of proteorhodopsin. J. Mol. Biol. 376, 35-41.
44. Scheuring, S., and Sturgis, J. N. (2005) Chromatic adaptation of photosynthetic membranes. Science 309, 484-487.
45. Fotiadis, D., Qian, P., Philippsen, A., Bullough, P. A., Engel, A., and Hunter, C. N. (2004) Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy. J. Biol. Chem. 279, 2063-2068.
46. Hoogenboom, B. W., Suda, K., Engel, A., and Fotiadis, D. (2007) The supramolecular assemblies of voltage-dependent anion channels in the native membrane. J. Mol. Biol. 370, 246-255.
47. Muller, D. J., Baumeister, W., and Engel, A. (1996) Conformational change of the hexagonally packed intermediate layer of Deinococcus radiodurans imaged by atomic force microscopy. J. Bacteriol. 178, 3025-3030.
48. Muller, D. J., and Engel, A. (1999) Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy. J. Mol. Biol. 285, 1347-1351.
49. Jaroslawski, S., Zadek, B., Ashcroft, F., Venien-Bryan, C., and Scheuring, S. (2007) Direct visualization of KirBac3.1 potassium channel gating by atomic force microscopy. J. Mol. Biol. 374, 500-505.
50. Yu, J., Bippes, C. A., Hand, G. M., Muller, D. J., and Sosinsky, G. E. (2007) Aminosulfonate modulated pH-induced conformational changes in connexin26 hemichannels. J. Biol. Chem. 282, 8895-8904.
51. Andersen, C., Schiffler, B., Charbit, A., and Benz, R. (2002) pH-induced collapse of the extracellular loops closes Escherichia coli maltoporin and allows the study of asymmetric sugar binding. J. Biol. Chem. 277, 41318-41325.
52. Viani, M. B., Pietrasanta, L. I., Thompson, J. B., Chand, A., Gebeshuber, I. C., Kindt, J. H., Richter, M., Hansma, H. G., and Hansma, P. K. (2000) Probing protein-protein interactions in real time. Nat. Struct. Biol. 7, 644-647.
53. Yokokawa, M., Wada, C., Ando, T., Sakai, N., Yagi, A., Yoshimura, S. H., and Takeyasu, K. (2006) Fast-scanning atomic force microscopy reveals the ATP/ADP-dependent conformational changes of GroEL. EMBO J. 25, 4567-4576.
54. Humphris, A. D., Miles, M., and Hobbs, J. K. (2005) A mechanical microscope: High-speed atomic force microscopy. Appl. Phys. Lett. 86.
55. Yokokawa, M., Yoshimura, S. H., Naito, Y., Ando, T., Yagi, A., Sakai, N., and Takeyasu, K. (2006) Fast-scanning atomic force microscopy reveals the molecular mechanism of DNA cleavage by ApaI endonuclease. IEE Proc.: Nanobiotechnol. 153, 60-66.
56. Kodera, N., Kinoshita, T., Ito, T., and Ando, T. (2003) High-resolution imaging of myosin motor in action by a high-speed atomic force microscope. Adv. Exp. Med. Biol. 538, 119-127.
57. Yang, Y., Mayer, K. M., and Hafner, J. H. (2007) Quantitative membrane electrostatics with the atomic force microscope. Biophys. J. 92, 1966-1974.
58. Heinz, W. F., and Hoh, J. H. (1999) Relative surface charge density mapping with the atomic force microscope. Biophys. J. 76, 528-538.
59. Philippsen, A., Im, W., Engel, A., Schirmer, T., Roux, B., and Muller, D. J. (2002) Imaging the electrostatic potential of transmembrane channels: Atomic probe microscopy on OmpF porin. Biophys. J. 82, 1667-1676.
60. Frederix, P. L. T. M., Gullo, M. R., Akiyama, T., Tonin, A., de Rooij, N. F., Staufer, U., and Engel, A. (2005) Assessment of insulated conductive cantilevers for biology and electrochemistry. Nanotechnology 16, 997-1005.
61. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M., and Gaub, H. E. (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276, 1109-1112.
62. Rief, M., Oesterhelt, F., Heymann, B., and Gaub, H. E. (1997) Single molecule force spectroscopy on polysaccharides by AFM. Science 275, 1295-1298.
63. Rief, M., Clausen-Schaumann, H., and Gaub, H. E. (1999) Sequence-dependent mechanics of single DNA molecules. Nat. Struct. Biol. 6, 346-349.
64. Muller, D. J., Baumeister, W., and Engel, A. (1999) Controlled unzipping of a bacterial surface layer with atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 96, 13170-13174.
65. Oesterhelt, F., Oesterhelt, D., Pfeiffer, M., Engel, A., Gaub, H. E., and Muller, D. J. (2000) Unfolding pathways of individual bacteriorhodopsins. Science 288, 143-146.
66. Muller, D. J., Kessler, M., Oesterhelt, F., Moeller, C., Oesterhelt, D., and Gaub, H. (2002) Stability of bacteriorhodopsin α-helices and loops analyzed by single-molecule force spectroscopy. Biophys. J. 83, 3578-3588.
67. Janovjak, H., Kessler, M., Gaub, H., Oesterhelt, D., and Muller, D. J. (2003) Unfolding pathways of native bacteriorhodopsin depend on temperature. EMBO J. 22, 5220-5229.
68. Sapra, K. T., Besir, H., Oesterhelt, D., and Muller, D. J. (2006) Characterizing molecular interactions in different bacteriorhodopsin assemblies by single-molecule force spectroscopy. J. Mol. Biol. 355, 640-650.
69. 2+ in native bovine rhodopsin. J. Biol. Chem. 282, 11377-11385.
70. Sapra, K. T., Balasubramanian, G. P., Labudde, D., Bowie, J. U., and Muller, D. J. (2008) Point mutations in membrane proteins reshape energy landscape and populate different unfolding pathways. J. Mol. Biol. 376, 1076-1090.
71. Sapra, K. T., Doehner, J., Renugopalakrishnan, V., Padros, E., and Muller, D. J. (2008) Role of extracellular glutamic acids in the stability and energy landscape of bacteriorhodopsin Biophys. J. (in press)
72. Kedrov, A., Janovjak, H., Ziegler, C., Kuhlbrandt, W., and Muller, D. J. (2006) Observing folding pathways and kinetics of a single sodium-proton antiporter from Escherichia coli. J. Mol. Biol. 355, 2-8.
73. Kessler, M., Gottschalk, K. E., Janovjak, H., Muller, D. J., and Gaub, H. E. (2006) Bacteriorhodopsin folds into the membrane against an external force. J. Mol. Biol. 357, 644-654.
74. Möller, C., Fotiadis, D., Suda, K., Engel, A., Kessler, M., and Muller, D. J. (2003) Determining molecular forces that stabilize human aquaporin-1. J. Struct. Biol. 142, 369-378.
75. Kedrov, A., Janovjak, H., Sapra, K. T., and Muller, D. J. (2007) Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 36, 233-260.
76. Haltia, T., and Freire, E. (1995) Forces and factors that contribute to the structural stability of membrane proteins. Biochim. Biophys. Acta 1228, 1-27.
77. Janovjak, H., Muller, D. J., and Humphris, A. D. L. (2005) Molecular force modulation spectroscopy revealing the dynamic response of single bacteriorhodopsins. Biophys. J. 88, 1423-1431.
78. Bippes, C. A., Humphris, A. D., Stark, M., Muller, D. J., and Janovjak, H. (2006) Direct measurement of single-molecule viscoelasticity in atomic force microscope force-extension experiments. Eur. Biophys. J. 35, 287-292.
79. Janovjak, H., Sapra, K. T., and Muller, D. J. (2005) Complex stability of single proteins explored by forced unfolding experiments. Biophys. J. 88, L37-L39.
80. Cisneros, D. A., Oberbarnscheidt, L., Pannier, A., Klare, J. P., Helenius, J., Engelhard, M., Oesterhelt, F., and Muller, D. J. (2008) Transducer binding establishes localized interactions to tune sensory rhodopsin II. Structure . (in press).
81. Kedrov, A., Krieg, M., Ziegler, C., Kuhlbrandt, W., and Muller, D. J. (2005) Locating ligand binding and activation of a single antiporter. EMBO Rep. 6, 668-674.
82. Kedrov, A., Wegmann, S., Smits, S. H., Goswami, P., Baumann, H., and Muller, D. J. (2007) Detecting molecular interactions that stabilize, activate and guide ligand-binding of the sodium/proton antiporter MjNhaP1 from Methanococcus jannaschii. J. Struct. Biol. 159, 290-301.
83. Kedrov, A., Ziegler, C., and Muller, D. J. (2006) Differentiating ligand and inhibitor interactions of a single antiporter. J. Mol. Biol. 362, 925-932.
84. Moy, V. T., Florin, E.-L., and Gaub, H. E. (1994) Intermolecular forces and energies between ligands and receptors. Science 266, 257-259.
85. Evans, E. (1998) Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Faraday Discuss. 111, 1-16.
86. Hinterdorfer, P., and Dufrene, Y. F. (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat. Methods 3, 347-355.
87. Benoit, M., Gabriel, D., Gerisch, G., and Gaub, H. E. (2000) Discrete interactions in cell adhesion measured by single-molecule force spectroscopy. Nat. Cell Biol. 2, 313-317.
88. Helenius, J., Heisenberg, C. P., Gaub, H. E., and Muller, D. J. (2008) Single-cell force spectroscopy. J. Cell Sci. 121, 1785-1791.
89. Wolynes, P. G., Onuchic, J. N., and Thirumalai, D. (1995) Navigating the folding routes. Science 267, 1619-1620.
90. Evans, E. A., and Calderwood, D. A. (2007) Forces and bond dynamics in cell adhesion. Science 316, 1148-1153.
91. White, S. H., and von Heijne, G. (2005) Transmembrane helices before, during, and after insertion. Curr. Opin. Struct. Biol. 15, 378-386.
92. Ganchev, D. N., Rijkers, D. T., Snel, M. M., Killian, J. A., and de Kruijff, B. (2004) Strength of integration of transmembrane α-helical peptides in lipid bilayers as determined by atomic force spectroscopy. Biochemistry 43, 14987-14993.
93. Contera, S. A.,Lemaitre, V., de Planque, M. R., Watts, A., and Ryan, J. F. (2005) Unfolding and extraction of a transmembrane α-helical peptide: Dynamic force spectroscopy and molecular dynamics simulations. Biophys. J. 89, 3129-3140.
94. Janovjak, H., Sapra, K. T., Kedrov, A., and Muller, D. J. (2008) From Valleys, to Ridges: Exploring the Dynamic Energy Landscape of Single Membrane Proteins. ChemPhysChem 9, 954-966.
95. Janovjak, H., Struckmeier, J., Hubain, M., Kedrov, A., Kessler, M., and Muller, D. J. (2004) Probing the energy landscape of the membrane protein bacteriorhodopsin. Structure 12, 871-879.
96. Engelman, D. M., Chen, Y., Chin, C. N., Curran, A. R., Dixon, A. M., Dupuy, A. D., Lee, A. S., Lehnert, U., Matthews, E. E., Reshetnyak, Y. K., Senes, A., and Popot, J. L. (2003) Membrane protein folding: Beyond the two stage model. FEBS Lett. 555, 122-125.
97. Janovjak, H., Knaus, H., and Muller, D. J. (2007) Transmembrane helices have rough energy surfaces. J. Am. Chem. Soc. 129, 246-247.
98. Sanders, C. R., and Myers, J. K. (2004) Disease-related misassembly of membrane proteins. Annu. Rev. Biophys. Biomol. Struct. 33, 25-51.
99. + antiporter and insights into mechanism of action and regulation by pH. Nature 435, 1197-1202.
100. Kedrov, A., Appel, M., Baumann, H., Ziegler, C., and Muller, D. J. (2008) Examining the dynamic energy landscape of an antiporter upon inhibitor binding. J. Mol. Biol. 375, 1258-1266.