Atomic force microscopy: A multifaceted tool to study membrane proteins and their interactions with ligands

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 1 PARTA, 2014, Pages 56-68

  Whited, Allison M ^a   Park, Paul S H ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Energy landscape; Force spectroscopy; Imaging; Molecular interaction; Protein structure

Indexed keywords

ALPHA2BBETA3 INTEGRIN; BACTERIORHODOPSIN; G PROTEIN COUPLED RECEPTOR; INTEGRIN; LIGAND; MEMBRANE PROTEIN; MLOTIK1 PROTEIN; POTASSIUM CHANNEL; SODIUM PROTON EXCHANGE PROTEIN; UNCLASSIFIED DRUG;

ATOMIC FORCE MICROSCOPY; CELL COMMUNICATION; DRUG DEVELOPMENT; HUMAN; HYDROPHOBICITY; LIGAND BINDING; LIPID BILAYER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVIEW; SPECTROSCOPY;

AFM; ATOMIC FORCE MICROSCOPY; DFS; DYNAMIC SINGLE-MOLECULE FORCE SPECTROSCOPY; ENERGY LANDSCAPE; F-D; FORCE SPECTROSCOPY; FORCE-DISTANCE; G PROTEIN-COUPLED RECEPTOR; GPCR; HIGHLY ORDERED PYROLYTIC GRAPHITE; HOPG; ICAM-1; IMAGING; INTERCELLULAR ADHESION MOLECULE-1; LEUKOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; LFA-1; LHRH; LUTEINIZING HORMONE-RELEASING HORMONE; MOLECULAR INTERACTION; PE40; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA EXOTOXIN 40; SCANNING TUNNELING MICROSCOPY; SINGLE-MOLECULE FORCE SPECTROSCOPY; SMFS; STM;

LIGANDS; MEMBRANE PROTEINS; MICROSCOPY, ATOMIC FORCE; MOLECULAR PROBES; PROTEIN BINDING;

EID: 84888351252     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.04.011     Document Type: Review

References (129)

1. D.J. Muller, and Y.F. Dufrene Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology Nat. Nanotechnol. 3 2008 261 269 (Pubitemid 351668045)
2. I. Casuso, F. Rico, and S. Scheuring Biological AFM: where we come from-where we are-where we may go J. Mol. Recognit. 24 2011 406 413
3. C.M. Yip Atomic force microscopy of macromolecular interactions Curr. Opin. Struct. Biol. 11 2001 567 572 (Pubitemid 32972018)
4. A. Engel, and H.E. Gaub Structure and mechanics of membrane proteins Annu. Rev. Biochem. 77 2008 127 148
5. D.J. Muller AFM: a nanotool in membrane biology Biochemistry 47 2008 7986 7998
6. D. Fotiadis Atomic force microscopy for the study of membrane proteins Curr. Opin. Biotechnol. 23 2012 510 515
7. G. Binnig, C.F. Quate, and C. Gerber Atomic force microscope Phys. Rev. Lett. 56 1986 930 933
8. G. Binnig, H. Rohrer, C. Gerber, and E. Weibel Tunneling through a controllable vacuum gap Appl. Phys. Lett. 40 1982 178 180
9. B. Drake, C.B. Prater, A.L. Weisenhorn, S.A. Gould, T.R. Albrecht, C.F. Quate, D.S. Cannell, H.G. Hansma, and P.K. Hansma Imaging crystals, polymers, and processes in water with the atomic force microscope Science 243 1989 1586 1589
10. S.M. Lindsay, L.A. Nagahara, T. Thundat, U. Knipping, R.L. Rill, B. Drake, C.B. Prater, A.L. Weisenhorn, S.A. Gould, and P.K. Hansma STM and AFM images of nucleosome DNA under water J. Biomol. Struct. Dyn. 7 1989 279 287 (Pubitemid 19272812)
11. C. Gerber, and H.P. Lang How the doors to the nanoworld were opened Nat. Nanotechnol. 1 2006 3 5
12. P. Parot, Y.F. Dufrene, P. Hinterdorfer, C. Le Grimellec, D. Navajas, J.L. Pellequer, and S. Scheuring Past, present and future of atomic force microscopy in life sciences and medicine J. Mol. Recognit. 20 2007 418 431
13. K. El Kirat, I. Burton, V. Dupres, and Y.F. Dufrene Sample preparation procedures for biological atomic force microscopy J. Microsc. 218 2005 199 207 (Pubitemid 40812394)
14. D.J. Muller, A. Engel, and M. Amrein Preparation techniques for the observation of native biological systems with the atomic force microscope Biosens. Bioelectron. 12 1997 867 877 (Pubitemid 28015300)
15. D.J. Muller, and A. Engel Atomic force microscopy and spectroscopy of native membrane proteins Nat. Protoc. 2 2007 2191 2197 (Pubitemid 351565857)
16. T. Puntheeranurak, I. Neundlinger, R.K. Kinne, and P. Hinterdorfer Single-molecule recognition force spectroscopy of transmembrane transporters on living cells Nat. Protoc. 6 2011 1443 1452
17. G.M. Clayton, S.G. Aller, J. Wang, V. Unger, and J.H. Morais-Cabral Combining electron crystallography and X-ray crystallography to study the MlotiK1 cyclic nucleotide-regulated potassium channel J. Struct. Biol. 167 2009 220 226
18. H. Zheng, W. Liu, L.Y. Anderson, and Q.X. Jiang Lipid-dependent gating of a voltage-gated potassium channel Nat. Commun. 2 2011 250
19. + channel and its dependence on the lipid membrane Proc. Natl. Acad. Sci. U. S. A. 102 2005 15441 15446 (Pubitemid 41528076)
20. P. Fechner, T. Boudier, S. Mangenot, S. Jaroslawski, J.N. Sturgis, and S. Scheuring Structural information, resolution, and noise in high-resolution atomic force microscopy topographs Biophys. J. 96 2009 3822 3831
21. J.L. Alonso, and W.H. Goldmann Feeling the forces: atomic force microscopy in cell biology Life Sci. 72 2003 2553 2560 (Pubitemid 36369696)
22. P.T. Frederix, B.W. Hoogenboom, D. Fotiadis, D.J. Muller, and A. Engel Atomic force microscopy of biological samples MRS Bull. 29 2004 449 455
23. H.G. Hansma, and J.H. Hoh Biomolecular imaging with the atomic force microscope Annu. Rev. Biophys. Biomol. Struct. 23 1994 115 139 (Pubitemid 24217364)
24. Q. Zhong, D. Inniss, K. Kjoller, and V.B. Elings Fractured polymer silica fiber surface studied by tapping mode atomic-force microscopy Surf. Sci. 290 1993 L688 L692
25. S.N. Magonov, V. Elings, and M.H. Whangbo Phase imaging and stiffness in tapping-mode atomic force microscopy Surf. Sci. 375 1997 L385 L391
26. I. Schmitz, M. Schreiner, G. Friedbacher, and M. Grasserbauer Phase imaging as an extension to tapping mode AFM for the identification of material properties on humidity-sensitive surfaces Appl. Surf. Sci. 115 1997 190 198 (Pubitemid 127435030)
27. M.A. Hussain, A. Agnihotri, and C.A. Siedlecki AFM imaging of ligand binding to platelet integrin αIIbβ3 receptors reconstituted into planar lipid bilayers Langmuir 21 2005 6979 6986 (Pubitemid 41084487)
28. N. Kieffer, and D.R. Phillips Platelet membrane glycoproteins: functions in cellular interactions Annu. Rev. Cell Biol. 6 1990 329 357
29. R.O. Hynes Integrins: versatility, modulation, and signaling in cell adhesion Cell 69 1992 11 25
30. T.L. Lau, C. Kim, M.H. Ginsberg, and T.S. Ulmer The structure of the integrin αIIbβ3 transmembrane complex explains integrin transmembrane signalling EMBO J. 28 2009 1351 1361
31. J.P. Xiong, T. Stehle, B. Diefenbach, R. Zhang, R. Dunker, D.L. Scott, A. Joachimiak, S.L. Goodman, and M.A. Arnaout Crystal structure of the extracellular segment of integrin αVβ3 Science 294 2001 339 345 (Pubitemid 32963395)
32. O. Vinogradova, A. Velyvis, A. Velyviene, B. Hu, T. Haas, E. Plow, and J. Qin A structural mechanism of integrin αIIbβ3 "inside-out" activation as regulated by its cytoplasmic face Cell 110 2002 587 597 (Pubitemid 35247839)
33. J.W. Weisel, C.V. Stauffacher, E. Bullitt, and C. Cohen A model for fibrinogen: domains and sequence Science 230 1985 1388 1391 (Pubitemid 16105171)
34. J.M. Kollman, L. Pandi, M.R. Sawaya, M. Riley, and R.F. Doolittle Crystal structure of human fibrinogen Biochemistry 48 2009 3877 3886
35. M.A. Hussain, and C.A. Siedlecki The platelet integrin αIIbβ3 imaged by atomic force microscopy on model surfaces Micron 35 2004 565 573 (Pubitemid 38836834)
36. P.S. Sit, and R.E. Marchant Surface-dependent conformations of human fibrinogen observed by atomic force microscopy under aqueous conditions Thromb. Haemost. 82 1999 1053 1060 (Pubitemid 29419718)
37. D. Fotiadis, S. Scheuring, S.A. Müller, A. Engel, and D.J. Müller Imaging and manipulation of biological structures with the AFM Micron 33 2002 385 397 (Pubitemid 34231290)
38. D.M. Czajkowsky, and Z. Shao Submolecular resolution of single macromolecules with atomic force microscopy FEBS Lett. 430 1998 51 54 (Pubitemid 28307030)
39. S.A. Mari, J. Pessoa, S. Altieri, U. Hensen, L. Thomas, J.H. Morais-Cabral, and D.J. Muller Gating of the MlotiK1 potassium channel involves large rearrangements of the cyclic nucleotide-binding domains Proc. Natl. Acad. Sci. U. S. A. 108 2011 20802 20807
40. + channel J. Gen. Physiol. 124 2004 203 210 (Pubitemid 39244521)
41. U.B. Kaupp, and R. Seifert Cyclic nucleotide-gated ion channels Physiol. Rev. 82 2002 769 824 (Pubitemid 34743338)
42. K.B. Craven, and W.N. Zagotta CNG and HCN channels: two peas, one pod Annu. Rev. Physiol. 68 2006 375 401
43. T. Ando High-speed atomic force microscopy coming of age Nanotechnology 23 2012 062001
44. I. Casuso, F. Rico, and S. Scheuring High-speed atomic force microscopy: structure and dynamics of single proteins Curr. Opin. Chem. Biol. 15 2011 704 709
45. M. Shibata, H. Yamashita, T. Uchihashi, H. Kandori, and T. Ando High-speed atomic force microscopy shows dynamic molecular processes in photoactivated bacteriorhodopsin Nat. Nanotechnol. 5 2010 208 212
46. U. Haupts, J. Tittor, and D. Oesterhelt Closing in on bacteriorhodopsin: progress in understanding the molecule Annu. Rev. Biophys. Biomol. Struct. 28 1999 367 399 (Pubitemid 29319263)
47. J.K. Lanyi Bacteriorhodopsin Annu. Rev. Physiol. 66 2004 665 688 (Pubitemid 40614459)
48. A. Noy Force spectroscopy 101: how to design, perform, and analyze an AFM-based single molecule force spectroscopy experiment Curr. Opin. Chem. Biol. 15 2011 710 718
49. E.M. Puchner, and H.E. Gaub Force and function: probing proteins with AFM-based force spectroscopy Curr. Opin. Struct. Biol. 19 2009 605 614
50. M. Rief, and H. Grubmuller Force spectroscopy of single biomolecules Chemphyschem 3 2002 255 261
51. K.C. Neuman, and A. Nagy Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy Nat. Methods 5 2008 491 505 (Pubitemid 351761756)
52. C. Bustamante, J.C. Macosko, and G.J. Wuite Grabbing the cat by the tail: manipulating molecules one by one Nat. Rev. Mol. Cell Biol. 1 2000 130 136
53. E.L. Florin, V.T. Moy, and H.E. Gaub Adhesion forces between individual ligand-receptor pairs Science 264 1994 415 417 (Pubitemid 24179839)
54. V.T. Moy, E.L. Florin, and H.E. Gaub Intermolecular forces and energies between ligands and receptors Science 266 1994 257 259 (Pubitemid 24343509)
55. G.U. Lee, D.A. Kidwell, and R.J. Colton Sensing discrete streptavidin-biotin interactions with atomic force microscopy Langmuir 10 1994 354 357
56. R. Barattin, and N. Voyer Chemical modifications of AFM tips for the study of molecular recognition events Chem. Commun. (Camb.) 2008 1513 1532 (Pubitemid 351423052)
57. P. Hinterdorfer, and Y.F. Dufrene Detection and localization of single molecular recognition events using atomic force microscopy Nat. Methods 3 2006 347 355
58. E. Evans Probing the relation between force - lifetime - and chemistry in single molecular bonds Annu. Rev. Biophys. Biomol. Struct. 30 2001 105 128 (Pubitemid 32566158)
59. E. Evans, and K. Ritchie Dynamic strength of molecular adhesion bonds Biophys. J. 72 1997 1541 1555 (Pubitemid 27133095)
60. G.I. Bell Models for the specific adhesion of cells to cells Science 200 1978 618 627
61. H. Dietz, and M. Rief Exploring the energy landscape of GFP by single-molecule mechanical experiments Proc. Natl. Acad. Sci. U. S. A. 101 2004 16192 16197 (Pubitemid 39552821)
62. O.K. Dudko, G. Hummer, and A. Szabo Theory, analysis, and interpretation of single-molecule force spectroscopy experiments Proc. Natl. Acad. Sci. U. S. A. 105 2008 15755 15760
63. O.K. Dudko, G. Hummer, and A. Szabo Intrinsic rates and activation free energies from single-molecule pulling experiments Phys. Rev. Lett. 96 2006 108101
64. A. Fuhrmann, and R. Ros Single-molecule force spectroscopy: a method for quantitative analysis of ligand-receptor interactions Nanomedicine 5 2010 657 666
65. R. Merkel, P. Nassoy, A. Leung, K. Ritchie, and E. Evans Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy Nature 397 1999 50 53 (Pubitemid 29038244)
66. R.W. Friddle, A. Noy, and J.J. De Yoreo Interpreting the widespread nonlinear force spectra of intermolecular bonds Proc. Natl. Acad. Sci. U. S. A. 109 2012 13573 13578
67. L. Wildling, C. Rankl, T. Haselgrubler, H.J. Gruber, M. Holy, A.H. Newman, M.F. Zou, R. Zhu, M. Freissmuth, H.H. Sitte, and P. Hinterdorfer Probing binding pocket of serotonin transporter by single molecular force spectroscopy on living cells J. Biol. Chem. 287 2012 105 113
68. C.K. Lee, Y.M. Wang, L.S. Huang, and S. Lin Atomic force microscopy: determination of unbinding force, off rate and energy barrier for protein-ligand interaction Micron 38 2007 446 461 (Pubitemid 46415734)
69. K. Lundstrom An overview on GPCRs and drug discovery: structure-based drug design and structural biology on GPCRs Methods Mol. Biol. 552 2009 51 66
70. S.S. Dharap, and T. Minko Targeted proapoptotic LHRH-BH3 peptide Pharm. Res. 20 2003 889 896 (Pubitemid 36628435)
71. S.S. Dharap, Y. Wang, P. Chandna, J.J. Khandare, B. Qiu, S. Gunaseelan, P.J. Sinko, S. Stein, A. Farmanfarmaian, and T. Minko Tumor-specific targeting of an anticancer drug delivery system by LHRH peptide Proc. Natl. Acad. Sci. U. S. A. 102 2005 12962 12967 (Pubitemid 41279472)
72. J. Zhang, G. Wu, C. Song, Y. Li, H. Qiao, P. Zhu, P. Hinterdorfer, B. Zhang, and J. Tang Single molecular recognition force spectroscopy study of a luteinizing hormone-releasing hormone analogue as a carcinoma target drug J. Phys. Chem. B 116 2012 13331 13337
73. A. Ebner, L. Wildling, A.S.M. Kamruzzahan, C. Rankl, J. Wruss, C.D. Hahn, M. Holzl, R. Zhu, F. Kienberger, D. Blaas, P. Hinterdorfer, and H.J. Gruber A new, simple method for linking of antibodies to atomic force microscopy tips Bioconjug. Chem. 18 2007 1176 1184 (Pubitemid 47122640)
74. X. Zhang, E. Wojcikiewicz, and V.T. Moy Force spectroscopy of the leukocyte function-associated antigen-1/intercellular adhesion molecule-1 interaction Biophys. J. 83 2002 2270 2279
75. F. Sanchez-Madrid, P. Simon, S. Thompson, and T.A. Springer Mapping of antigenic and functional epitopes on the alpha- and beta-subunits of two related mouse glycoproteins involved in cell interactions, LFA-1 and Mac-1 J. Exp. Med. 158 1983 586 602 (Pubitemid 13049410)
76. M. Stewart, and N. Hogg Regulation of leukocyte integrin function: affinity vs. avidity J. Cell. Biochem. 61 1996 554 561 (Pubitemid 26240132)
77. A. Kedrov, H. Janovjak, K.T. Sapra, and D.J. Muller Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy Annu. Rev. Biophys. Biomol. Struct. 36 2007 233 260 (Pubitemid 46998118)
78. F. Oesterhelt, D. Oesterhelt, M. Pfeiffer, A. Engel, H.E. Gaub, and D.J. Müller Unfolding pathways of individual bacteriorhodopsins Science 288 2000 143 146 (Pubitemid 30203048)
79. T.E. Fisher, A.F. Oberhauser, M. Carrion-Vazquez, P.E. Marszalek, and J.M. Fernandez The study of protein mechanics with the atomic force microscope Trends Biochem. Sci. 24 1999 379 384 (Pubitemid 29450444)
80. C. Bustamante, J.F. Marko, E.D. Siggia, and S. Smith Entropic elasticity of lambda-phage DNA Science 265 1994 1599 1600
81. K.T. Sapra, G.P. Balasubramanian, D. Labudde, J.U. Bowie, and D.J. Muller Point mutations in membrane proteins reshape energy landscape and populate different unfolding pathways J. Mol. Biol. 376 2008 1076 1090
82. S. Kawamura, A.T. Colozo, L. Ge, D.J. Muller, and P.S. Park Structural, energetic, and mechanical perturbations in rhodopsin mutant that causes congenital stationary night blindness J. Biol. Chem. 287 2012 21826 21835
83. P.S. Park, K.T. Sapra, B. Jastrzebska, T. Maeda, A. Maeda, W. Pulawski, M. Kono, J. Lem, R.K. Crouch, S. Filipek, D.J. Muller, and K. Palczewski Modulation of molecular interactions and function by rhodopsin palmitylation Biochemistry 48 2009 4294 4304
84. M. Zocher, C. Zhang, S.G. Rasmussen, B.K. Kobilka, and D.J. Muller Cholesterol increases kinetic, energetic, and mechanical stability of the human β2-adrenergic receptor Proc. Natl. Acad. Sci. U. S. A. 109 2012 E3463 E3472
85. A. Kedrov, M. Krieg, C. Ziegler, W. Kuhlbrandt, and D.J. Muller Locating ligand binding and activation of a single antiporter EMBO Rep. 6 2005 668 674 (Pubitemid 41122436)
86. A. Kedrov, C. Ziegler, and D.J. Muller Differentiating ligand and inhibitor interactions of a single antiporter J. Mol. Biol. 362 2006 925 932 (Pubitemid 44353514)
87. + antiporter Trends Biochem. Sci. 33 2008 435 443
88. H. Janovjak, H. Knaus, and D.J. Muller Transmembrane helices have rough energy surfaces J. Am. Chem. Soc. 129 2007 246 247 (Pubitemid 46106605)
89. K.T. Sapra, P.S. Park, K. Palczewski, and D.J. Muller Mechanical properties of bovine rhodopsin and bacteriorhodopsin: possible roles in folding and function Langmuir 24 2008 1330 1337 (Pubitemid 351345853)
90. G. Milligan, P. Svoboda, and C.M. Brown Why are there so many adrenoceptor subtypes? Biochem. Pharmacol. 48 1994 1059 1071 (Pubitemid 24298355)
91. S. Kawamura, A.T. Colozo, D.J. Muller, and P.S. Park Conservation of molecular interactions stabilizing bovine and mouse rhodopsin Biochemistry 49 2010 10412 10420
92. S. Kawamura, M. Gerstung, A.T. Colozo, J. Helenius, A. Maeda, N. Beerenwinkel, P.S. Park, and D.J. Muller Kinetic, energetic, and mechanical differences between dark-state rhodopsin and opsin Structure 21 2013 426 437
93. M. Zocher, J.J. Fung, B.K. Kobilka, and D.J. Muller Ligand-specific interactions modulate kinetic, energetic, and mechanical properties of the human β2 adrenergic receptor Structure 20 2012 1391 1402
94. M. Leitner, G.E. Fantner, E.J. Fantner, K. Ivanova, T. Ivanov, I. Rangelow, A. Ebner, M. Rangl, J. Tang, and P. Hinterdorfer Increased imaging speed and force sensitivity for bio-applications with small cantilevers using a conventional AFM setup Micron 43 2012 1399 1407
95. C.M. Yip Correlative optical and scanning probe microscopies for mapping interactions at membranes Methods Mol. Biol. 950 2013 439 456
96. J.E. Verity, N. Chhabra, K. Sinnathamby, and C.M. Yip Tracking molecular interactions in membranes by simultaneous ATR-FTIR-AFM Biophys. J. 97 2009 1225 1231
97. N.G. Walter, C.Y. Huang, A.J. Manzo, and M.A. Sobhy Do-it-yourself guide: how to use the modern single-molecule toolkit Nat. Methods 5 2008 475 489 (Pubitemid 351761755)
98. P.S. Park Ensemble of G protein-coupled receptor active states Curr. Med. Chem. 19 2012 1146 1154
99. E. Freire Statistical thermodynamic linkage between conformational and binding equilibria Adv. Protein Chem. 51 1998 255 279 (Pubitemid 28252475)
100. V.J. Hilser, E.B. Garcia-Moreno, T.G. Oas, G. Kapp, and S.T. Whitten A statistical thermodynamic model of the protein ensemble Chem. Rev. 106 2006 1545 1558 (Pubitemid 43792771)
101. B. Ma, M. Shatsky, H.J. Wolfson, and R. Nussinov Multiple diverse ligands binding at a single protein site: a matter of pre-existing populations Protein Sci. 11 2002 184 197 (Pubitemid 34075781)
102. K.A. Dill, and H.S. Chan From Levinthal to pathways to funnels Nat. Struct. Biol. 4 1997 10 19 (Pubitemid 27020916)
103. M. Vendruscolo, and C.M. Dobson Structural biology. Dynamic visions of enzymatic reactions Science 313 2006 1586 1587 (Pubitemid 44414023)
104. M. Schlierf, H. Li, and J.M. Fernandez The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques Proc. Natl. Acad. Sci. U. S. A. 101 2004 7299 7304 (Pubitemid 38638027)
105. I. Casuso, and S. Scheuring Automated setpoint adjustment for biological contact mode atomic force microscopy imaging Nanotechnology 21 2010 035104
106. J. Struckmeier, R. Wahl, M. Leuschner, J. Nunes, H. Janovjak, U. Geisler, G. Hofmann, T. Jahnke, and D.J. Muller Fully automated single-molecule force spectroscopy for screening applications Nanotechnology 19 2008 384020
107. P.D. Bosshart, P.L. Frederix, and A. Engel Reference-free alignment and sorting of single-molecule force spectroscopy data Biophys. J. 102 2012 2202 2211
108. P.D. Bosshart, F. Casagrande, P.L. Frederix, M. Ratera, C.A. Bippes, D.J. Muller, M. Palacin, A. Engel, and D. Fotiadis High-throughput single-molecule force spectroscopy for membrane proteins Nanotechnology 19 2008 384014
109. D.J. Muller, G.M. Hand, A. Engel, and G.E. Sosinsky Conformational changes in surface structures of isolated connexin 26 gap junctions EMBO J. 21 2002 3598 3607 (Pubitemid 34787034)
110. J. Yu, C.A. Bippes, G.M. Hand, D.J. Muller, and G.E. Sosinsky Aminosulfonate modulated pH-induced conformational changes in connexin26 hemichannels J. Biol. Chem. 282 2007 8895 8904 (Pubitemid 47093512)
111. S. Jaroslawski, B. Zadek, F. Ashcroft, C. Venien-Bryan, and S. Scheuring Direct visualization of KirBac3.1 potassium channel gating by atomic force microscopy J. Mol. Biol. 374 2007 500 505 (Pubitemid 350007655)
112. D.J. Muller, and A. Engel Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy J. Mol. Biol. 285 1999 1347 1351 (Pubitemid 29060437)
113. S.A. Mari, S. Koster, C.A. Bippes, O. Yildiz, W. Kuhlbrandt, and D.J. Muller pH-induced conformational change of the beta-barrel-forming protein OmpG reconstituted into native E. coli lipids J. Mol. Biol. 396 2009 610 616
114. Y. Shinozaki, K. Sumitomo, M. Tsuda, S. Koizumi, K. Inoue, and K. Torimitsu Direct observation of ATP-induced conformational changes in single P2X(4) receptors PLoS Biol. 7 2009 e1000103
115. P.P. Lehenkari, and M.A. Horton Single integrin molecule adhesion forces in intact cells measured by atomic force microscopy Biochem. Biophys. Res. Commun. 259 1999 645 650 (Pubitemid 29335587)
116. J.L. Maciaszek, H. Soh, R.S. Walikonis, A.V. Tzingounis, and G. Lykotrafitis Topography of native SK channels revealed by force nanoscopy in living neurons J. Neurosci. 32 2012 11435 11440
117. P.S. Raman, C.S. Alves, D. Wirtz, and K. Konstantopoulos Single-molecule binding of CD44 to fibrin versus P-selectin predicts their distinct shear-dependent interactions in cancer J. Cell Sci. 124 2011 1903 1910
118. S. Sasuga, R. Abe, O. Nikaido, S. Kiyosaki, H. Sekiguchi, A. Ikai, and T. Osada Interaction between pheromone and its receptor of the fission yeast Schizosaccharomyces pombe examined by a force spectroscopy study J. Biomed. Biotechnol. 2012 2012 804793
119. S. Wielert-Badt, P. Hinterdorfer, H.J. Gruber, J.T. Lin, D. Badt, B. Wimmer, H. Schindler, and R.K. Kinne Single molecule recognition of protein binding epitopes in brush border membranes by force microscopy Biophys. J. 82 2002 2767 2774 (Pubitemid 34441313)
120. +-glucose co-transporter SGLT1 in living cells J. Cell Sci. 119 2006 2960 2967 (Pubitemid 44177874)
121. T. Puntheeranurak, B. Wimmer, F. Castaneda, H.J. Gruber, P. Hinterdorfer, and R.K. Kinne Substrate specificity of sugar transport by rabbit SGLT1: single-molecule atomic force microscopy versus transport studies Biochemistry 46 2007 2797 2804 (Pubitemid 46417918)
122. J. Yu, Q. Wang, X. Shi, X. Ma, H. Yang, Y.G. Chen, and X. Fang Single-molecule force spectroscopy study of interaction between transforming growth factor beta1 and its receptor in living cells J. Phys. Chem. B 111 2007 13619 13625 (Pubitemid 350275466)
123. A. Kedrov, A.M. Hellawell, A. Klosin, R.B. Broadhurst, E.R.S. Kunji, and D.J. Muller Probing the interactions of carboxy-atractyloside and atractyloside with the yeast mitochondrial ADP/ATP carrier Structure 18 2010 39 46
124. +-coupled betaine symporter BetP Proc. Natl. Acad. Sci. U. S. A. 108 2011 E890 E898
125. A. Kedrov, S. Wegmann, S.H. Smits, P. Goswami, H. Baumann, and D.J. Muller Detecting molecular interactions that stabilize, activate and guide ligand-binding of the sodium/proton antiporter MjNhaP1 from Methanococcus jannaschii J. Struct. Biol. 159 2007 290 301 (Pubitemid 47095401)
126. A. Kedrov, M. Appel, H. Baumann, C. Ziegler, and D.J. Muller Examining the dynamic energy landscape of an antiporter upon inhibitor binding J. Mol. Biol. 375 2008 1258 1266
127. M. Damaghi, C. Bippes, S. Koster, O. Yildiz, S.A. Mari, W. Kuhlbrandt, and D.J. Muller pH-dependent interactions guide the folding and gate the transmembrane pore of the beta-barrel membrane protein OmpG J. Mol. Biol. 397 2010 878 882
128. M. Damaghi, K.T. Sapra, S. Koster, O. Yildiz, W. Kuhlbrandt, and D.J. Muller Dual energy landscape: the functional state of the beta-barrel outer membrane protein G molds its unfolding energy landscape Proteomics 10 2010 4151 4162
129. C.A. Bippes, A. Zeltina, F. Casagrande, M. Ratera, M. Palacin, D.J. Muller, and D. Fotiadis Substrate binding tunes conformational flexibility and kinetic stability of an amino acid antiporter J. Biol. Chem. 284 2009 18651 18663