Single-molecule force spectroscopy from nanodiscs: An assay to quantify folding, stability, and interactions of native membrane proteins

ACS Nano

Volumn 6, Issue 1, 2012, Pages 961-971

  Zocher, Michael ^a,b   Roos, Christian ^c   Wegmann, Susanne ^a   Bosshart, Patrick D ^a   Dötsch, Volker ^c   Bernhard, Frank ^c   Müller, Daniel J ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

AFM; atomic force microscopy; bacteriorhodopsin . circular dichroism; DMPC; membrane scaffold protein 1; purple membrane; reconstitution; SMFS; unfolding intermediates; unfolding pathways

Indexed keywords

AFM; ATOMIC FORCE; DMPC; PURPLE MEMBRANES; RECONSTITUTION; SMFS; UNFOLDING INTERMEDIATES; UNFOLDING PATHWAYS;

ATOMIC FORCE MICROSCOPY; BIOLOGICAL MEMBRANES; DICHROISM; MEMBRANES; SCAFFOLDS (BIOLOGY);

PROTEINS;

BACTERIORHODOPSIN; MEMBRANE PROTEIN; NANOMATERIAL;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING SITE; CHEMISTRY; GENETIC PROCEDURES; LIPID BILAYER; MATERIALS TESTING; METHODOLOGY; PARTICLE SIZE; PROTEIN BINDING; ULTRASTRUCTURE;

BACTERIORHODOPSINS; BINDING SITES; LIPID BILAYERS; MATERIALS TESTING; MEMBRANE PROTEINS; MICROSCOPY, ATOMIC FORCE; MOLECULAR PROBE TECHNIQUES; NANOSTRUCTURES; PARTICLE SIZE; PROTEIN BINDING;

EID: 84856198231     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn204624p     Document Type: Article

References (76)

1. Alberts, B.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K.; Walter, P. Membrane Proteins. In Molecular Biology of the Cell; Anderson, M., Granum, S., Eds.; Taylor and Francis: New York, 2007; pp 629-649.
2. Wallin, E.; von Heijne, G. Genome-Wide Analysis of Integral Membrane Proteins from Eubacterial, Archaean, and Eukaryotic Organisms Protein Sci. 1998, 7, 1029-1038
3. Dill, K. A.; Chan, H. S. From Levinthal to Pathways to Funnels Nat. Struct. Biol. 1997, 4, 10-19
4. White, S. H.; Wimley, W. C. Membrane Protein Folding and Stability: Physical Principles Annu. Rev. Biophys. Biomol. Struct. 1999, 28, 319-365
5. Bowie, J. U. Solving the Membrane Protein Folding Problem Nature 2005, 438, 581-589
6. Engelman, D. M. Membranes Are More Mosaic Than Fluid Nature 2005, 438, 578-580
7. Lingwood, D.; Simons, K. Lipid Rafts as a Membrane-Organizing Principle Science 2010, 327, 46-50
8. Bayburt, T. H.; Grinkova, Y. V.; Sligar, S. G. Self-Assembly of Discoidal Phospholipid Bilayer Nanoparticles with Membrane Scaffold Proteins Nano Lett. 2002, 2, 853-856
9. Sligar, S. G. Finding a Single-Molecule Solution for Membrane Proteins Biochem. Biophys. Res. Commun. 2003, 312, 115-119
10. Denisov, I. G.; Grinkova, Y. V.; Lazarides, A. A.; Sligar, S. G. Directed Self-Assembly of Monodisperse Phospholipid Bilayer Nanodiscs with Controlled Size J. Am. Chem. Soc. 2004, 126, 3477-3487
11. Boldog, T.; Grimme, S.; Li, M.; Sligar, S. G.; Hazelbauer, G. L. Nanodiscs Separate Chemoreceptor Oligomeric States and Reveal Their Signaling Properties Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 11509-11514
12. Bayburt, T. H.; Sligar, S. G. Single-Molecule Height Measurements on Microsomal Cytochrome P450 in Nanometer-Scale Phospholipid Bilayer Disks Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 6725-6730
13. Alami, M.; Dalal, K.; Lelj-Garolla, B.; Sligar, S. G.; Duong, F. Nanodiscs Unravel the Interaction between the SecYEG Channel and Its Cytosolic Partner SecA EMBO J. 2007, 26, 1995-2004
14. Bayburt, T. H.; Sligar, S. G. Self-Assembly of Single Integral Membrane Proteins into Soluble Nanoscale Phospholipid Bilayers Protein Sci. 2003, 12, 2476-2481
15. Leitz, A. J.; Bayburt, T. H.; Barnakov, A. N.; Springer, B. A.; Sligar, S. G. Functional Reconstitution of Beta2-Adrenergic Receptors Utilizing Self-Assembling Nanodisc Technology BioTechniques 2006, 40, 601-602, 604, 606.
16. Whorton, M. R.; Bokoch, M. P.; Rasmussen, S. G.; Huang, B.; Zare, R. N.; Kobilka, B.; Sunahara, R. K. A Monomeric G Protein-Coupled Receptor Isolated in a High-Density Lipoprotein Particle Efficiently Activates Its G Protein Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 7682-7687
17. Bayburt, T. H.; Vishnivetskiy, S. A.; McLean, M. A.; Morizumi, T.; Huang, C. C.; Tesmer, J. J.; Ernst, O. P.; Sligar, S. G.; Gurevich, V. V. Monomeric Rhodopsin Is Sufficient for Normal Rhodopsin Kinase (GRK1) Phosphorylation and Arrestin-1 Binding J. Biol. Chem. 2011, 286, 1420-1428
18. Kijac, A. Z.; Li, Y.; Sligar, S. G.; Rienstra, C. M. Magic-Angle Spinning Solid-State NMR Spectroscopy of Nanodisc-Embedded Human CYP3A4 Biochemistry 2007, 46, 13696-13703
19. Raschle, T.; Hiller, S.; Yu, T. Y.; Rice, A. J.; Walz, T.; Wagner, G. Structural and Functional Characterization of the Integral Membrane Protein VDAC-1 in Lipid Bilayer Nanodiscs J. Am. Chem. Soc. 2009, 131, 17777-17779
20. Kijac, A.; Shih, A. Y.; Nieuwkoop, A. J.; Schulten, K.; Sligar, S. G.; Rienstra, C. M. Lipid-Protein Correlations in Nanoscale Phospholipid Bilayers Determined by Solid-State Nuclear Magnetic Resonance Biochemistry 2010, 49, 9190-9198
21. Borch, J.; Roepstorff, P.; Moller-Jensen, J. Nanodisc-Based Co-Immunoprecipitation for Mass Spectrometric Identification of Membrane-Interacting Proteins Mol. Cell. Proteomics 2011, 10, O110-006775
22. Kedrov, A.; Janovjak, H.; Sapra, K. T.; Muller, D. J. Deciphering Molecular Interactions of Native Membrane Proteins by Single-Molecule Force Spectroscopy Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 233-260
23. Engel, A.; Gaub, H. E. Structure and Mechanics of Membrane Proteins Annu. Rev. Biochem. 2008, 77, 127-148
24. Janovjak, H.; Kessler, M.; Oesterhelt, D.; Gaub, H.; Muller, D. J. Unfolding Pathways of Native Bacteriorhodopsin Depend on Temperature EMBO J. 2003, 22, 5220-5229
25. Kedrov, A.; Krieg, M.; Ziegler, C.; Kuhlbrandt, W.; Muller, D. J. Locating Ligand Binding and Activation of a Single Antiporter EMBO Rep. 2005, 6, 668-674
26. 2+ in Native Bovine Rhodopsin J. Biol. Chem. 2007, 282, 11377-11385
27. +-Coupled Betaine Symporter BetP Proc. Natl. Acad. Sci. U. S. A. 2011, 108, E890-898
28. Sapra, K. T.; Besir, H.; Oesterhelt, D.; Muller, D. J. Characterizing Molecular Interactions in Different Bacteriorhodopsin Assemblies by Single-Molecule Force Spectroscopy J. Mol. Biol. 2006, 355, 640-650
29. Kedrov, A.; Appel, M.; Baumann, H.; Ziegler, C.; Muller, D. J. Examining the Dynamic Energy Landscape of an Antiporter Upon Inhibitor Binding J. Mol. Biol. 2008, 375, 1258-1266
30. Bippes, C. A.; Zeltina, A.; Casagrande, F.; Ratera, M.; Palacin, M.; Muller, D. J.; Fotiadis, D. Substrate Binding Tunes Conformational Flexibility and Kinetic Stability of an Amino Acid Antiporter J. Biol. Chem. 2009, 284, 18651-18663
31. Kedrov, A.; Hellawell, A. M.; Klosin, A.; Broadhurst, R. B.; Kunji, E. R.; Muller, D. J. Probing the Interactions of Carboxy-Atractyloside and Atractyloside with the Yeast Mitochondrial ADP/ATP Carrier Structure 2010, 18, 39-46
32. Sapra, K. T.; Balasubramanian, G. P.; Labudde, D.; Bowie, J. U.; Muller, D. J. Point Mutations in Membrane Proteins Reshape Energy Landscape and Populate Different Unfolding Pathways J. Mol. Biol. 2008, 376, 1076-1090
33. Sapra, K. T.; Doehner, J.; Renugopalakrishnan, V.; Padros, E.; Muller, D. J. Role of Extracellular Glutamic Acids in the Stability and Energy Landscape of Bacteriorhodopsin Biophys. J. 2008, 95, 3407-3418
34. Cisneros, D. A.; Oberbarnscheidt, L.; Pannier, A.; Klare, J. P.; Helenius, J.; Engelhard, M.; Oesterhelt, F.; Muller, D. J. Transducer Binding Establishes Localized Interactions to Tune Sensory Rhodopsin II Structure 2008, 16, 1206-1213
35. Opekarova, M.; Tanner, W. Specific Lipid Requirements of Membrane Proteins - a Putative Bottleneck in Heterologous Expression Biochim. Biophys. Acta 2003, 1610, 11-22
36. Seddon, A. M.; Curnow, P.; Booth, P. J. Membrane Proteins, Lipids and Detergents: Not Just a Soap Opera Biochim. Biophys. Acta 2004, 1666, 105-117
37. Oesterhelt, F.; Oesterhelt, D.; Pfeiffer, M.; Engel, A.; Gaub, H. E.; Muller, D. J. Unfolding Pathways of Individual Bacteriorhodopsins Science 2000, 288, 143-146
38. Muller, D. J.; Amrein, M.; Engel, A. Adsorption of Biological Molecules to a Solid Support for Scanning Probe Microscopy J. Struct. Biol. 1997, 119, 172-188
39. Bosshart, P. D.; Casagrande, F.; Frederix, P. L.; Ratera, M.; Bippes, C. A.; Muller, D. J.; Palacin, M.; Engel, A.; Fotiadis, D. High-Throughput Single-Molecule Force Spectroscopy for Membrane Proteins Nanotechnology 2008, 19, 384014
40. Struckmeier, J.; Wahl, R.; Leuschner, M.; Nunes, J.; Janovjak, H.; Geisler, U.; Hofmann, G.; Jahnke, T.; Muller, D. J. Fully Automated Single-Molecule Force Spectroscopy for Screening Applications Nanotechnology 2008, 19, 384020
41. Haupts, U.; Tittor, J.; Oesterhelt, D. Closing in on Bacteriorhodopsin: Progress in Understanding the Molecule Annu. Rev. Biophys. Biomol. Struct. 1999, 28, 367-399
42. Dencher, N. A.; Sass, H. J.; Buldt, G. Water and Bacteriorhodopsin: Structure, Dynamics, and Function Biochim. Biophys. Acta 2000, 1460, 192-203
43. Cartailler, J. P.; Luecke, H. X-Ray Crystallographic Analysis of Lipid-Protein Interactions in the Bacteriorhodopsin Purple Membrane Annu. Rev. Biophys. Biomol. Struct. 2003, 32, 285-310
44. Hirai, T.; Subramaniam, S.; Lanyi, J. K. Structural Snapshots of Conformational Changes in a Seven-Helix Membrane Protein: Lessons from Bacteriorhodopsin Curr. Opin. Struct. Biol. 2009, 19, 433-439
45. Huang, K. S.; Bayley, H.; Liao, M. J.; London, E.; Khorana, H. G. Refolding of an Integral Membrane Protein. Denaturation, Renaturation, and Reconstitution of Intact Bacteriorhodopsin and Two Proteolytic Fragments J. Biol. Chem. 1981, 256, 3802-3809
46. Brouillette, C. G.; Muccio, D. D.; Finney, T. K. pH Dependence of Bacteriorhodopsin Thermal Unfolding Biochemistry 1987, 26, 7431-7438
47. Popot, J. L.; Gerchman, S. E.; Engelman, D. M. Refolding of Bacteriorhodopsin in Lipid Bilayers. A Thermodynamically Controlled Two-Stage Process J. Mol. Biol. 1987, 198, 655-676
48. 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. et al. Membrane Protein Folding: Beyond the Two Stage Model FEBS Lett. 2003, 555, 122-125
49. Rehorek, M.; Heyn, M. P. Binding of All-Trans-Retinal to the Purple Membrane. Evidence for Cooperativity and Determination of the Extinction Coefficient Biochemistry 1979, 18, 4977-4983
50. Heyn, M. P.; Cherry, R. J.; Dencher, N. A. Lipid - Protein Interactions in Bacteriorhodopsin - Dimyristoylphosphatidylcholine Vesicles Biochemistry 1981, 20, 840-849
51. Isenbarger, T. A.; Krebs, M. P. Thermodynamic Stability of the Bacteriorhodopsin Lattice as Measured by Lipid Dilution Biochemistry 2001, 40, 11923-11931
52. Bayburt, T. H.; Grinkova, Y. V.; Sligar, S. G. Assembly of Single Bacteriorhodopsin Trimers in Bilayer Nanodiscs Arch. Biochem. Biophys. 2006, 450, 215-222
53. Muller, D. J.; Kessler, M.; Oesterhelt, F.; Moller, C.; Oesterhelt, D.; Gaub, H. Stability of Bacteriorhodopsin Alpha-Helices and Loops Analyzed by Single-Molecule Force Spectroscopy Biophys. J. 2002, 83, 3578-3588
54. Kessler, M.; Gaub, H. E. Unfolding Barriers in Bacteriorhodopsin Probed from the Cytoplasmic and the Extracellular Side by AFM Structure 2006, 14, 521-527
55. Janovjak, H.; Struckmeier, J.; Hubain, M.; Kedrov, A.; Kessler, M.; Muller, D. J. Probing the Energy Landscape of the Membrane Protein Bacteriorhodopsin Structure 2004, 12, 871-879
56. Sapra, K. T.; Park, P. S.; Palczewski, K.; Muller, D. J. Mechanical Properties of Bovine Rhodopsin and Bacteriorhodopsin: Possible Roles in Folding and Function Langmuir 2008, 24, 1330-1337
57. Dufrene, Y. F.; Evans, E.; Engel, A.; Helenius, J.; Gaub, H. E.; Muller, D. J. Five Challenges to Bringing Single-Molecule Force Spectroscopy into Living Cells Nat. Methods 2011, 8, 123-127
58. Sapra, K. T.; Park, P. S. H.; Filipek, S.; Engel, A.; Muller, D. J.; Palczewski, K. Detecting Molecular Interactions That Stabilize Native Bovine Rhodopsin J. Mol. Biol. 2006, 358, 255-269
59. Janovjak, H.; Sapra, K. T.; Kedrov, A.; Muller, D. J. From Valleys to Ridges: Exploring the Dynamic Energy Landscape of Single Membrane Proteins ChemPhysChem 2008, 9, 954-966
60. Damaghi, M.; Bippes, C.; Koster, S.; Yildiz, O.; Mari, S. A.; Kuhlbrandt, W.; Muller, D. J. pH-Dependent Interactions Guide the Folding and Gate the Transmembrane Pore of the Beta-Barrel Membrane Protein OmpG J. Mol. Biol. 2010, 397, 878-882
61. Brouillette, C. G.; McMichens, R. B.; Stern, L. J.; Khorana, H. G. Structure and Thermal Stability of Monomeric Bacteriorhodopsin in Mixed Phospholipid/Detergent Micelles Proteins 1989, 5, 38-46
62. Heyes, C. D.; El-Sayed, M. A. The Role of the Native Lipids and Lattice Structure in Bacteriorhodopsin Protein Conformation and Stability as Studied by Temperature-Dependent Fourier Transform-Infrared Spectroscopy J. Biol. Chem. 2002, 277, 29437-29443
63. Lee, A. G. How Lipids Affect the Activities of Integral Membrane Proteins Biochim. Biophys. Acta 2004, 1666, 62-87
64. Hunte, C. Specific Protein-Lipid Interactions in Membrane Proteins Biochem. Soc. Trans. 2005, 33, 938-942
65. Hunte, C.; Richers, S. Lipids and Membrane Protein Structures Curr. Opin. Struct. Biol. 2008, 18, 406-411
66. Rief, M.; Pascual, J.; Saraste, M.; Gaub, H. E. Single Molecule Force Spectroscopy of Spectrin Repeats: Low Unfolding Forces in Helix Bundles J. Mol. Biol. 1999, 286, 553-561
67. Stahl, S. W.; Puchner, E. M.; Gaub, H. E. Photothermal Cantilever Actuation for Fast Single-Molecule Force Spectroscopy Rev. Sci. Instrum. 2009, 80, 073702
68. Kobayashi, K.; Yamada, H.; Matsushige, K. Reduction of Frequency Noise and Frequency Shift by Phase Shifting Elements in Frequency Modulation Atomic Force Microscopy Rev. Sci. Instrum. 2011, 82, 033702
69. Sahin, O.; Magonov, S.; Su, C.; Quate, C. F.; Solgaard, O. An Atomic Force Microscope Tip Designed to Measure Time-Varying Nanomechanical Forces Nat. Nanotechnol. 2007, 2, 507-514
70. Lang, H. P.; Hegner, M.; Gerber, C. Cantilever Array Sensors Mater. Today 2005, 8, 30-36
71. Favre, M.; Polesel-Maris, J.; Overstolz, T.; Niedermann, P.; Dasen, S.; Gruener, G.; Ischer, R.; Vettiger, P.; Liley, M.; Heinzelmann, H. et al. Parallel AFM Imaging and Force Spectroscopy Using Two-Dimensional Probe Arrays for Applications in Cell Biology J. Mol. Recognit. 2011, 24, 446-452
72. King, G. M.; Carter, A. R.; Churnside, A. B.; Eberle, L. S.; Perkins, T. T. Ultrastable Atomic Force Microscopy: Atomic-Scale Stability and Registration in Ambient Conditions Nano Lett. 2009, 9, 1451-1456
73. Oesterhelt, D.; Stoeckenius, W. Isolation of the Cell Membrane of Halobacterium Halobium and Its Fractionation into Red and Purple Membrane Methods Enzymol. 1974, 31, 667-678
74. Mukai, Y.; Kamo, N.; Mitaku, S. Light-Induced Denaturation of Bacteriorhodopsin Solubilized by Octyl-Beta-Glucoside Protein Eng. 1999, 12, 755-759
75. Florin, E. L.; Rief, M.; Lehmann, H.; Ludwig, Dornmair, C.; Moy, V. T.; Gaub, H. E. Sensing Specific Molecular-Interactions with the Atomic-Force Microscope Biosens. Bioelectron. 1995, 10, 895-901
76. Butt, H.-J.; Jaschke, M. Calculation of Thermal Noise in Atomic Force Microscopy Nanotechnol. 1995, 6, 1-7