Surface plasmon resonance applied to G protein-coupled receptors

Biomedical Spectroscopy and Imaging

Volumn 2, Issue 3, 2013, Pages 155-181

  Locatelli Hoops, Silvia ^a   Yeliseev, Alexei A ^a   Gawrisch, Klaus ^a   Gorshkova, Inna ^b  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

Author keywords

G protein coupled receptors; Surface plasmon resonance

Indexed keywords

EID: 85013614244     PISSN: 22128794     EISSN: 22128808     Source Type: Journal    
DOI: 10.3233/BSI-130045     Document Type: Article

References (83)

1. D. Altschuh, H. Bjorkelund, J. Strandgard, L. Choulier, M. Malmqvist and K. Andersson, Deciphering complex protein interaction kinetics using Interaction Map, Biochem. Biophys. Res. Commun. 428 (2012), 74-79.
2. T.H. Bayburt, A.J. Leitz, G. Xie, D.D. Oprian and S.G. Sligar, Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins, J. Biol. Chem. 282 (2007), 14875-14881.
3. T.H. Bayburt and S.G. Sligar, Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers, Protein. Sci. 12 (2003), 2476-2481.
4. T.H. Bayburt and S.G. Sligar, Membrane protein assembly into nanodiscs, FEBS Lett. 584 (2010), 1721-1727.
5. I. Benilova, V.I. Chegel, Y.V. Ushenin, J. Vidic, A.P. Soldatkin, C. Martelet, E. Pajot and N. Jaffrezic-Renault, Stimulation of human olfactory receptor 17-40 with odorants probed by surface plasmon resonance, Eur. Biophys. J. 37 (2008), 807-814.
6. Biacore 3000 Instrument Handbook, GE Healthcare, Uppsala, 2007.
7. Biacore Sensor Surface Handbook, GE Healthcare, Uppsala, 2007.
8. BIAevaluation Software Handbook, GE Healthcare, Uppsala, 2007.
9. C. Bieri, O.P. Ernst, S. Heyse, K.P. Hofmann and H. Vogel, Micropatterned immobilization of a G protein-coupled receptor and direct detection of G protein activation, Nat. Biotechnol. 17 (1999), 1105-1108.
10. C. Blanpain, I. Migeotte, B. Lee, J. Vakili, B.J. Doranz, C. Govaerts, G. Vassart, R.W. Doms and M. Parmentier, CCR5 binds multiple CC-chemokines: MCP-3 acts as a natural antagonist, Blood 94 (1999), 1899-1905.
11. D. Charvolin, J.B. Perez, F. Rouviere, F. Giusti, P. Bazzacco, A. Abdine, F. Rappaport, K.L. Martinez and J.L. Popot, The use of amphipols as universal molecular adapters to immobilize membrane proteins onto solid supports, Proc. Natl. Acad. Sci. USA 106 (2009), 405-410.
12. K. Chen, H. Obinata and T. Izumi, Detection of G protein-coupled receptor-mediated cellular response involved in cytoskeletal rearrangement using surface plasmon resonance, Biosens. Bioelectron. 25 (2010), 1675-1680.
13. W.A. Clark, X. Jian, L. Chen and J.K. Northup, Independent and synergistic interaction of retinal G-protein subunits with bovine rhodopsin measured by surface plasmon resonance, Biochem. J. 358 (2001), 389-397.
14. P. Colin, Y. Benureau, I. Staropoli, Y. Wang, N. Gonzalez, J. Alcami, O. Hartley, A. Brelot, F. Arenzana-Seisdedos and B. Lagane, HIV-1 exploits CCR5 conformational heterogeneity to escape inhibition by chemokines, Proc. Natl. Acad. Sci. USA 110 (2013), 9475-9480.
15. M. Congreve, R.L. Rich, D.G. Myszka, F. Figaroa, G. Siegal and F.H. Marshall, Fragment screening of stabilized G-protein-coupled receptors using biophysical methods, Method Enzymol. 493 (2011), 115-136.
16. B.L. Cook, D. Steuerwald, L. Kaiser, J. Graveland-Bikker, M. Vanberghem, A.P. Berke, K. Herlihy, H. Pick, H. Vogel and S. Zhang, Large-scale production and study of a synthetic G protein-coupled receptor: human olfactory receptor 17-4, Proc. Natl. Acad. Sci. USA 106 (2009), 11925-11930.
17. M.A. Cooper, Advances in membrane receptor screening and analysis, J. Mol. Recognit. 17 (2004), 286-315.
18. M.A. Cooper, A.C. Try, J. Carroll, D.J. Ellar and D.H. Williams, Surface plasmon resonance analysis at a supported lipid monolayer, Biochim. Biophys. Acta 1373 (1998), 101-111.
19. N.J. De Mol and M.J.E. Fisher, Surface Plasmon Resonance: Methods and Protocols, N.J. De Mol and M.J.E. Fisher, eds, Methods in Molecular Biology, Vol. 627, Springer, New York, 2010.
20. V. Fruh, I.J. Ap and G. Siegal, How to catch a membrane protein in action: a review of functional membrane protein immobilization strategies and their applications, Chem. Rev. 111 (2010), 640-656.
21. E.T. Gedig, Surface chemistry in SPR technology, in: Handbook of Surface Plasmon Resonance, R.B.M. Schasfoort and A.J.A.J. Tudos, eds, RSC Publishing, Cambridge, 2008, pp. 173-218.
22. I.I. Gorshkova, J. Svitel, F. Razjouyan and P. Schuck, Bayesian analysis of heterogeneity in the distribution of binding properties of immobilized surface sites, Langmuir 24 (2008), 11577-11586.
23. R. Grisshammer, Understanding recombinant expression of membrane proteins, Curr. Opin. Biotechnol. 17 (2006), 337-340.
24. P.J. Harding, T.C. Hadingham, J.M. McDonnell and A. Watts, Direct analysis of a GPCR-agonist interaction by surface plasmon resonance, Eur. Biophys. J. 35 (2006), 709-712.
25. S. Heyse, O.P. Ernst, Z. Dienes, K.P. Hofmann and H. Vogel, Incorporation of rhodopsin in laterally structured supported membranes: observation of transducin activation with spatially and time-resolved surface plasmon resonance, Biochemistry 37 (1998), 507-522.
26. T.L. Hoffman, G. Canziani, L. Jia, J. Rucker and R.W. Doms, A biosensor assay for studying ligand-membrane receptor interactions: binding of antibodies and HIV-1 Env to chemokine receptors, Proc. Natl. Acad. Sci. USA 97 (2000), 11215-11220.
27. J. Homola, Surface Plasmon Resonance Based Sensors, O.S. Wolfbeis, ed., Springer Series on Chemical Sensors and Biosensors, Vol. 4, Springer, Berlin Heidelberg, 2006.
28. T. Huber, A.V. Botelho, K. Beyer and M.F. Brown, Membrane model for the G-protein-coupled receptor rhodopsin: hydrophobic interface and dynamical structure, Biophys. J. 86 (2004), 2078-2100.
29. L. Kai, C. Roos, S. Haberstock, D. Proverbio, Y. Ma, F. Junge, M. Karbyshev, V. Dotsch and F. Bernhard, Systems for the cell-free synthesis of proteins, Method Mol. Biol. 800 (2012), 201-225.
30. L. Kaiser, J. Graveland-Bikker, D. Steuerwald, M. Vanberghem, K. Herlihy and S. Zhang, Efficient cell-free production of olfactory receptors: detergent optimization, structure, and ligand binding analyses, Proc. Natl. Acad. Sci. USA 105 (2008), 15726-15731.
31. O.P. Karlsson and S. Lofas, Flow-mediated on-surface reconstitution of G-protein coupled receptors for applications in surface plasmon resonance biosensors, Anal. Biochem. 300 (2002), 132-138.
32. K.E. Komolov, M. Aguila, D. Toledo, J. Manyosa, P. Garriga and K.W. Koch, On-chip photoactivation of heterologously expressed rhodopsin allows kinetic analysis of G-protein signaling by surface plasmon resonance spectroscopy, Anal. Bioanal. Chem. 397 (2010), 2967-2976.
33. K.E. Komolov, I.I. Senin, P.P. Philippov and K.W. Koch, Surface plasmon resonance study of G protein/receptor coupling in a lipid bilayer-free system, Anal. Chem. 78 (2006), 1228-1234.
34. R.P.H. Kooyman, Physics of surface plasmon resonance, in: Handbook of Surface Plasmon Resonance, R.B.M. Schasfoort and A.J. Tudos, eds, RSC Publishing, Cambridge, 2008, pp. 15-34.
35. E. Kretschmann and H. Raether, Radiative decay of non radiative surface plasmons excited by light, Z. Naturforsch. Pt. A 23 (1968), 2135-2136.
36. G. Lebon, K. Bennett, A. Jazayeri and C.G. Tate, Thermostabilisation of an agonist-bound conformation of the human adenosine A(2A) receptor, J. Mol. Biol. 409 (2011), 298-310.
37. A.J. Leitz, T.H. Bayburt, A.N. Barnakov, B.A. Springer and S.G. Sligar, Functional reconstitution of beta2-adrenergic receptors utilizing self-assembling nanodisc technology, Biotechniques 40 (2006), 601-612.
38. S. Locatelli-Hoops, I. Gorshkova, K. Gawrisch and A.A. Yeliseev, Expression, surface immobilization, and characterization of functional recombinant cannabinoid receptor CB2, Biochim. Biophys. Acta - Proteins and Proteomics 1834(10) (2013), 2045-2056.
39. K. Michalke, C. Huyghe, J. Lichiere, M.-E. Graviere, M. Siponen, G. Sciara, I. Lepaul, R. Wagner, C. Magg, R. Rudolph, C. Cambillau and A. Desmyter, Mammalian G protein-coupled receptor expression in Escherichia coli: II. Refolding and biophysical characterization of mouse cannabinoid receptor 1 and human parathyroid hormone receptor 1, Anal. Biochem. 401 (2010), 74-80.
40. J.L. Miller and C.G. Tate, Engineering an ultra-thermostable beta(1)-adrenoceptor, J. Mol. Biol. 413 (2011), 628-638.
41. J. Minic, J. Grosclaude, J. Aioun, M.A. Persuy, T. Gorojankina, R. Salesse, E. Pajot-Augy, Y.X. Hou, S. Helali, N. Jaffrezic-Renault, F. Bessueille, A. Errachid, G. Gomila, O. Ruiz and J. Samitier, Immobilization of native membranebound rhodopsin on biosensor surfaces, Biochim. Biophys. Acta - Gen Subjects 1724 (2005), 324-332.
42. D.C. Mitchell, J. Kibelbek and B.J. Litman, Effect of phosphorylation on receptor conformation: the metarhodopsin I in equilibrium with metarhodopsin II equilibrium in multiply phosphorylated rhodopsin, Biochemistry 31 (1992), 8107-8111.
43. R.S. Molday and D. MacKenzie, Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes, Biochemistry 22 (1983), 653-660.
44. I. Navratilova, J. Besnard and A.L. Hopkins, Screening for GPCR ligands using surface plasmon resonance, ACS Med. Chem. Lett. 2 (2011), 549-554.
45. I. Navratilova, M. Dioszegi and D.G. Myszka, Analyzing ligand and small molecule binding activity of solubilized GPCRs using biosensor technology, Anal. Biochem. 355 (2006), 132-139.
46. I. Navratilova, D.G. Myszka and R.L. Rich, Probing membrane protein interactions with real-time biosensor technology, in: Biophysical Analysis of Membrane Proteins, E. Pebay-Peyroula, ed., Wiley-VCH, Weinheim, 2008, pp. 121-140.
47. I. Navratilova, M. Pancera, R.T. Wyatt and D.G. Myszka, A biosensor-based approach toward purification and crystallization of G protein-coupled receptors, Anal. Biochem. 353 (2006), 278-283.
48. I. Navratilova, J. Sodroski and D.G. Myszka, Solubilization, stabilization, and purification of chemokine receptors using biosensor technology, Anal. Biochem. 339 (2005), 271-281.
49. L. Neumann, T. Wohland, R.J. Whelan, R.N. Zare and B.K. Kobilka, Functional immobilization of a ligand-activated G-protein-coupled receptor, Chem. Bio. Chem. 3 (2002), 993-998.
50. S.L. Niu, B. Doctrow and D.C. Mitchell, Rhodopsin activity varies in proteoliposomes prepared by different techniques, Biochemistry 48 (2009), 156-163.
51. J. Northup, Measuring rhodopsin-G-protein interactions by surface plasmon resonance, Method Mol. Biol. 261 (2004), 93-112.
52. A. Otto, Excitation of nonradiative surface plasma waves in silver by method of frustrated total reflection, Z. Phys. 216 (1968), 398-410.
53. N.M. Rao, V. Silin, K.D. Ridge, J.T. Woodward and A.L. Plant, Cell membrane hybrid bilayers containing the G-proteincoupled receptor CCR5, Anal. Biochem. 307 (2002), 117-130.
54. R.L. Rich, J. Errey, F. Marshall and D.G. Myszka, Biacore analysis with stabilized G-protein-coupled receptors, Anal. Biochem. 409 (2011), 267-272.
55. R.L. Rich, A.R. Miles, B.K. Gale and D.G. Myszka, Detergent screening of a G-protein-coupled receptor using serial and array biosensor technologies, Anal. Biochem. 386 (2009), 98-104.
56. R.L. Rich and D.G. Myszka, Grading the commercial optical biosensor literature-class of 2008: ‘The mighty binders’, J. Mol. Recognit. 23 (2010), 1-64.
57. R.L. Rich and D.G. Myszka, Survey of the 2009 commercial optical biosensor literature, J. Mol. Recognit. 24 (2011), 892-914.
58. Z. Salamon, Y. Wang, J.L. Soulages, M.F. Brown and G. Tollin, Surface plasmon resonance spectroscopy studies of membrane proteins: Transducin binding and activation by rhodopsin monitored in thin membrane films, Biophys. J. 71 (1996), 283-294.
59. V. Sarramegn, I. Muller, A. Milon and F. Talmont, Recombinant G protein-coupled receptors from expression to renaturation: a challenge towards structure, Cell. Mol. Life Sci. 63 (2006), 1149-1164.
60. R.B.M. Schasfoort and A. McWhirter, SPR instrumentation, in: Handbook of Surface Plasmon Resonance, R.B.M. Schasfoort and A.J. Tudos, eds, RSC Publishing, Cambridge, 2008, pp. 35-80.
61. K. Schroder-Tittmann, E. Bosse-Doenecke, S. Reedtz-Runge, C. Ihling, A. Sinz, K. Tittmann and R. Rudolph, Recombinant expression, in vitro refolding, and biophysical characterization of the human glucagon-like peptide-1 receptor, Biochemistry 49 (2010), 7956-7965.
62. P. Schuck, Use of surface plasmon resonance to probe the equilibrium and dynamic aspects of interactions between biological macromolecules, Annu. Rev. Biophys. Biomol. Struct. 26 (1997), 541-566.
63. P. Schuck and A.P. Minton, Kinetic analysis of biosensor data: elementary tests for self-consistency, Trends Biochem. Sci. 21 (1996), 458-460.
64. S. Sen, V.P. Jaakola, P. Pirila, M. Finel and A. Goldman, Functional studies with membrane-bound and detergentsolubilized alpha(2)-adrenergic receptors expressed in Sf9 cells, Biochim Biophys Acta - Biomembranes 1712 (2005), 62-70.
65. V.I. Silin, E.A. Karlik, K.D. Ridge and D.J. Vanderah, Development of surface-based assays for transmembrane proteins: selective immobilization of functional CCR5, a G protein-coupled receptor, Anal. Biochem. 349 (2006), 247-253.
66. E. Stenberg, B. Persson, H. Roos and C. Urbaniczky, Quantitative-determination of surface concentration of protein with surface-plasmon resonance using radiolabeled proteins, J. Colloid Interface Sci. 143 (1991), 513-526.
67. P. Stenlund, G.J. Babcock, J. Sodroski and D.G. Myszka, Capture and reconstitution of G protein-coupled receptors on a biosensor surface, Anal. Biochem. 316 (2003), 243-250.
68. E.J. Sundberg, P.S. Andersen, I.I. Gorshkova and P. Schuck, Surface plasmon resonance biosensing in the study of ternary systems of interacting proteins, in: Protein Interactions: Biophysical Approaches for the Study of Complex Reversible Systems, P. Schuck, ed., Springer, New York, 2007, pp. 97-141.
69. J. Svitel, A. Balbo, R.A. Mariuzza, N.R. Gonzales and P. Schuck, Combined affinity and rate constant distributions of ligand populations from experimental surface binding kinetics and equilibria, Biophys. J. 84 (2003), 4062-4077.
70. J. Svitel, H. Boukari, D. Van Ryk, R.C. Willson and P. Schuck, Probing the functional heterogeneity of surface binding sites by analysis of experimental binding traces and the effect of mass transport limitation, Biophys. J. 92 (2007), 1742-1758.
71. C.G. Tate and G.F. Schertler, Engineering G protein-coupled receptors to facilitate their structure determination, Curr. Opin. Struct. Biol. 19 (2009), 386-395.
72. A. Vaish, V. Silin, M.L. Walker, K.L. Steffens, S. Krueger, A.A. Yeliseev, K. Gawrisch and D.J. Vanderah, A generalized strategy for immobilizing uniformly oriented membrane proteins at solid interfaces, Chem. Commun. 49 (2013), 2685-2687.
73. A.J. Venkatakrishnan, X. Deupi, G. Lebon, C.G. Tate, G.F. Schertler and M.M. Babu, Molecular signatures of G-proteincoupled receptors, Nature 494 (2013), 185-194.
74. J. Vidic, J. Grosclaude, R. Monnerie, M.A. Persuy, K. Badonnel, C. Baly, M. Caillol, L. Briand, R. Salesse and E. Pajot-Augy, On a chip demonstration of a functional role for odorant binding protein in the preservation of olfactory receptor activity at high odorant concentration, Lab. Chip. 8 (2008), 678-688.
75. J. Vidic, M. Pla-Roca, J. Grosclaude, M.A. Persuy, R. Monnerie, D. Caballero, A. Errachid, Y. Hou, N. Jaffrezic-Renault, R. Salesse, E. Pajot-Augy and J. Samitier, Gold surface functionalization and patterning for specific immobilization of olfactory receptors carried by nanosomes, Anal. Chem. 79 (2007), 3280-3290.
76. J.M. Vidic, J. Grosclaude, M.A. Persuy, J. Aioun, R. Salesse and E. Pajot-Augy, Quantitative assessment of olfactory receptors activity in immobilized nanosomes: a novel concept for bioelectronic nose, Lab. Chip. 6 (2006), 1026-1032.
77. K. Vukoti, T. Kimura, L. Macke, K. Gawrisch and A. Yeliseev, Stabilization of functional recombinant cannabinoid receptor CB(2) in detergent micelles and lipid bilayers, PLoS One 7 (2012), e46290.
78. A. Yeliseev and K. Vukoti, Expression of G-protein-coupled receptors, in: Production of Membrane Proteins, A.S. Robinson, ed., Wiley-VCH, Weinheim, 2011, pp. 219-248.
79. A. Yeliseev, L. Zoubak and K. Gawrisch, Use of dual affinity tags for expression and purification of functional peripheral cannabinoid receptor, Protein Expr. Purif. 53 (2007), 153-163.
80. A.A. Yeliseev, K.K. Wong, O. Soubias and K. Gawrisch, Expression of human peripheral cannabinoid receptor for structural studies, Protein Sci. 14 (2005), 2638-2653.
81. C. Yoshiura, Y. Kofuku, T. Ueda, Y. Mase, M. Yokogawa, M. Osawa, Y. Terashima, K. Matsushima and I. Shimada, NMR analyses of the interaction between CCR5 and its ligand using functional reconstitution of CCR5 in lipid bilayers, J. Am. Chem. Soc. 132 (2010), 6768-6777.
82. H. Zhao, I.I. Gorshkova, G.L. Fu and P. Schuck, A comparison of binding surfaces for SPR biosensing using an antibody- antigen system and affinity distribution analysis, Methods 59 (2013), 328-335.
83. A. Zhukov, S.P. Andrews, J.C. Errey, N. Robertson, B. Tehan, J.S. Mason, F.H. Marshall, M. Weir and M. Congreve, Biophysical mapping of the adenosine A2A receptor, J. Med. Chem. 54 (2011), 4312-4323.