Modulation of G-protein coupled receptor sample quality by modified cell-free expression protocols: A case study of the human endothelin A receptor

Journal of Structural Biology

Volumn 172, Issue 1, 2010, Pages 94-106

  Junge, Friederike ^a   Luh, Laura M ^a   Proverbio, Davide ^a   Schäfer, Birgit ^a   Abele, Rupert ^a   Beyermann, Michael ^b   Dötsch, Volker ^a   Bernhard, Frank ^a  

^a GOETHE UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

Author keywords

Agonist binding; Cell free expression; Endothelin A receptor; G protein coupled receptors; Ligand affinity chromatography; Solubilization

Indexed keywords

DETERGENT; ENDOTHELIN A RECEPTOR; ENDOTHELIN B RECEPTOR; G PROTEIN COUPLED RECEPTOR; MEMBRANE PROTEIN;

AFFINITY CHROMATOGRAPHY; ANISOTROPY; ARTICLE; CELL FREE SYSTEM; EMISSION ANISOTROPY; GENE EXPRESSION SYSTEM; HUMAN; LIGAND BINDING; LIPID BILAYER; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN QUALITY; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SOLUBILIZATION;

BINDING, COMPETITIVE; BLOTTING, WESTERN; CELL-FREE SYSTEM; CHROMATOGRAPHY, AFFINITY; CIRCULAR DICHROISM; DETERGENTS; FLUORESCENCE POLARIZATION; HUMANS; LIGANDS; PROTEIN STABILITY; PROTEOMICS; RADIOLIGAND ASSAY; RECEPTOR, ENDOTHELIN A; RECEPTORS, G-PROTEIN-COUPLED; REPRODUCIBILITY OF RESULTS; SOLUBILITY;

EID: 77956188838     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.05.004     Document Type: Article

References (70)

1. Andre N., Cherouati N., Prual C., Steffan T., Zeder-Lutz G., Magnin T., Pattus F., Michel H., Wagner R., Reinhart C. Enhancing functional production of G protein-coupled receptors in Pichia pastoris to levels required for structural studies via a single expression screen. Protein Sci. 2006, 15:1115-1126.
2. Bagnato A., Natali P.G. Endothelin receptors as novel targets in tumor therapy. J. Transl. Med. 2004, 2:16.
3. Baneres J.L., Parello J. Structure-based analysis of GPCR function: evidence for a novel pentameric assembly between the dimeric leukotriene B4 receptor BLT1 and the G-protein. J. Mol. Biol. 2003, 329:815-829.
4. Baneres J.L., Mesnier D., Martin A., Joubert L., Dumuis A., Bockaert J. Molecular characterization of a purified 5-HT4 receptor: a structural basis for drug efficacy. J. Biol. Chem. 2005, 280:20253-20260.
5. Bazarsuren A., Grauschopf U., Wozny M., Reusch D., Hoffmann E., Schaefer W., Panzner S., Rudolph R. In vitro folding, functional characterization, and disulfide pattern of the extracellular domain of human GLP-1 receptor. Biophys. Chem. 2002, 96:305-318.
6. Cherezov V., Rosenbaum D.M., Hanson M.A., Rasmussen S.G., Thian F.S., Kobilka T.S., Choi H.J., Kuhn P., Weis W.I., Kobilka B.K., Stevens R.C. High-resolution crystal structure of an engineered human {beta}2-adrenergic G protein coupled receptor. Science 2007, 318:1258-1265.
7. Cramer H., Schmenger K., Heinrich K., Horstmeyer A., Boning H., Breit A., Piiper A., Lundstrom K., Muller-Esterl W., Schroeder C. Coupling of endothelin receptors to the ERK/MAP kinase pathway. Roles of palmitoylation and G(alpha)q. Eur. J. Biochem. 2001, 268:5449-5459.
8. Dahmane T., Damian M., Mary S., Popot J.L., Baneres J.L. Amphipol-assisted in vitro folding of G protein-coupled receptors. Biochemistry 2009, 48:6516-6521.
9. Dalbey R.E., Chen M. Sec-translocase mediated membrane protein biogenesis. Biochim. Biophys. Acta 2004, 1694:37-53.
10. Davenport A.P. International Union of Pharmacology. XXIX. Update on endothelin receptor nomenclature. Pharmacol. Rev. 2002, 54:219-226.
11. Desmarets J., Gresser O., Guedin D., Frelin C. Interaction of endothelin-1 with cloned bovine ETA receptors: biochemical parameters and functional consequences. Biochemistry 1996, 35:14868-14875.
12. Drew D., Froderberg L., Baars L., de Gier J.W. Assembly and overexpression of membrane proteins in Escherichia coli. Biochim. Biophys. Acta 2003, 1610:3-10.
13. Endo Y., Sawasaki T. Advances in genome-wide protein expression using the wheat germ cell-free system. Methods Mol. Biol. 2005, 310:145-167.
14. Evans N.J., Walker J.W. Endothelin receptor dimers evaluated by FRET, ligand binding, and calcium mobilization. Biophys. J. 2008, 95:483-492.
15. Fitzsimons C.P., Monczor F., Fernandez N., Shayo C., Davio C. Mepyramine, a histamine H1 receptor inverse agonist, binds preferentially to a G protein-coupled form of the receptor and sequesters G protein. J. Biol. Chem. 2004, 279:34431-34439.
16. Gourdon P., Alfredsson A., Pedersen A., Malmerberg E., Nyblom M., Widell M., Berntsson R., Pinhassi J., Braiman M., Hansson O., Bonander N., Karlsson G., Neutze R. Optimized in vitro and in vivo expression of proteorhodops: a seven-transmembrane proton pump. Protein Expr. Purif. 2008, 58:103-113.
17. Gregan B., Jurgensen J., Papsdorf G., Furkert J., Schaefer M., Beyermann M., Rosenthal W., Oksche A. Ligand-dependent differences in the internalization of endothelin A and endothelin B receptor heterodimers. J. Biol. Chem. 2004, 279:27679-27687.
18. Gregan B., Schaefer M., Rosenthal W., Oksche A. Fluorescence resonance energy transfer analysis reveals the existence of endothelin-A and endothelin-B receptor homodimers. J. Cardiovasc. Pharmacol. 2004, 44(Suppl 1.):S30-S33.
19. Grisshammer R., White J.F., Trinh L.B., Shiloach J. Large-scale expression and purification of a G-protein-coupled receptor for structure determination - an overview. J. Struct. Funct. Genomics 2005, 6:159-163.
20. Hay D.L., Poyner D.R., Sexton P.M. GPCR modulation by RAMPs. Pharmacol. Ther. 2006, 109:173-197.
21. Haynes W.G., Webb D.J. Endothelin as a regulator of cardiovascular function in health and disease. J. Hypertens. 1998, 16:1081-1098.
22. Ishihara G., Goto M., Saeki M., Ito K., Hori T., Kigawa T., Shirouzu M., Yokoyama S. Expression of G protein coupled receptors in a cell-free translational system using detergents and thioredoxin-fusion vectors. Protein Expr. Purif. 2005, 41:27-37.
23. Junge F., Schneider B., Reckel S., Schwarz D., Dötsch V., Bernhard F. Large-scale production of functional membrane proteins. Cell. Mol. Life Sci. 2008, 65:1729-1755.
24. Kaiser L., Graveland-Bikker J., Steuerwald D., Vanberghem M., Herlihy K., Zhang S. Efficient cell-free production of olfactory receptors: detergent optimization, structure, and ligand binding analyses. Proc. Natl. Acad. Sci. USA 2008, 105:15726-15731.
25. Kalmbach R., Chizhov I., Schumacher M.C., Friedrich T., Bamberg E., Engelhard M. Functional cell-free synthesis of a seven helix membrane prote: in situ insertion of bacteriorhodopsin into liposomes. J. Mol. Biol. 2007, 371:639-648.
26. Kamonchanok S., Balog C.I., van der Does A.M., Booth R., de Grip W.J., Deelder A.M., Bakker R.A., Leurs R., Hensbergen P.J. GPCR proteomics: mass spectrometric and functional analysis of histamine H1 receptor after baculovirus-driven and in vitro cell free expression. J. Proteome Res. 2008, 7:621-629.
27. Katzen F., Fletcher J.E., Yang J.P., Kang D., Peterson T.C., Cappuccio J.A., Blanchette C.D., Sulchek T., Chromy B.A., Hoeprich P.D., Coleman M.A., Kudlicki W. Insertion of membrane proteins into discoidal membranes using a cell-free protein expression approach. J. Proteome Res. 2008, 7:3535-3542.
28. Katzen F., Peterson T.C., Kudlicki W. Membrane protein expression: no cells required. Trends Biotechnol. 2009, 27:455-460.
29. Keller T., Schwarz D., Bernhard F., Dötsch V., Hunte C., Gorboulev V., Koepsell H. Cell free expression and functional reconstitution of eukaryotic drug transporters. Biochemistry 2008, 47:4552-4564.
30. Klabunde T., Hessler G. Drug design strategies for targeting G-protein-coupled receptors. Chembiochem 2002, 3:928-944.
31. Klammt C., Löhr F., Schäfer B., Haase W., Dötsch V., Rüterjans H., Glaubitz C., Bernhard F. High level cell-free expression and specific labeling of integral membrane proteins. Eur. J. Biochem. 2004, 271:568-580.
32. Klammt C., Schwarz D., Fendler K., Haase W., Dötsch V., Bernhard F. Evaluation of detergents for the soluble expression of alpha-helical and beta-barrel-type integral membrane proteins by a preparative scale individual cell-free expression system. FEBS J. 2005, 272:6024-6038.
33. Klammt C., Schwarz D., Eifler N., Engel A., Piehler J., Haase W., Hahn S., Dötsch V., Bernhard F. Cell-free production of G protein-coupled receptors for functional and structural studies. J. Struct. Biol. 2007, 158:482-493.
34. Klammt C., Srivastava A., Eifler N., Junge F., Beyermann M., Schwarz D., Michel H., Dötsch V., Bernhard F. Functional analysis of cell-free-produced human endothelin B receptor reveals transmembrane segment 1 as an essential area for ET-1 binding and homodimer formation. FEBS J. 2007, 274:3257-3269.
35. Koglin A., Klammt C., Trbovic N., Schwarz D., Schneider B., Schafer B., Lohr F., Bernhard F., Dötsch V. Combination of cell-free expression and NMR spectroscopy as a new approach for structural investigation of membrane proteins. Magn. Reson. Chem. 2006, 44:S17-S23.
36. Kopeina G.S., Afonina Z.A., Gromova K.V., Shirokov V.A., Vasiliev V.D., Spirin A.S. Step-wise formation of eukaryotic double-row polyribosomes and circular translation of polysomal mRNA. Nucleic Acids Res. 2008, 36:2476-2488.
37. Kristiansen K. Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacol. Ther. 2004, 103:21-80.
38. Liguori L., Marques B., Villegas-Mendez A., Rothe R., Lenormand J.L. Production of membrane proteins using cell-free expression systems. Expert Rev. Proteomics 2007, 4:79-90.
39. Link A.J., Skretas G., Strauch E.M., Chari N.S., Georgiou G. Efficient production of membrane-integrated and detergent-soluble G protein-coupled receptors in Escherichia coli. Protein Sci. 2008, 17:1857-1863.
40. Lundstrom K. Latest development in drug discovery on G protein-coupled receptors. Curr. Protein Pept. Sci. 2006, 7:465-470.
41. Magnani F., Shibata Y., Serrano-Vega M.J., Tate C.G. Co-evolving stability and conformational homogeneity of the human adenosine A2a receptor. Proc. Natl. Acad. Sci. USA 2008, 105:10744-10749.
42. Magnin T., Fiez-Vandal C., Potier N., Coquard A., Leray I., Steffan T., Logez C., Alkhalfioui F., Pattus F., Wagner R. A novel, generic and effective method for the rapid purification of G protein-coupled receptors. Protein Expr. Purif. 2009, 64:1-7.
43. Michalke K., Graviere M.E., Huyghe C., Vincentelli R., Wagner R., Pattus F., Schroeder K., Oschmann J., Rudolph R., Cambillau C., Desmyter A. Mammalian G-protein-coupled receptor expression in Escherichia coli: I. High-throughput large-scale production as inclusion bodies. Anal. Biochem. 2009, 386:147-155.
44. Milligan G. G protein-coupled receptor dimerization: function and ligand pharmacology. Mol. Pharmacol. 2004, 66:1-7.
45. Prata C., Giusti F., Gohon Y., Pucci B., Popot J.L., Tribet C. Nonionic amphiphilic polymers derived from tris(hydroxymethyl)-acrylamidomethane keep membrane proteins soluble and native in the absence of detergent. Biopolymers 2000, 56:77-84.
46. Rasmussen S.G., Choi H.J., Rosenbaum D.M., Kobilka T.S., Thian F.S., Edwards P.C., Burghammer M., Ratnala V.R., Sanishvili R., Fischetti R.F., Schertler G.F., Weis W.I., Kobilka B.K. Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 2007, 450:383-387.
47. Ren H., Yu D., Ge B., Cook B., Xu Z., Zhang S. High-level production, solubilization and purification of synthetic human GPCR chemokine receptors CCR5, CCR3, CXCR4 and CX3CR1. PLoS One 2009, 4:e4509.
48. Rios C.D., Jordan B.A., Gomes I., Devi L.A. G-protein-coupled receptor dimerization: modulation of receptor function. Pharmacol. Ther. 2001, 92:71-87.
49. Rosenbaum D.M., Rasmussen S.G., Kobilka B.K. The structure and function of G-protein-coupled receptors. Nature 2009, 459:356-363.
50. Russell F.D., Molenaar P. The human heart endothelin system: ET-1 synthesis, storage, release and effect. Trends Pharmacol. Sci. 2000, 21:353-359.
51. Saeki T., Ihara M., Fukuroda T., Yamagiwa M., Yano M. [Ala1,3,11,15]endothelin-1 analogs with ETB agonistic activity. Biochem. Biophys. Res. Commun. 1991, 179:286-292.
52. Sakurai T., Yanagisawa M., Masaki T. Molecular characterization of endothelin receptors. Trends Pharmacol. Sci. 1992, 13:103-108.
53. Sarramegna V., Talmont F., Demange P., Milon A. Heterologous expression of G-protein-coupled receptors: comparison of expression systems from the standpoint of large-scale production and purification. Cell. Mol. Life Sci. 2003, 60:1529-1546.
54. Schneider B., Junge F., Shirokov V.A., Durst F., Schwarz D., Dötsch V., Bernhard F. Membrane protein expression in cell-free systems. Methods Mol. Biol. 2010, 601:165-186.
55. Schwarz, D., Klammt, C., Koglin, A., Durst, F., Löhr, F., Dötsch, V., Bernhard, F., 2008. Cell-free expression approaches for the production and characterization of membrane proteins. In: Kudlicki, W.A., Katzen, F., Bennett, R. (Eds.), Cell-Free Expression. Landes Bioscience, Eurekah Bioscience, Austin.
56. Schwarz D., Junge F., Durst F., Frölich N., Schneider B., Reckel S., Sobhanifar S., Dötsch V., Bernhard F. Preparative scale expression of membrane proteins in Escherichia coli-based continuous exchange cell-free systems. Nat. Protoc. 2007, 2:2945-2957.
57. Serrano-Vega M.J., Magnani F., Shibata Y., Tate C.G. Conformational thermostabilization of the beta1-adrenergic receptor in a detergent-resistant form. Proc. Natl. Acad. Sci. USA 2008, 105:877-882.
58. Shibata Y., White J.F., Serrano-Vega M.J., Magnani F., Aloia A.L., Grisshammer R., Tate C.G. Thermostabilization of the neurotensin receptor NTS1. J. Mol. Biol. 2009, 390:262-277.
59. Shraga-Levine Z., Sokolovsky M. Functional role for glycosylated subtypes of rat endothelin receptors. Biochem. Biophys. Res. Commun. 1998, 246:495-500.
60. Slotboom D.J., Duurkens R.H., Olieman K., Erkens G.B. Static light scattering to characterize membrane proteins in detergent solution. Methods 2008, 46:73-82.
61. Spirin A.S. High-throughput cell-free systems for synthesis of functionally active proteins. Trends Biotechnol. 2004, 22:538-545.
62. Standfuss J., Xie G., Edwards P.C., Burghammer M., Oprian D.D., Schertler G.F. Crystal structure of a thermally stable rhodopsin mutant. J. Mol. Biol. 2007, 372:1179-1188.
63. Tate C.G., Haase J., Baker C., Boorsma M., Magnani F., Vallis Y., Williams D.C. Comparison of seven different heterologous protein expression systems for the production of the serotonin transporter. Biochim. Biophys. Acta 2003, 1610:141-153.
64. Wagner S., Bader M.L., Drew D., de Gier J.W. Rationalizing membrane protein overexpression. Trends Biotechnol. 2006, 24:364-371.
65. Warne T., Serrano-Vega M.J., Baker J.G., Moukhametzianov R., Edwards P.C., Henderson R., Leslie A.G., Tate C.G., Schertler G.F. Structure of a beta1-adrenergic G-protein-coupled receptor. Nature 2008, 454:486-491.
66. White J.F., Trinh L.B., Shiloach J., Grisshammer R. Automated large-scale purification of a G protein-coupled receptor for neurotensin. FEBS Lett. 2004, 564:289-293.
67. Wuu J.J., Swartz J.R. High yield cell-free production of integral membrane proteins without refolding or detergents. Biochim. Biophys. Acta 2008, 1778:1237-1250.
68. Yeliseev A.A., Wong K.K., Soubias O., Gawrisch K. Expression of human peripheral cannabinoid receptor for structural studies. Protein Sci. 2005, 14:2638-2653.
69. Yokoyama S. Protein expression systems for structural genomics and proteomics. Curr. Opin. Chem. Biol. 2003, 7:39-43.
70. Zhang Z., Austin S.C., Smyth E.M. Glycosylation of the human prostacyclin receptor: role in ligand binding and signal transduction. Mol. Pharmacol. 2001, 60:480-487.