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 Journal

Volumn 274, Issue 13, 2007, Pages 3257-3269

  Klammt, Christian ^a   Srivastava, Ankita ^b   Eifler, Nora ^c   Junge, Friederike ^a   Beyermann, Michael ^d   Schwarz, Daniel ^a   Michel, Hartmut ^b   Doetsch, Volker ^a   Bernhard, Frank ^a  

^a GOETHE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^c UNIVERSITY OF BASEL   (Switzerland)

^d LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

Author keywords

Cell free expression; Detergent micelles; Endothelin 1 ligand binding site; G protein coupled receptor; Single particle analysis

Indexed keywords

AMINO ACID; DETERGENT; DIMER; ENDOTHELIN 1; ENDOTHELIN B RECEPTOR; G PROTEIN COUPLED RECEPTOR; HOMODIMER; OLIGOMER; PROTEIN SUBUNIT; RHODOPSIN;

ANALYTIC METHOD; ARTICLE; CELL FREE SYSTEM; ELUTION; LIGAND BINDING; MICELLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN SYNTHESIS; RECEPTOR UPREGULATION; SAMPLE; SOLUBILIZATION; SURFACE PLASMON RESONANCE;

AMINO ACID SEQUENCE; BINDING SITES; CELL MEMBRANE; CELL-FREE SYSTEM; DIMERIZATION; ENDOTHELIN-1; HUMANS; KINETICS; LIGANDS; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RECEPTOR, ENDOTHELIN B; RECEPTORS, G-PROTEIN-COUPLED; SURFACE PLASMON RESONANCE;

EID: 34347391677     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05854.x     Document Type: Article

References (54)

1. Bockaert J Pin JP (1999) Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J 18, 1723 1729.
2. Kristiansen K (2004) 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 103, 21 80.
3. Klabunde T Hessler G (2002) Drug design strategies for targeting G-protein-coupled receptors. Chembiochem 3, 928 944.
4. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, LeTrong I, Teller DC, Okada T, Stenkamp RE et al. (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289, 739 745.
5. Massotte D (2003) G protein-coupled receptor overexpression with the baculovirus-insect cell system: a tool for structural and functional studies. Biochim Biophys Acta 1610, 77 89.
6. Sarramegna V, Talmont F, Demange P Milon A (2003) Heterologous expression of G-protein-coupled receptors: comparison of expression systems from the standpoint of large-scale production and purification. Cell Mol Life Sci 60, 1529 1546.
7. Tate CG, Haase J, Baker C, Boorsma M, Magnani F, Vallis Y Williams DC (2003) Comparison of seven different heterologous protein expression systems for the production of the serotonin transporter. Biochim Biophys Acta 1610, 141 153.
8. Akermoun M, Koglin M, Zvalova-Iooss D, Folschweiller N, Dowell SJ Gearing KL (2005) Characterization of 16 human G protein-coupled receptors expressed in baculovirus-infected insect cells. Protein Express Purif 44, 65 74.
9. Lundstrom K (2005) Structural biology of G protein-coupled receptors. Bioorg Med Chem Lett 15, 3654 3657.
10. André N, Cherouati N, Prual C, Steffan T, Zeder-Lutz G, Magnin T, Pattuì F, Michel H, Wagner R Reinhart C (2006) Enhancing functional production of G protein-coupled receptors in Pichia pastoris to levels required for structural studies via a single expression screen. Protein Sci 15, 1115 1126.
11. Lundstrom K, Wagner R, Reinhart C, Desmyter A, Cherouati N, Magnin T, Zeder-Lutz G, Courtot M, Prual C, Andre N et al. (2006) Structural genomics on membrane proteins: comparison of more than 100 GPCRs in 3 expression systems. J Struct Funct Genomics 7, 77 91.
12. Berrier C, Park KH, Abes S, Bibonne A, Betton JM Ghazi A (2004) Cell-free synthesis of a functional ion channel in the absence of a membrane and in the presence of detergent. Biochemistry 43, 12585 12591.
13. Elbaz Y, Steiner-Mordoch S, Danieli T Schuldiner S (2004) In vitro synthesis of fully functional EmrE, a multidrug transporter, and study of its oligomeric state. Proc Natl Acad Sci USA 101, 1519 1524.
14. Klammt C, Löhr F, Schäfer B, Haase W, Dötsch V, Rüterjans H, Glaubitz C Bernhard F (2004) High level cell-free expression and specific labeling of integral membrane proteins. Eur J Biochem 271, 568 580.
15. Klammt C, Schwarz D, Fendler K, Haase W, Dötsch V Bernhard F (2005) 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 272, 6024 6038.
16. Ishihara G, Goto M, Saeki M, Ito K, Hori T, Kigawa T, Shirouzu M Yokoyama S (2005) Expression of G protein coupled receptors in a cell-free translational system using detergents and thioredoxin-fusion vectors. Protein Express Purif 41, 27 37.
17. Klammt C, Schwarz D, Löhr F, Schneider B, Dötsch V Bernhard F (2006) Cell-free expression as an emerging technique for the large scale production of integral membrane proteins. FEBS J 273, 4141 4153.
18. Schwarz D, Klammt C, Koglin A, Löhr F, Schneider B, Dötsch V Bernhard F (2006) Preparative scale cell-free expression systems: new tools for the large scale preparation of integral membrane proteins for functional and structural studies. Methods 41, 355 369.
19. Sokolowsky M (1995) Endothelin receptor subtypes and their role in transmembrane signalling mechanisms. Pharmacol Ther 68, 435 471.
20. Miyauchi T Masaki T (1999) Pathophysiology of endothelin in the cardiovascular system. Annu Rev Physiol 61, 391 415.
21. D'Orléans-Juste P, Labonté J, Bkaily G, Choufani S, Plante M Honoré JC (2002) Function of the endothelin B receptor in cardiovascular physiology and pathophysiology. Pharmacol Ther 95, 221 238.
22. Klammt C, Schwarz D, Eifler N, Engel A, Piehler J, Haase W, Hahn S, Dötsch V Bernhard F (2007) Cell-free production of G protein-coupled receptors for functional and structural studies. J Struct Biol XX, doi: 10.1016/j.jsb.2007.01.006.
23. Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A Palczewski K (2003) Atomic-force microscopy: rhodopsin dimers in native disc membranes. Nature 421, 127 128.
24. Fotiadis D, Jastrzebska B, Philippsen A, Müller DJ, Palczewski K Engel A (2006) Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr Opin Struct Biol 16, 252 259.
25. Grisshammer R, White JF, Trinh LB Shiloach J (2005) Large-scale expression and purification of a G-protein-coupled receptor for structure determination - an overview. J Struct Funct Genom 6, 159 163.
26. Satoh M, Miyamoto C, Terashima H, Tachibana Y, Wada K, Watanabe T, Hayes AE, Gentz R Furuichi Y (1997) Human endothelin receptors ETa and ETB expressed in baculovirus-infected insect cells. Eur J Biochem 249, 803 811.
27. Doi T, Hiroaki Y, Arimoto I, Fujiyoshi Y, Okamoto T, Satoh M Furuichi Y (1997) Characterization of human endothelin B receptor and mutant receptors expressed in insect cells. Eur J Biochem 248, 139 148.
28. Ozawa K, Headlam MJ, Schaeffer PM, Henderson BR, Dixon NE Otting G (2004) Optimization of an Escherichia coli system for cell-free synthesis of selectively 15N-labelled proteins for rapid analysis by NMR spectroscopy. Eur J Biochem 271, 4084 4093.
29. Torizawa T, Shimizu M, Taoka M, Miyano H Kainosho M (2004) Efficient protocol of isotopically labelled proteins by cell-free synthesis: a practical protocol. J Biomol NMR 30, 311 325.
30. Trbovic N, Klammt C, Koglin A, Löhr F, Bernhard F Dötsch V (2005) Efficient strategy for the rapid backbone assignment of membrane proteins. J Am Chem Soc 127, 13504 13505.
31. Stenlund P, Babcock GJ, Sodrowski J Myszka DG (2003) Capture and reconstitution of G protein-coupled receptors on a biosensor surface. Anal Biochem 316, 243 250.
32. Okamoto Y, Ninomiya H Masaki T (1998) Posttranslational modifications of endothelin receptor type B. Trends Cardiovasc Med 8, 327 329.
33. Galeffi P, Lombardi A, Pietraforte I, Novelli F, Donato MD, Sperandei M, Tornambe A, Fraioli R, Martayan A, Natali PG et al. (2006) Functional expression of a single-chain antibody to ErbB-2 in plants and cell-free systems. J Transl Med 4, 39 52.
34. Sen S, Jaakola VP, Pirila P, Finel M Goldman A (2005) Functional studies with membrane-bound and detergent-solubilized a2-adrenergic receptors expressed in Sf9 cells. Biochim Biophys Acta 1712, 62 70.
35. Harding PJ, Hadingham TC, McDonnell JM Watts A (2006) Direct analysis of a GPCR-agonist interaction by surface plasmon resonance. Eur Biophys J 35, 709 712.
36. Takasuka T, Sakurai T, Goto K, Furuichi Y Watanabe T (1994) Human endothelin receptor ETB. Amino acid sequence requirements for super stable complex formation with its ligand. J Biol Chem 269, 7509 7513.
37. De León H Garcia R (1995) Characterization of endothelin receptor subtypes in isolated rat renal preglomerular microvessels. Reg Peptides 60, 1 8.
38. Elshourbagy NA, Korman DR, Wu HL, Sylvester DR, Lee JA, Nuthalaganti P, Bergsma DJ, Kumar CS Nambi P (1993) Molecular characterization and regulation of the human endothelin receptors. J Biol Chem 268, 3873 3879.
39. Nakamichi K, Ihara M, Kobayashi M, Saeki T, Ishikawa K Yano M (1992) Different distribution of endothelin receptor subtypes in pulmonary tissues revealed by the novel selective ligands BQ-123 and [Ala1,3,11,15]ET-1. Biochem Biophys Res Commun 182, 144 150.
40. Saeki T, Ihara M, Fukuroda T, Yamagiwa M Yano M (1991) [Ala1,3,11,15]Endothelin-1 analogs with ETB agonistic activity. Biochem Biophys Res Commun 179, 286 292.
41. Schiller H, Haase W, Molsberger E, Janssen P, Michel H Reilander H (2000) The human ET (B) endothelin receptor heterologously produced in the methylotrophic yeast Pichia pastoris shows high-affinity binding and induction of stacked membranes. Receptors Channels 7, 93 107.
42. Hara M, Tozawa F, Itazaki K, Mihara S Fujimoto M (1998) Endothelin ETB receptors show different binding profiles in intact cells and cell membrane preparations. Eur J Pharmacol 345, 339 342.
43. Hay DL, Poyner DR Sexton PM (2006) GPCR modulation by RAMPs. Pharmacol Ther 109, 173 197.
44. Wada K, Hashido K, Terashima H, Adachi M, Fujii Y, Hiraoka O, Furuichi Y Miyamoto C (1995) Ligand binding domain of the human endothelin-B subtype receptor. Protein Express Purif 6, 228 236.
45. Boivin S, Tessier S, Aubin J, Lampron P, Detheux M Fournier A (2004) Identification of a binding domain of the endothelin-B receptor using a selective IRL-1620-derived photoprobe. Biochemistry 43, 11516 11525.
46. Lee JA, Brinkmann JA, Longton ED, Peishoff CE, Lago MA, Leber JD, Cousins RD, Gao A, Stadel JM, Kumar CS et al. (1994) Lysine 182 of endothelin B receptor modulates agonist selectivity and antagonist affinity: evidence for the overlap of peptide and non-peptide ligand binding sites. Biochemistry 48, 14543 14549.
47. Hebert TE Bouvier M (1998) Structural and functional aspects of G protein-coupled receptor oligomerization. Biochem Cell Biol 76, 1 10.
48. Schöneberg T, Schultz G Gudermann T (1999) Structural basis of G protein-coupled receptor function. Mol Cell Endocrinol 151, 181 193.
49. Rios CD, Jordan BA, Gomes I Devi LA (2001) G-protein-coupled receptor dimerization: modulation of receptor function. Pharmacol Ther 92, 71 87.
50. Gregan B, Schaefer M, Rosenthal W Oksche A (2004) Fluorescence resonance energy transfer analysis reveals the existence of endothelin-A and endothelin-B receptor homodimers. J Cardiovasc Pharmacol 44, S30 S33.
51. Ludtke SJ, Baldwin PR Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128, 82 97.
52. Penczek P, Radermacher M Frank J (1992) Three-dimensional reconstruction of single particles embedded in ice. Ultramicroscopy 40, 33 53.
53. Frank J, Verschoor A Boublik M (1982) Multivariate statistical analysis of ribosome electron micrographs. L and R lateral views of the 40 S subunit from HeLa cells. J Mol Biol 161, 107 133.
54. Frank J, Radermacher M, Pencek P, Zhu J, Li Y, Ladjadj M Leith A (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116, 190 199.