The full-length mu-opioid receptor: A conformational study by circular dichroism in trifluoroethanol and membrane-mimetic environments

Journal of Membrane Biology

Volumn 223, Issue 1, 2008, Pages 49-57

  Muller, Isabelle ^a   Sarramégna, Valérie ^a,b   Renault, Marie ^a   Lafaquière, Vincent ^a   Sebai, Sarra ^a   Milon, Alain ^a   Talmont, Franck ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE LA NOUVELLE CALÉDONIE   (New Caledonia)

Author keywords

Circular dichroism; Detergent; Folding; G protein coupled receptor; Mu opioid receptor; Trifluoroethanol

Indexed keywords

DETERGENT; DODECYL SULFATE SODIUM; ENHANCED GREEN FLUORESCENT PROTEIN; MU OPIATE RECEPTOR; TRIFLUOROETHANOL;

ARTICLE; CIRCULAR DICHROISM; CONFORMATION; HUMAN; HYDROPHOBICITY; MICELLE; NONHUMAN; PH; PROTEIN FOLDING; PROTEIN STRUCTURE;

CIRCULAR DICHROISM; DETERGENTS; GREEN FLUORESCENT PROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; HYDROPHOBICITY; MEMBRANE PROTEINS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RADIOLIGAND ASSAY; RECEPTORS, OPIOID, MU; RECOMBINANT FUSION PROTEINS; SOLUBILITY; TRIFLUOROETHANOL;

EID: 47649098227     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00232-008-9112-x     Document Type: Article

References (60)

1. Arevalo E, Estephan R, Madeo J, Arshava B, Dumont M, Becker JM, Naider F (2003) Biosynthesis and biophysical analysis of domains of a yeast G protein-coupled receptor. Biopolymers 71:516-531
2. Arunkumar AI, Kumar TK, Jayaraman G, Samuel D, Yu C (1996) Induction of helical conformation in all beta-sheet proteins by trifluoroethanol. J Biomol Struct Dyn 14:381-385
3. Bane SE, Velasquez JE, Robinson AS (2007) Expression and purification of milligram levels of inactive G protein-coupled receptors in E. coli. Protein Expr Purif 52:348-355
4. 4 binding to recombinant BLT1. J Mol Biol 329:801-814
5. Baneres JL, Mesnier D, Martin A, Joubert L, Dumuis A, Bockaert J (2005) Molecular characterization of a purified 5-HT4 receptor: a structural basis for drug efficacy. J Biol Chem 280:20253-20260
6. Booth PJ (2003) The trials and tribulations of membrane protein folding in vitro. Biochim Biophys Acta 1610:51-56
7. Buck M (1998) Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q Rev Biophys 31:297-355
8. 2-adrenergic G protein-coupled receptor. Science 318:1258-1265
9. Choi G, Guo J, Makriyannis A (2005) The conformation of the cytoplasmic helix 8 of the CB1 cannabinoid receptor using NMR and circular dichroism. Biochim Biophys Acta 1668:1-9
10. 1H NMR spectroscopy in aqueous and membrane-like environments. J Pept Res 60:169-177
11. Ding FX, Schreiber D, VerBerkmoes NC, Becker JM, Naider F (2002) The chain length dependence of helix formation of the second transmembrane domain of a G protein-coupled receptor of Saccharomyces cerevisiae. J Biol Chem 277:14483-14492
12. Feng GJ, Kellett E, Scorer CA, Wilde J, White JH, Milligan G (2003) Selective interactions between helix VIII of the human mu-opioid receptors and the C terminus of periplakin disrupt G protein activation. J Biol Chem 278:33400-33407
13. Fowler CB, Pogozheva ID, LeVine H 3rd, Mosberg HI (2004a) Refinement of a homology model of the mu-opioid receptor using distance constraints from intrinsic and engineered zinc-binding sites. Biochemistry 43:8700-8710
14. Fowler CB, Pogozheva ID, Lomize AL, LeVine H 3rd, Mosberg HI (2004b) Complex of an active mu-opioid receptor with a cyclic peptide agonist modeled from experimental constraints. Biochemistry 43:15796-15810
15. Fraser NJ (2006) Expression and functional purification of a glycosylation deficient version of the human adenosine 2a receptor for structural studies. Protein Expr Purif 49:129-137
16. Hamed MM, Robinson RM, Mattice WL (1983) Helix formation upon acidification of protein-dodecyl sulfate complexes. Biochim Biophys Acta 743:260-267
17. Hutchinson EG, Thornton JM (1996) PROMOTIF-a program to identify and analyze structural motifs in proteins. Protein Sci 5:212-220
18. Johnson WC (1999) Analyzing protein circular dichroism spectra for accurate secondary structures. Proteins 35:307-312
19. Kerman A, Ananthanarayanan VS (2005) Expression and spectroscopic characterization of a large fragment of the mu-opioid receptor. Biochim Biophys Acta 1747:133-140
20. Kerman A, Ananthanarayanan VS (2007) Conformation of a double-membrane-spanning fragment of a G protein-coupled receptor: effects of hydrophobic environment and pH. Biochim Biophys Acta 1768:1199-1210
21. Kiefer H (2003) In vitro folding of alpha-helical membrane proteins. Biochim Biophys Acta 1610:57-62
22. Kiefer H, Krieger J, Olszewski JD, Von Heijne G, Prestwich GD, Breer H (1996) Expression of an olfactory receptor in Escherichia coli: purification, reconstitution, and ligand binding. Biochemistry 35:16077-16084
23. Lazarova T, Brewin KA, Stoeber K, Robinson CR (2004) Characterization of peptides corresponding to the seven transmembrane domains of human adenosine A2a receptor. Biochemistry 43:12945-12954
24. 2 adrenergic receptor: effect of DTT on receptor conformation monitored by circular dichroism and fluorescence spectroscopy. Biochemistry 35:14445-14451
25. Matthes HW, Maldonado R, Simonin F, Valverde O, Slowe S, Kitchen I, Befort K, Dierich A, Le Meur M, Dolle P, Tzavara E, Hanoune J, Roques BP, Kieffer BL (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383:819-823
26. Molina PE (2006) Opioids and opiates: analgesia with cardiovascular, haemodynamic and immune implications in critical illness. J Intern Med 259:138-154
27. Montserret R, McLeish MJ, Bockmann A, Geourjon C, Penin F (2000) Involvement of electrostatic interactions in the mechanism of peptide folding induced by sodium dodecyl sulfate binding. Biochemistry 39:8362-8373
28. O'Malley MA, Lazarova T, Britton ZT, Robinson AS (2007) High-level expression in Saccharomyces cerevisiae enables isolation and spectroscopic characterization of functional human adenosine A2a receptor. J Struct Biol 159:166-178
29. Ormo M, Cubitt AB, Kallio K, Gross LA, Tsien RY, Remington SJ (1996) Crystal structure of the Aequorea victoria green fluorescent protein. Science 273:1392-1395
30. Palchevskyy SS, Posokhov YO, Olivier B, Popot JL, Pucci B, Ladokhin AS (2006) Chaperoning of insertion of membrane proteins into lipid bilayers by hemifluorinated surfactants: application to diphtheria toxin. Biochemistry 45:2629-2635
31. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289:739-745
32. Palm GJ, Zdanov A, Gaitanaris GA, Stauber R, Pavlakis GN, Wlodawer A (1997) The structural basis for spectral variations in green fluorescent protein. Nat Struct Biol 4:361-365
33. Park K, Perczel A, Fasman GD (1992) Differentiation between transmembrane helices and peripheral helices by the deconvolution of circular dichroism spectra of membrane proteins. Protein Sci 1:1032-1049
34. Peterson GL, Toumadje A, Johnson WC Jr, Schimerlik MI (1995) Purification of recombinant porcine m2 muscarinic acetylcholine receptor from Chinese hamster ovary cells. Circular dichroism spectra and ligand binding properties. J Biol Chem 270:17808-17814
35. Phillips GNJ (2006) The three-dimensional structure of green fluorescent protein and its implication for function and design. John Wiley, Hoboken, NJ
36. Popot JL, Berry EA, Charvolin D, Creuzenet C, Ebel C, Engelman DM, Flotenmeyer M, Giusti F, Gohon Y, Hong Q, Lakey JH, Leonard K, Shuman HA, Timmins P, Warschawski DE, Zito F, Zoonens M, Pucci B, Tribet C (2003) Amphipols: polymeric surfactants for membrane biology research. Cell Mol Life Sci 60:1559-1574
37. Popot JL, Engelman DM (1990) Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29:4031-4037
38. Provencher SW, Glockner J (1981) Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20:33-37
39. 2 adrenergic G-protein-coupled receptor. Nature 450:383-387
40. Rigby AC, Grant CW, Shaw GS (1998) Solution and solid state conformation of the human EGF receptor transmembrane region. Biochim Biophys Acta 1371:241-253
41. Sarramegna V, Demange P, Milon A, Talmont F (2002a) Optimizing functional versus total expression of the human mu-opioid receptor in Pichia pastoris. Protein Expr Purif 24:212-220
42. Sarramegna V, Talmont F, Seree de Roch M, Milon A, Demange P (2002b) Green fluorescent protein as a reporter of human mu-opioid receptor overexpression and localization in the methylotrophic yeast Pichia pastoris. J Biotechnol 99:23-39
43. Sarramegna V, Talmont F, Demange P, Milon A (2003) Heterologous expression of G-protein-coupled receptors: comparison of expression systems fron the standpoint of large-scale production and purification. Cell Mol Life Sci 60:1529-1546
44. Sarramegna V, Muller I, Mousseau G, Froment C, Monsarrat B, Milon A, Talmont F (2005) Solubilization, purification, and mass spectrometry analysis of the human mu-opioid receptor expressed in Pichia pastoris. Protein Expr Purif 43:85-93
45. Sarramegna V, Muller I, Milon A, Talmont F (2006) Recombinant G protein-coupled receptors from expression to renaturation: a challenge towards structure. Cell Mol Life Sci 63:1149-1164
46. Schievano E, Calisti T, Menegazzo I, Battistutta R, Peggion E, Mammi S, Palu G, Loregian A (2004) pH-dependent conformational changes and topology of a herpesvirus translocating peptide in a membrane-mimetic environment. Biochemistry 43:9343-9351
47. Schlyer S, Horuk R (2006) I want a new drug: G-protein-coupled receptors in drug development. Drug Discov Today 11:481-493
48. Sreerama N, Venyaminov SY, Woody RW (1999) Estimation of the number of alphahelical and betastrand segments in proteins using CD spectroscopy. Protein Sci 8:370-380
49. Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287:252-260
50. Sreerama N, Woody RW (2004) On the analysis of membrane protein circular dichroism spectra. Protein Sci 13:100-112
51. Stevens TJ, Arkin IT (2000) Do more complex organisms have a greater proportion of membrane proteins in their genomes? Proteins 39:417-420
52. Thevenin D, Lazarova T, Roberts MF, Robinson CR (2005) Oligomerization of the fifth transmembrane domain from the adenosine A2A receptor. Protein Sci 14:2177-2186
53. Tyndall JD, Sandilya R (2005) GPCR agonists and antagonists in the clinic. Med Chem 1:405-421
54. Venyaminov S, Yang J (1996) Determination of protein secondary structure. Plenum Press, New York
55. Visser NV, Hink MA, Borst JW, van der Krogt GN, Visser AJ (2002) Circular dichroism spectroscopy of fluorescent proteins. FEBS Lett 521:31-35
56. Wu CS, Ikeda K, Yang JT (1981) Ordered conformation of polypeptides and proteins in acidic dodecyl sulfate solution. Biochemistry 20:566-570
57. Wu CS, Yang JT (1978) Conformation of naturally-occurring peptides in surfactant solution: its relation to the structure-forming potential of amino acid sequence. Biochem Biophys Res Commun 82:85-91
58. Xie XQ, Zhao J, Zheng H (2004) Expression, purification, and isotope labeling of cannabinoid CB2 receptor fragment, CB2(180-233). Protein Expr Purif 38:61-68
59. Yang F, Moss LG, Phillips GN Jr (1996) The molecular structure of green fluorescent protein. Nat Biotechnol 14:1246-1251
60. Zhang Y, Devries ME, Skolnick J (2006) Structure modeling of all identified G protein-coupled receptors in the human genome. PLoS Comput Biol 2:e13