Cholesterol content drives distinct pharmacological behaviours of μ-opioid receptor in different microdomains of the CHO plasma membrane

Molecular Membrane Biology

Volumn 25, Issue 5, 2008, Pages 423-435

  Gaibelet, G ^a   Millot, C ^a   Lebrun, C ^a   Ravault, S ^a   Sauliere A ^a   Andre A ^a   Lagane, B ^a   Lopez, A ^a,b  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

Confinement; Conformation; GPCR; Lateral organization

Indexed keywords

CHOLESTEROL; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLARGINYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; FATTY ACID; G PROTEIN COUPLED RECEPTOR; LIPID; MORPHINE; MU OPIATE RECEPTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE; STEROL;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CHEMICAL ANALYSIS; CONTROLLED STUDY; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE;

ANIMALS; CHO CELLS; CHOLESTEROL; CRICETINAE; CRICETULUS; HUMANS; MEMBRANE MICRODOMAINS; RECEPTORS, OPIOID, MU; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 48249143210     PISSN: 09687688     EISSN: 14645203     Source Type: Journal    
DOI: 10.1080/09687680802203380     Document Type: Article

References (48)

1. Pike LJ. 2004. Lipid rafts: heterogeneity on the high seas. Biochem J 378:281-292.
2. Ge M, Gidwani A, Brown HA, Holowka D, Baird B, Freed JH. 2003. Ordered and disordered phases coexist in plasma membrane vesicles of RBL-2H3 mast cells. An ESR study. Biophys J 85:1278-1288.
3. London E. 2002. Insights into lipid raft structure and formation from experiments in model membranes. Curr Opin Struct Biol 12:480-486.
4. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K. 2003. Resistance of cell membranes to different detergents. Proc Natl Acad Sci USA 100:5795-5800.
5. Ipsen JH, Karlstrom G, Mouritsen OG, Wennerstrom H, Zuckermann MJ. 1987. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta 905:162-172.
6. Gandhavadi M, Allende D, Vidal A, Simon SA, McIntosh TJ. 2002. Structure, composition, and peptide binding properties of detergent soluble bilayers and detergent resistant rafts. Biophys J 82:1469-1482.
7. Gimpl G, Fahrenholz F. 2002. Cholesterol as stabilizer of the oxytocin receptor. Biochim Biophys Acta 1564:384-392.
8. Scanlon SM, Williams DC, Schloss P. 2001. Membrane cholesterol modulates serotonin transporter activity. Biochemistry 40:10507-10513.
9. Nunez MT, Glass J. 1982. Reconstitution of the transferrin receptor in lipid vesicles. Effect of cholesterol on the binding of transferrin. Biochemistry 21:4139-4143.
10. Pike LJ, Casey L. 2002. Cholesterol levels modulate EGF receptor-mediated signaling by altering receptor function and trafficking. Biochemistry 41:10315-10322.
11. Westover EJ, Covey DF, Brockman HL, Brown RE, Pike LJ. 2003. Cholesterol depletion results in site-specific increases in epidermal growth factor receptor phosphorylation due to membrane level effects. Studies with cholesterol enantiomers. J Biol Chem 278:51125-51133.
12. Polozova A, Litman BJ. 2000. Cholesterol dependent recruitment of di22:6-PC by a G protein-coupled receptor into lateral domains. Biophys J 79:2632-2643.
13. Niu SL, Mitchell DC, Litman BJ. 2002. Manipulation of cholesterol levels in rod disk membranes by methyl-beta-cyclodextrin: effects on receptor activation. J Biol Chem 277:20139-20145.
14. Niu SL, Mitchell DC, Lim SY, Wen ZM, Kim HY, Salem N Jr, Litman BJ. 2004. Reduced G protein-coupled signaling efficiency in retinal rod outer segments in response to N-3 fatty acid deficiency. J Biol Chem 279:31098-31104.
15. Pang L, Graziano M, Wang S. 1999. Membrane cholesterol modulates galanin-GalR2 interaction. Biochemistry 38:12003-12011.
16. Harikumar KG, Puri V, Singh RD, Hanada K, Pagano RE, Miller LJ. 2005. Differential Effects of modification of membrane cholesterol and sphingolipids on the conformation, function, and trafficking of the G protein-coupled cholecystokinin receptor. J Biol Chem 280:2176-2185.
17. Emmerson PJ, Clark MJ, Medzihradsky F, Remmers AE. 1999. Membrane microviscosity modulates mu-opioid receptor conformational transitions and agonist efficacy. J Neurochem 73:289-300.
18. Farahbakhsh ZT, Deamer DW, Lee NM, Loh HH. 1986. Enzymatic reconstitution of brain membrane and membrane opiate receptors. J Neurochem 46:953-962.
19. Lagane B, Gaibelet G, Meilhoc E, Masson JM, Cezanne L, Lopez A. 2000. Role of sterols in modulating the human mu-opioid receptor function in Saccharomyces cerevisiae. J Biol Chem 275:33197-33200.
20. Pucadyil TJ, Chattopadhyay A. 2004. Cholesterol modulates ligand binding and G-protein coupling to serotonin (1A) receptors from bovine hippocampus. Biochim Biophys Acta 1663:188-200.
21. Gimpl G, Klein U, Reilander H, Fahrenholz F. 1995. Expression of the human oxytocin receptor in baculovirus-infected insect cells: high-affinity binding is induced by a cholesterol-cyclodextrin complex. Biochemistry 34:13794-13801.
22. Klein U, Gimpl G, Fahrenholz F. 1995. Alteration of the myometrial plasma membrane cholesterol content with beta-cyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry 34:13784-13793.
23. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS, Choi HJ, Kuhn P, Weis WI, Kobilka BK, Stevens RC. 2007. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318:1258-1265.
24. Gimpl G, Fahrenholz F. 2000. Human oxytocin receptors in cholesterol-rich vs. cholesterol-poor microdomains of the plasma membrane. Eur J Biochem 267:2483-2497.
25. Cézanne L, Navarro L, Tocanne JF. 1992. Isolation of the plasma membrane and organelles from Chinese hamster ovary cells. Biochim Biophys Acta 1112:205-214.
26. Zak B, Dickenman RC, White EG, Burnett H, Cherney PJ. 1954. Rapid estimation of free and total cholesterol. Am J Clin Pathol 24:1307-1315.
27. Leborgne N, Cézanne L, Teulières C, Canut H, Tocanne JF, Boudet AM. 1992. Lateral and rotational mobilities of lipids in specific cellular membranes of Eucalyptus gunnii. Plant Physiol 100:246-254.
28. Christian AE, Haynes MP, Phillips MC, Rothblat GH. 1997. Use of cyclodextrins for manipulating cellular cholesterol content. J Lipid Res 38:2264-2272.
29. Huang P, Xu W, Yoon SI, Chen C, Chong PL, Liu-Chen LY. 2007. Cholesterol reduction by methyl-beta-cyclodextrin attenuates the delta opioid receptor-mediated signaling in neuronal cells but enhances it in non-neuronal cells. Biochem Pharmacol 73:534-549.
30. Prendergast FG, Haugland RP, Callahan PJ. 1981. 1-[4-(trimethylamino) phenyl]-6-phenylhexa-1,3,5-triene: synthesis, fluorescence properties and use as fluorescence probe of lipid bilayers. Biochemistry 20:7333-7338.
31. Van Blitterswijk WJ, Van Hoeven RP, Van der Meer BW. 1981. Lipid structural order parameters (reciprocal of fluidity) in biomembranes derived from steady-state fluorescence polarization measurements. Biochim Biophys Acta 644:323-332.
32. Gaibelet G, Capeyrou R, Dietrich G, Emorine LJ. 1997. Identification in the mu-opioid receptor of cysteine residues responsible for inactivation of ligand binding by thiol alkylating and reducing agents. FEBS Lett 408:135-140.
33. Gaibelet G, Meilhoc E, Riond J, Saves I, Exner T, Liaubet L, Nurnberg B, Masson JM, Emorine LJ. 1999. Nonselective coupling of the human mu-opioid receptor to multiple inhibitory G-protein isoforms. Eur J Biochem 261:517-523.
34. Cantor RS. 1999. The influence of membrane lateral pressures on simple geometric models of protein conformational equilibria. Chem Phys Lipids 101:45-56.
35. Fukuda K, Kato S, Mori K. 1995. Location of regions of the opioid receptor involved in selective agonist binding. J Biol Chem 270:6702-6709.
36. Wieland C, Jakobs KH, Wieland T. 1994. Altered guanine nucleoside triphosphate binding to transducin by cholera toxin-catalysed ADP-ribosylation. Cell Signal 6:487-492.
37. Gray RE, Munks MW, Haynes RR, Olsen GD. 2001. Mu opioid receptor efficacy and potency of morphine-6-glucuronide in neonatal guinea pig brainstem membranes: comparison with transfected CHO cells. Brain Res Bull 54:499-505.
38. Garner AE, Smith A, Hooper NM. 2008. Visualization of detergent solubilisation of membranes: Implications for the isolation of rafts. Biophys J. 94:1326-1340.
39. Bagnat M, Keranen S, Shevchenko A, Simons K. 2000. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci USA 97:3254-3259.
40. Samama P, Cotecchia S, Costa T, Lefkowitz RJ. 1993. A mutation-induced activated state of the beta 2-adrenergic receptor. Extending the ternary complex model. J Biol Chem 268:4625-4636.
41. Berchiche YA, Chow KY, Lagane B, Leduc M, Percherancier Y, Fujii N, Tamamura H, Bachelerie F, Heveker N. 2007. Direct assessment of CXCR4 mutant conformations reveals complex link between receptor structure and G(alpha)(i) activation. J Biol Chem 282:5111-5115.
42. Babiychuk B, Draeger A. 2006. Biochemical characterization of detergent-resistant membranes: a systematic approach. Biochem J 397:407-416.
43. Li XM, Momsen MM, Smaby JM, Brockman HL, Brown RE. 2001. Cholesterol decreases the interfacial elasticity and detergent solubility of sphingomyelins. Biochemistry 40:5954-5963.
44. Zhao H, Loh HH, Law PY. 2006. Adenylyl cyclase superactivation induced by long-term treatment with opioid agonist is dependent on receptor localized within lipid rafts and is independent of receptor internalization. Mol Pharmacol 69:1421-1432.
45. André A, Gaibelet G, Le Guyader L, Welby M, Lopez A, Lebrun C. 2008. Membrane partitioning of various delta-opioid receptor forms before and after agonist activations: the effect of cholesterol. Biochim Biophys Acta: 1178:1483-1492.
46. Salamon Z, Cowell S, Varga E, Yamamura HI, Hruby VJ, Tollin G. 2000. Plasmon resonance studies of agonist/antagonist binding to the human delta-opioid receptor: new structural insights into receptor-ligand interactions. Biophys J 79:2463-2474.
47. Le Guyader L, Le Roux C, Mazères S, Gaspard-Iloughmane H, Gornitzka H, Millot C, Mingotaud C, Lopez A. 2007. Changes of the membrane lipid organization characterized by means of a new cholesterol-pyrene probe. Biophys J 93:4462-4473.
48. Saulière A, Gaibelet G, Millot C, Mazères S, Lopez A, Salomé L. 2006. Diffusion of the mu opioid receptor at the surface of human neuroblastoma SH-SY5Y cells is restricted to permeable domains. FEBS Lett 580:5227-5231.