Two classes of cholesterol binding sites for the β2AR revealed by thermostability and NMR

Biophysical Journal

Volumn 107, Issue 10, 2014, Pages 2305-2312

  Gater, Deborah L ^a,b   Saurel, Olivier ^a   Iordanov, Iordan ^a   Liu, Wei ^c   Cherezov, Vadim ^c   Milon, Alain ^a  

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

^b KHALIFA UNIVERSITY   (United Arab Emirates)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CHOLESTEROL; PROTEIN BINDING;

BINDING SITE; CHEMISTRY; ENZYME SPECIFICITY; HUMAN; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN DENATURATION; PROTEIN STABILITY; TEMPERATURE;

BINDING SITES; CHOLESTEROL; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN STABILITY; RECEPTORS, ADRENERGIC, BETA-2; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 84912119192     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.10.011     Document Type: Article

References (62)

1. A.D. Albert, J.E. Young, and P.L. Yeagle Rhodopsin-cholesterol interactions in bovine rod outer segment disk membranes Biochim. Biophys. Acta 1285 1996 47 55
2. U. Klein, G. Gimpl, and F. Fahrenholz Alteration of the myometrial plasma membrane cholesterol content with beta-cyclodextrin modulates the binding affinity of the oxytocin receptor Biochemistry 34 1995 13784 13793
3. U. Klein, and F. Fahrenholz Reconstitution of the myometrial oxytocin receptor into proteoliposomes. Dependence of oxytocin binding on cholesterol Eur. J. Biochem. 220 1994 559 567
4. J. Oates, and A. Watts Uncovering the intimate relationship between lipids, cholesterol and GPCR activation Curr. Opin. Struct. Biol. 21 2011 802 807
5. V. Cherezov, and D.M. Rosenbaum R.C. Stevens High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor Science 318 2007 1258 1265
6. V. Cherezov, and J. Liu R.C. Stevens LCP-FRAP assay for pre-screening membrane proteins for in meso crystallization Cryst. Growth Des. 8 2008 4307 4315
7. T. Warne, and R. Moukhametzianov C.G. Tate The structural basis for agonist and partial agonist action on a β(1)-adrenergic receptor Nature 469 2011 241 244
8. W. Liu, and E. Chun R.C. Stevens Structural basis for allosteric regulation of GPCRs by sodium ions Science 337 2012 232 236
9. A. Manglik, and A.C. Kruse S. Granier Crystal structure of the μ-opioid receptor bound to a morphinan antagonist Nature 485 2012 321 326
10. D. Wacker, and C. Wang R.C. Stevens Structural features for functional selectivity at serotonin receptors Science 340 2013 615 619
11. H. Wu, and C. Wang R.C. Stevens Structure of a class C GPCR metabotropic glutamate receptor 1 bound to an allosteric modulator Science 344 2014 58 64
12. K. Zhang, and J. Zhang Q. Zhao Structure of the human P2Y12 receptor in complex with an antithrombotic drug Nature 509 2014 115 118
13. V. Cherezov Lipidic cubic phase technologies for membrane protein structural studies Curr. Opin. Struct. Biol. 21 2011 559 566
14. W. Liu, and M.A. Hanson V. Cherezov LCP-Tm: an assay to measure and understand stability of membrane proteins in a membrane environment Biophys. J. 98 2010 1539 1548
15. E.M. Landau, and J.P. Rosenbusch Lipidic cubic phases: a novel concept for the crystallization of membrane proteins Proc. Natl. Acad. Sci. USA 93 1996 14532 14535
16. M. Caffrey, and V. Cherezov Crystallizing membrane proteins using lipidic mesophases Nat. Protoc. 4 2009 706 731
17. C.V. Kulkarni, and W. Wachter S. Ahualli Monoolein: a magic lipid? Phys. Chem. Chem. Phys. 13 2011 3004 3021
18. P.O. Eriksson, and G. Lindblom Lipid and water diffusion in bicontinuous cubic phases measured by NMR Biophys. J. 64 1993 129 136
19. J.C. Panitz, and M. Gradzielski A. Wokaun Self-diffusion of surfactants, hydrocarbons, and water in an L1 phase and a cubic phase - influence of surfactant and hydrocarbon chain lengths J. Phys. Chem 98 1994 6812 6817
20. E. Boyle-Roden, and N. Hoefer M. Caffrey High resolution 1H NMR of a lipid cubic phase using a solution NMR probe J. Magn. Reson. 189 2007 13 19
21. A. Nowacka, and P.C. Mohr D. Topgaard Polarization transfer solid-state NMR for studying surfactant phase behavior Langmuir 26 2010 16848 16856
22. P. Hakansson, and P.O. Westlund Nuclear magnetic relaxation study of the microstructure of a bicontinuous cubic phase Phys. Chem. Chem. Phys. 6 2004 4321 4329
23. K.I. Momot, and K. Takegoshi T.J. Larkin Inhomogeneous NMR line shape as a probe of microscopic organization of bicontinuous cubic phases J. Phys. Chem. B 112 2008 6636 6645
24. M. Mayer, and B. Meyer Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor J. Am. Chem. Soc. 123 2001 6108 6117
25. B. Meyer, and T. Peters NMR spectroscopy techniques for screening and identifying ligand binding to protein receptors Angew. Chem. Int. Ed. Engl. 42 2003 864 890
26. C.S. Nagaraja Heteronuclear saturation transfer difference (HSTD) experiment for detection of ligand binding to proteins Chem. Phys. Lett. 420 2006 340 346
27. C. Räuber, and S. Berger 13C-NMR detection of STD spectra Magn. Reson. Chem. 48 2010 91 93
28. K.E. Kövér, and E. Wéber G. Batta (15)N and (13)C group-selective techniques extend the scope of STD NMR detection of weak host-guest interactions and ligand screening Chem. Bio. Chem 11 2010 2182 2187
29. J.L. Wagstaff, S.L. Taylor, and M.J. Howard Recent developments and applications of saturation transfer difference nuclear magnetic resonance (STD NMR) spectroscopy Mol. Biosyst. 9 2013 571 577
30. O. Soubias, and K. Gawrisch Rhodopsin-lipid interactions studied by NMR Methods Enzymol. 522 2013 209 227
31. M. Renault, and O. Saurel A. Milon Solution state NMR structure and dynamics of KpOmpA, a 210 residue transmembrane domain possessing a high potential for immunological applications J. Mol. Biol. 385 2009 117 130
32. A.K. Covington, and M. Paabo R.G. Bates Use of the glass electrode in deuterium oxide and the relation between the standardized pD (paD) scale and the operational pH in heavy water Anal. Chem. 40 1968 700 706
33. F. Jolibois, and O. Soubias A. Milon Understanding sterol-membrane interactions, part I: Hartree-Fock versus C-13 and H-1 NMR isotropic chemical shifts of sterols in solution and analysis of hydrogen-bonding effects Chemistry 10 2004 5996 6004
34. O. Soubias, and F. Jolibois A. Milon Understanding sterol-membrane interactions, part II: complete 1H and 13C assignments by solid-state NMR spectroscopy and determination of the hydrogen-bonding partners of cholesterol in a lipid bilayer Chemistry 10 2004 6005 6014
35. 13C NMR spectra of sterol derivatives, intermediates in the synthesis of ecdy-and brassinosteroids Chem. Nat. Compounds. 35 1999 642 645
36. M. Mousavi, S.S.F. Yu, and D.-L.M. Tzou A (13)C solid-state NMR analysis of vitamin D compounds Solid State Nucl. Magn. Reson. 36 2009 24 31
37. O. Soubias, and F. Jolibois V. Réat Determination of the orientation and dynamics of ergosterol in model membranes using uniform 13C labeling and dynamically averaged 13C chemical shift anisotropies as experimental restraints Biophys. J. 89 2005 1120 1131
38. D.L. Gater, and V. Réat V. Cherezov Hydrogen bonding of cholesterol in the lipidic cubic phase Langmuir 29 2013 8031 8038
39. P. Singh, and M. Jafurulla A. Chattopadhyay Desmosterol replaces cholesterol for ligand binding function of the serotonin (1A) receptor in solubilized hippocampal membranes: support for nonannular binding sites for cholesterol? Biochim. Biophys. Acta 1808 2011 2428 2434
40. A. Chattopadhyay, and Y.D. Paila M. Vairamani Differential effects of cholesterol and 7-dehydrocholesterol on ligand binding of solubilized hippocampal serotonin1A receptors: implications in SLOS Biochem. Biophys. Res. Commun. 363 2007 800 805
41. G. Gimpl, and F. Fahrenholz Cholesterol as stabilizer of the oxytocin receptor Biochim. Biophys. Acta 1564 2002 384 392
42. G. Gimpl, and U. Klein F. Fahrenholz Expression of the human oxytocin receptor in baculovirus-infected insect cells: high-affinity binding is induced by a cholesterol-cyclodextrin complex Biochemistry 34 1995 13794 13801
43. M. Jafurulla, and A. Chattopadhyay Membrane lipids in the function of serotonin and adrenergic receptors Curr. Med. Chem. 20 2013 47 55
44. 2-adrenergic receptor via cholesterol occupancy sites Biophys. J. 106 2014 1290 1300
45. Y. Xiang, and V.O. Rybin B. Kobilka Caveolar localization dictates physiologic signaling of beta 2-adrenoceptors in neonatal cardiac myocytes J. Biol. Chem. 277 2002 34280 34286
46. X. Cang, and Y. Du H. Jiang Mapping the functional binding sites of cholesterol in β2-adrenergic receptor by long-time molecular dynamics simulations J. Phys. Chem. B 117 2013 1085 1094
47. Y.D. Paila, and E. Jindal A. Chattopadhyay Cholesterol depletion enhances adrenergic signaling in cardiac myocytes Biochim. Biophys. Acta 1808 2011 461 465
48. M. Scarselli, P. Annibale, and A. Radenovic Cell type-specific β2-adrenergic receptor clusters identified using photoactivated localization microscopy are not lipid raft related, but depend on actin cytoskeleton integrity J. Biol. Chem. 287 2012 16768 16780
49. S.M. Pontier, and Y. Percherancier M. Bouvier Cholesterol-dependent separation of the beta2-adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction J. Biol. Chem. 283 2008 24659 24672
50. O. Soubias, and K. Gawrisch The role of the lipid matrix for structure and function of the GPCR rhodopsin Biochim. Biophys. Acta 1818 2012 234 240
51. A.P. Mone, and B.J. Litman Cholesterol increases the stability of rhodopsin in egg PC vesicles to thermally induced unfolding Biophys. J. 57 1990 A74
52. D.C. Mitchell, S.L. Niu, and B.J. Litman Optimization of receptor-G protein coupling by bilayer lipid composition I: kinetics of rhodopsin-transducin binding J. Biol. Chem. 276 2001 42801 42806
53. S.L. Niu, D.C. Mitchell, and B.J. Litman Optimization of receptor-G protein coupling by bilayer lipid composition II: formation of metarhodopsin II-transducin complex J. Biol. Chem. 276 2001 42807 42811
54. M.F. Brown Curvature forces in membrane lipid-protein interactions Biochemistry 51 2012 9782 9795
55. A.V. Botelho, and N.J. Gibson M.F. Brown Conformational energetics of rhodopsin modulated by nonlamellar-forming lipids Biochemistry 41 2002 6354 6368
56. A. Grossfield, S.E. Feller, and M.C. Pitman A role for direct interactions in the modulation of rhodopsin by omega-3 polyunsaturated lipids Proc. Natl. Acad. Sci. USA 103 2006 4888 4893
57. G. Gimpl, K. Burger, and F. Fahrenholz Cholesterol as modulator of receptor function Biochemistry 36 1997 10959 10974
58. G. Gimpl, and F. Fahrenholz Human oxytocin receptors in cholesterol-rich vs. cholesterol-poor microdomains of the plasma membrane Eur. J. Biochem. 267 2000 2483 2497
59. A. Reversi, and V. Rimoldi B. Chini Effects of cholesterol manipulation on the signaling of the human oxytocin receptor Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 2006 R861 R869
60. S. Muth, A. Fries, and G. Gimpl Cholesterol-induced conformational changes in the oxytocin receptor Biochem. J. 437 2011 541 553
61. K. Burger, G. Gimpl, and F. Fahrenholz Regulation of receptor function by cholesterol Cell. Mol. Life Sci. 57 2000 1577 1592
62. V. Wiegand, and G. Gimpl Specification of the cholesterol interaction with the oxytocin receptor using a chimeric receptor approach Eur. J. Pharmacol. 676 2012 12 19