The role of hydrophobic amino acids in the structure and function of the rhodopsin family of G protein-coupled receptors

Methods in Enzymology

Volumn 520, Issue , 2013, Pages 99-115

  Caltabiano, Gianluigi ^a   Gonzalez, Angel ^a   Cordomí, Arnau ^a   Campillo, Mercedes ^a   Pardo, Leonardo ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Activation; coupled receptors; G protein; Hydrophobic residues; Keywords; Oligomerization; Structure and function

Indexed keywords

AMINO ACID; ARGININE; BETA 2 ADRENERGIC RECEPTOR; G PROTEIN COUPLED RECEPTOR; OPSIN; RHODOPSIN; TRANSDUCIN; TYROSINE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DISEASE ASSOCIATION; EXTRACELLULAR SPACE; LIGAND BINDING; LIPID BILAYER; MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INDUCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RETINITIS PIGMENTOSA; SEQUENCE ANALYSIS;

EID: 84872525314     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/B978-0-12-391861-1.00005-8     Document Type: Chapter

References (91)

1. T.E. Angel, M.R. Chance, and K. Palczewski Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors Proceedings of the National Academy of Sciences of the United States of America 106 2009 8555 8560
2. T.E. Angel, S. Gupta, B. Jastrzebska, K. Palczewski, and M.R. Chance Structural waters define a functional channel mediating activation of the GPCR, rhodopsin Proceedings of the National Academy of Sciences of the United States of America 106 2009 14367 14372
3. R.A. Bakker, A. Jongejan, K. Sansuk, U. Hacksell, H. Timmerman, and M.R. Brann Constitutively active mutants of the histamine H1 receptor suggest a conserved hydrophobic asparagine-cage that constrains the activation of class A G protein-coupled receptors Molecular Pharmacology 73 2008 94 103 (Pubitemid 350294200)
4. J.A. Ballesteros, A.D. Jensen, G. Liapakis, S.G. Rasmussen, L. Shi, and U. Gether Activation of the beta 2-adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6 Journal of Biological Chemistry 276 2001 29171 29177
5. J. Ballesteros, S. Kitanovic, F. Guarnieri, P. Davies, B.J. Fromme, and K. Konvicka Functional microdomains in G-protein-coupled receptors: The conserved arginine cage motif in the gonadotropin-releasing hormone receptor Journal of Biological Chemistry 273 1998 10445 10453 (Pubitemid 28227654)
6. J.A. Ballesteros, and H. Weinstein Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors Methods in Neurosciences 25 1995 366 428
7. T.J. Baranski, P. Herzmark, O. Lichtarge, B.O. Gerber, J. Trueheart, and E.C. Meng C5a receptor activation. Genetic identification of critical residues in four transmembrane helices Journal of Biological Chemistry 274 1999 15757 15765
8. S. Blattermann, L. Peters, P.A. Ottersbach, A. Bock, V. Konya, and C.D. Weaver A biased ligand for OXE-R uncouples Galpha and Gbetagamma signaling within a heterotrimer Nature Chemical Biology 8 2012 631 638
9. A. Bock, N. Merten, R. Schrage, C. Dallanoce, J. Batz, and J. Klockner The allosteric vestibule of a seven transmembrane helical receptor controls G-protein coupling Nature Communications 3 2012 1044
10. M.P. Bokoch, Y. Zou, S.G. Rasmussen, C.W. Liu, R. Nygaard, and D.M. Rosenbaum Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor Nature 463 2010 108 112
11. L. Bosch-Presegue, L. Iarriccio, M. Aguila, D. Toledo, E. Ramon, and A. Cordomi Hydrophobic amino acids at the cytoplasmic ends of helices 3 and 6 of rhodopsin conjointly modulate transducin activation Archives of Biochemistry and Biophysics 506 2011 142 149
12. E.Y. Chien, W. Liu, Q. Zhao, V. Katritch, G.W. Han, and M.A. Hanson Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist Science 330 2010 1091 1095
13. H.W. Choe, Y.J. Kim, J.H. Park, T. Morizumi, E.F. Pai, and N. Krauss Crystal structure of metarhodopsin II Nature 471 2011 651 655
14. K.Y. Chung, S.G. Rasmussen, T. Liu, S. Li, B.T. DeVree, and P.S. Chae Conformational changes in the G protein Gs induced by the beta2 adrenergic receptor Nature 477 2011 611 615
15. B.R. Conklin, Z. Farfel, K.D. Lustig, D. Julius, and H.R. Bourne Substitution of three amino acids switches receptor specificity of Gq alpha to that of Gi alpha Nature 363 1993 274 276 (Pubitemid 23158533)
16. B.R. Conklin, P. Herzmark, S. Ishida, T.A. Voyno-Yasenetskaya, Y. Sun, and Z. Farfel Carboxyl-terminal mutations of Gq alpha and Gs alpha that alter the fidelity of receptor activation Molecular Pharmacology 50 1996 885 890 (Pubitemid 26347709)
17. P.W. Day, S.G. Rasmussen, C. Parnot, J.J. Fung, A. Masood, and T.S. Kobilka A monoclonal antibody for G protein-coupled receptor crystallography Nature Methods 4 2007 927 929 (Pubitemid 350042381)
18. T. de la Fuente, M. Martin-Fontecha, J. Sallander, B. Benhamu, M. Campillo, and R.A. Medina Benzimidazole derivatives as New Serotonin 5-HT(6) receptor antagonists. Molecular mechanisms of receptor inactivation Journal of Medicinal Chemistry 53 2010 1357 1369
19. X. Deupi, N. Dolker, M. Lopez-Rodriguez, M. Campillo, J. Ballesteros, and L. Pardo Structural models of class A G protein-coupled receptors as a tool for drug design: Insights on transmembrane bundle plasticity Current Topics in Medicinal Chemistry 7 2007 999 1006
20. X. Deupi, P. Edwards, A. Singhal, B. Nickle, D. Oprian, and G. Schertler Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II Proceedings of the National Academy of Sciences of the United States of America 109 2012 119 124
21. X. Deupi, M. Olivella, C. Govaerts, J.A. Ballesteros, M. Campillo, and L. Pardo Ser and Thr residues modulate the conformation of pro-kinked transmembrane alpha-helices Biophysical Journal 86 2004 105 115 (Pubitemid 38067440)
22. R.O. Dror, A.C. Pan, D.H. Arlow, D.W. Borhani, P. Maragakis, and Y. Shan Pathway and mechanism of drug binding to G-protein-coupled receptors Proceedings of the National Academy of Sciences of the United States of America 108 2011 13118 13123
23. O.P. Ernst, V. Gramse, M. Kolbe, K.P. Hofmann, and M. Heck Monomeric G protein-coupled receptor rhodopsin in solution activates its G protein transducin at the diffusion limit Proceedings of the National Academy of Sciences of the United States of America 104 2007 10859 10864 (Pubitemid 47175191)
24. B.A. Ersoy, L. Pardo, S. Zhang, D.A. Thompson, G. Millhauser, and C. Govaerts Mechanism of N-terminal modulation of activity at the melanocortin-4 receptor GPCR Nature Chemical Biology 8 2012 725 730
25. S. Ferre, R. Baler, M. Bouvier, M.G. Caron, L.A. Devi, and T. Durroux Building a new conceptual framework for receptor heteromers Nature Chemical Biology 5 2009 131 134
26. R. Fredriksson, and H.B. Schioth The repertoire of G-protein-coupled receptors in fully sequenced genomes Molecular Pharmacology 67 2005 1414 1425 (Pubitemid 40594140)
27. J.J. Fung, X. Deupi, L. Pardo, X.J. Yao, G.A. Velez-Ruiz, and B.T. Devree Ligand-regulated oligomerization of beta(2)-adrenoceptors in a model lipid bilayer The EMBO Journal 28 2009 2384 2392
28. P.D. Garcia, R. Onrust, S.M. Bell, T.P. Sakmar, and H.R. Bourne Transducin-alpha C-terminal mutations prevent activation by rhodopsin: A new assay using recombinant proteins expressed in cultured cells The EMBO Journal 14 1995 4460 4469
29. A. Gonzalez, A. Cordomi, G. Caltabiano, M. Campillo, and L. Pardo Impact of helix irregularities on sequence alignment and homology modelling of G protein-coupled receptors Chembiochem 13 2012 1393 1399
30. A. Gonzalez, T. Perez-Acle, L. Pardo, and X. Deupi Molecular basis of ligand dissociation in beta-adrenergic receptors PLoS One 6 2011 e23815
31. C. Govaerts, C. Blanpain, X. Deupi, S. Ballet, J.A. Ballesteros, and S.J. Wodak The TxP motif in the second transmembrane helix of CCR5: A structural determinant in chemokine-induced activation Journal of Biological Chemistry 276 2001 13217 13225
32. C. Govaerts, A. Lefort, S. Costagliola, S. Wodak, J.A. Ballesteros, and L. Pardo A conserved Asn in TM7 is a on/off switch in the activation of the TSH receptor Journal of Biological Chemistry 276 2001 22991 22999
33. W. Guo, L. Shi, M. Filizola, H. Weinstein, and J.A. Javitch Crosstalk in G protein-coupled receptors: Changes at the transmembrane homodimer interface determine activation Proceedings of the National Academy of Sciences of the United States of America 102 2005 17495 17500 (Pubitemid 41740894)
34. W. Guo, E. Urizar, M. Kralikova, J.C. Mobarec, L. Shi, and M. Filizola Dopamine D2 receptors form higher order oligomers at physiological expression levels The EMBO Journal 27 2008 2293 2304
35. K. Haga, A.C. Kruse, H. Asada, T. Yurugi-Kobayashi, M. Shiroishi, and C. Zhang Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist Nature 482 2012 547 551
36. M. Han, S.W. Lin, M. Minkova, S.O. Smith, and T.P. Sakmar Functional interaction of transmembrane helices 3 and 6 in rhodopsin. Replacement of phenylalanine 261 by alanine causes reversion of phenotype of a glycine 121 replacement mutant Journal of Biological Chemistry 271 1996 32337 32342 (Pubitemid 26422274)
37. Y. Han, I.S. Moreira, E. Urizar, H. Weinstein, and J.A. Javitch Allosteric communication between protomers of dopamine class A GPCR dimers modulates activation Nature Chemical Biology 5 2009 688 695
38. M.A. Hanson, C.B. Roth, E. Jo, M.T. Griffith, F.L. Scott, and G. Reinhart Crystal structure of a lipid G protein-coupled receptor Science 335 2012 851 855
39. P.W. Hildebrand, P. Scheerer, J.H. Park, H.W. Choe, R. Piechnick, and O.P. Ernst A ligand channel through the G protein coupled receptor opsin PLoS One 4 2009 e4382
40. S.-H. Hsu, and C.-W. Luo Molecular dissection of G protein preference using Gsalpha chimeras reveals novel ligand signaling of GPCRs American Journal of Physiology, Endocrinology and Metabolism 293 2007 E1021 1029
41. D.P. Hurst, A. Grossfield, D.L. Lynch, S. Feller, T.D. Romo, and K. Gawrisch A lipid pathway for ligand binding is necessary for a cannabinoid G protein-coupled receptor Journal of Biological Chemistry 285 2010 17954 17964
42. P. Imming, C. Sinning, and A. Meyer Drugs, their targets and the nature and number of drug targets Nature Reviews. Drug Discovery 5 2006 821 834 (Pubitemid 44480536)
43. V.P. Jaakola, M.T. Griffith, M.A. Hanson, V. Cherezov, E.Y. Chien, and J.R. Lane The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist Science 322 2008 1211 1217
44. 1 receptor activation Nature Chemical Biology 1 2005 98 103
45. V. Katritch, V. Cherezov, and R.C. Stevens Diversity and modularity of G protein-coupled receptor structures Trends in Pharmacological Sciences 33 2012 17 27
46. J.M. Klco, T.B. Lassere, and T.J. Baranski C5a receptor oligomerization. I. Disulfide trapping reveals oligomers and potential contact surfaces in a G protein-coupled receptor Journal of Biological Chemistry 278 2003 35345 35353 (Pubitemid 37102303)
47. L. Laue, W.Y. Chan, A.J. Hsueh, M. Kudo, S.Y. Hsu, and S.M. Wu Genetic heterogeneity of constitutively activating mutations of the human luteinizing hormone receptor in familial male-limited precocious puberty Proceedings of the National Academy of Sciences of the United States of America 92 1995 1906 1910
48. J. Li, P.C. Edwards, M. Burghammer, C. Villa, and G.F. Schertler Structure of bovine rhodopsin in a trigonal crystal form Journal of Molecular Biology 343 2004 1409 1438 (Pubitemid 39387834)
49. G. Liapakis, A. Cordomi, and L. Pardo The G-protein coupled receptor family: Actors with many faces Current Pharmaceutical Design 18 2012 175 185
50. S. Madabushi, A.K. Gross, A. Philippi, E.C. Meng, T.G. Wensel, and O. Lichtarge Evolutionary trace of G protein-coupled receptors reveals clusters of residues that determine global and class-specific functions Journal of Biological Chemistry 279 2004 8126 8132 (Pubitemid 38294703)
51. A. Manglik, A.C. Kruse, T.S. Kobilka, F.S. Thian, J.M. Mathiesen, and R.K. Sunahara Crystal structure of the micro-opioid receptor bound to a morphinan antagonist Nature 485 2012 321 326
52. E.L. Martin, S. Rens-Domiano, P.J. Schatz, and H.E. Hamm Potent peptide analogues of a G protein receptor-binding region obtained with a combinatorial library Journal of Biological Chemistry 271 1996 361 366 (Pubitemid 26026603)
53. D. Massotte, and B.L. Kieffer The second extracellular loop: A damper for G protein-coupled receptors? Nature Structural and Molecular Biology 12 2005 287 288 (Pubitemid 43093080)
54. T. Mirzadegan, G. Benko, S. Filipek, and K. Palczewski Sequence analyses of G-protein-coupled receptors: Similarities to rhodopsin Biochemistry 42 2003 2759 2767 (Pubitemid 36331518)
55. J.C. Mobarec, R. Sanchez, and M. Filizola Modern homology modeling of G-protein coupled receptors: Which structural template to use? Journal of Medicinal Chemistry 52 2009 5207 5216
56. M. Natochin, K.G. Muradov, R.L. McEntaffer, and N.O. Artemyev Rhodopsin recognition by mutant G(s)alpha containing C-terminal residues of transducin Journal of Biological Chemistry 275 2000 2669 2675 (Pubitemid 30082035)
57. G. Navarro, S. Ferre, A. Cordomi, E. Moreno, J. Mallol, and V. Casado Interactions between intracellular domains as key determinants of the quaternary structure and function of receptor heteromers Journal of Biological Chemistry 285 2010 27346 27359
58. R. Nygaard, T.M. Frimurer, B. Holst, M.M. Rosenkilde, and T.W. Schwartz Ligand binding and micro-switches in 7TM receptor structures Trends in Pharmacological Sciences 30 2009 249 259
59. W.M. Oldham, and H.E. Hamm Heterotrimeric G protein activation by G-protein-coupled receptors Nature Reviews. Molecular Cell Biology 9 2008 60 71
60. K. Palczewski, T. Kumasaka, T. Hori, C.A. Behnke, H. Motoshima, and B.A. Fox Crystal structure of rhodopsin: A G protein-coupled receptor Science 289 2000 739 745 (Pubitemid 30650186)
61. L. Pardo, X. Deupi, N. Dolker, M.L. Lopez-Rodriguez, and M. Campillo The role of internal water molecules in the structure and function of the rhodopsin family of G protein-coupled receptors Chembiochem 8 2007 19 24 (Pubitemid 46121564)
62. J.H. Park, P. Scheerer, K.P. Hofmann, H.W. Choe, and O.P. Ernst Crystal structure of the ligand-free G-protein-coupled receptor opsin Nature 454 2008 183 187 (Pubitemid 351969893)
63. M.C. Peeters, G.J. van Westen, Q. Li, and A.P. Ijzerman Importance of the extracellular loops in G protein-coupled receptors for ligand recognition and receptor activation Trends in Pharmacological Sciences 32 2011 35 42
64. L. Pellissier, J. Sallander, M. Campillo, F. Gaven, E. Queffeulou, and M. Pillot Conformational toggle switches implicated in basal constitutive and agonist-induced activated states of 5-HT4 receptors Molecular Pharmacology 75 2009 982 990
65. J.P. Pin, R. Neubig, M. Bouvier, L. Devi, M. Filizola, and J.A. Javitch International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers Pharmacological Reviews 59 2007 5 13 (Pubitemid 46335687)
66. C. Prioleau, I. Visiers, B.J. Ebersole, H. Weinstein, and S.C. Sealfon Conserved helix 7 tyrosine acts as a multistate conformational switch in the 5HT2C receptor. Identification of a novel "locked-on" phenotype and double revertant mutations Journal of Biological Chemistry 277 2002 36577 36584
67. S.G. Rasmussen, H.J. Choi, J.J. Fung, E. Pardon, P. Casarosa, and P.S. Chae Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor Nature 469 2011 175 180
68. S.G. Rasmussen, B.T. DeVree, Y. Zou, A.C. Kruse, K.Y. Chung, and T.S. Kobilka Crystal structure of the beta2 adrenergic receptor-Gs protein complex Nature 477 2011 549 555
69. U. Ringkananont, J. Van Durme, L. Montanelli, F. Ugrasbul, Y.M. Yu, and R.E. Weiss Repulsive separation of the cytoplasmic ends of transmembrane helices 3 and 6 is linked to receptor activation in a novel thyrotropin receptor mutant (M626I) Molecular Endocrinology 20 2006 893 903
70. S.L. Ritter, and R.A. Hall Fine-tuning of GPCR activity by receptor-interacting proteins Nature Reviews. Molecular Cell Biology 10 2009 819 830
71. D.M. Rosenbaum, V. Cherezov, M.A. Hanson, S.G. Rasmussen, F.S. Thian, and T.S. Kobilka GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function Science 318 2007 1266 1273 (Pubitemid 350172885)
72. D.M. Rosenbaum, S.G. Rasmussen, and B.K. Kobilka The structure and function of G-protein-coupled receptors Nature 459 2009 356 363
73. M.M. Rosenkilde, T. Benned-Jensen, T.M. Frimurer, and T.W. Schwartz The minor binding pocket: A major player in 7TM receptor activation Trends in Pharmacological Sciences 31 2010 567 574
74. K. Sansuk, X. Deupi, I.R. Torrecillas, A. Jongejan, S. Nijmeijer, and R.A. Bakker A structural insight into the reorientation of transmembrane domains 3 and 5 during family A G protein-coupled receptor activation Molecular Pharmacology 79 2011 262 269
75. A. Scheer, F. Fanelli, T. Costa, P.G. De Benedetti, and S. Cotecchia Constitutively active mutants of the alpha 1B-adrenergic receptor: Role of highly conserved polar amino acids in receptor activation The EMBO Journal 15 1996 3566 3578 (Pubitemid 26239769)
76. P. Scheerer, J.H. Park, P.W. Hildebrand, Y.J. Kim, N. Krauss, and H.W. Choe Crystal structure of opsin in its G-protein-interacting conformation Nature 455 2008 497 502
77. R. Schroder, N. Merten, J.M. Mathiesen, L. Martini, A. Kruljac-Letunic, and F. Krop The C-terminal tail of CRTH2 is a key molecular determinant that constrains Galphai and downstream signaling cascade activation Journal of Biological Chemistry 284 2009 1324 1336
78. M.J. Serrano-Vega, F. Magnani, Y. Shibata, and C.G. Tate Conformational thermostabilization of the beta1-adrenergic receptor in a detergent-resistant form Proceedings of the National Academy of Sciences of the United States of America 105 2008 877 882 (Pubitemid 351282049)
79. D.A. Shapiro, K. Kristiansen, D.M. Weiner, W.K. Kroeze, and B.L. Roth Evidence for a model of agonist-induced activation of 5-hydroxytryptamine 2A serotonin receptors that involves the disruption of a strong ionic interaction between helices 3 and 6 Journal of Biological Chemistry 277 2002 11441 11449 (Pubitemid 34952912)
80. L. Shi, G. Liapakis, R. Xu, F. Guarnieri, J.A. Ballesteros, and J.A. Javitch Beta2 adrenergic receptor activation. Modulation of the proline kink in transmembrane 6 by a rotamer toggle switch Journal of Biological Chemistry 277 2002 40989 40996 (Pubitemid 35215688)
81. T. Shimamura, M. Shiroishi, S. Weyand, H. Tsujimoto, G. Winter, and V. Katritch Structure of the human histamine H1 receptor complex with doxepin Nature 475 2011 65 70
82. M.I. Simon, M.P. Strathmann, and N. Gautam Diversity of G proteins in signal transduction Science 252 1991 802 808 (Pubitemid 121000516)
83. M.J. Smit, H.F. Vischer, R.A. Bakker, A. Jongejan, H. Timmerman, and L. Pardo Pharmacogenomic and structural analysis of constitutive G protein-coupled receptor activity Annual Review of Pharmacology and Toxicology 47 2007 53 87
84. J.Y. Springael, C. de Poorter, X. Deupi, J. Van Durme, L. Pardo, and M. Parmentier The activation mechanism of chemokine receptor CCR5 involves common structural changes but a different network of interhelical interactions relative to rhodopsin Cellular Signalling 19 2007 1446 1456 (Pubitemid 46818910)
85. J. Standfuss, P.C. Edwards, A. D'Antona, M. Fransen, G. Xie, and D.D. Oprian The structural basis of agonist-induced activation in constitutively active rhodopsin Nature 471 2011 656 660
86. Y. Sun, D. McGarrigle, and X.Y. Huang When a G protein-coupled receptor does not couple to a G protein Molecular BioSystems 3 2007 849 854 (Pubitemid 350115412)
87. E. Urizar, S. Claeysen, X. Deupi, C. Govaerts, S. Costagliola, and G. Vassart An activation switch in the rhodopsin family of G protein-coupled receptors: The thyrotropin receptor Journal of Biological Chemistry 280 2005 17135 17141 (Pubitemid 41389178)
88. B. Vroling, M. Sanders, C. Baakman, A. Borrmann, S. Verhoeven, and J. Klomp GPCRDB: Information system for G protein-coupled receptors Nucleic Acids Research 39 2011 D309 319
89. T. Warne, M.J. Serrano-Vega, J.G. Baker, R. Moukhametzianov, P.C. Edwards, and R. Henderson Structure of a beta(1)-adrenergic G-protein-coupled receptor Nature 454 2008 486 491
90. M.R. Whorton, M.P. Bokoch, S.G. Rasmussen, B. Huang, R.N. Zare, and B. Kobilka A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein Proceedings of the National Academy of Sciences of the United States of America 104 2007 7682 7687 (Pubitemid 47185966)
91. B. Wu, E.Y. Chien, C.D. Mol, G. Fenalti, W. Liu, and V. Katritch Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists Science 330 2010 1066 1071