Sequence, structure and ligand binding evolution of rhodopsin-Like G protein-coupled receptors: A crystal structure-based phylogenetic analysis

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Wolf, Steffen ^a,b   Grünewald, Stefan ^a  

^a Chinese Academy of Sciences   (China)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOGENIC AMINE; G PROTEIN COUPLED RECEPTOR; MUSCARINIC RECEPTOR; OPIATE RECEPTOR; RHODOPSIN; LIGAND; OPSIN; SODIUM;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CENTRAL NERVOUS SYSTEM; CRYSTAL STRUCTURE; HUMAN; LIGAND BINDING; MOLECULAR EVOLUTION; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; HUMANS; LIGANDS; OPSINS; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, OPIOID; RHODOPSIN; SODIUM;

EID: 84928226628     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123533     Document Type: Article

References (95)

1. Pierce KL, Premont RT, Lefkowitz RJ (2002) Signalling: Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3: 639-650. PMID: 12209124
2. Lundstrom K (2006) Latest development in drug discovery on G protein-coupled receptors. Curr Protein Pept Sc 7: 465-470. PMID: 17073697
3. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, et al. (2000) Crystal structure of rhodopsin: AG protein-coupled receptor. Science 289: 739-745. PMID: 10926528
4. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SGF, Thian FS, et al. (2007) High-Resolution Crystal Structure of an Engineered Human β2-Adrenergic G Protein Coupled Receptor. Science 318: 1258-1265. PMID: 17962520
5. Rasmussen SGF, Choi H-J, Rosenbaum DM, Kobilka TS, Thian FS, et al. (2007) Crystal structure of the human β2 adrenergic G-protein-coupled receptor. Nature 450: 383-387. PMID: 17952055
6. Warne T, Serrano-Vega MJ, Baker JG, Moukhametzianov R, Edwards PC, et al. (2008) Structure of a β1-adrenergic G-protein-coupled receptor. Nature 454: 486-491. doi: 10.1038/nature07101 PMID: 18594507
7. Jaakola VP, Griffith MT, Hanson MA, Cherezov V, Chien EYT, et al. (2008) The 2.6 Angstrom Crystal Structure of a Human A2A Adenosine Receptor Bound to an Antagonist. Science 322: 1211-1217. doi: 10.1126/science.1164772 PMID: 18832607
8. Chien EYT, Liu W, Zhao Q, Katritch V, Won Han G, et al. (2010) Structure of the Human Dopamine D3 Receptor in Complex with a D2/D3 Selective Antagonist. Science 330: 1091-1095. doi: 10.1126/ science.1197410 PMID: 21097933
9. Wu B, Chien EYT, Mol CD, Fenalti G, Liu W, et al. (2010) Structures of the CXCR4 Chemokine GPCR with Small-Molecule and Cyclic Peptide Antagonists. Science 330: 1066-1071. doi: 10.1126/science. 1194396 PMID: 20929726
10. Shimamura T, Shiroishi M, Weyand S, Tsujimoto H, Winter G, et al. (2011) Structure of the human histamine H1 receptor complex with doxepin. Nature 475: 65-70. doi: 10.1038/nature10236 PMID: 21697825
11. Hanson MA, Roth CB, Jo E, Griffith MT, Scott FL, et al. (2012) Crystal Structure of a Lipid G Protein- Coupled Receptor. Science 335: 851-855. doi: 10.1126/science.1215904 PMID: 22344443
12. Haga K, Kruse AC, Asada H, Yurugi-Kobayashi T, Shiroishi M, et al. (2012) Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 482: 547-551. doi: 10.1038/ nature10753 PMID: 22278061
13. Kruse AC, Hu J, Pan AC, Arlow DH, Rosenbaum DM, et al. (2012) Structure and dynamics of the M3 muscarinic acetylcholine receptor. Nature 482: 552-556. doi: 10.1038/nature10867 PMID: 22358844
14. Manglik A, Kruse AC, Kobilka TS, Thian FS, Mathiesen JM, et al. (2012) Crystal structure of the μ-opioid receptor bound to a morphinan antagonist. Nature 485: 321-326. doi: 10.1038/nature10954 PMID: 22437502
15. Wu H, Wacker D, Mileni M, Katritch V, Han GW, et al. (2012) Structure of the human κ-opioid receptor in complex with JDTic. Nature 485: 327-332. doi: 10.1038/nature10939 PMID: 22437504
16. Thompson AA, Liu W, Chun E, Katritch V, Wu H, et al. (2012) Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature 485: 395-399. doi: 10.1038/nature11085 PMID: 22596163
17. Granier S, Manglik A, Kruse AC, Kobilka TS, Thian FS, et al. (2012) Structure of the δ-opioid receptor bound to naltrindole. Nature 485: 400-404. doi: 10.1038/nature11111 PMID: 22596164
18. White JF, Noinaj N, Shibata Y, Love J, Kloss B, et al. (2012) Structure of the agonist-bound neurotensin receptor. Nature 490: 508-513. doi: 10.1038/nature11558 PMID: 23051748
19. Zhang C, Srinivasan Y, Arlow DH, Fung JJ, Palmer D, et al. (2012) High-resolution crystal structure of human protease-activated receptor 1. Science 492: 387-392. doi: 10.1038/nature11701 PMID: 23222541
20. Liu W, Chun E, Thompson AA, Chubukov P, Xu F, et al. (2012) Structural Basis for Allosteric Regulation of GPCRs by Sodium Ions. Science 337: 232-236. doi: 10.1126/science.1219218 PMID: 22798613
21. Wang C, Jiang Y, Ma J, Wu H, Wacker D, et al. (2013) Structural Basis for Molecular Recognition at Serotonin Receptors. Science 340: 610-614. doi: 10.1126/science.1232807 PMID: 23519210
22. Wacker D, Wang C, Katritch V, Han GW, Huang XP, et al. (2013) Structural Features for Functional Selectivity at Serotonin Receptors. Science 340: 615-619. doi: 10.1126/science.1232808 PMID: 23519215
23. Siu FY, He M, de Graaf C, Han GW, Yang D, et al. (2013) Structure of the human glucagon class B G-protein-coupled receptor. Nature 499: 444-449. doi: 10.1038/nature12393 PMID: 23863937
24. Wang C, Wu H, Katritch V, Han GW, Huang X-P, et al. (2013) Structure of the human smoothened receptor bound to an antitumour agent. Nature 497: 338-343. doi: 10.1038/nature12167 PMID: 23636324
25. Hollenstein K, Kean J, Bortolato A, Cheng RKY, Doré AS, et al. (2013) Structure of class B GPCR corti-cotropin- releasing factor receptor 1. Nature 499: 438-443. doi: 10.1038/nature12357 PMID: 23863939
26. Tan Q, Zhu Y, Li J, Chen Z, Han GW, et al. (2013) Structure of the CCR5 Chemokine Receptor-HIV Entry Inhibitor Maraviroc Complex. Science 341: 1387-1390. doi: 10.1126/science.1241475 PMID: 24030490
27. Zhang K, Zhang J, Gao Z-G, Zhang D, Zhu L, et al. (2014) Structure of the human P2Y12 receptor in complex with an antithrombotic drug. Nature 509: 115-118. doi: 10.1038/nature13083 PMID: 24670650
28. Wu H, Wang C, Gregory KJ, Han GW, Cho HP, et al. (2014) Structure of a Class C GPCR Metabotropic Glutamate Receptor 1 Bound to an Allosteric Modulator. Science 344: 58-64. doi: 10.1126/science. 1249489 PMID: 24603153
29. Kolakowski LF Jr (1994) GCRDb: a G-protein-coupled receptor database. Receptor Channel 2: 1-7.
30. Fredriksson R (2003) The gpcr in human genome form five families. Mol Pharmacol 63: 1256-1272. PMID: 12761335
31. Allaby RG, Woodwark M (2007) Phylogenomic Analysis Reveals Extensive Phylogenetic Mosaicism in the Human GPCR Superfamily. Evol Bioinform Online 3: 357-370. PMID: 19468313
32. Pele J, Abdi H, Moreau M, Thybert D, Chabbert M (2011) Multidimensional scaling reveals the main evolutionary pathways of class A G-protein-coupled receptors. Plos One 6: e19094. doi: 10.1371/ journal.pone.0019094 PMID: 21544207
33. Chung S, Funakoshi T, Civelli O (2009) Orphan GPCR research. Brit J Pharmacol 153: S339-S346.
34. Gutiérrez-de-Terán H, Massink A, Rodríguez D, Liu W, Han GW, et al. (2013) The Role of a Sodium Ion Binding Site in the Allosteric Modulation of the A2A Adenosine G Protein-Coupled Receptor. Structure 21: 2175-2185. doi: 10.1016/j.str.2013.09.020 PMID: 24210756
35. Fenalti G, Giguere PM, Katritch V, Huang X- P, Thompson AA, et al. (2014) Molecular control of δ-opioid receptor signalling. Nature 506: 191-196. doi: 10.1038/nature12944 PMID: 24413399
36. Okada T, Sugihara M, Bondar A-N, Elstner M, Entel P, et al. (2004) The Retinal Conformation and its Environment in Rhodopsin in Light of a New 2.2 Å Crystal Structure. J Mol Biol 342: 571-583. PMID: 15327956
37. Rosenbaum DM, Cherezov V, Hanson MA, Rasmussen SGF, Thian FS, et al. (2007) GPCR Engineering Yields High-Resolution Structural Insights into 2-Adrenergic Receptor Function. Science 318: 1266-1273. PMID: 17962519
38. Schrödinger, LLC (2010) The PyMOL Molecular Graphics System, Version 1.3r1.
39. Ballesteros J, Weinstein H (1995) Integrated methods for the construction of three dimensional models and computational probing of structure function relations in G protein-coupled receptors. In: Sealfon S, Conn P, editors. San Diego, CA: Methods Neurosci, Vol. 25. pp. 366-428.
40. Goncalves JA, South K, Ahuja S, Zaitseva E, Opefi CA, et al. (2010) Highly conserved tyrosine stabilizes the active state of rhodopsin. Proc Natl Acad Sci USA 107: 19861-19866. doi: 10.1073/pnas. 1009405107 PMID: 21041664
41. Elgeti M, Kazmin R, Heck M, Morizumi T, Ritter E, et al. (2011) Conserved Tyr223 5.58Plays Different Roles in the Activation and G-Protein Interaction of Rhodopsin. J Am Chem Soc 133: 7159-7165. doi: 10.1021/ja200545n PMID: 21506561
42. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321. doi: 10.1093/sysbio/syq010 PMID: 20525638
43. Kuhner MK, Felsenstein J (1994) Simulation Comparison of Phylogeny Algorithms Under Equal and Unequal Evolutionary Rates. Mol Biol Evol 11: 459-468. PMID: 8015439
44. Huson DH, Scornavacca C (2012) Dendroscope 3: An Interactive Tool for Rooted Phylogenetic Trees and Networks. Syst Biol 61: 1061-1067. d doi: 10.1093/sysbio/sys062 PMID: 22780991
45. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267. PMID: 16221896
46. Jones DT, Taylor WR, Thornton JM (1992) The Rapid Generation of Mutation Data Matrices From Protein Sequences. Comput Appl Biosci 8: 275-282. PMID: 1633570
47. Lichtarge O, Bourne HR, Cohen FE (1996) An evolutionary trace method defines binding surfaces common to protein families. J Mol Biol 257: 342-358. PMID: 8609628
48. Mihalek I, Reš I, Lichtarge O (2004) A Family of Evolution-Entropy Hybrid Methods for Ranking Protein Residues by Importance. J Mol Biol 336: 1265-1282. PMID: 15037084
49. Henikoff S, Henikoff JG (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89: 10915-10919. PMID: 1438297
50. Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195-202. PMID: 10493868
51. Bryson K, McGuffin LJ, Marsden RL, Ward JJ, Sodhi JS, et al. (2005) Protein structure prediction servers at University College London. Nucleic Acids Res 33: W36-W38. PMID: 15980489
52. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. PMID: 9254694
53. The UniProt Consortium (2013) Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 42: D191-D198. doi: 10.1093/nar/gkt1140 PMID: 24253303
54. Edgar R (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797. PMID: 15034147
55. Jafurulla M, Chattopadhyay A (2012) Membrane Lipids in the Function of Serotonin and Adrenergic Receptors. CMC 20: 47-55.
56. Clamp M, Cuff J, Searle SM, Barton GJ (2004) The Jalview Java alignment editor. Bioinformatics 20: 426-427. PMID: 14960472
57. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191. doi: 10.1093/ bioinformatics/btp033 PMID: 19151095
58. Bryant D (2003) Neighbor-Net: An Agglomerative Method for the Construction of Phylogenetic Networks. Mol Biol Evol 21: 255-265. PMID: 14660700
59. Madabushi S, Gross AK, Philippi A, Meng EC, Wensel TG, et al. (2004) Evolutionary Trace of G Pro-tein- coupled Receptors Reveals Clusters of Residues That Determine Global and Class-specific Functions. J Biol Chem 279: 8126-8132. PMID: 14660595
60. Rodriguez GJ, Yao R, Lichtarge O, Wensel TG (2010) Evolution-guided discovery and recoding of allosteric pathway specificity determinants in psychoactive bioamine receptors. Proc Natl Acad Sci USA 107: 7787-7792. doi: 10.1073/pnas.0914877107 PMID: 20385837
61. Mombaerts P (2001) The human repertoire of odorant receptor genes and pseudogenes. Annu Rev Genomics Hum Genet 2: 493-510. PMID: 11701659
62. Niimura Y (2009) On the origin and evolution of vertebrate olfactory receptor genes: comparative genome analysis among 23 chordate species. Genome Biol Evol 1: 34-44. doi: 10.1093/gbe/evp003 PMID: 20333175
63. Krishnan A, Almén MS, Fredriksson R, Schioth HB (2012) The Origin of GPCRs: Identification of Mammalian like Rhodopsin, Adhesion, Glutamate and Frizzled GPCRs in Fungi. Plos One 7: e29817. doi: 10.1371/journal.pone.0029817 PMID: 22238661
64. Gelis L, Wolf S, Hatt H, Neuhaus EM, Gerwert K (2012) Prediction of a ligand-binding niche within a human olfactory receptor by combining site-directed mutagenesis with dynamic homology modeling. Angew Chem Int Ed Engl 51: 1274-1278. doi: 10.1002/anie.201103980 PMID: 22144177
65. Park JH, Morizumi T, Li Y, Hong JE, Pai EF, et al. (2013) Opsin, a structural model for olfactory receptors?Angew Chem Int Ed Engl 52: 11021-11024. doi: 10.1002/anie.201302374 PMID: 24038729
66. Feigin ME, Xue B, Hammell MC, Muthuswamy SK (2014) G-protein-coupled receptor GPR161 is overexpressed in breast cancer and is a promoter of cell proliferation and invasion. Proc Natl Acad Sci USA 111: 4191-4196. doi: 10.1073/pnas.1320239111 PMID: 24599592
67. Rasmussen SGF, Choi H-J, Fung JJ, Pardon E, Casarosa P, et al. (2010) Structure of a nanobody-stabilized active state of the β2 adrenoceptor. Nature 469: 175-180.
68. Rosenbaum DM, Zhang C, Lyons JA, Holl R, Aragao D, et al. (2010) Structure and function of an irreversible agonist-β2 adrenoceptor complex. Nature 469: 236-240.
69. Rasmussen SGF, DeVree BT, Zou Y, Kruse AC, Chung KY, et al. (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477: 549-555. doi: 10.1038/nature10361 PMID: 21772288
70. Lebon G, Warne T, Edwards PC, Bennett K, Langmead CJ, et al. (2011) Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 474: 521-525. doi: 10. 1038/nature10136 PMID: 21593763
71. Warne T, Moukhametzianov R, Baker JG, Nehmé R, Edwards PC, et al. (2010) The structural basis for agonist and partial agonist action on a β1-adrenergic receptor. Nature 469: 241-244.
72. Deupi X, Edwards P, Singhal A, Nickle B, Oprian D, et al. (2012) Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II. Proc Natl Acad Sci USA 109: 119-124. doi: 10. 1073/pnas.1114089108 PMID: 22198838
73. Vogel R (2001) Conformations of the Active and Inactive States of Opsin. J Biol Chem 276: 38487-38493. PMID: 11502747
74. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauß N, et al. (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455: 497-502. doi: 10.1038/nature07330 PMID: 18818650
75. Choe H-W, Kim YJ, Park JH, Morizumi T, Pai EF, et al. (2011) Crystal structure of metarhodopsin II. Nature 471: 651-655. doi: 10.1038/nature09789 PMID: 21389988
76. Park JH, Scheerer P, Hofmann KP, Choe HW, Ernst OP (2008) Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454: 183-187. doi: 10.1038/nature07063 PMID: 18563085
77. Ahuja S, Hornak V, Yan ECY, Syrett N, Goncalves JA, et al. (2009) Helix movement is coupled to displacement of the second extracellular loop in rhodopsin activation. Nat Struct Mol Biol 16: 168-175. doi: 10.1038/nsmb.1549 PMID: 19182802
78. Feuda R, Hamilton SC, McInerney JO, Pisani D (2012) Metazoan opsin evolution reveals a simple route to animal vision. Proc Natl Acad Sci USA 109: 18868-18872. doi: 10.1073/pnas.1204609109 PMID: 23112152
79. Gehring WJ (2012) The evolution of vision. WIREs Dev Biol 3: 1-40. 80. Firestein S (2001) How the olfactory system makes sense of scents. Nature 413: 211-218. PMID: 11557990
80. Bianchet MA, Bains G, Pelosi P, Pevsner J, Snyder SH, et al. (1996) The three-dimensional structure of bovine odorant binding protein and its mechanism of odor recognition. Nat Struct Mol Biol 3: 934-939.
81. Laughlin JD, Ha TS, Jones DNM, Smith DP (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133: 1255-1265. doi: 10.1016/j. cell.2008.04.046 PMID: 18585358
82. Ernst OP, Lodowski DT, Elstner M, Hegemann P, Brown LS, et al. (2014) Microbial and Animal Rhodopsins: Structures, Functions, and Molecular Mechanisms. Chem Rev 114: 126-163. doi: 10.1021/ cr4003769 PMID: 24364740
83. Schuenke M, Schulte E, Schumacher U (2010) THIEME Atlas of Anatomy: Head and Neuroanatomy. Thieme. 414 p.
84. Hankins M, Peirson S, Foster R (2008) Melanopsin: an exciting photopigment. Trends Neurosci 31: 27-36. PMID: 18054803
85. Murakami M, Kouyama T (2008) Crystal structure of squid rhodopsin. Nature 453: 363-367. doi: 10. 1038/nature06925 PMID: 18480818
86. Surgand J- S, Rodrigo J, Kellenberger E, Rognan D (2005) A chemogenomic analysis of the transmembrane binding cavity of human G-protein-coupled receptors. Proteins 62: 509-538.
87. Katritch V, Fenalti G, Abola EE, Roth BL, Cherezov V, et al. (2014) Allosteric sodium in class A GPCR signaling. Trends Biochem Sci 39: 233-244. doi: 10.1016/j.tibs.2014.03.002 PMID: 24767681
88. Miller-Gallacher JL, Nehmé R, Warne T, Edwards PC, Schertler GFX, et al. (2014) The 2.1 Å Resolution Structure of Cyanopindolol-Bound β1-Adrenoceptor Identifies an Intramembrane Na+ Ion that Stabilises the Ligand-Free Receptor. Plos One 9: e92727. doi: 10.1371/journal.pone.0092727 PMID: 24663151
89. Gerwert K, Freier E, Wolf S (2014) The role of protein-bound water molecules in microbial rhodopsins. BBA-Bioenergetics 1837: 606-613.
90. Filipek S, Palczewski K, Yuan S, Vogel H (2014) Activation of G-protein-coupled receptors correlates with the formation of a continuous internal water pathway. Nat Commun 5: 1-10.
91. Yuan S, Hu Z, Filipek S, Vogel H (2015) W2466. 48 Opens a Gate for a Continuous Intrinsic Water Pathway during Activation of the Adenosine A2A Receptor. Angew Chem Int Ed Engl. 127: 566-569.
92. Angel TE, Chance MR, Palczewski K (2009) Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors. Proc Natl Acad Sci USA 106: 8555-8560. doi: 10.1073/pnas.0903545106 PMID: 19433801
93. Kane B, Svensson B, Ferguson D (2006) Molecular recognition of opioid receptor ligands. AAPS J 8: E126-E137. PMID: 16584119
94. Stewart A, Wong K, Cachat J, Gaikwad S, Kyzar E, et al. (2011) Zebrafish models to study drug abuserelated phenotypes. Rev Neuroscience 22: 95. doi: 10.1515/RNS.2011.011 PMID: 21615264
95. Molinari P, Vezzi V, Sbraccia M, Gro C, Riitano D, et al. (2010) Morphine-like Opiates Selectively Antagonize Receptor-Arrestin Interactions. J Biol Chem 285: 12522-12535. doi: 10.1074/jbc.M109. 059410 PMID: 20189994