Phe369(7.38) at human 5-HT 7 receptors confers interspecies selectivity to antagonists and partial agonists

British Journal of Pharmacology

Volumn 159, Issue 5, 2010, Pages 1069-1081

  Varin, Thibault ^a   Gutiérrez De Terán, Hugo ^b   Castro, Marián ^c   Brea, José ^c   Fabis, Frederic ^a   Dauphin, François ^a,f   Åqvist, Johan ^d   Lepailleur, Alban ^a   Perez, Pilar ^e   Burgueño, Javier ^e   Vela, José Miguel ^e   Loza, Maria Isabel ^c   Rodrigo, Jordi ^a  

^a CENTRE D ETUDES ET DE RECHERCHE SUR LE MÉDICAMENT DE NORMANDIE   (France)

^b Instituto de Salud Carlos III   (Spain)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^d UPPSALA UNIVERSITY   (Sweden)

^e Laboratorios Esteve   (Spain)

^f UNIVERSITÉ DE CAEN   (France)

Author keywords

Binding affinity; GPCRs; Interspecies selectivity; Molecular modelling; Site directed mutagenesis

Indexed keywords

3 [2 [2 (4 METHYL 1 PIPERIDINYL)ETHYL] 1 PYRROLIDINESULFONYL]PHENOL; CYCLIC AMP; MR 22423; MR 22433; MR 23284; MR 25020; MR 25040; MR 25052; MR 25053; SB 656104A; SEROTONIN 7 AGONIST; SEROTONIN 7 ANTAGONIST; SEROTONIN 7 RECEPTOR; SEROTONIN AGONIST; SEROTONIN ANTAGONIST; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL CULTURE; DRUG BINDING; DRUG STRUCTURE; HUMAN; LIGAND BINDING; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; SIMULATION; SITE DIRECTED MUTAGENESIS;

ANIMALS; BINDING SITES; BINDING, COMPETITIVE; CELL LINE; COMPUTER SIMULATION; CYCLIC AMP; HUMANS; LIGANDS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SEROTONIN; SEROTONIN AGONISTS; SEROTONIN ANTAGONISTS; SPECIES SPECIFICITY;

EID: 77949385516     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2009.00481.x     Document Type: Article

References (74)

1. Adham N, Zgombick JM, Bard J, Branchek TA (1998). Functional characterization of the recombinant human 5-hydroxytryptamine7(a) receptor isoform coupled to adenylate cyclase stimulation. J Pharmacol Exp Ther 287: 508-514.
2. Alexander SPH, Mathie A, Peters JA (2008). Guide to receptors and channels (GRAC), 3rd edn. Br J Pharmacol 153 (Suppl. 2): S1-S209.
3. Ander M, Luzhkov VB, Aqvist J (2008). Ligand binding to the voltage-gated Kv1.5 potassium channel in the open state-docking and computer simulations of a homology model. Biophys J 94: 820-831.
4. Åqvist J, Medina C, Samuelsson JE (1994). A new method for predicting binding affinity in computer-aided drug design. Protein Eng 7: 385-391.
5. Attwood TK (2001). A compendium of specific motifs for diagnosing GPCR subtypes. Trends Pharmacol Sci 22: 162-165.
6. Baldwin JM, Schertler GF, Unger VM (1997). An alpha-carbon template for the transmembrane helices in the rhodopsin family of G-protein-coupled receptors. J Mol Biol 272: 144-164.
7. Ballesteros JA, Jensen AD, Liapakis G, Rasmussen SG, Shi L, Gether U et al. (2001). Activation of the beta 2-adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6. J Biol Chem 276: 29171-29177.
8. Ballesteros JA, Weinstein H (1994). Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors. In: Methods in Neurosciences. Academic Press: San Diego, pp. 366-428.
9. Barnes NM, Sharp T (1999). A review of central 5-HT receptors and their function. Neuropharmacology 38: 1083-1152.
10. Bissantz C (2003). Conformational changes of G protein-coupled receptors during their activation by agonist binding. J Recept Signal Transduct Res 23: 123-153.
11. Bissantz C, Logean A, Rognan D (2004). High-throughput modeling of human G-protein coupled receptors: amino acid sequence alignment, three-dimensional model building, and receptor library screening. J Chem Inf Comput Sci 44: 1162-1176.
12. Boess FG, Monsma FJ, Jr., Meyer V, Zwingelstein C, Sleight AJ (1997). Interaction of tryptamine and ergoline compounds with threonine 196 in the ligand binding site of the 5-hydroxytryptamine6 receptor. Mol Pharmacol 52: 515-523.
13. Bonaventure P, Kelly L, Aluisio L, Shelton J, Lord B, Galici R et al. (2007). Selective blockade of 5-hydroxytryptamine (5-HT)7 receptors enhances 5-HT transmission, antidepressant-like behavior, and rapid eye movement sleep suppression induced by citalopram in rodents. J Pharmacol Exp Ther 321: 690-698.
14. Braden MR, Nichols DE (2007). Assessment of the roles of serines 5.43(239) and 5.46(242) for binding and potency of agonist ligands at the human serotonin 5-HT2A receptor. Mol Pharmacol 72: 1200-1209.
15. Brea J, Rodrigo J, Carrieri A, Sanz F, Cadavid MI, Enguix MJ et al. (2002). New serotonin 5-HT(2A), 5-HT(2B), and 5-HT(2C) receptor antagonists: synthesis, pharmacology, 3D-QSAR, and molecular modeling of (aminoalkyl)benzo and heterocycloalkanones. J Med Chem 45: 54-71.
16. Brenchat A, Romero L, Garcia M, Pujol M, Burgueno J, Torrens A et al. (2009). 5-HT7 receptor activation inhibits mechanical hypersensitivity secondary to capsaicin sensitization in mice. Pain 141: 239-247.
17. Bruno IJ, Cole JC, Lommerse JP, Rowland RS, Taylor R, Verdonk ML (1997). IsoStar: a library of information about nonbonded interactions. J Comput Aided Mol Des 11: 525-537.
18. Case DA, Darden TA, Cheatham TE, III, Simmerling CL, Wang J, Duke RE et al. (2004). AMBER 8.0. San Francisco: University of California.
19. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS et al. (2007). High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318: 1258-1265.
20. Choudhary MS, Sachs N, Uluer A, Glennon RA,Westkaemper RB, Roth BL (1995). Differential ergoline and ergopeptine binding to 5-hydroxytryptamine2A receptors: ergolines require an aromatic residue at position 340 for high affinity binding. Mol Pharmacol 47: 450-457.
21. Cullen BR (1987). Use of eukaryotic expression technology in the functional analysis of cloned genes. Methods Enzymol 152: 684-704.
22. Czeh B, Michaelis T, Watanabe T, Frahm J, de Biurrun G, van Kampen M et al. (2001). Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA 98: 12796-12801.
23. de Graaf C, Rognan D (2008). Selective structure-based virtual screening for full and partial agonists of the beta2 adrenergic receptor. J Med Chem 51: 6620.
24. Deng Q, Clemas JA, Chrebet G, Fischer P, Hale JJ, Li Z et al. (2007). Identification of Leu276 of the S1P1 receptor and Phe263 of the S1P3 receptor in interaction with receptor specific agonists by molecular modeling, site-directed mutagenesis, and affinity studies. Mol Pharmacol 71: 724-735.
25. Dezi C, Brea J, Alvarado M, Ravina E, Masaguer CF, Loza MI et al. (2007). Multistructure 3D-QSAR studies on a series of conformationally constrained butyrophenones docked into a new homology model of the 5-HT2A receptor. J Med Chem 50: 3242-3255.
26. Guscott M, Bristow LJ, Hadingham K, Rosahl TW, Beer MS, Stanton JA et al. (2005). Genetic knockout and pharmacological blockade studies of the 5-HT7 receptor suggest therapeutic potential in depression. Neuropharmacology 48: 492-502.
27. Gutiérrez-de-Terán H, Correia C, Rodríguez D, Carvalho MA, Brea J, Cadavid MI et al. (2009). Identification of Novel Scaffolds from an Original Chemical Library as Potential Antipsychotics. QSAR Comb Sci doi: 10/1002/qsar200860198.
28. Gutiérrez-de-Terán H, Nervall M, Ersmark K, Dunn BM, Hallberg A, Åqvist J (2006). Inhibitor binding to the plasmepsin IV aspartic protease from plasmodium falciparum. Biochemistry 45: 10529-10541.
29. Hedlund PB, Huitron-Resendiz S, Henriksen SJ, Sutcliffe JG (2005). 5-HT7 receptor inhibition and inactivation induce antidepressant-like behavior and sleep pattern. Biol Psychiatry 58: 831-837.
30. Hedlund PB, Sutcliffe JG (2004). Functional, molecular and pharmacological advances in 5-HT7 receptor research. Trends Pharmacol Sci 25: 481-486.
31. Henikoff S, Henikoff JG (1992). Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89: 10915-10919.
32. Horn F, Bettler E, Oliveira L, Campagne F, Cohen FE, Vriend G (2003). GPCRDB information system for G protein-coupled receptors. Nucleic Acids Res 31: 294-297.
33. Hoyer D, Clarke DE, Fozard JR, Hartig PR, Martin GR, Mylecharane EJ et al. (1994). International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (Serotonin). Pharmacol Rev 46: 157-203.
34. Hoyer D, Hannon JP, Martin GR (2002). Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71: 533-554.
35. Huang XP, Nagy PI, Williams FE, Peseckis SM, Messer WS, Jr. (1999). Roles of threonine 192 and asparagine 382 in agonist and antagonist interactions with M1 muscarinic receptors. Br J Pharmacol 126: 735-745.
36. Jones G, Willett P, Glen RC, Leach AR, Taylor R (1997). Development and validation of a genetic algorithm for flexible docking. J Mol Biol 267: 727-748.
37. Jorgensen WL, Maxwell DS, TiradoRives J (1996). Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 118: 11225-11236.
38. King G, Warshel A (1989). A surface constrained all-atom solvent model for effective simulations of polar solutions. J Chem Phys 91: 3647-3661.
39. Kristiansen K (2004). Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacol Ther 103: 21-80.
40. Kristiansen K, Kroeze WK, Willins DL, Gelber EI, Savage JE, Glennon RA et al. (2000). A highly conserved aspartic acid (Asp-155) anchors the terminal amine moiety of tryptamines and is involved in membrane targeting of the 5-HT(2A) serotonin receptor but does not participate in activation via a 'salt-bridge disruption' mechanism. J Pharmacol Exp Ther 293: 735-746.
41. Laurila JM, Xhaard H, Ruuskanen JO, Rantanen MJ, Karlsson HK, Johnson MS et al. (2007). The second extracellular loop of alpha2A-adrenoceptors contributes to the binding of yohimbine analogues. Br J Pharmacol 151: 1293-1304.
42. Lepailleur A, Bureau R, Lemaîtra S, Dauphin F, Lancelot JC, Contesse V et al. (2004). Molecular design based on 3D pharmacophores. Applications to 5-HT7 receptors. J Chem Inf Comput Sci 44: 1148-1152. [Correction added after online publication 25 February 2010: the above reference was added to the list.]
43. Lepailleur A, Bureau R, Paillet-Loilier M, Fabis F, Saettel N, Lemaitre S et al. (2005). Molecular modeling studies focused on 5-HT7 versus 5-HT1A selectivity. Discovery of novel phenylpyrrole derivatives with high affinity for 5-HT7 receptors. J Chem Inf Model 45: 1075-1081.
44. Li JH, Choe H, Wang AF, Maiti K, Wang C, Salam A et al. (2005). Extracellular loop 3 (EL3) and EL3-proximal transmembrane helix 7 of the mammalian type I and type II gonadotropin-releasing hormone (GnRH) receptors determine differential ligand selectivity to GnRH-I and GnRH-II. Mol Pharmacol 67: 1099-1110.
45. Lopez-Rodriguez ML, Porras E, Benhamu B, Ramos JA, Morcillo MJ, Lavandera JL (2000). First pharmacophoric hypothesis for 5-HT7 antagonism. Bioorg Med Chem Lett 10: 1097-1100.
46. Lopez-Rodriguez ML, Porras E, Morcillo MJ, Benhamu B, Soto LJ, Lavandera JL et al. (2003). Optimization of the pharmacophore model for 5-HT7R antagonism. Design and synthesis of new naphtholactam and naphthosultam derivatives. J Med Chem 46: 5638-5650.
47. Manivet P, Schneider B, Smith JC, Choi DS, Maroteaux L, Kellermann O et al. (2002). The serotonin binding site of human and murine 5-HT2B receptors: molecular modeling and site-directed mutagenesis. J Biol Chem 277: 17170-17178.
48. Marelius J, Hansson T, Åqvist J (1998). Calculation of ligand binding free energies from molecular dynamics simulations. Int J Quantum Chem 69: 77-88.
49. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A (2000). Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29: 291-325.
50. Martin-Cora FJ, Pazos A (2004). Autoradiographic distribution of 5-HT7 receptors in the human brain using [3H]mesulergine: comparison to other mammalian species. Br J Pharmacol 141: 92-104.
51. Martinez JM, Martinez L (2003). Packing optimization for automated generation of complex system's initial configurations for molecular dynamics and docking. J Comput Chem 24: 819-825.
52. Medina RA, Sallander J, Benhamu B, Porras E, Campillo M, Pardo L et al. (2009). Synthesis of new serotonin 5-HT7 receptor ligands. Determinants of 5-HT7/5-HT1A receptor selectivity. J Med Chem 52: 2384-2392.
53. Mialet J, Dahmoune Y, Lezoualc'h F, Berque-Bestel I, Eftekhari P, Hoebeke J et al. (2000). Exploration of the ligand binding site of the human 5-HT(4) receptor by site-directed mutagenesis and molecular modeling. Br J Pharmacol 130: 527-538.
54. Michel AD, Clay WC, Ng SW, Roman S, Thompson K, Condreay JP et al. (2008). Identification of regions of the P2X(7) receptor that contribute to human and rat species differences in antagonist effects. Br J Pharmacol 155: 738-751.
55. Michino M, Abola E, Participants GA, Brooks, III, CL, Dixon JS, Moult J et al. (2009). Community-wide blind assessment of methods for GPCR structure modeling and docking. Nat Rev Drug Discov doi:10.1038/nrd2877.
56. Nandam LS, Jhaveri D, Bartlett P (2007). 5-HT7, neurogenesis and antidepressants: a promising therapeutic axis for treating depression. Clin Exp Pharmacol Physiol 34: 546-551.
57. Nordling E, Homan E (2004). Generalization of a targeted library design protocol: application to 5-HT7 receptor ligands. J Chem Inf Comput Sci 44: 2207-2215.
58. Paillet-Loilier M, Fabis F, Lepailleur A, Bureau R, Butt-Gueulle S, Dauphin F et al. (2005). Phenylpyrroles, a new chemolibrary virtual screening class of 5-HT7 receptor ligands. Bioorg Med Chem Lett 15: 3753-3757.
59. Paillet-Loilier M, Fabis F, Lepailleur A, Bureau R, Butt-Gueulle S, Dauphin F et al. (2007). Novel aminoethylbiphenyls as 5-HT7 receptor ligands. Bioorg Med Chem Lett 17: 3018-3022.
60. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E et al. (2005). Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
61. Rasmussen SG, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC et al. (2007). Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 450: 383-387.
62. Rezmann-Vitti LA, Louis SN, Nero TL, Jackman GP, Machida CA, Louis WJ (2004). Site-directed mutagenesis of the rat beta1-adrenoceptor. Involvement of Tyr356 (7.43) in (+/-)cyanopindolol but not (+/-)[125Iodo]cyanopindolol binding. Eur J Med Chem 39: 625-631.
63. Rosenbaum DM, Cherezov V, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS et al. (2007). GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 318: 1266-1273.
64. Selent J, Lopez L, Sanz F, PastorM(2008). Multi-receptor binding profile of clozapine and olanzapine: a structural study based on the new beta2 adrenergic receptor template. ChemMedChem 3: 1194-1198.
65. Shapiro DA, Kristiansen K, Weiner DM, Kroeze WK, Roth BL (2002). 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. J Biol Chem 277: 11441-11449.
66. Sylte I, Bronowska A, Dahl SG (2001). Ligand induced conformational states of the 5-HT(1A) receptor. Eur J Pharmacol 416: 33-41.
67. Thomas DR, Hagan JJ (2004). 5-HT7 receptors. Curr Drug Targets CNS Neurol Disord 3: 81-90.
68. Thomas DR, Melotto S, Massagrande M, Gribble AD, Jeffrey P, Stevens AJ et al. (2003). SB-656104-A, a novel selective 5-HT7 receptor antagonist, modulates REM sleep in rats. Br J Pharmacol 139: 705-714.
69. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997). The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
70. Tucker AL, Robeva AS, Taylor HE, Holeton D, Bockner M, Lynch KR et al. (1994). A1 adenosine receptors. Two amino acids are responsible for species differences in ligand recognition. J Biol Chem 269: 27900-27906.
71. Vermeulen ES, Schmidt AW, Sprouse JS,Wikstrom HV, Grol CJ (2003). Characterization of the 5-HT(7) receptor. Determination of the pharmacophore for 5-HT(7) receptor agonism and CoMFA-based modeling of the agonist binding site. J Med Chem 46: 5365-5374.
72. Vermeulen ES, van Smeden M, Schmidt AW, Sprouse JS,Wikstrom HV, Grol CJ (2004). Novel 5-HT7 receptor inverse agonists. Synthesis and molecular modeling of arylpiperazine- and 1,2,3,4-tetrahydroisoquinoline-based arylsulfonamides. J Med Chem 47: 5451-5466.
73. Wilcox RE, Ragan JE, Pearlman RS, Brusniak MY, Eglen RM, Bonhaus DW et al. (2001). High-affinity interactions of ligands at recombinant guinea pig 5HT7 receptors. J Comput Aided Mol Des 15: 883-909.
74. Wolf S, Bockmann M, Howeler U, Schlitter J, Gerwert K (2008). Simulations of a G protein-coupled receptor homology model predict dynamic features and a ligand binding site. FEBS Lett 582: 3335-3342.