Modeling of the OX1R-orexin-A complex suggests two alternative binding modes Computational analysis

BMC Structural Biology

Volumn 15, Issue 1, 2015, Pages

  Karhu, Lasse ^a   Turku, Ainoleena ^a   Xhaard, Henri ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

G protein coupled receptor; GPCR; Multidimensional scaling; Orexin A; OX1 receptor; Peptide docking; Pose selection

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; GLUTAMINE; HISTIDINE; NEUROTENSIN RECEPTOR; OREXIN; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; OREXIN A; PEPTIDE; TYROSINE; HCRTR1 PROTEIN, HUMAN; OREXIN RECEPTOR; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CLUSTER ANALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; HYDROGEN BOND; MOLECULAR DOCKING; MULTIDIMENSIONAL SCALING; SITE DIRECTED MUTAGENESIS; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN SECONDARY STRUCTURE; STRUCTURAL HOMOLOGY;

BINDING SITES; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MUTATION; OREXIN RECEPTORS; OREXINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84931044463     PISSN: None     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/s12900-015-0036-2     Document Type: Article

References (57)

1. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell. 1998;92:573-85.
2. Sakurai T, Mieda M, Tsujino N. The orexin system: roles in sleep/wake regulation. Ann N Y Acad Sci. 2010;1200:149-61.
3. Laburthe M, Voisin T. The orexin receptor OX1R in colon cancer: a promising therapeutic target and a new paradigm in G protein-coupled receptor signalling through ITIMs. Br J Pharmacol. 2012;165:1678-87.
4. Scammell TE, Winrow CJ. Orexin receptors: pharmacology and therapeutic opportunities. Annu Rev Pharmacol Toxicol. 2011;51:243-66.
5. Haynes AC, Jackson B, Chapman H, Tadayyon M, Johns A, Porter RA, et al. A selective orexin-1 receptor antagonist reduces food consumption in male and female rats. Regul Pept. 2000;96:45-51.
6. De Lecea L, Kilduff TS, Peyron C, Gao X-B, Foye PE, Danielson PE, et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A. 1998;95:322-7.
7. Lee J-H, Bang E, Chae K-J, Kim J-Y, Lee DW, Lee W. Solution structure of a new hypothalamic neuropeptide, human hypocretin-2/orexin-B. Eur J Biochem. 1999;266:831-9.
8. Takai T, Takaya T, Nakano M, Akutsu H, Nakagawa A, Aimoto S, et al. Orexin-A is composed of a highly conserved C-terminal and a specific, hydrophilic N-terminal region, revealing the structural basis of specific recognition by the orexin-1 receptor. J Pept Sci. 2006;12:443-54.
9. Darker JG, Porter RA, Eggleston DS, Smart D, Brough SJ, Sabido-David C, et al. Structure-activity analysis of truncated orexin-A analogues at the orexin-1 receptor. Bioorg Med Chem Lett. 2001;11:737-40.
10. Ammoun S, Holmqvist T, Shariatmadari R, Oonk HB, Detheux M, Parmentier M, et al. Distinct recognition of OX1 and OX2 receptors by orexin peptides. J Pharmacol Exp Ther. 2003;305:507-14.
11. Lang M, Söll RM, Dürrenberger F, Dautzenberg FM, Beck-Sickinger AG. Structure-activity studies of orexin A and orexin B at the human orexin 1 and orexin 2 receptors led to orexin 2 receptor selective and orexin 1 receptor preferring. J Med Chem. 2004;47:1153-60.
12. Asahi S, Egashira S-I, Matsuda M, Iwaasa H, Kanatani A, Ohkubo M, et al. Development of an orexin-2 receptor selective agonist, [Ala (11), D-Leu (15)] orexin-B. Bioorg Med Chem Lett. 2003;13:111-3.
13. Yin J, Mobarec JC, Kolb P, Rosenbaum DM. Crystal structure of the human OX2 orexin receptor bound to the insomnia drug suvorexant. Nature. 2015;519:247-50.
14. Malherbe P, Roche O, Marcuz A, Kratzeisen C, Wettstein JG, Bissantz C. Mapping the binding pocket of dual antagonist almorexant to human orexin 1 and Orexin 2 receptors: comparison with the selective OX1 antagonist SB-674042 and the selective OX2 antagonist N-Ethyl-2-[(6-methoxy-pyridin-3-yl)-(toluene-2-sulfonyl)-amino]-N-py. Mol Pharmacol. 2010;78:81-93.
15. Tran D-T, Bonaventure P, Hack M, Mirzadegan T, Dvorak C, Letavic M, et al. Chimeric, mutant orexin receptors show key interactions between orexin receptors, peptides and antagonists. Eur J Pharmacol. 2011;667:120-8.
16. Putula J, Kukkonen JP. Mapping of the binding sites for the OX1 orexin receptor antagonist, SB-334867, using orexin/hypocretin receptor chimaeras. Neurosci Lett. 2012;506:111-5.
17. Michino M, Abola E, GPCR Dock 2008 participants, Brooks CL, Dixon JS, Moult J, et al. Community-wide assessment of GPCR structure modelling and ligand docking: GPCR Dock 2008. Nat Rev Drug Discov. 2009;8:455-63.
18. Kufareva I, Rueda M, Katritch V, GPCR Dock 2010 participants, Stevens RC, Abagyan R. Status of GPCR modeling and docking as reflected by community-wide GPCR Dock 2010 assessment. Structure. 2011;19:1108-26.
19. Kufareva I, Katritch V, Participants of GPCR Dock 2013, Stevens RC, Abagyan R. Advances in GPCR modeling evaluated by the GPCR dock 2013 assessment: meeting new challenges. Structure. 2014;22:1120-39.
20. Trellet M, Melquiond ASJ, Bonvin AMJJ. A unified conformational selection and induced fit approach to protein-peptide docking. PLoS One. 2013;8:e58769.
21. Raveh B, London N, Schueler-Furman O. Sub-angstrom modeling of complexes between flexible peptides and globular proteins. Proteins. 2010;78:2029-40.
22. Antes I. DynaDock: a new molecular dynamics-based algorithm for protein-peptide docking including receptor flexibility. Proteins. 2010;78:1084-104.
23. Prusis P, Schiöth HB, Muceniece R, Herzyk P, Afshar M, Hubbard RE, et al. Modeling of the three-dimensional structure of the human melanocortin 1 receptor, using an automated method and docking of a rigid cyclic melanocyte-stimulating hormone core peptide. J Mol Graph Model. 1997;15:307-17.
24. De Wachter R, De Graaf C, Keresztes A, Vandormael B, Ballet S, Rognan D, et al. Synthesis, biological evaluation, and automated docking of constrained analogues of the opioid peptide H-Dmt- D -Ala-Phe-Gly- 5-tetrahydro-2-benzazepin-3-one Scaffold. J Med Chem. 2011;54:6538-47.
25. Chandrashekaran IR, Rao GS, Cowsik SM. Molecular modeling of the peptide agonist-binding site in a neurokinin-2 receptor. J Chem Inf Model. 2009;49:1734-40.
26. 3 receptor complex. J Chem Inf Model. 2011;51:2932-8.
27. Matsoukas M-T, Potamitis C, Plotas P, Androutsou M, Agelis G, Matsoukas J, et al. Insights into AT1 receptor activation through AngII binding studies. J Chem Inf Model. 2013;53:2798-811.
28. Heifetz A, Barker O, Morris GB, Law RJ, Slack M, Biggin PC. Toward an understanding of agonist binding to human Orexin-1 and Orexin-2 receptors with G-protein-coupled receptor modeling and site-directed mutagenesis. Biochem. 2013;52:8246-60.
29. Rodrigo J, Pena A, Murat B, Trueba M, Durroux T, Guillon G. Mapping the binding site of Arginine Vasopressin to V 1a and V 1b Vasopressin receptors. Mol Endocrinol. 2007;21:512-23.
30. Chen R, Li L, Weng Z. ZDOCK: an initial-stage protein-docking algorithm. Proteins. 2003;52:80-7.
31. Li L, Chen R, Weng Z. RDOCK: refinement of rigid-body protein docking predictions. Proteins. 2003;53:693-707.
32. Discovery Studio. Version 3.5. San Diego, CA: Accelrys Software Inc; 2012
33. Ballesteros JA, Weinstein H. Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors. Methods Neurosci. 1995;25:366-428.
34. Wu B, Chien EYT, Mol CD, Fenalti G, Liu W, Katritch V, et al. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science. 2010;330:1066-71.
35. White JF, Noinaj N, Shibata Y, Love J, Kloss B, Xu F, et al. Structure of the agonist-bound neurotensin receptor. Nature. 2012;490:508-13.
36. Manglik A, Kruse AC, Kobilka TS, Thian FS, Mathiesen JM, Sunahara RK, et al. Crystal structure of the μ-opioid receptor bound to a morphinan antagonist. Nature. 2012;485:321-6.
37. Wu H, Wacker D, Mileni M, Katritch V, Han GW, Vardy E, et al. Structure of the human κ-opioid receptor in complex with JDTic. Nature. 2012;485:327-32.
38. Granier S, Manglik A, Kruse AC, Kobilka TS, Thian FS, Weis WI, et al. Structure of the δ-opioid receptor bound to naltrindole. Nature. 2012;485:400-4.
39. Thompson AA, Liu W, Chun E, Katritch V, Wu H, Vardy E, et al. Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature. 2012;485:395-9.
40. Fredriksson R, Lagerström MC, Lundin L-G, Schiöth HB. The G-protein-coupled receptors in the human genome form five main families: phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol. 2003;63:1256-72.
41. Maestro. Version 9.4. New York, NY: Shrdinger, LLC; 2013.
42. Chien EYT, Liu W, Zhao Q, Katritch V, Han GW, Hanson MA, et al. Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist. Science. 2010;330:1091-905.
43. Egloff P, Hillenbrand M, Klenk C, Batyuk A, Heine P, Balada S, et al. Structure of signaling-competent neurotensin receptor 1 obtained by directed evolution in Escherichia coli. Proc Natl Acad Sci U S A. 2014;111:E655-62.
44. Səli A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 1993;234:779-815.
45. Daura X, Gademann K, Jaun B, Seebach D, Van Gunsteren WF, Mark AE. Peptide folding: when simulation meets experiment. Angew Chemie Int Ed. 1999;38:236-40.
46. Matlab. Version R2013a. Natick, MA: MathWorks Inc; 2013.
47. Hubbard SJ, Thornton JM. Naccess. London, England: Department of Biochemistry and Molecular Biology, University College London; 1993.
48. Isberg V, de Graaf C, Bortolato A, Cherezov V, Katritch V, Marshall FH, et al. Generic GPCR residue numbers - aligning topology maps while minding the gaps. Trends Pharmacol Sci. 2015;36:22-31.
49. Voss NR, Gerstein M. 3V: cavity, channel and cleft volume calculator and extractor. Nucleic Acids Res. 2010;38(Web Server issue):W555-62.
50. Putula J, Pihlajamaa T, Kukkonen JP. Calcium affects OX1 orexin (hypocretin) receptor responses by modifying both orexin binding and the signal transduction machinery. Br J Pharmacol. 2014;171:5816-28.
51. Warne T, Moukhametzianov R, Baker JG, Nehme R, Edwards PC, Leslie AGW, et al. The structural basis for agonist and partial agonist action on a β1-adrenergic receptor. Nature. 2011;469:241-4.
52. Rasmussen SGF, Choi H-J, Fung JJ, Pardon E, Casarosa P, Chae PS, et al. Structure of a nanobody-stabilized active state of the β(2) adrenoceptor. Nature. 2011;469:175-80.
53. Xhaard H, Rantanen V-V, Nyronen T, Johnson MS. Molecular evolution of adrenoceptors and dopamine receptors: implications for the binding of catecholamines. J Med Chem. 2006;49:1706-19.
54. Kitabgi P. Functional domains of the subtype 1 neurotensin receptor (NTS1). Peptides. 2006;27:2461-8.
55. Härterich S, Koschatzky S, Einsiedel J, Gmeiner P. Novel insights into GPCR-peptide interactions: mutations in extracellular loop 1, ligand backbone methylations and molecular modeling of neurotensin receptor 1. Bioorg Med Chem. 2008;16:9359-68.
56. Xhaard H, Nyrönen T, Rantanen V-V, Ruuskanen JO, Laurila J, Salminen T, et al. Model structures of α2-adrenoceptors in complex with automatically docked antagonist ligands raise the possibility of interactions dissimilar from agonist ligands. J Struct Biol. 2005;150:126-43.
57. Barton GJ. ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng. 1993;6:37-40.