An Aromatic Microdomain at the Cannabinoid CB1 Receptor Constitutes an Agonist/Inverse Agonist Binding Region

Journal of Medicinal Chemistry

Volumn 46, Issue 24, 2003, Pages 5139-5152

  McAllister, Sean D ^a   Rizvi, Gulrukh ^a   Anavi Goffer, Sharon ^a   Hurst, Dow P ^b   Barnett Norris, Judy ^b   Lynch, Diane L ^b   Reggio, Patricia H ^b   Abood, Mary E ^a  

^a CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

^b KENNESAW STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR AGONIST; CANNABINOID RECEPTOR ANTAGONIST; G PROTEIN COUPLED RECEPTOR; RIMONABANT;

AGONIST; AROMATIZATION; ARTICLE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG STRUCTURE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYDROGEN BOND; IMMUNOCYTOCHEMISTRY; LIGAND BINDING; POINT MUTATION; RECEPTOR AFFINITY;

BINDING SITES; CYCLOHEXANOLS; HUMANS; IMMUNOCHEMISTRY; LIGANDS; MODELS, MOLECULAR; MORPHOLINES; NAPHTHALENES; PIPERIDINES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PYRAZOLES; RADIOLIGAND ASSAY; RECEPTOR, CANNABINOID, CB1;

EID: 0242522905     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm0302647     Document Type: Article

References (58)

1. Onaivi, E. The Biology of Marijuana: From Gene to Behaviour; Harwood Academic Publishers: Reading, U.K., 2002.
2. 1 antagonist SR 141716A. J. Biol. Chem. 1996, 271, 6941-6946.
3. Shire, D.; Calandra, B.; Bouaboula, M.; Barth, F.; Rinaldi-Carmona, M.; Casellas, P.; Ferrara, P. Cannabinoid receptor interactions with the antagonists SR 141716A and SR 144528. Life Sci. 1999, 65, 627-635.
4. Chin, C. N.; Murphy, J. W.; Huffman, J. W.; Kendall, D. A. The third transmembrane helix of the cannabinoid receptor plays a role in the selectivity of aminoalkylindoles for CB2, peripheral cannabinoid receptor. J. Pharmacol. Exp. Ther. 1999, 291, 837-844.
5. Song, Z. H.; Slowey, C. A.; Hurst, D. P.; Reggio, P. H. The difference between the CB(1) and CB(2) cannabinoid receptors at position 5.46 is crucial for the selectivity of WIN55212-2 for CB(2). Mol. Pharmacol. 1999, 56, 834-840.
6. 1 Receptor. Mol. Pharmacol. 2002, 62, 1274-1287.
7. McAllister, S. D.; Tao, Q.; Barnett-Norris, J.; Buehner, K.; Hurst, D. P.; Guarnieri, F.; Reggio, P. H.; Nowell Harmon, K. W.; Cabral, G. A.; Abood, M. E. A critical role for a tyrosine residue in the cannabinoid receptors for ligand recognition. Biochem. Pharmacol. 2002, 63, 2121-2136.
8. Shi, L.; Liapakis, G.; Xu, R.; Guarnieri, F.; Ballesteros, J. A.; Javitch, J. A. Beta2 adrenergic receptor activation. Modulation of the proline kink in transmembrane 6 by a rotamer toggle switch. J. Biol. Chem. 2002, 277, 40989-40996.
9. 1 Receptor V6.43/I6.46 Groove Induces a Helix 6 Active Conformation. Int. J. Quantum Chem. 2002.
10. Farrens, D.; Altenbach, C.; Ynag, K.; Hubbell, W.; Khorana, H. Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science 1996, 274, 768-770.
11. Gether, U.; Lin, S.; Ghanouni, P.; Ballesteros, J.; Weinstein, H.; Kobilka, B. Agonists induce conformational changes in transmembrane domains III and VI of the beta2 adrenoceptor. EMBO J. 1997, 16, 6737-6747.
12. Ghanouni, P.; Steenhuis, J. J.; Farrens, D. L.; Kobilka, B. K. Agonist-induced conformational changes in the G-protein-coupling domain of the beta 2 adrenergic receptor. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 5997-6002.
13. Jensen, A. D.; Guarnieri, F.; Rasmussen, S. G.; Asmar, F.; Ballesteros, J. A.; Gether, U. Agonist-induced conformational changes at the cytoplasmic side of transmembrane segment 6 in the beta 2 adrenergic receptor mapped by site-selective fluorescent labeling. J Biol. Chem. 2001, 276, 9279-9290.
14. Javitch, J. A.; Fu, D.; Liapakis, G.; Chen, J. Constitutive activation of the b2 adrenergic receptor alters the orientation of its sixth membrane-spanning segment. J. Biol. Chem, 1997, 272, 18546-18549.
15. Hulme, E. C.; Lu, Z. L.; Ward, S.; Allman, K.; Curtis, C. The conformational switch in 7-transmembrane receptors: the muscarinic receptor paradigm. Eur. J. Pharmacol. 1999, 375, 247-260.
16. Leff, P. The two-state model of receptor activation. Trends Pharmacol. Sci. 1995, 16, 89-97.
17. Samama, P.; Pei, G.; Costa, T.; Cotecchia, S.; Lefkowitz, R. J. Negative antagonists promote an inactive conformation of the beta 2-adrenergic receptor. Mol. Pharmacol. 1994, 45, 390-394.
18. Burley, S.; Petsko, G. Aromatic-aromatic interaction: A mechanism of protein structure stabilization. Science 1985, 229, 23-28.
19. Bouaboula, M.; Perrachon, S.; Milligan, L.; Canat, X.; Rinaldi-Carmona, M.; Portier, M.; Barth, F.; Calandra, B.; Pecceu, F.; Lupker, J.; Maffrand, J.-P.; LeFur, G.; Casellas, P. A selective inverse agonist for central cannabinoid receptor inhibits mitogen-activated protein kinase activation stimulated by insulin or insulin-like growth factor 1. J. Biol. Chem. 1997, 272, 22330-22339.
20. 1 cannabinoid receptor activity. Mol Pharmacol 1998, 54, 1064-1072.
21. Meschler, J. P.; Kraichely, D. M.; Wilken, G. H.; Howlett, A. C. Inverse agonist properties of N-(piperidin-1-yl)-5-(4-chlorophe-nyl)-1-(2,4-dichlorophenyl) -4-methyl-1H-pyrazole-3-carboxamide HCl (SR141716A) and 1-(2-chlorophenyl)-4-cyano-5-(4-methoxyphenyl)-1H-pyrazole-3-carboxylic acid phenylamide (CP-272871) for the CB(1) cannabinoid receptor. Biochem. Pharmacol. 2000, 60, 1315-1323.
22. Thomas, B. F.; Gilliam, A. F.; Burch, D. F.; Roche, M. J.; Seltzman, H. H. Comparative receptor binding analyses of cannabinoid agonists and antagonists. J. Pharmacol. Exp. Ther. 1998, 285, 285-292.
23. Katoch-Rouse, R.; Pavlova, O. A.; Caulder, T.; Hoffman, A. F.; Mukhin, A. G.; Horti, A. G. Synthesis, structure-activity relationship, and evaluation of SR141716 analogues: Development of central cannabinoid receptor ligands with lower lipophilicity. J. Med. Chem. 2003, 46, 642-645.
24. D'Ambra, T. E.; Estep, K. G.; Bell, M. R.; Eissenstat, M. A.; Josef, K. A.; Ward, S. J.; Haycock, D. A.; Baizman, E. R.; Casiano, F. M.; Beglin, N. C. Conformationally restrained analogues of pravadoline: nanomolar potent, enantioselective, (aminoalkyl)-indole agonists of the cannabinoid receptor. J. Med. Chem. 1992, 35, 124-135.
25. 1 receptor. J. Med. Chem. 2002, 45, 3649-3659.
26. Palczewski, K.; Kumasaka, T.; Hori, T.; Behnke, C. A.; Motoshima, H.; Fox, B. A.; Le Trong, I.; Teller, D. C.; Okada, T.; Stenkamp, R. E.; Yamamoto, M.; Miyano, M. Crystal structure of rhodopsin: A G protein-coupled receptor. Science 2000, 289, 739-745.
27. Barnett-Norris, J.; Guarnieri, F.; Hurst, D. P.; Reggio, P. H. Exploration of biologically relevant conformations of anandamide, 2-arachidonylglycerol, and their analogues using conformational memories. J. Med. Chem. 1998, 41, 4861-4872.
28. LaLonde, J. M.; Levenson, M. A.; Roe, J. J.; Bernlohr, D. A.; Banaszak, L. J. Adipocyte lipid-binding protein complexed with arachidonic acid. Titration calorimetry and X-ray crystallographic studies. J. Biol. Chem. 1994, 269, 25339-25347.
29. Song, Z.-H.; Bonner, T. I. A lysine residue of the cannabinoid receptor is critical for receptor recognition by several agonists but not WIN55212-2. Mol. Pharmacol. 1996, 49, 891-896.
30. Pinto, J. C.; Potie, F.; Rice, K. C.; Boring, D.; Johnson, M. R.; Evans, D. M.; Wilken, G. H.; Cantrell, C. H.; Howlett, A. C. Cannabinoid receptor binding and agonist activity of amides and esters of arachidonic acid. Mol. Pharmacol. 1994, 46, 516-522.
31. 1). J. Pharmacol. Exp. Ther. 1999, 289, 1427-1433.
32. Bonechi, C.; Brizzi, A.; Brizzi, V.; Francoli, M.; Donati, A.; Rossi, C. Conformational Analysis of N-arachidonylethanolamide (Anandamide) Using Nuclear Magnetic Resonance and Theoretical Calculations. Magn. Reson. Chem. 2001, 39, 432-437.
33. Barnett-Norris, J.; Hurst, D. P.; Reggio, P. H. The influence of cannabinoid receptor second extracellular loop conformation on the binding of CP55940. 2003 Symposium on the Cannabinoids; International Cannabinoid Research Society, Burlington, VT: Cornwall, Ontario, Canada, 2003; p 78.
34. 2 cannabinoid receptor. J. Neurochem. 2000, 75, 2485-2491.
35. Ward, W. H.; Timms, D.; Fersht, A. R. Protein engineering and the study of structure-function relationships in receptors. Trends. Pharmacol. Sci. 1990, 11, 280-284.
36. Sansom, M. S.; Weinstein, H. Hinges, swivels and switches: the role of prolines in signaling via transmembrane alpha-helices. Trends. Pharmacol. Sci. 2000, 21, 445-451.
37. Ballesteros, J. A.; Deupi, X.; Olivella, M.; Haaksma, E. E.; Pardo, L. Serine and threonine residues bend alpha-helices in the chi-(1) = g(-) conformation. Biophys. J. 2000, 79, 2754-2760.
38. Hunter, C.; Singh, J.; Thornton, J. π-π interactions: The geometry and energetics of phenylalanine-phenylalanine inter-actions in proteins. J. Mol. Biol. 1991, 218.
39. Sinnokrot, M. O.; Valeev, E. F.; Sherrill, C. D. Estimates of the ab initio limit for pi-pi interactions: The benzene dimer. J. Am. Chem. Soc. 2002, 124, 10887-10893.
40. Lan, R.; Liu, Q.; Fan, P.; Lin, S.; Fernando, S. R.; McCallion, D.; Pertwee, R.; Makriyannis, A. Structure-activity relationships of pyrazole derivatives as cannabinoid receptor antagonists. J. Med. Chem. 1999, 42, 769-776.
41. Wiley, J. L.; Jefferson, R. G.; Grier, M. C.; Mahadevan, A.; Razdan, R. K.; Martin, B. R. Novel pyrazole cannabinoids: insights into CB(1) receptor recognition and activation. J. Pharmacol. Exp. Ther. 2001, 296, 1013-1022.
42. 1 cannabinoid receptor. J. Med. Chem. 2002, 45, 1447-1459.
43. Huffman, J.; Dai, D.; Martin, B.; Compton, D. Design, Synthesis and Pharmacology of Cannabimimetic Indoles. Bioorg. Med. Chem. Lett. 1994, 4, 563-566.
44. Eissenstat, M. A.; Bell, M. R.; D'Ambra, T. E.; Alexander, E. J.; Daum, S. J.; Ackerman, J. H.; Gruett, M. D.; Kumar, V.; Estep, K. G.; Olefirowicz, E. M. Aminoalkylindoles: structure-activity relationships of novel cannabinoid mimetics. J. Med. Chem. 1995, 38, 3094-3105.
45. 2 receptors: Insights gained from (E)- and (Z)-naphthylidene indenes. J. Med. Chem. 1998, 41, 5177-5187.
46. 1 Cannabinoid Receptor. Bioorg. Med. Chem. 2003, 11, 539-549.
47. Brandl, M.; Weiss, M. S.; Jabs, A.; Suhnel, J.; Hilgenfeld, R. C-H⋯[pi]-Interactions in Proteins. J. Mol. Biol. 2001, 307, 357-377.
48. Bracey, M. H.; Hanson, M. A.; Masuda, K. R.; Stevens, R. C.; Cravatt, B. F. Structural adaptations in a membrane enzyme that terminates endocannabinoid signaling. Science 2002, 298, 1793-1796.
49. Malkowski, M. G.; Ginell, S. L.; Smith, W. L.; Garavito, R. M. The productive conformation of arachidonic acid bound to prostaglandin synthase. Science 2000, 289, 1933-1937.
50. Ballesteros, J. A.; Weinstein, H. Integrated methods for the construction of three-dimensional models and computational probing of structure function relations in G protein-coupled receptors. Methods in Neuroscience; Academic Press: San Diego, 1995; pp 366-428.
51. Lin, S.; Sakmar, T. Specific tryptophan UV-absorbance changes are probes of the transition of rhodopsin to its active state. Biochemistry 1996, 35, 11149-11159.
52. 2 adrenegic receptor involves disruption of an ionic link between the cytoplasmic ends of transmembrane segments 3 and 6. J. Biol. Chem. 2001, 276, 29171-29177.
53. 1 cannabinoid receptor gene. Biochem. Pharmacol. 1997, 53, 207-214.
54. 1 receptor: Determination of helix ends and helix orientation. Life Sci. 1995, 56, 1971-1982.
55. Gerard, C. M.; Mollereau, C.; Vassart, G.; Parmentier, M. Molecular cloning of a human cannabinoid receptor which is also expressed in testis. Biochem. J. 1991, 279, 129-134.
56. 2): Evidence for subtype specificity. Mol. Pharmacol. 1999, 55, 605-613.
57. 2 receptors disrupts G-protein coupling. J. Pharmacol. Exp. Ther. 1998, 28,5, 651-658.
58. Cheng, Y. C.; Prusoff, W. H. Relationships between the inhibition constant (Ki) and the concentration of inhibitor that causes 50% inhibition (IC50) on an enzymatic reaction. Biochem Pharmacol 1973, 22, 3099-3108.