Mutation studies of Ser7.39 and Ser2.60 in the human CB1 cannabinoid receptor: Evidence for a serine-induced bend in CB1 transmembrane helix 7

Molecular Pharmacology

Volumn 71, Issue 6, 2007, Pages 1512-1524

  Kapur, Ankur ^a   Hurst, Dow P ^b   Fleischer, Daniel ^a   Whitnell, Rob ^b,d   Thakur, Ganesh A ^c   Makriyannis, Alexandros ^c   Reggio, Patricia H ^b   Abood, Mary E ^a  

^a CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

^d GUILFORD COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA HYDROXY 3 (1,1' DIMETHYLHEPTYL)HEXAHYDROCANNABINOL; 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; AM 4056; CANNABINOID 1 RECEPTOR; CANNABINOID DERIVATIVE; DEXANABINOL; DOCKING PROTEIN; PHOSPHOROTHIOIC ACID DERIVATIVE; RADIOLIGAND; RECOMBINANT RECEPTOR; SERINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BIOASSAY; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENCY; DRUG PROTEIN BINDING; EMBRYO; GENE MUTATION; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOASSAY; RECEPTOR UPREGULATION; WILD TYPE;

BINDING, COMPETITIVE; CYCLOHEXANOLS; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN STRUCTURE, SECONDARY; RECEPTOR, CANNABINOID, CB1; SERINE;

EID: 34347352212     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.107.034645     Document Type: Article

References (62)

1. Abood ME (2005) Molecular biology of cannabinoid receptors. Handb Exp Pharmacol (168):81-115.
2. 2-adrenergic receptors control the equilibrium between active and inactive receptor states. Mol Pharmacol 57:198-210.
3. Arnis S, Fahmy K, Hofmann KP, and Sakmar TP (1994) A conserved carboxylic acid group mediates light-dependent proton uptake and signaling by rhodopsin. J Biol Chem 269:23879-23881.
4. Ballesteros JA, Deupi X, Olivella M, Haaksma EE, and Pardo L (2000) Serine and threonine residues bend alpha-helices in the chi(1) = g(-) conformation. Biophys J 79:2754-2760.
5. Ballesteros JA, Shi L, and Javitch JA (2001) Structural mimicry in G protein-coupled receptors: implications of the high-resolution structure of rhodopsin for structure-function analysis of rhodopsin-like receptors [published erratum appears in Mol Pharmacol 61:247, 2002]. Mol Pharmacol 60:1-19.
6. Ballesteros JA and 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 Methods in Neuroscience (Conn PM and Sealfon SM eds) pp 366-428, Academic Press, San Diego.
7. Barnett-Norris J, Hurst DP, Buehner K, Ballesteros JA, Guarnieri F, and Reggio PH (2002) Agonist alkyl tail interaction with cannabinoid CB1 receptor V6.43/I6.46 groove induces a Helix 6 active conformation. Int J Quantum Chem 88:76-86.
8. Barnett-Norris J, Hurst DP and Reggio PH (2003) The influence of cannabinoid receptor second extracellular loop conformation on the binding of CP55940, in 2003 Symposium on the Cannabinoids, p 79, International Cannabinoid Research Society, Cornwall, Ontario.
9. Bramblett RD, Panu AM, Ballesteros JA, and Reggio PH (1995) Construction of a 3D model of the cannabinoid CB1 receptor: determination of helix ends and helix orientation. Life Sci 56:1971-1982.
10. Cheng Y and Prusoff WH (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 22:3099-3108.
11. Chin C, Abadji V, Lucas-Lenard J, and Kendall D (1998) Ligand binding and modulation of cyclic AMP levels depends on the chemical nature of residue 192 of the human cannabinoid receptor 1. J Neurochem 70:366-373.
12. D'Antona AM, Ahn KH, and Kendall DA (2006) Mutations of CB(1) T210 produce active and inactive receptor forms: correlations with ligand affinity, receptor stability, and cellular localization. Biochemistry 45:5606-5617.
13. Farrens D, Altenbach C, Ynag K, Hubbell W, and Khorana H (1996) Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science (Wash DC) 274:768-770.
14. Fay JF, Dunham TD, and Farrens DL (2005) Cysteine residues in the human cannabinoid receptor: only C257 and C264 are required for a functional receptor, and steric bulk at C386 impairs antagonist SR141716A binding. Biochemistry 44:8757-8769.
15. Felder CC, Joyce KE, Briley EM, Mansouri J, Mackie K, Blond O, Lai Y, Ma AL, and Mitchell RL (1995) Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors. Mol Pharmacol 48:443-450.
16. Fiser A, Do RK, and Sali A (2000) Modeling of loops in protein structures. Protein Sci 9:1753-1773.
17. Gérard CM, Mollereau C, Vassart G, and Parmentier M (1991) Molecular cloning of a human cannabinoid receptor which is also expressed in testis. Biochem J 279: 129-134.
18. Ghanouni P, Steenhuis JJ, Farrens DL, and Kobilka BK (2001) Agonist-induced conformational changes in the G-protein-coupling domain of the beta 2 adrenergic receptor. Proc Natl Acad Sci USA 98:5997-6002
19. Gouldson PR, Kidley NJ, Bywater RP, Psaroudakis G, Brooks HD, Diaz C, Shire D, and Reynolds CA (2004) Toward the active conformations of rhodopsin and the beta2-adrenergic receptor. Proteins 56:67-84.
20. Gratkowski H, Lear JD, and DeGrado WF (2001) Polar side chains drive the association of model transmembrane peptides. Proc Natl Acad Sci USA 98:880-885.
21. Gray TM and Matthews BW (1984) Intrahelical hydrogen bonding of serine, threonine and cysteine residues within alpha helices and its relevance to membrane-bound proteins. J Mol Biol 175:75-81.
22. Guarnieri F and Weinstein H (1996) Conformational memories and the exploration of biologically relevant peptide conformations: an illustration for the gonadotropin-releasing hormone. J Am Chem Soc 118:5580-5589.
23. Hassan SA, Guarnieri F, and Mehler EL (2000a) Characterization of hydrogen bonding in a continuum solvent model. J Phys Chem B 104:6490-6498.
24. Hassan SA, Guarnieri F, and Mehler EL (2000b) A general treatment of solvent effects based on screened coulomb potentials. J Phys Chem B 104:6478-6489.
25. Hassan SA, Mehler EL, and Weinstein H (2002) Structure calculation of protein segments connecting domains with defined secondary structure: A simulated annealing Monte Carlo combined with biased scaled collective variables technique, in Computational Methods for Macromolecules: Challenges and Applications (Gan HH ed) pp 197-231, Springer Verlag, New York.
26. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, et al. (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161-202.
27. Huffman JW, Yu S, Showalter V, Abood ME, Wiley JL, Compton DR, Martin BR, Bramblett RD, and Reggio PH (1996) Synthesis and Pharmacology of a very potent cannabinoid lacking a phenolic hydroxyl with high affinity for the CB2 receptor. J Med Chem 39:3875-3877.
28. Hurst D, Umejiego U, Lynch D, Seltzman H, Hyatt S, Roche M, McAllister S, Fleischer D, Kapur A, Abood M, et al. (2006) Biarylpyrazole inverse agonists at the cannabinoid CB1 receptor: importance of the C-3 carboxamide oxygen/lysine3.28(192) interaction. J Med Chem 49:5969-5987.
29. Hurst DP, Lynch DL, Barnett-Norris J, Hyatt SM, Seltzman HH, Zhong M, Song ZH, Nie J, Lewis D, and Reggio PH (2002) N-(Piperidin-1-yl)-5-(4- chlorophenyl)-1-(2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide (SR141716A) Interaction with LYS 3.28(192) Is crucial for its inverse agonism at the cannabinoid CB1 receptor. Mol Pharmacol 62:1274-1287.
30. Javitch JA, Fu D, Liapakis G, and Chen J (1997) Constitutive activation of the b2 adrenergic receptor alters the orientation of its sixth membrane-spanning segment. J Biol Chem 272:18546-18549.
31. Jensen AD, Guarnieri F, Rasmussen SG, Asmar F, Ballesteros JA, and Gether U (2001) Agonist-induced conformational changes at the cytoplasmic side of transmembrane segment 6 in the β2 adrenergic receptor mapped by site-selective fluorescent labeling. J Biol Chem 276:9279-9290.
32. Li J, Edwards PC, Burghammer M, Villa C, and Schertler GF (2004) Structure of bovine rhodopsin in a trigonal crystal form. J Mol Biol 343:1409-1438.
33. Lin SW and Sakmar TP (1996) Specific tryptophan UV-absorbance changes are probes of the transition of rhodopsin to its active state. Biochemistry 35:11149-11159.
34. McAllister SD, Hurst DP, Barnett-Norris J, Lynch D, Reggio PH, and Abood ME (2004) Structural mimicry in class A G protein-coupled receptor rotamer toggle switches: the importance of the F3.36(201)/W6.48(357) interaction in cannabinoid CB1 receptor activation. J Biol Chem 279:48024-48037.
35. McAllister SD, Rizvi G, Anavi-Goffer S, Hurst DP, Barnett-Norris J, Lynch DL, Reggio PH, and Abood ME (2003) An aromatic microdomain at the cannabinoid CB(1) receptor constitutes an agonist/inverse agonist binding region. J Med Chem 46:5139-5152.
36. McAllister SD, Tao Q, Barnett-Norris J, Buehner K, Hurst DP, Guarnieri F, Reggio PH, Nowell Harmon KW, Cabral GA, and Abood ME (2002) A critical role for a tyrosine residue in the cannabinoid receptors for ligand recognition. Biochem Pharmacol 63:2121-2136.
37. Melvin LS, Milne GM, Johnson MR, Subramaniam B, Wilken GH, and Howlett AC (1993) Structure-activity relationships for cannabinoid receptor-binding and analgesic activity: studies of bicyclic cannabinoid analogs. Mol Pharmacol 44:1008-1015.
38. Mirzadegan T, Benko G, Filipek S, and Palczewski K (2003) Sequence analyses of G-protein-coupled receptors: similarities to rhodopsin. Biochemistry 42:2759-2767.
39. Mohamadi F, Richards N, Guida W, Liskamp R, Lipton M, Caulfield C, Chang G, Hendrickson T, and Still W (1990) MacroModel- an integrated softward system for modeling organic and bioorganic molecules using molecular mechanics. J Comput Chem 11:440-467.
40. Munro S, Thomas KL, and Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature (Lond) 365:61-65.
41. Nakanishi J, Takarada T, Yunoki S, Kikuchi Y, and Maeda M (2006) FRET-based monitoring of conformational change of the beta2 adrenergic receptor in living cells. Biochem Biophys Res Commun 343:1191-1196.
42. Okada T, Fujiyoshi Y, Silow M, Navarro J, Landau EM, and Shichida Y (2002) Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography. Proc Natl Acad Sci USA 99:5982-5987.
43. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, et al. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science (Wash DC) 289:739-745.
44. Picone RP, Fournier DJ, and Makriyannis A (2002) Ligand based structural studies of the CB1 cannabinoid receptor. J Pept Res 60:348-356.
45. Picone RP, Khanolkar AD, Xu W, Ayotte LA, Thakur GA, Hurst DP, Abood ME, Reggio PH, Fournier DJ, and Makriyannis A (2005) (-)-7′-Isothiocyanato-11- hydroxy-1′,1′-dimethylheptylhexahydrocannabinol (AM841), a high-affinity electrophilic ligand, interacts covalently with a cysteine in helix six and activates the CB1 cannabinoid receptor. Mol Pharmacol 68:1623-1635.
46. Price MR, Baillie GL, Thomas A, Stevenson LA, Easson M, Goodwin R, McLean A, McIntosh L, Goodwin G, Walker G, et al. (2005) Allosteric modulation of the cannabinoid CB1 receptor. Mol Pharmacol 68:1484-1495.
47. Reggio PH (2005) Cannabinoid receptors and their ligands: ligand-ligand and ligand-receptor modeling approaches. Handb Exp Pharmacol (168):247-281.
48. Reggio PH, Panu AM, and Miles S (1993) Characterization of a region of steric interference at the cannabinoid receptor using the active analog approach. J Med Chem 36:1761-1771.
49. Rhee MH (2002) Functional role of serine residues of transmembrane dopamin VII in signal transduction of CB2 cannabinoid receptor. J Vet Sci 3:185-191.
50. Sali A and Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779-815.
51. Salo OM, Lahtela-Kakkonen M, Gynther J, Jarvinen T, and Poso A (2004) Development of a 3D model for the human cannabinoid CB1 receptor. J Med Chem 47:3048-3057.
52. Salom D, Lodowski DT, Stenkamp RE, Trong IL, Golczak M, Jastrzebska B, Harris T, Ballesteros JA, and Palczewski K (2006) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc Natl Acad Sci USA 103:16123-16128.
53. Schertler GF (2005) Structure of rhodopsin and the metarhodopsin I photointermediate. Curr Opin Struct Biol 15:408-415.
54. Shi L, Liapakis G, Xu R, Guarnieri F, Ballesteros JA, and Javitch JA (2002) Beta 2 adrenergic receptor activation. Modulation of the proline kink in transmembrane 6 by a rotamer toggle switch. J Biol Chem 277:40989-40996.
55. Song Z-H and Bonner TI (1996) A lysine residue of the cannabinoid receptor is critical for receptor recognition by several agonists but not WIN55212-2. Mol Pharmacol 49:891-896.
56. Szundi I, Ruprecht JJ, Epps J, Villa C, Swartz TE, Lewis JW, Schertler GF, and Kliger DS (2006) Rhodopsin photointermediates in two-dimensional crystals at physiological temperatures. Biochemistry 45:4974-4982
57. Tao Q, McAllister S, Andreassi J, Nowell K, Cabral G, Hurst D, Bachtel K, Ekman M, Reggio P, and Abood M (1999) Role of a conserved lysine residue in the peripheral cannabinoid receptor (CB2): evidence for subtype specificity. Mol Pharmacol 55:605-613.
58. Ulfers AL, McMurry JL, Kendall DA, and Mierke DF (2002) Structure of the third intracellular loop of the human cannabinoid 1 receptor. Biochemistry 41:11344-11350.
59. Visiers I, Braunheim BB, and Weinstein H (2000) Prokink: a protocol for numerical evaluation of helix distortions by proline. Protein Eng 13:603-606.
60. Ward SD, Hamdan FF, Bloodworth LM, Siddiqui NA, Li JH, and Wess J (2006) Use of an in situ disulfide cross-linking strategy to study the dynamic properties of the cytoplasmic end of transmembrane domain VI of the M(3) muscarinic acetylcholine receptor. Biochemistry 45:676-685.
61. Xie XQ, Melvin LS, and Makriyannis A (1996) The conformational properties of the highly selective cannabinoid receptor ligand CP-55,940. J Biol Chem 271:10640-10647.
62. Zhang R, Hurst DP, Barnett-Norris J, Reggio PH, and Song ZH (2005) Cysteine 2.59(89) in the second transmembrane domain of human cb2 receptor is accessible within the ligand binding crevice: evidence for possible CB2 deviation from a rhodopsin template. Mol Pharmacol 68:69-83.