Hydrophobic residues in helix 8 of cannabinoid receptor 1 are critical for structural and functional Properties

Biochemistry

Volumn 49, Issue 3, 2010, Pages 502-511

  Ahn, Kwang H ^a   Nishiyama, Akiko ^a   Mierke, Dale F ^b   Kendall, Debra A ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b Dartmouth College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPHILICS; BINDING ANALYSIS; BINDING ISOTHERMS; C TERMINUS; CANNABINOID RECEPTORS; CLASS A; FUNCTIONAL PROPERTIES; G PROTEIN ACTIVATION; G PROTEIN COUPLED RECEPTORS; GLOBAL FEATURE; HELICAL DOMAINS; HELICAL STRUCTURES; HUMAN CANNABINOID RECEPTORS; HYDROPHOBIC AND HYDROPHILIC; HYDROPHOBIC GROUPS; HYDROPHOBIC RESIDUES; LIGAND BINDING; POSITIVELY CHARGED; RECEPTOR LOCALIZATION; THRESHOLD LEVELS; TRANS-MEMBRANE DOMAINS; WILD TYPES;

ACTIVATION ANALYSIS; AMINO ACIDS; CIRCULAR DICHROISM SPECTROSCOPY; CONFOCAL MICROSCOPY; DICHROISM; ORGANIC ACIDS; PROTEINS;

HYDROPHOBICITY;

AMPHOPHILE; ARGININE; CANNABINOID 1 RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLUTAMINE; LEUCINE; MEMBRANE PROTEIN; MUTANT PROTEIN; PHENYLALANINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE INSERTION; HUMAN; HUMAN CELL; HYDROPHILICITY; HYDROPHOBICITY; ISOTHERM; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; BINDING SITES; CELL LINE; CIRCULAR DICHROISM; HUMANS; HYDROPHOBICITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; RECEPTOR, CANNABINOID, CB1; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 74949128254     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901619r     Document Type: Article

References (47)

1. Howlett, A. C., Barth, F., Bonner, T. I., Cabral, G., Casellas, P., Devane, W. A., Felder, C. C., Herkenham, M., Mackie, K., Martin, B. R., Mechoulam, R., and Pertwee, R. G. (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol. Rev. 54, 161-202.
2. Glass, M., and Felder, C. C. (1997) Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors augments cAMP accumulation in striatal neurons: Evidence for a Gs linkage to the CB1 receptor. J. Neurosci. 17, 5327-5333.
3. Lauckner, J. E., Hille, B., and Mackie, K. (2005) The cannabinoid agonist WIN55,212-2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 19144-19149.
4. Porter, A. C., and Felder, C. C. (2001) The endocannabinoid nervous system: Unique opportunities for therapeutic intervention. Pharmacol. Ther. 90, 45-60.
5. Gardner, E. L., and Vorel, S. R. (1998) Cannabinoid transmission and reward-related events. Neurobiol. Dis. 5, 502-533.
6. Harkany, T., Guzmán, M., Galve-Roperh, I., Berghuis, P., Devi, L. A., and Mackie, K. (2007) The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol. Sci. 28, 83-92.
7. Kreitzer, A. C., and Regehr, W. G. (2002) Retrograde signaling by endocannabinoids. Curr. Opin. Neurobiol. 12, 324-330.
8. Pertwee, R. G. (2008) Ligands that target cannabinoid receptors in the brain: FromTHCto anandamide and beyond. Addict. Biol. 13, 147-159.
9. Ferguson, S. S. (2001) Evolving concepts in G protein-coupled receptor endocytosis: The role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24.
10. Jin, W., Brown, S., Roche, J. P., Hsieh, C., Celver, J. P., Kovoor, A., Chavkin, C., and Mackie, K. (1999) Distinct domains of the CB1 cannabinoid receptor mediate desensitization and internalization. J. Neurosci. 19, 3773-3780.
11. Wu, D. F., Yang, L. Q., Goschke, A., Stumm, R., Brandenburg, L. O., Liang, Y. J., Höllt, V., and Koch, T. (2008) Role of receptor internalization in the agonist-induced desensitization of cannabinoid type 1 receptors. J. Neurochem. 104, 1132-1143.
12. Hsieh, C., Brown, S., Derleth, C., and Mackie, K. (1999) Internalization and recycling of the CB1 cannabinoid receptor. J. Neurochem. 73, 493-501.
13. Leterrier, C., Bonnard, D., Carrel, D., Rossier, J., and Lenkei, Z. (2004) Constitutive endocytic cycle of the CB1 cannabinoid receptor. J. Biol. Chem. 279, 36013-36021.
14. Martini, L., Waldhoer, M., Pusch, M., Kharazia, V., Fong, J., Lee, J. H., Freissmuth, C., and Whistler, J. L. (2007) Ligand-induced down-regulation of the cannabinoid 1 receptor is mediated by the G-protein-coupled receptor-associated sorting protein GASP1. FASEB J. 21, 802-811.
15. Daigle, T. L., Kwok, M. L., and Mackie, K. (2008) Regulation of CB1 cannabinoid receptor internalization by a promiscuous phosphorylation-dependent mechanism. J. Neurochem. 106, 70-82.
16. Ahn, K. H., Pellegrini, M., Tsomaia, N., Yatawara, A. K., Kendall, D. A., and Mierke, D. F. (2009) Structural analysis of the human cannabinoid receptor one carboxyl-terminus identifies two amphipathic helices. Biopolymers 91, 565-573.
17. Conner, M., Hicks, M. R., Dafforn, T., Knowles, T. J., Ludwig, C., Staddon, S., Overduin, M., Günther, U. L., Thome, J., Wheatley, M., Poyner, D. R., and Conner, A. C. (2008) Functional and biophysical analysis of the C-terminus of the CGRP-receptor: A family B GPCR. Biochemistry 47, 8434-844.
18. Murakami, M., and Kouyama, T. (2008) Crystal structure of squid rhodopsin. Nature 453, 363-367.
19. Delos Santos, N. M., Gardner, L. A., White, S. W., and Bahouth, S. W. (2006) Characterization of the residues in helix 8 of the human β1-adrenergic receptor that are involved in coupling the receptor to G proteins. J. Biol. Chem. 281, 12896-12907.
20. Zhong, M., Navratil, A. M., Clay, C., and Sanborn, B. M. (2004) Residues in the hydrophilic face of putative helix 8 of oxytocin receptor are important for receptor function. Biochemistry 43, 3490-3498.
21. Tetsuka, M., Saito, Y., Imai, K., Doi, H., and Maruyama, K. (2004) The basic residues in the membrane-proximal C-terminal tail of the rat melanin-concentrating hormone receptor 1 are required for receptor function. Endocrinology 145, 3712-3723.
22. Swift, S., Leger, A. J., Talavera, J., Zhang, L., Bohm, A., and Kuliopulos, A. (2006) Role of the PAR1 receptor 8th helix in signaling: The 7-8-1 receptor activation mechanism. J. Biol. Chem. 281, 4109-4116.
23. Oksche, A., Dehe, M., Schülein, R., Wiesner, B., and Rosenthal, W. (1998) Folding and cell surface expression of the vasopressin V2 receptor: Requirement of the intracellular C-terminus. FEBS Lett. 424, 57-62.
24. Duvernay, M. T., Zhou, F., and Wu, G. (2004) A conserved motif for the transport of G protein-coupled receptors from the endoplasmic reticulum to the cell surface. J. Biol. Chem. 279, 30741-30750.
25. Thielen, A., Oueslati, M., Hermosilla, R., Krause, G., Oksche, A., Rosenthal, W., and Schülein, R. (2005) The hydrophobic amino acid residues in the membrane-proximal C tail of the G protein-coupled vasopressin V2 receptor are necessary for transport-competent receptor folding. FEBS Lett. 579, 5227-5235.
26. Chen, C., and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7, 2745-2752.
27. Abadji, V., Lucas-Lenard, J. M., Chin, C., and Kendall, D. A. (1999) Involvement of the carboxyl terminus of the third intracellular loop of the cannabinoid CB1 receptor in constitutive activation of Gs. J. Neurochem. 72, 2032-2038.
28. Murphy, J. W., and Kendall, D. A. (2003) Integrity of extracellular loop 1 of the human cannabinoid receptor 1 is critical for high-affinity binding of the ligand CP 55,940 but not SR 141716A. Biochem. Pharmacol. 65, 1623-1631.
29. Bolte, S., and Cordelières, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232.
30. Rozenfeld, R., and Devi, L. A. (2008) Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J. 22, 2311-2322.
31. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le, T. I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289, 739-745.
32. Jaakola, V. P., Griffith, M. T., Hanson, M. A., Cherezov, V., Chien, E. Y., Lane, J. R., Ijzerman, A. P., and Stevens, R. C. (2008) The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322, 1211-1217.
33. Cherezov, V., Rosenbaum, D. M., Hanson, M. A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., Choi, H. J., Kuhn, P., Weis, W. I., Kobilka, B. K., and Stevens, R. C. (2007) High-resolution crystal structure of an engineered human β2-adrenergic G protein-coupled receptor. Science 318, 1258-1265.
34. Rasmussen, S. G., Choi, H. J., Rosenbaum, D. M., Kobilka, T. S., Thian, F. S., Edwards, P. C., Burghammer, M., Ratnala, V. R., Sanishvili, R., Fischetti, R. F., Schertler, G. F., Weis, W. I., and Kobilka, B. K. (2007) Crystal structure of the human β2 adrenergic G-protein-coupled receptor. Nature 450, 383-387.
35. Rosenbaum, D. M., Cherezov, V., Hanson, M. A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., Choi, H. J., Yao, X. J., Weis, W. I., Stevens, R. C., and Kobilka, B. K. (2007) GPCR engineering yields high-resolution structural insights into β2-adrenergic receptor function. Science 318, 1266-1273.
36. Warne, T., Serrano-Vega, M. J., Baker, J. G., Moukhametzianov, R., Edwards, P. C., Henderson, R., Leslie, A. G., Tate, C. G., and Schertler, G. F. (2008) Structure of a β1-adrenergic G-protein-coupled receptor. Nature 454, 486-491.
37. Marin, E. P., Krishna, A. G., Zvyaga, T. A., Isele, J., Siebert, F., and Sakmar, T. P. (2000) The amino terminus of the fourth cytoplasmic loop of rhodopsin modulates rhodopsin-transducin interaction. J. Biol. Chem. 275, 1930-1936.
38. Bermak, J. C., Li, M., Bullock, C., and Zhou, Q. Y. (2001) Regulation of transport of the dopamine D1 receptor by a new membrane-associated ER protein. Nat. Cell Biol. 3, 492-498.
39. Robert, J., Clauser, E., Petit, P. X., and Ventura,M.A. (2005)Anovel C-terminal motif is necessary for the export of the vasopressin V1b/V3 receptor to the plasma membrane. J. Biol. Chem. 280, 2300-2308.
40. Mukhopadhyay, S., Cowsik, S. M., Lynn, A. M., Welsh, W. J., and Howlett, A. C. (1999) Regulation of Gi by the CB1 cannabinoid receptor C-terminal juxtamembrane region: Structural requirements determined by peptide analysis. Biochemistry 38, 3447-3455.
41. Xie, X. Q., and Chen, J. Z. (2005) NMR structural comparison of the cytoplasmic juxtamembrane domains of G-protein-coupled CB1 and CB2 receptors in membrane mimetic dodecylphosphocholine micelles. J. Biol. Chem. 280, 3605-3612.
42. Choi, G., Guo, J., and Makriyannis, A. (2005) The conformation of the cytoplasmic helix 8 of the CB1 cannabinoid receptor using NMR and circular dichroism. Biochim. Biophys. Acta 1668, 1-9.
43. Grace, C. R., Cowsik, S. M., Shim, J. Y., Welsh, W. J., and Howlett, A. C. (2007) Unique helical conformation of the fourth cytoplasmic loop of the CB1 cannabinoid receptor in a negatively charged environment. J. Struct. Biol. 159, 359-368.
44. Suvorova, E. S., Gripentrog, J. M., Oppermann, M., and Miettinen, H. M. (2008) Role of the carboxyl terminal di-leucine in phosphorylation and internalization of C5a receptor. Biochim. Biophys. Acta 1783, 1261-1270.
45. Duvernay, M. T., Dong, C., Zhang, X., Zhou, F., Nichols, C. D., and Wu, G. (2009) Anterograde trafficking of G protein-coupled receptors: Function of the C-terminal F(X)6LL motif in export from the endoplasmic reticulum. Mol. Pharmacol. 75, 751-761.
46. Mukhopadhyay, S., and Howlett, A. C. (2001) CB1 receptor-G protein association. Subtype selectivity is determined by distinct intracellular domains. Eur. J. Biochem. 268, 499-505.
47. Anavi-Goffer, S., Fleischer, D., Hurst, D. P., Lynch, D. L., Barnett-Norris, J., Shi, S., Lewis, D. L., Mukhopadhyay, S., Howlett, A. C., Reggio, P. H., and Abood, M. E. (2007) Helix 8 Leu in the CB1 cannabinoid receptor contributes to selective signal transduction mechanisms. J. Biol. Chem. 282, 25100-25113.