Agonist activation of the G protein-coupled receptor GPR35 involves transmembrane domain III and is transduced via Gα 13 and β-arrestin-2

British Journal of Pharmacology

Volumn 162, Issue 3, 2011, Pages 733-748

  Jenkins, Laura ^a   Alvarez Curto, Elisa ^a   Campbell, Kate ^a   De Munnik, Sabrina ^a   Canals, Meritxell ^a   Schlyer, Sabine ^b   Milligan, Graeme ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b BOEHRINGER INGELHEIM PHARMACEUTICALS INC   (United States)

Author keywords

G protein coupled receptor; GPR35; kynurenic acid; species orthologues; zaprinast

Indexed keywords

ALANINE; ARGININE; BETA ARRESTIN 2; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 35; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA13; KYNURENIC ACID; TYROSINE; UNCLASSIFIED DRUG; ZAPRINAST;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CELL MEMBRANE; CELL STRAIN HEK293; CELL SURFACE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTERNALIZATION; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ANIMALS; ARRESTINS; BIOLOGICAL ASSAY; CELLS, CULTURED; COLON; EXCITATORY AMINO ACID ANTAGONISTS; GANGLIA, SPINAL; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HUMANS; KYNURENIC ACID; PHOSPHODIESTERASE INHIBITORS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PURINONES; RATS; RECEPTORS, G-PROTEIN-COUPLED; TRANSFECTION;

EID: 78649881120     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.01082.x     Document Type: Article

References (48)

1. Ballesteros JA, Weinstein H, (1995). Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G-protein coupled receptors. Methods Neurosci 25: 366-428.
2. Barth MC, Ahluwalia N, Anderson TJ, Hardy GJ, Sinha S, Alvarez-Cardona JA, et al. (2009). Kynurenic acid triggers firm arrest of leukocytes to vascular endothelium under flow conditions. J Biol Chem 284: 19189-19195.
3. Brown AJ, (2007). Novel cannabinoid receptors. Br J Pharmacol 152: 567-575.
4. Burt AR, Carr IC, Mullaney I, Anderson NG, Milligan G, (1996). Agonist activation of p42 and p44 mitogen-activated protein kinases following expression of the mouse delta opioid receptor in Rat-1 fibroblasts: effects of receptor expression levels and comparisons with G-protein activation. Biochem J 320: 227-235.
5. Canals M, Milligan G, (2008). Constitutive activity of the cannabinoid CB1 receptor regulates the function of co-expressed Mu opioid receptors. J Biol Chem 283: 11424-11434.
6. Canals M, Jenkins L, Kellett E, Milligan G, (2006). Up-regulation of the angiotensin II type 1 receptor by the MAS proto-oncogene is due to constitutive activation of Gq/G11 by MAS. J Biol Chem 281: 16757-16767.
7. Corbin JD, Francis SH, (2002). Pharmacology of phosphodiesterase-5 inhibitors. Int J Clin Pract 56: 453-459.
8. Emkey R, Rankl NB, (2009). Screening G protein-coupled receptors: measurement of intracellular calcium using the fluorometric imaging plate reader. Methods Mol Biol 565: 145-158.
9. Fredriksson R, Schioth HB, (2005). The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol Pharmacol 67: 1414-1425.
10. Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB, (2003). The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 63: 1256-1272.
11. Grigoriadis DE, Hoare SR, Lechner SM, Slee DH, Williams JA, (2009). Drugability of extracellular targets: discovery of small molecule drugs targeting allosteric, functional, and subunit-selective sites on GPCRs and ion channels. Neuropsychopharmacology 34: 106-125.
12. Hamdan FF, Audet M, Garneau P, Pelletier J, Bouvier M, (2005). High-throughput screening of G protein-coupled receptor antagonists using a bioluminescence resonance energy transfer 1-based beta-arrestin2 recruitment assay. J Biomol Screen 10: 463-475.
13. Harmar AJ, Hills RA, Rosser EM, Jones M, Buneman OP, Dunbar DR, et al. (2009). IUPHAR-DB: the IUPHAR database of G protein-coupled receptors and ion channels. Nucleic Acids Res 37: D680-D685.
14. Kenakin T, (2007). Functional selectivity through protean and biased agonism: who steers the ship? Mol Pharmacol 72: 1393-1401.
15. Kocan M, Pfleger KD, (2009). Detection of GPCR/beta-arrestin interactions in live cells using bioluminescence resonance energy transfer technology. Methods Mol Biol 552: 305-117.
16. Kostenis E, Waelbroeck M, Milligan G, (2005). Techniques: promiscuous Galpha proteins in basic research and drug discovery. Trends Pharmacol Sci 26: 595-602.
17. Kuc D, Zgrajka W, Parada-Turska J, Urbanik-Sypniewska T, Turski WA, (2008). Micromolar concentration of kynurenic acid in rat small intestine. Amino Acids 35: 503-505.
18. Lane JR, Henderson D, Powney B, Wise A, Rees S, Daniels D, et al. (2008). Antibodies that identify only the active conformation of G(i) family G protein alpha subunits. FASEB J 22: 1924-1932.
19. van der Lee MM, Blomenrohr M, van der Doelen AA, Wat JW, Smits N, Hanson BJ, et al. (2009). Pharmacological characterization of receptor redistribution and beta-arrestin recruitment assays for the cannabinoid receptor 1. J Biomol Screen 14: 811-823.
20. Leonard J, Chu ZL, Unett DJ, Gatlin JE, Gaidarov I, Qui J, et al. (2005). GPR35 and modulators thereof for the treatment of metabolic-related disorders. World Intellectual Property Organization Patent WO 2005/119252 A2.
21. Liu C, Wu J, Zhu J, Kuei C, Yu J, Shelton J, et al. (2009). Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81. J Biol Chem 284: 2811-2822.
22. Lorenz WW, McCann RO, Longiaru M, Cormier MJ, (1991). Isolation and expression of a cDNA encoding Renilla reniformis luciferase. Proc Natl Acad Sci USA 88: 4438-4442.
23. Lundstrom K, (2009). An overview on GPCRs and drug discovery: structure-based drug design and structural biology on GPCRs. Methods Mol Biol 552: 51-66.
24. Marchese A, Paing MM, Temple BR, Trejo J, (2008). G protein-coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol 48: 601-629.
25. Milligan G, (2003). Principles: extending the utility of [35S]GTP gamma S binding assays. Trends Pharmacol Sci 24: 87-90.
26. Milligan G, Rees S, (1999). Chimaeric G alpha proteins: their potential use in drug discovery. Trends Pharmacol Sci 20: 118-124.
27. Milligan G, Stoddart LA, Smith NJ, (2009). Agonism and allosterism: the pharmacology of the free fatty acid receptors FFA2 and FFA3. Br J Pharmacol 158: 146-153.
28. Moore CA, Milano SK, Benovic JL, (2007). Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 69: 451-482.
29. Nevalainen T, Irving AJ, (2010). GPR55, a lysophosphatidylinositol receptor with cannabinoid sensitivity? Curr Top Med Chem 10: 799-813.
30. Noguchi K, Ishii S, Shimizu T, (2003). Identification of p2y9/GPR23 as a novel G protein-coupled receptor for lysophosphatidic acid, structurally distant from the Edg family. J Biol Chem 278: 25600-25606.
31. O'Dowd BF, Nguyen T, Marchese A, Cheng R, Lynch KR, Heng HH, et al. (1998). Discovery of three novel G-protein-coupled receptor genes. Genomics 47: 310-313.
32. Ohshiro H, Tonai-Kachi H, Ichikawa K, (2008). GPR35 is a functional receptor in rat dorsal root ganglion neurons. Biochem Biophys Res Commun 365: 344-348.
33. Okumura S, Baba H, Kumada T, Nanmoku K, Nakajima H, Nakane Y, et al. (2004). Cloning of a G-protein-coupled receptor that shows an activity to transform NIH3T3 cells and is expressed in gastric cancer cells. Cancer Sci 95: 131-135.
34. Paluszkiewicz P, Zgrajka W, Saran T, Schabowski J, Piedra JL, Fedkiv O, et al. (2009). High concentration of kynurenic acid in bile and pancreatic juice. Amino Acids 37: 637-641.
35. Pfleger KD, Dalrymple MB, Dromey JR, Eidne KA, (2007). Monitoring interactions between G-protein-coupled receptors and beta-arrestins. Biochem Soc Trans 35: 764-766.
36. Ryberg E, Larsson N, Sjogren S, Hjorth S, Hermansson NO, Leonova J, et al. (2007). The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 152: 1092-1101.
37. Smith NJ, Stoddart LA, Devine NM, Jenkins L, Milligan G, (2009). The action and mode of binding of thiazolidinedione ligands at free fatty acid receptor 1. J Biol Chem 284: 17527-17539.
38. Stoddart LA, Smith NJ, Jenkins L, Brown AJ, Milligan G, (2008a). Conserved polar residues in transmembrane domains V, VI, and VII of free fatty acid receptor 2 and free fatty acid receptor 3 are required for the binding and function of short chain fatty acids. J Biol Chem 283: 32913-32924.
39. Stoddart LA, Smith NJ, Milligan G, (2008b). International Union of Pharmacology. LXXI. Free fatty acid receptors FFA1,-2, and-3: pharmacology and pathophysiological functions. Pharmacol Rev 60: 405-417.
40. Stone TW, Darlington LG, (2002). Endogenous kynurenines as targets for drug discovery and development. Nat Rev Drug Discov 1: 609-620.
41. Taniguchi Y, Tonai-Kachi H, Shinjo K, (2006). Zaprinast, a well-known cyclic guanosine monophosphate-specific phosphodiesterase inhibitor, is an agonist for GPR35. FEBS Lett 580: 5003-5008.
42. Tunaru S, Lattig J, Kero J, Krause G, Offermanns S, (2005). Characterization of determinants of ligand binding to the nicotinic acid receptor GPR109A (HM74A/PUMA-G). Mol Pharmacol 68: 1271-1280.
43. Wang J, Simonavicius N, Wu X, Swaminath G, Reagan J, Tian H, et al. (2006). Kynurenic acid as a ligand for orphan G protein-coupled receptor GPR35. J Biol Chem 281: 22021-22028.
44. Williams C, Hill SJ, (2009). GPCR signaling: understanding the pathway to successful drug discovery. Methods Mol Biol 552: 39-50.
45. Worzfeld T, Wettschureck N, Offermanns S, (2008). G(12)/G(13)-mediated signalling in mammalian physiology and disease. Trends Pharmacol Sci 29: 582-589.
46. Xiao SH, Reagan JD, Lee PH, Fu A, Schwandner R, Zhao X, et al. (2008). High throughput screening for orphan and liganded GPCRs. Comb Chem High Throughput Screen 11: 195-215.
47. Yang Y, Lu JY, Wu X, Summer S, Whoriskey J, Saris C, et al. (2010). G-protein-coupled receptor 35 is a target of the asthma drugs cromolyn disodium and nedocromil sodium. Pharmacology 86: 1-5.
48. Yin H, Chu A, Li W, Wang B, Shelton F, Otero F, et al. (2009). Lipid G protein-coupled receptor ligand identification using beta-arrestin PathHunter assay. J Biol Chem 284: 12328-12338.