Ligand-selective activation of heterologously-expressed mammalian olfactory receptor

Cell Calcium

Volumn 56, Issue 4, 2014, Pages 245-256

  Ukhanov, K ^a   Bobkov, Y ^a   Corey, E A ^a   Ache, B W ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Biased signaling; Functional assay; HEK293T; MOR EG; Olfactory receptor; Olfr73

Indexed keywords

4 ETHYLGUAIACOL; 4 PROPYLGUAIACOL; 4 VINYLGUAIACOL; ACETYL EUGENOL; ADENYLATE CYCLASE; CYCLIC NUCLEOTIDE GATED CHANNEL; ETHYL VANILLIN; EUGENOL; FORSKOLIN; G PROTEIN COUPLED RECEPTOR; ISOEUGENOL; METHYL EUGENOL; ORIVONE; PHOSPHOLIPASE C; POLYFUNCTIONAL GROUP; UNCLASSIFIED DRUG; VANILLIN; CALCIUM; CYCLIC AMP; EUGENOL-RESPONSIVE OLFACTORY RECEPTOR, MOUSE; LIGAND; OLFACTORY RECEPTOR;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CHEMICAL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; EVOKED RESPONSE; EXTRACELLULAR CALCIUM; GENE EXPRESSION SYSTEM; HUMAN; HUMAN CELL; LIGAND BINDING; MACULA DENSA; MOUSE; NONHUMAN; OLFACTORY RECEPTOR; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HETEROZYGOTE; MAMMAL; METABOLISM; PHYSIOLOGY;

ADENYLATE CYCLASE; ANIMALS; CALCIUM; CYCLIC AMP; GENE EXPRESSION; HETEROZYGOTE; HUMANS; LIGANDS; MAMMALS; MICE; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION; TYPE C PHOSPHOLIPASES;

EID: 85013706221     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.07.012     Document Type: Article

References (48)

1. Fisher A., Heldman E., Gurwitz D., Haring R., Barak D., Meshulam H., Marciano D., Brandeis R., Pittel Z., Segal M., et al. Selective signaling via unique M1 muscarinic agonists. Ann. N. Y. Acad. Sci. 1993, 695:300-303.
2. Gurwitz D., Haring R., Heldman E., Fraser C.M., Manor D., Fisher A. Discrete activation of transduction pathways associated with acetylcholine m1 receptor by several muscarinic ligands. Eur. J. Pharmacol. 1994, 267:21-31.
3. Kenakin T. Agonist-receptor efficacy. I: Mechanisms of efficacy and receptor promiscuity. Trends Pharmacol. Sci. 1995, 16:188-192.
4. Zocher M., Fung J.J., Kobilka B.K., Muller D.J. Ligand-specific interactions modulate kinetic, energetic, and mechanical properties of the human beta2 adrenergic receptor. Structure 2012, 20:1391-1402.
5. Kenakin T.P. Biased signalling and allosteric machines: new vistas and challenges for drug discovery. Br. J. Pharmacol. 2012, 165:1659-1669.
6. Gonzalez-Maeso J., Sealfon S.C. Functional selectivity in GPCR heterocomplexes. Mini Rev. Med. Chem. 2012, 12:851-855.
7. Woehler A., Ponimaskin E.G. G protein-mediated signaling: same receptor, multiple effectors. Curr. Mol. Pharmacol. 2009, 2:237-248.
8. Shenoy S.K., Lefkowitz R.J. beta-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol. Sci. 2011, 32:521-533.
9. Dolphin A.C. G protein modulation of voltage-gated calcium channels. Pharmacol. Rev. 2003, 55:607-627.
10. Altier C. GPCR and voltage-gated calcium channels (VGCC) signaling complexes. Subcell. Biochem. 2012, 63:241-262.
11. Doupnik C.A. GPCR-Kir channel signaling complexes: defining rules of engagement. J. Recept. Signal Transduct. Res. 2008, 28:83-91.
12. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 1991, 65:175-187.
13. Spehr M., Wetzel C.H., Hatt H., Ache B.W. 3-phosphoinositides modulate cyclic nucleotide signaling in olfactory receptor neurons. Neuron 2002, 33:731-739.
14. Ukhanov K., Bobkov Y., Ache B.W. Imaging ensemble activity in arthropod olfactory receptor neurons in situ. Cell Calcium 2011, 49:100-107.
15. Ukhanov K., Corey E.A., Brunert D., Klasen K., Ache B.W. Inhibitory odorant signaling in mammalian olfactory receptor neurons. J. Neurophysiol. 2010, 103:1114-1122.
16. Shirokova E., Schmiedeberg K., Bedner P., Niessen H., Willecke K., Raguse J.D., Meyerhof W., Krautwurst D. Identification of specific ligands for orphan olfactory receptors. G protein-dependent agonism and antagonism of odorants. J. Biol. Chem. 2005, 280:11807-11815.
17. Zhuang H., Matsunami H. Evaluating cell-surface expression and measuring activation of mammalian odorant receptors in heterologous cells. Nat. Protoc. 2008, 3:1402-1413.
18. Katada S., Nakagawa T., Kataoka H., Touhara K. Odorant response assays for a heterologously expressed olfactory receptor. Biochem. Biophys. Res. Commun. 2003, 305:964-969.
19. Lu M., Staszewski L., Echeverri F., Xu H., Moyer B.D. Endoplasmic reticulum degradation impedes olfactory G-protein coupled receptor functional expression. BMC Cell Biol. 2004, 5:34.
20. Krautwurst D., Yau K.W., Reed R.R. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 1998, 95:917-926.
21. Katada S., Hirokawa T., Oka Y., Suwa M., Touhara K. Structural basis for a broad but selective ligand spectrum of a mouse olfactory receptor: mapping the odorant-binding site. J. Neurosci. 2005, 25:1806-1815.
22. Baud O., Etter S., Spreafico M., Bordoli L., Schwede T., Vogel H., Pick H. The mouse eugenol odorant receptor: structural and functional plasticity of a broadly tuned odorant binding pocket. Biochemistry 2011, 50:843-853.
23. Cheng Z., Garvin D., Paguio A., Stecha P., Wood K., Fan F. Luciferase reporter assay system for deciphering GPCR pathways. Curr. Chem. Genomics 2010, 4:84-91.
24. Frings S., Seifert R., Godde M., Kaupp U.B. Profoundly different calcium permeation and blockage determine the specific function of distinct cyclic nucleotide-gated channels. Neuron 1995, 15:169-179.
25. Rich T.C., Tse T.E., Rohan J.G., Schaack J., Karpen J.W. In vivo assessment of local phosphodiesterase activity using tailored cyclic nucleotide-gated channels as cAMP sensors. J. Gen. Physiol. 2001, 118:63-78.
26. Pluznick J.L., Zou D.J., Zhang X., Yan Q., Rodriguez-Gil D.J., Eisner C., Wells E., Greer C.A., Wang T., Firestein S., Schnermann J., Caplan M.J. Functional expression of the olfactory signaling system in the kidney. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2059-2064.
27. Oka Y., Omura M., Kataoka H., Touhara K. Olfactory receptor antagonism between odorants. EMBO J. 2004, 23:120-126.
28. Abaffy T., Matsunami H., Luetje C.W. Functional analysis of a mammalian odorant receptor subfamily. J. Neurochem. 2006, 97:1506-1518.
29. Liu Y., Bakshi K., Zavalij P., Doyle M.P. Pericyclic reaction of a zwitterionic salt of an enedione-diazoester. A novel strategy for the synthesis of highly functionalized resorcinols. Org. Lett. 2010, 12:4304-4307.
30. Kajiya K., Inaki K., Tanaka M., Haga T., Kataoka H., Touhara K. Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci. 2001, 21:6018-6025.
31. Galandrin S., Bouvier M. Distinct signaling profiles of beta1 and beta2 adrenergic receptor ligands toward adenylyl cyclase and mitogen-activated protein kinase reveals the pluridimensionality of efficacy. Mol. Pharmacol. 2006, 70:1575-1584.
32. Kostenis E. Is Galpha16 the optimal tool for fishing ligands of orphan G-protein-coupled receptors?. Trends Pharmacol. Sci. 2001, 22:560-564.
33. Hamana H., Shou-xin L., Breuils L., Hirono J., Sato T. Heterologous functional expression system for odorant receptors. J. Neurosci. Methods 2010, 185:213-220.
34. Hill S.J., Williams C., May L.T. Insights into GPCR pharmacology from the measurement of changes in intracellular cyclic AMP; advantages and pitfalls of differing methodologies. Brit. J. Pharmacol. 2010, 161:1266-1275.
35. Vauquelin G. Determination of drug-receptor residence times by radioligand binding and functional assays: experimental strategies and physiological relevance. Medchemcomm 2012, 3:645-651.
36. Charlton S.J., Vauquelin G. Elusive equilibrium: the challenge of interpreting receptor pharmacology using calcium assays. Brit. J. Pharmacol. 2010, 161:1250-1265.
37. Gesty-Palmer D., Chen M., Reiter E., Ahn S., Nelson C.D., Wang S., Eckhardt A.E., Cowan C.L., Spurney R.F., Luttrell L.M., Lefkowitz R.J. Distinct beta-arrestin- and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation. J. Biol. Chem. 2006, 281:10856-10864.
38. Abou-Samra A.B., Juppner H., Force T., Freeman M.W., Kong X.F., Schipani E., Urena P., Richards J., Bonventre J.V., Potts J.T., et al. Expression cloning of a common receptor for parathyroid hormone and parathyroid hormone-related peptide from rat osteoblast-like cells: a single receptor stimulates intracellular accumulation of both cAMP and inositol trisphosphates and increases intracellular free calcium. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:2732-2736.
39. Visegrady A., Boros A., Nemethy Z., Kiss B., Keseru G.M. Application of the BD ACTOne (TM) technology for the high-throughput screening of G(s)-coupled receptor antagonists. J. Biomol. Screen. 2007, 12:1068-1073.
40. Berridge M.J. Cardiac calcium signalling. Biochem. Soc. Trans. 2003, 31:930-933.
41. Feinstein W.P., Zhu B., Leavesley S.J., Sayner S.L., Rich T.C. Assessment of cellular mechanisms contributing to cAMP compartmentalization in pulmonary microvascular endothelial cells. Am. J. Physiol. Cell Physiol. 2012, 302:C839-C852.
42. Kenakin T., Christopoulos A. Signalling bias in new drug discovery: detection, quantification and therapeutic impact. Nat. Rev. Drug Discov. 2013, 12:205-216.
43. Repicky S.E., Luetje C.W. Molecular receptive range variation among mouse odorant receptors for aliphatic carboxylic acids. J. Neurochem. 2009, 109:193-202.
44. Katada S., Tanaka M., Touhara K. Structural determinants for membrane trafficking and G protein selectivity of a mouse olfactory receptor. J. Neurochem. 2004, 90:1453-1463.
45. Kato A., Katada S., Touhara K. Amino acids involved in conformational dynamics and G protein coupling of an odorant receptor: targeting gain-of-function mutation. J. Neurochem. 2008, 107:1261-1270.
46. Wisler J.W., Xiao K., Thomsen A.R., Lefkowitz R.J. Recent developments in biased agonism. Curr. Opin. Cell Biol. 2014, 27:18-24.
47. Luttrell L.M. Minireview, More than just a hammer: ligand bias and pharmaceutical discovery. Mol. Endocrinol. 2014, 28:281-294.
48. Ukhanov K., Corey E.A., Ache B.W. Phosphoinositide 3-kinase dependent inhibition as a broad basis for opponent coding in mammalian olfactory receptor neurons. PLoS ONE 2013, 8:e61553.