Activation state of the M3 muscarinic acetylcholine receptor modulates mammalian odorant receptor signaling

Science Signaling

Volumn 4, Issue 155, 2011, Pages

  Li, Yun Rose ^a,b   Matsunami, Hiroaki ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; MUSCARINIC AGENT; MUSCARINIC M3 RECEPTOR; MUSCARINIC RECEPTOR BLOCKING AGENT; PROTEIN DERIVATIVE; RECEPTOR TRANSPORTING PROTEIN 1S; UNCLASSIFIED DRUG; ATROPINE; BENZOFURAN DERIVATIVE; CARBACHOL; CARRIER PROTEIN; CHOLINERGIC RECEPTOR STIMULATING AGENT; CYCLIC AMP; DARIFENACIN; FORSKOLIN; G PROTEIN COUPLED RECEPTOR; IONOMYCIN; IONOPHORE; PYRROLIDINE DERIVATIVE; RTP1 PROTEIN, HUMAN;

ARTICLE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SMELLING; TRANSACTIVATION; CELL STRAIN HEK293; DRUG EFFECT; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; OLFACTORY RECEPTOR; PROTEIN BINDING;

MAMMALIA;

ATROPINE; BENZOFURANS; CARBACHOL; CHOLINERGIC AGONISTS; CYCLIC AMP; FORSKOLIN; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; IONOMYCIN; IONOPHORES; MEMBRANE TRANSPORT PROTEINS; MUSCARINIC ANTAGONISTS; OLFACTORY RECEPTOR NEURONS; PROTEIN BINDING; PYRROLIDINES; RECEPTOR, MUSCARINIC M3; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 78651349003     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2001230     Document Type: Article

References (49)

1. L. Buck, R. Axel, A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell 65, 175-187 (1991).
2. S. Firestein, How the olfactory system makes sense of scents. Nature 413, 211-218 (2001).
3. L. B. Buck, Information coding in the vertebrate olfactory system. Annu. Rev. Neurosci. 19, 517-544 (1996).
4. G. M. Shepherd, Discrimination of molecular signals by the olfactory receptor neuron. Neuron 13, 771-790 (1994).
5. R. R. Reed, Signaling pathways in odorant detection. Neuron 8, 205-209 (1992).
6. D. Lancet, N. Ben-Arie, Olfactory receptors. Curr. Biol. 3, 668-674 (1993).
7. K. Klasen, E. A. Corey, F. Kuck, C. H. Wetzel, H. Hatt, B. W. Ache, Odorant-stimulated phosphoinositide signaling in mammalian olfactory receptor neurons. Cell. Signal. 22, 150-157 (2010).
8. I. Boekhoff, E. Tareilus, J. Strotmann, H. Breer, Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 9, 2453-2458 (1990).
9. B. Malnic, J. Hirono, T. Sato, L. B. Buck, Combinatorial receptor codes for odors. Cell 96, 713-723 (1999).
10. H. Saito, Q. Chi, H. Zhuang, H. Matsunami, J. D. Mainland, Odor coding by a mammalian receptor repertoire. Sci. Signal. 2, ra9 (2009).
11. P. Mombaerts, Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci. 5, 263-278 (2004).
12. L. E. Von Dannecker, A. F. Mercadante, B. Malnic, Ric-8B promotes functional expression of odorant receptors. Proc. Natl. Acad. Sci. U.S.A. 103, 9310-9314 (2006).
13. H. Saito, M. Kubota, R. W. Roberts, Q. Chi, H. Matsunami, RTP family members induce functional expression of mammalian odorant receptors. Cell 119, 679-691 (2004).
14. H. Zhuang, H. Matsunami, Synergism of accessory factors in functional expression of mammalian odorant receptors. J. Biol. Chem. 282, 15284-15293 (2007).
15. D. Krautwurst, K. W. Yau, R. R. Reed, Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95, 917-926 (1998).
16. C. Hague, M. A. Uberti, Z. Chen, C. F. Bush, S. V. Jones, K. J. Ressler, R. A. Hall, K. P. Minneman, Olfactory receptor surface expression is driven by association with the β2-adrenergic receptor. Proc. Natl. Acad. Sci. U.S.A. 101, 13672-13676 (2004).
17. C. F. Bush, S. V. Jones, A. N. Lyle, K. P. Minneman, K. J. Ressler, R. A. Hall, Specificity of olfactory receptor interactions with other G protein-coupled receptors. J. Biol. Chem. 282, 19042-19051 (2007).
18. G. Milligan, G protein-coupled receptor dimerisation: Molecular basis and relevance to function. Biochim. Biophys. Acta 1768, 825-835 (2007).
19. S. C. Prinster, C. Hague, R. A. Hall, Heterodimerization of G protein-coupled receptors: Specificity and functional significance. Pharmacol. Rev. 57, 289-298 (2005).
20. F. H. Marshall, Heterodimerization of G-protein-coupled receptors in the CNS. Curr. Opin. Pharmacol. 1, 40-44 (2001).
21. L. M. Luttrell, Reviews in molecular biology and biotechnology: Transmembrane signaling by G protein-coupled receptors. Mol. Biotechnol. 39, 239-264 (2008).
22. L. Barki-Harrington, L. M. Luttrell, H. A. Rockman, Dual inhibition of β-adrenergic and angiotensin II receptors by a single antagonist: A functional role for receptor-receptor interaction in vivo. Circulation 108, 1611-1618 (2003).
23. M. Chabre, M. le Maire, Monomeric G-protein-coupled receptor as a functional unit. Biochemistry 44, 9395-9403 (2005).
24. S. AbdAlla, H. Lother, U. Quitterer, AT1-receptor heterodimers show enhanced G-protein activation and altered receptor sequestration. Nature 407, 94-98 (2000).
25. J. L. Hansen, J. T. Hansen, T. Speerschneider, C. Lyngsø, N. Erikstrup, E. S. Burstein, D. M. Weiner, T. Walther, N. Makita, T. Iiri, N. Merten, E. Kostenis, S. P. Sheikh, Lack of evidence for AT1R/B2R heterodimerization in COS-7, HEK293, and NIH3T3 cells: How common is the AT1R/B2R heterodimer? J. Biol. Chem. 284, 1831-1839 (2009).
26. F. Y. Zeng, J. Wess, Identification and molecular characterization of m3 muscarinic receptor dimers. J. Biol. Chem. 274, 19487-19497 (1999).
27. J. B. Regard, I. T. Sato, S. R. Coughlin, Anatomical profiling of G protein-coupled receptor expression. Cell 135, 561-571 (2008).
28. S. Katada, T. Nakagawa, H. Kataoka, K. Touhara, Odorant response assays for a heterologously expressed olfactory receptor. Biochem. Biophys. Res. Commun. 305, 964-969 (2003).
29. H. Zhuang, H. Matsunami, Evaluating cell-surface expression and measuring activation of mammalian odorant receptors in heterologous cells. Nat. Protoc. 3, 1402-1413 (2008).
30. S. D. Liberles, L. B. Buck, A second class of chemosensory receptors in the olfactory epithelium. Nature 442, 645-650 (2006).
31. J. M. Lundberg, A. Anggård, P. Emson, J. Fahrenkrug, T. Hokfelt, Vasoactive intestinal polypeptide and cholinergic mechanisms in cat nasal mucosa: Studies on choline acetyltransferase and release of vasoactive intestinal polypeptide. Proc. Natl. Acad. Sci. U.S.A. 78, 5255-5259 (1981).
32. J. N. Baraniuk, S. J. Merck, Neuroregulation of human nasal mucosa. Ann. N. Y. Acad. Sci. 1170, 604-609 (2009).
33. B. Hedlund, G. M. Shepherd, Biochemical studies on muscarinic receptors in the salamander olfactory epithelium. FEBS Lett. 162, 428-431 (1983).
34. D. A. Wilson, M. L. Fletcher, R. M. Sullivan, Acetylcholine and olfactory perceptual learning. Learn. Mem. 11, 28-34 (2004).
35. S. Firestein, G. M. Shepherd, Neurotransmitter antagonists block some odor responses in olfactory receptor neurons. Neuroreport 3, 661-664 (1992).
36. H. E. Hamm, How activated receptors couple to G proteins. Proc. Natl. Acad. Sci. U.S.A. 98, 4819-4821 (2001).
37. Y. Liang, D. Fotiadis, S. Filipek, D. A. Saperstein, K. Palczewski, A. Engel, Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem. 278, 21655-21662 (2003).
38. H. Nakata, K. Yoshioka, T. Kamiya, Purinergic-receptor oligomerization: Implications for neural functions in the central nervous system. Neurotox. Res. 6, 291-297 (2004).
39. L. J. Brunet, G. H. Gold, J. Ngai, General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17, 681-693 (1996).
40. G. V. Ronnett, H. Cho, L. D. Hester, S. F. Wood, S. H. Snyder, Odorants differentially enhance phosphoinositide turnover and adenylyl cyclase in olfactory receptor neuronal cultures. J. Neurosci. 13, 1751-1758 (1993).
41. H. Breer, I. Boekhoff, J. Krieger, K. Raming, J. Strotmann, E. Tareilus, Molecular mechanisms of olfactory signal transduction. Soc. Gen. Physiol. Ser. 47, 93-108 (1992).
42. T. Miyamoto, D. Restrepo, E. J. Cragoe Jr., J. H. Teeter, IP3- and cAMP-induced responses in isolated olfactory receptor neurons from the channel catfish. J. Membr. Biol. 127, 173-183 (1992).
43. D. T. Jones, R. R. Reed, Molecular cloning of five GTP-binding protein cDNA species from rat olfactory neuroepithelium. J. Biol. Chem. 262, 14241-14249 (1987).
44. A. Berghard, L. B. Buck, Sensory transduction in vomeronasal neurons: Evidence for Gao, Gai2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J. Neurosci. 16, 909-918 (1996).
45. T. Sato, J. Hirono, M. Tonoike, M. Takebayashi, Tuning specificities to aliphatic odorants in mouse olfactory receptor neurons and their local distribution. J. Neurophysiol. 72, 2980-2989 (1994).
46. Y. Ishimaru, H. Inada, M. Kubota, H. Zhuang, M. Tominaga, H. Matsunami, Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc. Natl. Acad. Sci. U.S.A. 103, 12569-12574 (2006).
47. T. M. Wolever, D. J. Jenkins, A. L. Jenkins, R. G. Josse, The glycemic index: Methodology and clinical implications. Am. J. Clin. Nutr. 54, 846-854 (1991).
48. D. W. Laird, R. S. Molday, Evidence against the role of rhodopsin in rod outer segment binding to RPE cells. Invest. Ophthalmol. Vis. Sci. 29, 419-428 (1988).
49. Acknowledgments: We thank our lab members, particularlyW.-L. L. Liu and A. Toyama, for technical assistance. We are also grateful to R. Roberts for his assistance with image analysis. We thank J. Wess for advice, M. Cook (Duke Cancer Center) for FACS (fluorescence-activated cell sorting), and J. Coers for the plate reader. Funding: This work is supported by grants from NIH (DC005782) and the Human Frontier Science Program, as well as by the Duke University Department of Chemistry and Undergraduate Research Support Office. Author contributions: Y.R.L. and H.M. conceived the idea, conducted the experiments, analyzed the data, and wrote the paper. Competing interests: The authors plan to submit a patent application relevant to the work.