Exchanging ligand-binding specificity between a pair of mouse olfactory receptor paralogs reveals odorant recognition principles

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Baud, Olivia ^a   Yuan, Shuguang ^a   Veya, Luc ^a   Filipek, Slawomir ^b   Vogel, Horst ^a   Pick, Horst ^a  

^a EPFL   (Switzerland)

^b UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; BENZALDEHYDE DERIVATIVE; CYCLOPENTANE DERIVATIVE; ETHYL VANILLIN; FASCIN1 PROTEIN, MOUSE; FRAGRANCE; G PROTEIN COUPLED RECEPTOR; ISOPROTEIN; JASMONE; LIGAND; NOOTKATONE; OLFACTORY RECEPTOR; ORGANIC COMPOUND; OXYLIPIN; ROSE-OXIDE; SESQUITERPENE; TERPENE;

ANIMAL; BINDING COMPETITION; BINDING SITE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR DYNAMICS; MOUSE; ODOR; OLFACTORY RECEPTOR; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

ANIMALS; BENZALDEHYDES; BINDING SITES; BINDING, COMPETITIVE; CELL LINE; CYCLOPENTANES; LIGANDS; MICE; MICROFILAMENT PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; MONOTERPENES; MUTAGENESIS, SITE-DIRECTED; ODORANTS; ORGANIC CHEMICALS; OXYLIPINS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, ODORANT; SESQUITERPENES; SMELL;

EID: 84943593147     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14948     Document Type: Article

References (47)

1. Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175-187 (1991).
2. Zhang, X. M. & Firestein, S. The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 5, 124-133 (2002).
3. Malnic, B., Godfrey, P. A. & Buck, L. B. The human olfactory receptor gene family. Proc. Natl. Acad. Sci. USA 101, 2584-2589 (2004).
4. Zozulya, S., Echeverri, F. & Nguyen, T. The human olfactory receptor repertoire. Genome Biol 2, RESEARCH0018 (2001).
5. Mori, K. The olfactory system: from odor molecules to motivational behaviors. Springer. Japan, Tokyo (2014).
6. Sell, C. S. Chemistry and the sense of smell. Wiley. New Jersey (2014).
7. Kraft, P., Bajgrowicz, J. A., Denis, C. & Frater, G. Odds and Trends: Recent Developments in the Chemistry of Odorants. Angew. Chem. Int. Ed. Engl. 39, 2980-3010 (2000).
8. Firestein, S. How the olfactory system makes sense of scents. Nature 413, 211-218 (2001).
9. Reed, R. R. After the holy grail: Establishing a molecular basis for mammalian olfaction. Cell 116, 329-336 (2004).
10. Serizawa, S. et al. Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302, 2088-2094 (2003).
11. Malnic, B., Hirono, J., Sato, T. & Buck, L. B. Combinatorial receptor codes for odors. Cell 96, 713-723 (1999).
12. Lu, M., Echeverri, F. & Moyer, B. D. Endoplasmic reticulum retention, degradation, and aggregation of olfactory G-protein coupled receptors. Traffic 4, 416-433 (2003).
13. Bozza, T., Feinstein, P., Zheng, C. & Mombaerts, P. Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22, 3033-3043 (2002).
14. Araneda, R. C., Peterlin, Z., Zhang, X., Chesler, A. & Firestein, S. A. pharmacological profile of the aldehyde receptor repertoire in rat olfactory epithelium. J. Physiol. 555, 743-756 (2004).
15. Jacquier, V., Pick, H. & Vogel, H. Characterization of an extended receptive ligand repertoire of the human olfactory receptor OR17-40 comprising structurally related compounds. J. Neurochem. 97, 537-544 (2006).
16. Abaffy, T., Malhotra, A. & Luetje, C. W. The molecular basis for ligand specificity in a mouse olfactory receptor-A network of functionally important residues. J. Biol. Chem. 282, 1216-1224 (2007).
17. Grosmaitre, X. et al. SR1, a mouse odorant receptor with an unusually broad response profile. J. Neurosci. 29, 14545-14552 (2009).
18. Baud, O. et al. The Mouse Eugenol Odorant Receptor: Structural and Functional Plasticity of a Broadly Tuned Odorant Binding Pocket. Biochemistry 50, 843-853 (2011).
19. 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. 25, 1806-1815 (2005).
20. Abaffy, T., Matsunami, H. & Luetje, C. W. Functional analysis of a mammalian odorant receptor subfamily. J. Neurochem. 97, 1506-1518 (2006).
21. Man, O., Gilad, Y. & Lancet, D. Prediction of the odorant binding site of olfactory receptor proteins by human-mouse comparisons. Prot. Sci. 13, 240-254 (2004).
22. Schmiedeberg, K. et al. Structural determinants of odorant recognition by the human olfactory receptors OR1A1 and OR1A2. J. Struct. Biol. 159, 400-412 (2007).
23. Kajiya, K. et al. Molecular bases of odor discrimination: Reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci. 21, 6018-6025 (2001).
24. Rasmussen, S. G. et al. Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 477, 549-555 (2011).
25. Nygaard, R. et al. The dynamic process of beta(2)-adrenergic receptor activation. Cell 152, 532-542 (2013).
26. Yuan, S. G., Filipek, S., Palczewski, K. & Vogel, H. Activation of G-protein-coupled receptors correlates with the formation of a continuous internal water pathway. Nat. Commun. 5 (2014).
27. Doszczak, L. et al. Prediction of perception: probing the hOR17-4 olfactory receptor model with silicon analogues of bourgeonal and lilial. Angew. Chem. Int. Ed. Engl. 46, 3367-3371 (2007).
28. Brockhoff, A., Behrens, M., Niv, M. Y. & Meyerhof, W. Structural requirements of bitter taste receptor activation. Proc. Natl. Acad. Sci. USA. 107, 11110-11115 (2010).
29. Saito, H., Kubota, M., Roberts, R. W., Chi, Q. & Matsunami, H. RTP family members induce functional expression of mammalian odorant receptors. Cell 119, 679-691 (2004).
30. Zhuang, H. & Matsunami, H. Synergism of accessory factors in functional expression of mammalian odorant receptors. J. Biol. Chem. 282, 15284-15293 (2007).
31. Katada, S., Nakagawa, T., Kataoka, H. & Touhara, K. Odorant response assays for a heterologously expressed olfactory receptor. Biochem. Biophys. Res. Commun. 305, 964-969 (2003).
32. Adipietro, K. A., Mainland, J. D. & Matsunami, H. Functional Evolution of Mammalian Odorant Receptors. Plos Genetics 8 (2012).
33. Krautwurst, D., Yau, K. W. & Reed, R. R. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95, 917-926 (1998).
34. Kaupp, U. B. Olfactory signalling in vertebrates and insects: differences and commonalities. Nat. Rev. Neurosci. 11, 188-200 (2010).
35. Ostrom, R. S. et al. Localization of adenylyl cyclase Isoforms and G protein-coupled receptors in vascular smooth muscle cells: Expression in caveolin-rich and noncaveolin domains. Mol. Pharmacol. 62, 983-992 (2002).
36. Halgren, T. A. Identifying and characterizing binding sites and assessing druggability. J. Chem. Inf. Model. 49, 377-389 (2009).
37. Yuan, S., Vogel, H. & Filipek, S. The role of water and sodium ions in the activation of the mu-opioid receptor. Angew. Chem. Int. Ed. Engl. 52, 10112-10115 (2013).
38. Yuan, S., Hu, Z., Filipek, S. & Vogel, H. W246(6.48) opens a gate for a continuous intrinsic water pathway during activation of the adenosine A2A receptor. Angew. Chem. Int. Ed. Engl. 54, 556-559 (2015).
39. Standfuss, J. et al. The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471, 656-660 (2011).
40. Kahsai, A. W. et al. Multiple ligand-specific conformations of the beta2-adrenergic receptor. Nat. chem. biol. 7, 692-700 (2011).
41. Eswar, N. et al. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics/editoral board, Andreas D. Baxevanis⋯ [et al.] Chapter 5, Unit 5 6 (2006).
42. Wacker, D. et al. Conserved binding mode of human beta2 adrenergic receptor inverse agonists and antagonist revealed by X-ray crystallography. J. Am. Chem. Soc. 132, 11443-11445 (2010).
43. Thompson, J. D., Gibson, T. J. & Higgins, D. G. Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics/editoral board, Andreas D. Baxevanis⋯ [et al.] Chapter 2, Unit 2 3 (2002).
44. Lomize, M. A., Lomize, A. L., Pogozheva, I. D. & Mosberg, H. I. OPM: orientations of proteins in membranes database. Bioinformatics 22, 623-625 (2006).
45. Guo, Z. et al. Probing the alpha-helical structural stability of stapled p53 peptides: molecular dynamics simulations and analysis. Chem. Biol. Drug Des. 75, 348-359 (2010).
46. Schrödinger, L. Macromodel Version 9.9. (2011).
47. Friesner, R. A. et al. Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for proteinligand complexes. J. Med. Chem. 49, 6177-6196 (2006).