Structure-function relationships of olfactory and taste receptors

Chemical Senses

Volumn 43, Issue 2, 2018, Pages 81-87

  Behrens, Maik ^a   Briand, Loïc ^b   de March, Claire A ^c   Matsunami, Hiroaki ^c   Yamashita, Atsuko ^d   Meyerhof, Wolfgang ^a   Weyand, Simone ^e  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^b CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d OKAYAMA UNIVERSITY   (Japan)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Biochemistry; Functional assays; Molecular modeling; Olfaction; Structural biology; Taste

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; CALCIUM SENSING RECEPTOR; G PROTEIN COUPLED RECEPTOR; LIGAND; METABOTROPIC RECEPTOR;

BITTER TASTE; GUSTATORY SYSTEM; HEREDITY; HUMAN; MOLECULAR DOCKING; MOLECULAR MODEL; OLFACTORY RECEPTOR; PRIORITY JOURNAL; REVIEW; SMELLING; STRUCTURE ACTIVITY RELATION; TASTE BUD; UMAMI; ANIMAL; CHEMISTRY; ODOR; PHYSIOLOGY; TASTE;

ANIMALS; HUMANS; RECEPTORS, G-PROTEIN-COUPLED; SMELL; STRUCTURE-ACTIVITY RELATIONSHIP; TASTE BUDS; TASTE PERCEPTION;

EID: 85041506018     PISSN: 0379864X     EISSN: 14643553     Source Type: Journal    
DOI: 10.1093/chemse/bjx083     Document Type: Review

References (72)

1. Andréll J, Edwards PC, Zhang F, Daly M, Tate CG. 2016. Generation of tetracycline- inducible mammalian cell lines by flow cytometry for improved overproduction of membrane proteins. Methods Mol Biol. 1432:63-78.
2. Bae HE, Mortensen JS, Ribeiro O, Du Y, Ehsan M, Kobilka BK, Loland CJ, Byrne B, Chae PS. 2016. Tandem neopentyl glycol maltosides (TNMs) for membrane protein stabilisation. Chem Commun (Camb). 52:12104-12107.
3. Behrens M, Meyerhof W. 2015. Taste receptors. In: Parker JK, Elmore JS, Methven L, editors. Flavour development, analysis and perception in food and beverages. Cambridge, UK: Woodhead Publishing. p. 297-329.
4. Behrens M, Meyerhof W. 2016. G protein-coupled taste receptors. In: Zufall F, Munger SD, editors. Chemosensory transduction. London, UK: Elsevier Inc. p. 227-244.
5. Biarnés X, Marchiori A, Giorgetti A, Lanzara C, Gasparini P, Carloni P, Born S, BrockhoffA, Behrens M, Meyerhof W. 2010. Insights into the binding of Phenyltiocarbamide (PTC) agonist to its target human TAS2R38 bitter receptor. PLoS One. 5:e12394.
6. Born S, Levit A, Niv MY, Meyerhof W, Behrens M. 2013. The human bitter taste receptor TAS2R10 is tailored to accommodate numerous diverse ligands. J Neurosci. 33:201-213.
7. BrockhoffA, Behrens M, Niv MY, Meyerhof W. 2010. Structural requirements of bitter taste receptor activation. Proc Natl Acad Sci USA. 107:11110-11115.
8. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 65:175-187.
9. Carpenter B, Nehmé R, Warne T, Leslie AG, Tate CG. 2016. Structure of the adenosine A(2A) receptor bound to an engineered G protein. Nature. 536:104-107.
10. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS, Choi HJ, Kuhn P, Weis WI, Kobilka BK, et al. 2007. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science. 318:1258-1265.
11. Congreve M, Andrews SP, Doré AS, Hollenstein K, Hurrell E, Langmead CJ, Mason JS, Ng IW, Tehan B, et al. 2012. Discovery of 1,2,4-triazine derivatives as adenosine A(2A) antagonists using structure based drug design. J Med Chem. 55:1898-1903.
12. Congreve M, Langmead CJ, Mason JS, Marshall FH. 2011. Progress in structure based drug design for G protein-coupled receptors. J Med Chem. 54:4283-4311.
13. Cook BL, Steuerwald D, Kaiser L, Graveland-Bikker J, Vanberghem M, Berke AP, Herlihy K, Pick H, Vogel H, Zhang S. 2009. Large-scale production and study of a synthetic G protein-coupled receptor: human olfactory receptor 17-4. Proc Natl Acad Sci USA. 106:11925-11930.
14. de March CA, Golebiowski J. 2014. A computational microscope focused on the sense of smell. Biochimie. 107 Pt A:3-10.
15. de March CA, Kim SK, Antonczak S, Goddard WA 3rd, Golebiowski J. 2015a. G protein-coupled odorant receptors: from sequence to structure. Protein Sci. 24:1543-1548.
16. de March CA, Ryu S, Sicard G, Moon C, Golebiowski J. 2015b. Structure- odour relationships reviewed in the postgenomic era. Flavour Frag J. 30:342-361.
17. de March CA, Yu Y, Ni MJ, Adipietro KA, Matsunami H, Ma M, Golebiowski J. 2015. Conserved residues control activation of mammalian G proteincoupled odorant receptors. J Am Chem Soc. 137:8611-8616.
18. Di Pizio A, Levit A, Slutzki M, Behrens M, Karaman R, Niv MY. 2016. Chapter 18-Comparing Class A GPCRs to bitter taste receptors: structural motifs, ligand interactions and agonist-to-antagonist ratios. In: Arun KS, editor. Methods in cell biology. Academic Press. p. 401-427.
19. Di Pizio A, Niv MY. 2015. Promiscuity and selectivity of bitter molecules and their receptors. Bioorg Med Chem. 23:4082-4091.
20. Flock T, Ravarani CNJ, Sun D, Venkatakrishnan AJ, Kayikci M, Tate CG, Veprintsev DB, Babu MM. 2015. Universal allosteric mechanism for Ga activation by GPCRs. Nature. 524:173-179.
21. Floriano WB, Vaidehi N, Goddard WA 3rd, Singer MS, Shepherd GM. 2000. Molecular mechanisms underlying differential odor responses of a mouse olfactory receptor. Proc Natl Acad Sci USA. 97:10712-10716.
22. Fredriksson R, Lagerström MC, Lundin LG, Schiöth 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.
23. Gelis L, Wolf S, Hatt H, Neuhaus EM, Gerwert K. 2012. Prediction of a ligand-binding niche within a human olfactory receptor by combining site-directed mutagenesis with dynamic homology modeling. Angewandte Chemie International Edition. 51:1274-1278.
24. Geng Y, Bush M, Mosyak L, Wang F, Fan QR. 2013. Structural mechanism of ligand activation in human GABA(B) receptor. Nature. 504:254-259.
25. Geng Y, Mosyak L, Kurinov I, Zuo H, Sturchler E, Cheng TC, Subramanyam P, Brown AP, Brennan SC, Mun HC, et al. 2016. Structural mechanism of ligand activation in human calcium-sensing receptor. Elife. 5.
26. Ghosh E, Kumari P, Jaiman D, Shukla AK. 2015. Methodological advances: the unsung heroes of the GPCR structural revolution. Nat Rev Mol Cell Biol. 16:69-81.
27. Gimelbrant AA, Stoss TD, Landers TM, McClintock TS. 1999. Truncation releases olfactory receptors from the endoplasmic reticulum of heterologous cells. J Neurochem. 72:2301-2311.
28. Goehring A, Lee CH, Wang KH, Michel JC, Claxton DP, Baconguis I, AlthoffT, Fischer S, Garcia KC, Gouaux E. 2014. Screening and large-scale expression of membrane proteins in mammalian cells for structural studies. Nat Protoc. 9:2574-2585.
29. Hino T, Arakawa T, Iwanari H, Yurugi-Kobayashi T, Ikeda-Suno C, Nakada- Nakura Y, Kusano-Arai O, Weyand S, Shimamura T, Nomura N, et al. 2012. G-protein-coupled receptor inactivation by an allosteric inverseagonist antibody. Nature. 482:237-240.
30. Huang CY, Olieric V, Ma P, Howe N, Vogeley L, Liu X, Warshamanage R, Weinert T, Panepucci E, Kobilka B, et al. 2016. In meso in situ serial X-ray crystallography of soluble and membrane proteins at cryogenic temperatures. Acta Crystallogr D Struct Biol. 72:93-112.
31. Hussain H, Du Y, Scull NJ, Mortensen JS, Tarrasch J, Bae HE, Loland CJ, Byrne B, Kobilka BK, Chae PS. 2016. Accessible mannitol-based amphiphiles (MNAs) for membrane protein solubilisation and stabilisation. Chemistry. 22:7068-7073.
32. Jiang P, Cui M, Zhao B, Liu Z, Snyder LA, Benard LM, Osman R, Margolskee RF, Max M. 2005. Lactisole interacts with the transmembrane domains of human T1R3 to inhibit sweet taste. J Biol Chem. 280:15238-15246.
33. Jiang P, Cui M, Zhao B, Snyder LA, Benard LM, Osman R, Max M, Margolskee RF. 2005. Identification of the cyclamate interaction site within the transmembrane domain of the human sweet taste receptor subunit T1R3. J Biol Chem. 280:34296-34305.
34. Jiang P, Ji Q, Liu Z, Snyder LA, Benard LM, Margolskee RF, Max M. 2004. The cysteine-rich region of T1R3 determines responses to intensely sweet proteins. J Biol Chem. 279:45068-45075.
35. Katritch V, Cherezov V, Stevens RC. 2013. Structure-function of the G protein-coupled receptor superfamily. Annu Rev Pharmacol Toxicol. 53:531-556.
36. Kunishima N, Shimada Y, Tsuji Y, Sato T, Yamamoto M, Kumasaka T, Nakanishi S, Jingami H, Morikawa K. 2000. Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature. 407:971-977.
37. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E. 2002. Human receptors for sweet and umami taste. Proc Natl Acad Sci USA. 99:4692-4696.
38. Liang YL, Khoshouei M, Radjainia M, Zhang Y, Glukhova A, Tarrasch J, Thal DM, Furness SGB, Christopoulos G, Coudrat T, et al. 2017. Phaseplate cryo-EM structure of a class B GPCR-G-protein complex. Nature. 546:118-123.
39. Lossow K, Hübner S, Roudnitzky N, Slack JP, Pollastro F, Behrens M, Meyerhof W. 2016. Comprehensive analysis of mouse bitter taste receptors reveals different molecular receptive ranges for orthologous receptors in mice and humans. J Biol Chem. 291:15358-15377.
40. Lu M, Staszewski L, Echeverri F, Xu H, Moyer BD. 2004. Endoplasmic reticulum degradation impedes olfactory G-protein coupled receptor functional expression. BMC Cell Biol. 5:34.
41. Magnani F, Serrano-Vega MJ, Shibata Y, Abdul-Hussein S, Lebon G, Miller- Gallacher J, Singhal A, Strege A, Thomas JA, Tate CG. 2016. A mutagenesis and screening strategy to generate optimally thermostabilized membrane proteins for structural studies. Nat Protoc. 11:1554-1571.
42. Maîtrepierre E, Sigoillot M, Le Pessot L, Briand L. 2012. Recombinant expression, in vitro refolding, and biophysical characterization of the N-terminal domain of T1R3 taste receptor. Protein Expr Purif. 83:75-83.
43. Malnic B, Hirono J, Sato T, Buck LB. 1999. Combinatorial receptor codes for odors. Cell. 96:713-723.
44. Marchiori A, Capece L, Giorgetti A, Gasparini P, Behrens M, Carloni P, Meyerhof W. 2013. Coarse-grained/molecular mechanics of the TAS2R38 bitter taste receptor: experimentally-validated detailed structural prediction of agonist binding. PLoS One. 8:e64675.
45. Mason JS, Bortolato A, Congreve M, Marshall FH. 2012. New insights from structural biology into the druggability of G protein-coupled receptors. Trends Pharmacol Sci. 33:249-260.
46. Meyerhof W, Batram C, Kuhn C, BrockhoffA, Chudoba E, Bufe B, Appendino G, Behrens M. 2010. The molecular receptive ranges of human TAS2R bitter taste receptors. Chem Senses. 35:157-170.
47. Muto T, Tsuchiya D, Morikawa K, Jingami H. 2007. Structures of the extracellular regions of the group II/III metabotropic glutamate receptors. Proc Natl Acad Sci USA. 104:3759-3764.
48. Nakamura S, Itabashi T, Ogawa D, Okada T. 2013. Common and distinct mechanisms of activation of rhodopsin and other G protein-coupled receptors. Sci Rep. 3:1844.
49. Nango E, Akiyama S, Maki-Yonekura S, Ashikawa Y, Kusakabe Y, Krayukhina E, Maruno T, Uchiyama S, Nuemket N, Yonekura K, et al. 2016. Taste substance binding elicits conformational change of taste receptor T1r heterodimer extracellular domains. Sci Rep. 6:25745.
50. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS. 2002. An amino-acid taste receptor. Nature. 416:199-202.
51. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. 2001. Mammalian sweet taste receptors. Cell. 106:381-390.
52. Nie Y, Vigues S, Hobbs JR, Conn GL, Munger SD. 2005. Distinct contributions of T1R2 and T1R3 taste receptor subunits to the detection of sweet stimuli. Curr Biol. 15:1948-1952.
53. Nuemket N, Yasui N, Kusakabe Y, Nomura Y, Atsumi N, Akiyama S, Nango E, Kato Y, Kaneko MK, Takagi J, et al. 2017. Structural basis for perception of diverse chemical substances by T1r taste receptors. Nat Commun. 8:15530.
54. Pilpel Y, Lancet D. 1999. The variable and conserved interfaces of modeled olfactory receptor proteins. Protein Sci. 8:969-977.
55. Probst WC, Snyder LA, Schuster DI, Brosius J, Sealfon SC. 1992. Sequence alignment of the G-protein coupled receptor superfamily. DNA Cell Biol. 11:1-20.
56. Rosenbaum DM, Rasmussen SG, Kobilka BK. 2009. The structure and function of G-protein-coupled receptors. Nature. 459:356-363.
57. Saarenpää T, Jaakola VP, Goldman A. 2015. Baculovirus-mediated expression of GPCRs in insect cells. Methods Enzymol. 556:185-218.
58. Sandal M, Behrens M, BrockhoffA, Musiani F, Giorgetti A, Carloni P, Meyerhof W. 2015. Evidence for a transient additional ligand binding site in the TAS2R46 bitter taste receptor. J Chem Theory Comput. 11:4439-4449.
59. Sharma R, Ishimaru Y, Davison I, Ikegami K, Chien MS, You H, Chi Q, Kubota M, Yohda M, Ehlers M, et al. 2017. Olfactory receptor accessory proteins play crucial roles in receptor function and gene choice. Elife. 6.
60. Shi P, Zhang J, Yang H, Zhang YP. 2003. Adaptive diversification of bitter taste receptor genes in Mammalian evolution. Mol Biol Evol. 20:805-814.
61. Shimamura T, Shiroishi M, Weyand S, Tsujimoto H, Winter G, Katritch V, Abagyan R, Cherezov V, Liu W, Han GW, et al. 2011. Structure of the human histamine H1 receptor complex with doxepin. Nature. 475:65-70.
62. Tate CG, Schertler GF. 2009. Engineering G protein-coupled receptors to facilitate their structure determination. Curr Opin Struct Biol. 19:386-395.
63. Thomas J, Tate CG. 2014. Quality control in eukaryotic membrane protein overproduction. J Mol Biol. 426:4139-4154.
64. Topin J, de March CA, Charlier L, Ronin C, Antonczak S, Golebiowski J. 2014. Discrimination between olfactory receptor agonists and non-agonists. Chemistry. 20:10227-10230.
65. Venkatakrishnan AJ, Deupi X, Lebon G, Heydenreich FM, Flock T, Miljus T, Balaji S, Bouvier M, Veprintsev DB, Tate CG, et al. 2016. Diverse activation pathways in class A GPCRs converge near the G-protein-coupling region. Nature. 536:484-487.
66. Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF, Babu MM. 2013. Molecular signatures of G-protein-coupled receptors. Nature. 494:185-194.
67. Warne T, Moukhametzianov R, Baker JG, Nehmé R, Edwards PC, Leslie AG, Schertler GF, Tate CG. 2011. The structural basis for agonist and partial agonist action on a ß(1)-adrenergic receptor. Nature. 469:241-244.
68. Winnig M, Bufe B, Kratochwil NA, Slack JP, Meyerhof W. 2007. The binding site for neohesperidin dihydrochalcone at the human sweet taste receptor. BMC Struct Biol. 7:66.
69. Wu L, Pan Y, Chen GQ, Matsunami H, Zhuang H. 2012. Receptortransporting protein 1 short (RTP1S) mediates translocation and activation of odorant receptors by acting through multiple steps. J Biol Chem. 287:22287-22294.
70. Xu H, Staszewski L, Tang H, Adler E, Zoller M, Li X. 2004. Different functional roles of T1R subunits in the heteromeric taste receptors. Proc Natl Acad Sci USA. 101:14258-14263.
71. Yu Y, de March CA, Ni MJ, Adipietro KA, Golebiowski J, Matsunami H, Ma M. 2015. Responsiveness of G protein-coupled odorant receptors is partially attributed to the activation mechanism. Proc Natl Acad Sci USA. 112:14966-14971.
72. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS. 2003. The receptors for mammalian sweet and umami taste. Cell. 115:255-266.