Olfactory Receptor Proteins

  • Guenhaël SanzEmail author
  • Jean-François Gibrat
  • Edith Pajot-Augy


Bioelectronic noses can utilize olfactory receptors (ORs) as recognition elements. This chapter describes biochemical characteristics of these OR proteins. ORs being G protein-coupled receptors (GPCRs) are integral membrane proteins composed of seven transmembrane spanning helices. In mammals, there exist as many as 1,000 OR genes accounting for about 3 % of the genome. Unfortunately, no three-dimensional (3D) structure of OR is available and one must infer OR properties from those of better characterized GPCRs. The chapter offers a brief overview of the characteristics of known 3D structures of complexes of GPCRs with various types of ligands (agonists, inverse agonists, antagonists, etc.) and, in one case, also with a G protein. Based on these structural data, it then reviews hypotheses and experiments regarding the GPCR transduction mechanism. The chapter then describes how the set of known 3D structures (17 different GPCRs to date) can be used to model OR 3D structures that will be subsequently used as platform for ligand virtual screening. The following section examines the different mechanisms that regulate OR activity. Lastly, we focus on the use of OR proteins in bioelectronic noses.


Binding Pocket Virtual Screening Olfactory Receptor Olfactory Epithelium Inverse Agonist 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Gilad Y, Man O, Glusman G (2005) A comparison of the human and chimpanzee olfactory receptor gene repertoires. Genome Res 15:224–230PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Young JM, Trask BJ (2002) The sense of smell: genomics of vertebrate odorant receptors. Hum Mol Genet 11:1153–1160PubMedCrossRefGoogle Scholar
  3. 3.
    Quignon P, Kirkness E, Cadieu E, Touleimat N, Guyon R et al (2003) Comparison of the canine and human olfactory receptor gene repertoires. Genome Biol 4:R80.81–80.89Google Scholar
  4. 4.
    Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–902PubMedCrossRefGoogle Scholar
  5. 5.
    Zozulya S, Echeverri F, Nguyen T (2001) The human olfactory receptor repertoire. Genome Biol 2:0018.0011–0018.0012Google Scholar
  6. 6.
    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 63:1256–1272PubMedCrossRefGoogle Scholar
  7. 7.
    Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187PubMedCrossRefGoogle Scholar
  8. 8.
    Sanz G, Thomas-Danguin T, Hamdani EH, Le Poupon C, Briand L et al (2008) Relationships Between Molecular Structure and Perceived Odor Quality of Ligands for a Human Olfactory Receptor. Chem Senses 33(7):639–653PubMedCrossRefGoogle Scholar
  9. 9.
    Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel C et al (2003) Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299:2054–2058PubMedCrossRefGoogle Scholar
  10. 10.
    Spehr M, Schwane K, Heilmann S, Gisselmann G, Hummel T et al (2004) Dual capacity of a human olfactory receptor. Curr Biol 14:R832–R833Google Scholar
  11. 11.
    Braun T, Voland P, Kunz L, Prinz C, Gratzl M (2007) Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology 132:1890–1901PubMedCrossRefGoogle Scholar
  12. 12.
    Kidd M, Modlin IM, Gustafsson BI, Drozdov I, Hauso O et al (2008) Luminal regulation of normal and neoplastic human EC cell serotonin release is mediated by bile salts, amines, tastants, and olfactants. Am J Physiol Gastrointest Liver Physiol 295:G260–272Google Scholar
  13. 13.
    Griffin CA, Kafadar KA, Pavlath GK (2009) MOR23 promotes muscle regeneration and regulates cell adhesion and migration. Dev Cell 17:649–661PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Pluznick JL, Zou DJ, Zhang X, Yan Q, Rodriguez-Gil DJ et al (2009) Functional expression of the olfactory signaling system in the kidney. Proc Natl Acad Sci U S A 106:2059–2064PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Pluznick JL, Protzko RJ, Gevorgyan H, Peterlin Z, Sipos A et al (2013) Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proc Natl Acad Sci U S A 110:4410–4415PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Weng J, Wang J, Cai Y, Stafford LJ, Mitchell D et al (2005) Increased expression of prostate-specific G-protein-coupled receptor in human prostate intraepithelial neoplasia and prostate cancers. Int J Cancer 113:811–818PubMedCrossRefGoogle Scholar
  17. 17.
    Leja J, Essaghir A, Essand M, Wester K, Oberg K et al (2009) Novel markers for enterochromaffin cells and gastrointestinal neuroendocrine carcinomas. Mod Pathol 22:261–272PubMedCrossRefGoogle Scholar
  18. 18.
    Muranen TA, Greco D, Fagerholm R, Kilpivaara O, Kampjarvi K et al (2011) Breast tumors from CHEK2 1100delC-mutation carriers: genomic landscape and clinical implications. Breast Cancer Res 13: R90Google Scholar
  19. 19.
    Zhang X, Bedigian AV, Wang W, Eggert US (2012) G protein-coupled receptors participate in cytokinesis. Cytoskeleton (Hoboken) 69:810–818CrossRefGoogle Scholar
  20. 20.
    Fukuda N, Touhara K (2006) Developmental expression patterns of testicular olfactory receptor genes during mouse spermatogenesis. Genes Cells 11:71–81PubMedCrossRefGoogle Scholar
  21. 21.
    Sanz G, Leray I, Dewaele A, Sobilo J, Lerondel S et al (2014) Promotion of cancer cell invasiveness and metastasis emergence caused by olfactory receptor stimulation. PLOS ONE 9(1):e85110Google Scholar
  22. 22.
    Regnauld K, Nguyen QD, Vakaet L, Bruyneel E, Launay JM et al (2002) G-protein alpha(olf) subunit promotes cellular invasion, survival, and neuroendocrine differentiation in digestive and urogenital epithelial cells. Oncogene 21:4020–4031PubMedCrossRefGoogle Scholar
  23. 23.
    Ukhanov K, Brunert D, Corey EA, Ache BW (2011) Phosphoinositide 3-kinase-dependent antagonism in Mammalian olfactory receptor neurons. J Neurosci 31:273–280PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Ukhanov K, Corey EA, Ache BW (2013) Phosphoinositide 3-kinase dependent inhibition as a broad basis for opponent coding in Mammalian olfactory receptor neurons. PLoS One 8:e61553PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Fredriksson R, Schioth HB (2005) The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol Pharmacol 67:1414–1425PubMedCrossRefGoogle Scholar
  26. 26.
    Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H et al (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739–745PubMedCrossRefGoogle Scholar
  27. 27.
    Rasmussen SG, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS et al (2007) Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 450:383–387PubMedCrossRefGoogle Scholar
  28. 28.
    Park SH, Das BB, Casagrande F, Tian Y, Nothnagel HJ et al (2012) Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491:779–783PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Rasmussen SG, Choi HJ, Fung JJ, Pardon E, Casarosa P et al (2011) Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor. Nature 469:175–180PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY et al (2011) Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 477:549–555PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Katritch V, Cherezov V, Stevens RC (2012) Diversity and modularity of G protein-coupled receptor structures. Trends Pharmacol Sci 33:17–27PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Pilpel Y, Lancet D (1999) The variable and conserved interfaces of modeled olfactory receptor proteins. Protein Sci 8:969–977PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Ballesteros JA, Weinstein H (1995) Integrated methods and computational probing of structure-function relations in G protein-coupled receptors. Methods Neurosci 25:366–428CrossRefGoogle Scholar
  34. 34.
    Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF et al (2013) Molecular signatures of G-protein-coupled receptors. Nature 494:185–194PubMedCrossRefGoogle Scholar
  35. 35.
    Choe HW, Kim YJ, Park JH, Morizumi T, Pai EF et al (2011) Crystal structure of metarhodopsin II. Nature 471:651–655PubMedCrossRefGoogle Scholar
  36. 36.
    Standfuss J, Edwards PC, D’Antona A, Fransen M, Xie G et al (2011) The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471:656–660PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Nygaard R, Zou Y, Dror RO, Mildorf TJ, Arlow DH et al (2013) The dynamic process of beta(2)-adrenergic receptor activation. Cell 152:532–542PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Deupi X, Standfuss J (2011) Structural insights into agonist-induced activation of G-protein-coupled receptors. Curr Opin Struct Biol 21:541–551PubMedCrossRefGoogle Scholar
  39. 39.
    Liu JJ, Horst R, Katritch V, Stevens RC, Wuthrich K (2012) Biased signaling pathways in beta2-adrenergic receptor characterized by 19F-NMR. Science 335:1106–1110PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Kenakin T (2011) Functional selectivity and biased receptor signaling. J Pharmacol Exp Ther 336:296–302PubMedCrossRefGoogle Scholar
  41. 41.
    Kontoyianni M, Liu Z (2012) Structure-based design in the GPCR target space. Curr Med Chem 19:544–556PubMedCrossRefGoogle Scholar
  42. 42.
    Nordstrom KJ, Sallman Almen M, Edstam MM, Fredriksson R, Schioth HB (2011) Independent HHsearch, Needleman–Wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families. Mol Biol Evol 28:2471–2480PubMedCrossRefGoogle Scholar
  43. 43.
    Costanzi S (2013) Modeling G protein-coupled receptors and their interactions with ligands. Curr Opin Struct Biol 23:185–190PubMedCrossRefGoogle Scholar
  44. 44.
    Xiang Z (2006) Advances in homology protein structure modeling. Curr Protein Pept Sci 7:217–227PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815PubMedCrossRefGoogle Scholar
  46. 46.
    Beuming T, Sherman W (2012) Current assessment of docking into GPCR crystal structures and homology models: successes, challenges, and guidelines. J Chem Inf Model 52:3263–3277PubMedCrossRefGoogle Scholar
  47. 47.
    Michalsky E, Goede A, Preissner R (2003) Loops In Proteins (LIP)—a comprehensive loop database for homology modelling. Protein Eng 16:979–985PubMedCrossRefGoogle Scholar
  48. 48.
    Congreve M, Langmead CJ, Mason JS, Marshall FH (2011) Progress in structure based drug design for G protein-coupled receptors. J Med Chem 54:4283–4311PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Kubinyi H (1997) QSAR and 3D QSAR in drug design. Drug Discov Today 2:457–467CrossRefGoogle Scholar
  50. 50.
    Kufareva I, Rueda M, Katritch V, Stevens RC, Abagyan R (2011) Status of GPCR modeling and docking as reflected by community-wide GPCR Dock 2010 assessment. Structure 19:1108–1126PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Zhukov A, Andrews SP, Errey JC, Robertson N, Tehan B et al (2011) Biophysical mapping of the adenosine A2A receptor. J Med Chem 54:4312–4323PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Jacobson KA, Gao ZG, Liang BT (2007) Neoceptors: reengineering GPCRs to recognize tailored ligands. Trends Pharmacol Sci 28:111–116PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Shoichet BK, Kobilka BK (2012) Structure-based drug screening for G-protein-coupled receptors. Trends Pharmacol Sci 33:268–272PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Launay G, Sanz G, Pajot E, Gibrat JF (2012) Modeling of mammalian olfactory receptors and docking of odorants. Biophys Rev 4:255–269CrossRefGoogle Scholar
  55. 55.
    Launay G, Teletchea S, Wade F, Pajot-Augy E, Gibrat JF et al (2012) Automatic modeling of mammalian olfactory receptors and docking of odorants. Protein Eng Des Sel 25:377–386PubMedCrossRefGoogle Scholar
  56. 56.
    Minic J, Persuy MA, Godel E, Aioun J, Connerton I et al (2005) Functional expression of olfactory receptors in yeast and development of a bioassay for odorant screening. FEBS J 272:524–537PubMedCrossRefGoogle Scholar
  57. 57.
    Minic Vidic J, Grosclaude J, Persuy MA, Aioun J, Salesse R et al (2006) Quantitative assessment of olfactory receptors activity in immobilized nanosomes: a novel concept for bioelectronic nose. Lab Chip 6:1026–1032CrossRefGoogle Scholar
  58. 58.
    Duchamp-Viret P, Duchamp A, Sicard G (1990) Olfactory discrimination over a wide concentration range. Comparison of receptor cell and bulb neuron abilities. Brain Res 517:256–262PubMedCrossRefGoogle Scholar
  59. 59.
    Grosmaitre X, Vassalli A, Mombaerts P, Shepherd GM, Ma M (2006) Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proc Natl Acad Sci U S A 103:170–1975CrossRefGoogle Scholar
  60. 60.
    Vidic J, Grosclaude J, Monnerie R, Persuy MA, Badonnel K et al (2008) On a chip demonstration of a functional role for Odorant Binding Protein in the preservation of olfactory receptor activity at high odorant concentration. Lab Chip 8:678–688PubMedCrossRefGoogle Scholar
  61. 61.
    Wade F, Espagne A, Persuy MA, Vidic J, Monnerie R et al (2011) Relationship between homo-oligomerization of a mammalian olfactory receptor and its activation state demonstrated by bioluminescence resonance energy transfer. J Biol Chem 286:15252–15259PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Matarazzo V, Zsürger N, Guillemot JC, Clot-Faybesse O, Botto JM et al (2002) Porcine odorant-binding protein selectively binds to a human olfactory receptor. Chem Senses 27:691–701PubMedCrossRefGoogle Scholar
  63. 63.
    Franco R, Casado V, Mallol J, Ferrada C, Ferré S et al (2006) The two-state dimer receptor model: a general model for receptor dimers. Mol Pharmacol 69:1905–1912PubMedCrossRefGoogle Scholar
  64. 64.
    Wetzel C, Oles M, Wellerdieck C, Kuczkowiak M, Gisselmann G et al (1999) Specificity and sensitivity of a human olfactory receptor functionally expressed in human embryonic kidney 293 cells and Xenopus Laevis oocytes. J Neurosci 19:7426–7433PubMedGoogle Scholar
  65. 65.
    Dulac C (2000) The physiology of taste, vintage 2000. Cell 100:607–610PubMedCrossRefGoogle Scholar
  66. 66.
    Goldsmith BR, Mitala JJ, Josue J, Castro A, Lerner MB et al (2011) Biomimetic Chemical Sensors Using Nanoelectronic Readout of Olfactory Receptor Proteins. ACS Nano 5:5408–5416PubMedCrossRefGoogle Scholar
  67. 67.
    Lee SH, Jin HJ, Song HS, Hong S, Park TH (2012) Bioelectronic nose with high sensitivity and selectivity using chemically functionalized carbon nanotube combined with human olfactory receptor. J Biotechnol 157:467–472PubMedCrossRefGoogle Scholar
  68. 68.
    Lee SH, Kwon OS, Song HS, Park SJ, Sung JH et al (2012) Mimicking the human smell sensing mechanism with an artificial nose platform. Biomaterials 33:1722–1729PubMedCrossRefGoogle Scholar
  69. 69.
    Jin HJ, Lee SH, Kim TH, Park J, Song HS et al (2012) Nanovesicle-based bioelectronic nose platform mimicking human olfactory signal transduction. Biosens Bioelectron 35:335–341PubMedCrossRefGoogle Scholar
  70. 70.
    Park J, Lim JH, Jin HJ, Namgung S, Lee SH et al (2012) A bioelectronic sensor based on canine olfactory nanovesicle-carbon nanotube hybrid structures for the fast assessment of food quality. Analyst 137:3249–3254PubMedCrossRefGoogle Scholar
  71. 71.
    Wu C, Du L, Wang D, Wang L, Zhao L et al (2011) A novel surface acoustic wave-based biosensor for highly sensitive functional assays of olfactory receptors. Biochem Biophys Res Commun 407:18–22PubMedCrossRefGoogle Scholar
  72. 72.
    Benilova IV, Minic Vidic J, Pajot-Augy E, Soldatkin AP, Martelet C et al (2008) Electrochemical study of human olfactory receptor OR 17–40 stimulation by odorants in solution. Mater Sci Eng C 28:633–639CrossRefGoogle Scholar
  73. 73.
    Dacres H, Wang J, Leitch V, Horne I, Anderson AR et al (2011) Greatly enhanced detection of a volatile ligand at femtomolar levels using bioluminescence resonance energy transfer (BRET). Biosens Bioelectr 29:119–124CrossRefGoogle Scholar
  74. 74.
    Fukutani Y, Nakamura T, Yorozu M, Ishii J, Kondo A et al (2012) The N-terminal replacement of an olfactory receptor for the development of a Yeast-based biomimetic odor sensor. Biotechnol Bioeng 109:205–212PubMedCrossRefGoogle Scholar
  75. 75.
    Radhika V, Proikas-Cezanne T, Jayaraman M, Onesime D, Ha JH et al (2007) Chemical sensing of DNT by engineered olfactory yeast strain. Nat Chem Biol 3:325–330PubMedCrossRefGoogle Scholar
  76. 76.
    Warne T, Edwards PC, Leslie AG, Tate CG (2012) Crystal structures of a stabilized beta1-adrenoceptor bound to the biased agonists bucindolol and carvedilol. Structure 20:841–849PubMedCrossRefGoogle Scholar
  77. 77.
    Wu H, Wacker D, Mileni M, Katritch V, Han GW et al (2012) Structure of the human kappa-opioid receptor in complex with JDTic. Nature 485:327–332PubMedCentralPubMedCrossRefGoogle Scholar
  78. 78.
    Okada T, Sugihara M, Bondar AN, Elstner M, Entel P et al (2004) The retinal conformation and its environment in rhodopsin in light of a new 2.2 A crystal structure. J Mol Biol 342:571–583PubMedCrossRefGoogle Scholar
  79. 79.
    Murakami M, Kouyama T (2008) Crystal structure of squid rhodopsin. Nature 453:363–367PubMedCrossRefGoogle Scholar
  80. 80.
    Hanson MA, Cherezov V, Griffith MT, Roth CB, Jaakola VP et al (2008) A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure 16:897–905PubMedCentralPubMedCrossRefGoogle Scholar
  81. 81.
    Wacker D, Fenalti G, Brown MA, Katritch V, Abagyan R et al (2010) Conserved binding mode of human beta2 adrenergic receptor inverse agonists and antagonist revealed by X-ray crystallography. J Am Chem Soc 132:11443–11445PubMedCentralPubMedCrossRefGoogle Scholar
  82. 82.
    Rosenbaum DM, Zhang C, Lyons JA, Holl R, Aragao D et al (2011) Structure and function of an irreversible agonist-beta(2) adrenoceptor complex. Nature 469:236–240PubMedCentralPubMedCrossRefGoogle Scholar
  83. 83.
    Warne T, Serrano-Vega MJ, Baker JG, Moukhametzianov R, Edwards PC et al (2008) Structure of a beta1-adrenergic G-protein-coupled receptor. Nature 454:486–491PubMedCentralPubMedCrossRefGoogle Scholar
  84. 84.
    Warne T, Moukhametzianov R, Baker JG, Nehme R, Edwards PC et al (2011) The structural basis for agonist and partial agonist action on a beta(1)-adrenergic receptor. Nature 469:241–244PubMedCentralPubMedCrossRefGoogle Scholar
  85. 85.
    Moukhametzianov R, Warne T, Edwards PC, Serrano-Vega MJ, Leslie AG et al (2011) Two distinct conformations of helix 6 observed in antagonist-bound structures of a beta1-adrenergic receptor. Proc Natl Acad Sci U S A 108:8228–8232PubMedCentralPubMedCrossRefGoogle Scholar
  86. 86.
    Jaakola VP, Griffith MT, Hanson MA, Cherezov V, Chien EY et al (2008) The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322:1211–1217PubMedCentralPubMedCrossRefGoogle Scholar
  87. 87.
    Xu F, Wu H, Katritch V, Han GW, Jacobson KA et al (2011) Structure of an agonist-bound human A2A adenosine receptor. Science 332:322–327PubMedCentralPubMedCrossRefGoogle Scholar
  88. 88.
    Lebon G, Warne T, Edwards PC, Bennett K, Langmead CJ et al (2011) Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 474:521–525PubMedCentralPubMedCrossRefGoogle Scholar
  89. 89.
    Dore AS, Robertson N, Errey JC, Ng I, Hollenstein K et al (2011) Structure of the adenosine A(2A) receptor in complex with ZM241385 and the xanthines XAC and caffeine. Structure 19:1283–1293PubMedCentralPubMedCrossRefGoogle Scholar
  90. 90.
    Wu B, Chien EY, Mol CD, Fenalti G, Liu W et al (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330:1066–1071PubMedCentralPubMedCrossRefGoogle Scholar
  91. 91.
    Chien EY, Liu W, Zhao Q, Katritch V, Han GW et al (2010) Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist. Science 330:1091–1095PubMedCentralPubMedCrossRefGoogle Scholar
  92. 92.
    Shimamura T, Shiroishi M, Weyand S, Tsujimoto H, Winter G et al (2011) Structure of the human histamine H1 receptor complex with doxepin. Nature 475:65–70PubMedCentralPubMedCrossRefGoogle Scholar
  93. 93.
    Hanson MA, Roth CB, Jo E, Griffith MT, Scott FL et al (2012) Crystal structure of a lipid G protein-coupled receptor. Science 335:851–855PubMedCentralPubMedCrossRefGoogle Scholar
  94. 94.
    Haga K, Kruse AC, Asada H, Yurugi-Kobayashi T, Shiroishi M et al (2012) Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 482:547–551PubMedCentralPubMedCrossRefGoogle Scholar
  95. 95.
    Kruse AC, Hu J, Pan AC, Arlow DH, Rosenbaum DM et al (2012) Structure and dynamics of the M3 muscarinic acetylcholine receptor. Nature 482:552–556PubMedCentralPubMedCrossRefGoogle Scholar
  96. 96.
    Manglik A, Kruse AC, Kobilka TS, Thian FS, Mathiesen JM et al (2012) Crystal structure of the micro-opioid receptor bound to a morphinan antagonist. Nature 485:321–326PubMedCentralPubMedCrossRefGoogle Scholar
  97. 97.
    Granier S, Manglik A, Kruse AC, Kobilka TS, Thian FS et al (2012) Structure of the delta-opioid receptor bound to naltrindole. Nature 485:400–404PubMedCentralPubMedCrossRefGoogle Scholar
  98. 98.
    Thompson AA, Liu W, Chun E, Katritch V, Wu H et al (2012) Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature 485:395–399PubMedCentralPubMedCrossRefGoogle Scholar
  99. 99.
    White JF, Noinaj N, Shibata Y, Love J, Kloss B et al (2012) Structure of the agonist-bound neurotensin receptor. Nature 490:508–513PubMedCentralPubMedCrossRefGoogle Scholar
  100. 100.
    Zhang C, Srinivasan Y, Arlow DH, Fung JJ, Palmer D et al (2012) High-resolution crystal structure of human protease-activated receptor 1. Nature 492:387–392PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Guenhaël Sanz
    • 1
    Email author
  • Jean-François Gibrat
    • 2
  • Edith Pajot-Augy
    • 1
  1. 1.INRA, UR1197 NeuroBiologie de l’OlfactionJouy-en-JosasFrance
  2. 2.INRA, UR1077 Mathématique Informatique et GénomeJouy-en-JosasFrance

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