Experimental evaluation of the generalized vibrational theory of G protein-coupled receptor activation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 22, 2017, Pages 5595-5600

  Hoehn, Ross D ^a   Nichols, David E ^b   McCorvy, John D ^b   Neven, Hartmut ^c   Kais, Sabre ^a,d  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c GOOGLE INC   (United States)

^d SANTA FE INSTITUTE   (United States)

Author keywords

Electron tunneling; Mechanism of action; Pharmacology; Protein; Quantum biology

Indexed keywords

4 IODO 2,5 DIMETHOXYAMPHETAMINE; G PROTEIN COUPLED RECEPTOR; N',N' DIMETHYLLYSERGAMIDE; SEROTONIN 2 AGONIST; UNCLASSIFIED DRUG; 4-IODO-2,5-DIMETHOXYPHENYLISOPROPYLAMINE; AMPHETAMINE DERIVATIVE; SEROTONIN 2A RECEPTOR;

ACTIVATION ANALYSIS; ARTICLE; BINDING KINETICS; CALCIUM TRANSPORT; DRUG MECHANISM; DRUG RECEPTOR BINDING; EC50; EVALUATION STUDY; EXPERIMENTAL STUDY; HUMAN; HUMAN CELL; NULL HYPOTHESIS; OLFACTORY RECEPTOR; PREDICTION; PRIORITY JOURNAL; RECEPTOR AFFINITY; RELATIVE BINDING AFFINITY; THEORETICAL STUDY; TURIN VIBRATIONAL THEORY; ENZYME ACTIVATION; METABOLISM; ODOR; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIBRATION;

AMPHETAMINES; ENZYME ACTIVATION; HUMANS; RECEPTOR, SEROTONIN, 5-HT2A; SEROTONIN 5-HT2 RECEPTOR AGONISTS; SIGNAL TRANSDUCTION; SMELL; VIBRATION;

EID: 85020029345     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1618422114     Document Type: Article

References (94)

1. Kesner RP, Hunsaker MR, Ziegler W (2011) The role of the dorsal and ventral hippocampusin olfactory working memory. Neurobiol Learn Mem 96:361-366.
2. Rolls ET (2000) The orbitofrontal cortex and reward. Cereb cortex 10:284-294.
3. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: Amolecular basis for odor recognition. Cell 65:175-187.
4. Jastrzebska B, Debinski A, Filipek S, Palczewski K (2011) Role of membrane integrityon G protein-coupled receptors: Rhodopsin stability and function. Prog Lipid Res50:267-277.
5. Manglik A, et al. (2015) Structural insights into the dynamic process of-2-adrenergicreceptor signaling. Cell 161:1101-1111.
6. Sounier R, et al. (2015) Propagation of conformational changes during-opioidreceptor activation. Nature 524:375-378.
7. Nygaard R, et al. (2013) The dynamic process of-2-adrenergic receptor activation. Cell 152:532-542.
8. Huang W, et al. (2015) Structural insights into-opioid receptor activation. Nature524:315-321.
9. Pande K, et al. (2016) Femtosecond structural dynamics drives the trans/cis isomerizationin photoactive yellow protein. Science 352:725-729.
10. Nango E, et al. (2016) A three-dimensional movie of structural changes in bacteriorhodopsin. Science 354:1552-1557.
11. Turin L (1996) A spectroscopic mechanism for primary olfactory reception. ChemSenses 21:773-791.
12. Turin L (2002) A method for the calculation of odor character from molecular structure. J Theor Biol 216:367-385.
13. Haffenden L, Yaylayan V, Fortin J (2001) Investigation of vibrational theory of olfactionwith variously labelled benzaldehydes. Food Chem 73:67-72.
14. Franco MI, Turin L, Mershin A, Skoulakis EMC (2011) Molecular vibration-sensingcomponent in Drosophila melanogaster olfaction. Proc Natl Acad Sci USA 108:3797-3802.
15. Gane S, et al. (2013) Molecular vibration-sensing component in human olfaction. PLoSOne 8:1-7.
16. GronenbergW, et al. (2014) Honeybees (Apis mellifera) learn to discriminate the smellof organic compounds from their respective deuterated isotopomers. Proc Biol Sci281:20133089.
17. Block E, et al. (2015) Implausibility of the vibrational theory of olfaction. Proc NatlAcad Sci USA 112:E2766-E2774.
18. Keller A, Vosshall LB (2004) A psychophysical test of the vibration theory of olfaction. Nat Neurosci 7:337-338.
19. Dyson GM (1928) Some aspects of the vibration theory of odor. Perfum Essent Oil Rec19:456-459.
20. Wright RH (1954) Odour and molecular vibration. I. Quantum and thermodynamicconsiderations. J Appl Chem 4:611-615.
21. Wright RH, Serenius RSE (1954) Odour and molecular vibration. II. Raman spectra ofsubstances with the nitrobenzene odour. J Appl Chem 4:615-621.
22. Kim J, Matsuyama S, Suzuki T (2004) Deuterated analogues of 4, 8-dimethyldecanal, the aggregation pheromone of Tribolium castaneum: Synthesis and pheromonalactivity. J Labelled Compd Radiopharm 47:921-934.
23. Drimyli E, Gaitanidis A, Maniati K, Turin L, Skoulakis EMC (2016) Differential electrophysiologicalresponses to odorant isotopologues in drosophilid antennae. eNeuro3:015215.
24. Paoli M, et al. (2016) Differential odour coding of isotopomers in the honeybee brain. Sci Rep 6:21893.
25. Wright R (1977) Odor and molecular vibration: Neural coding of olfactory information. J Theor Biol 64:473-502.
26. Wright RH (1983) Molecular vibration and odour blending. Chem Senses 8:103-106.
27. Doolittle RE, Beroza M, Keiser I, Schneider EL (1968) Deuteration of the melon flyattractant, cue-lure, its effect on olfactory response and infra-red absorption. JInsect Physiol 14:1697-1712.
28. Blum MS, Doolittle RE, Beroza M (1971) Alarm pheromones: Utilization in evaluationof olfactory theories. J Insect Physiol 17:2351-2361.
29. Barker RJ, Berdel RL, Waller GD (1973) The molecular basis for scent discrimination:Response to nitrobenzene-d5 of honey bees (Apis mellifera L. ) conditioned withnitrobenzene. Experientia 29:418-419.
30. Wright RH (1975) Odor and molecular vibration: Response to nitrobenzene-d5 ofhoney bees (Apis mellifera L. ) conditioned with nitrobenzene. Experientia 31:530.
31. Turin L, Yoshii F (2003) Structure-odor relations: A modern perspective. Handbook ofOlfaction and Gustation, ed Doty RL (CRC, Oxford), 2nd Ed, pp 457-515.
32. Maia ER, Magalhães DRB, Lerner DA, Berthomieu D, Bernassau JM (2014) Quantumcalculation for musk molecules infrared spectra towards the understanding of odor. Adv Chem 2014:1-13.
33. Chee HK, June OS (2013) Molecular vibration-activity relationship in the agonism ofadenosine receptors. Genomics Inform 11:282-288.
34. Chee HK, Yang JS, Joung JG, Zhang BT, Oh SJ (2015) Characteristic molecular vibrationsof adenosine receptor ligands. FEBS Lett 589:548-552.
35. Oh SJ (2012) Characteristics in molecular vibrational frequency patterns between agonistsand antagonists of histamine receptors. Genomics Inform 10:128-132.
36. Hoehn RD, Nichols D, Hartmut N, Sabre K (2015) Neuroreceptor activation byvibration-assisted tunneling. Sci Rep 5:9990.
37. Klika KD (2013) The potential of 13C isotopomers as a test for the vibrational theoryof olfactory sense recognition. ISRN Org Chem 2013:515810.
38. Turin L, Gane S, Georganakis D, Maniati K, Skoulakis EMC (2015) Plausibility of thevibrational theory of olfaction. Proc Natl Acad Sci USA 112:E3154.
39. Block E, Jang S, Matsunami H, Batista VS, Zhuang H (2015) Reply to turin, et al. : Vibrationaltheory of olfaction is implausible. Proc Natl Acad Sci USA 112:E3155.
40. Kaupp UB (2010) Olfactory signalling in vertebrates and insects: Differences and commonalities. Nat Rev Neurosci 11:188-200.
41. Pellegrino M, Nakagawa T (2009) Smelling the difference: Controversial ideas in insectolfaction. J Exp Biol 212:1973-1979.
42. Barwich AS (2016) What is so special about smell Olfaction as a model system inneurobiology. Postgrad Med J 92:27-33.
43. Crasto CJ (2009) Computational biology of olfactory receptors. Curr Bioinform 4:8-15.
44. Abaffy T (2015) Human olfactory receptors expression and their role in non-olfactorytissues a mini-review. J Pharmacogenomics Pharmacoproteomics 6:152.
45. Kang N, Koo J (2012) Olfactory receptors in non-chemosensory tissues. BMB Rep45:612-622.
46. Feldmesser E, et al. (2006) Widespread ectopic expression of olfactory receptor genes. BMC Genomics 7:121-121.
47. Vanderhaeghen P, Schurmans S, Vassart G, Parmentier M (1993) Olfactory receptorsare displayed on dog mature sperm cells. J Cell Biol 123:1441-1452.
48. Flegel C, et al. (2016) Characterization of the olfactory receptors expressed in humanspermatozoa. Front Mol Biosci 2:73.
49. Malki A, et al. (2015) Class I odorant receptors, TAS1R and TAS2R taste receptors, aremarkers for subpopulations of circulating leukocytes. J Leukoc Biol 97:533-545.
50. Gaudin JC, Breuils L, Haertlé T (2006) Mouse orthologs of human olfactory-like receptorsexpressed in the tongue. Gene 381:42-48.
51. Blache P, Gros L, Salazar G, Bataille D (1998) Cloning and tissue distribution of a newrat olfactory receptor-like (OL2). Biochem Biophys Res Commun 242:669-672.
52. Weber M, Pehl U, Breer H, Strotmann J (2002) Olfactory receptor expressed in gangliaof the autonomic nervous system. J Neurosci Res 68:176-184.
53. Pluznick JL, et al. (2009) Functional expression of the olfactory signaling system in thekidney. Proc Natl Acad Sci USA 106:2059-2064.
54. Goto T, Salpekar A, MonkM(2001) Expression of a testis-specific member of the olfactoryreceptor gene family in human primordial germ cells. Mol Hum Reprod 7:553-558.
55. Drutel G, et al. (1995) Cloning of OL1, a putative olfactory receptor and its expressionin the developing rat heart. Recept Channels 3:33-40.
56. Shulgin A, Shulgin A (1991) PIHKAL: A Chemical Love Story (Transform Press, Berkeley, CA).
57. Shulgin A, Shulgin A (1997) TIHKAL: The Continuation (Transform Press, Berkeley, CA).
58. Krzan M, et al. (2016) The quantum nature of drug-receptor interactions: Deuterationchanges binding affinities for histamine receptor ligands. PLoS One 11:1-16.
59. Ushio-Fukai M (2009) Vascular signaling through G protein coupled receptors-newconcepts. Curr Opin Nephrol Hypertens 18:153-159.
60. Brookes JC, Hartoutsiou F, Horsfield AP, Stoneham AM (2007) Could humans recognizeodor by phonon assisted tunneling Phys Rev Lett 98:038101.
61. Lambe J, Jaklevic RC (1968) Molecular vibration spectra by inelastic electron tunneling. Phys Rev 165:821-832.
62. Kirtley J, Scalapino DJ, Hansma PK (1976) Theory of vibrational mode intensities ininelastic electron tunneling spectroscopy. Phys Rev B 14:3177-3184.
63. Phillips WA, Adkins CJ (1985) A theory for the intensities of inelastic electrontunnellingspectra. Philos Mag B 52:739-750.
64. Frazier JL, Heitz JR (1975) Inhibition of olfaction in the moth Heliothis virescens bythe sulfhydryl reagent fluorescein mercuric acetate. Chem Senses 1:271-281.
65. Jia H, et al. (2016) Enhancement of odor-induced activity in the canine brain by zincnanoparticles: A functional MRI study in fully unrestrained conscious dogs. ChemSenses 41:53-67.
66. Moore CH, et al. (2012) Olfactory responses to explosives associated odorants areenhanced by zinc nanoparticles. Talanta 88:730-733.
67. Wang J, Luthey-Schulten ZA, Suslick KS (2003) Is the olfactory receptor a metalloproteinProc Natl Acad Sci USA 100:3035-3039.
68. Viswaprakash N, et al. (2009) Enhancement of odorant-induced responses in olfactoryreceptor neurons by zinc nanoparticles. Chem Senses 34:547-557.
69. Vodyanoy V (2010) Zinc nanoparticles interact with olfactory receptor neurons. BioMetals 23:1097-1103.
70. Hu C, Chan SI, Sawyer EB, Yu Y, Wang J (2014) Metalloprotein design using geneticcode expansion. Chem Soc Rev 43:6498-6510.
71. Seebungkert B, Lynch JW (2001) A common inhibitory binding site for zinc and odorantsat the voltage-gated K+ channel of rat olfactory receptor neurons. Eur J Neurosci14:353-362.
72. Kinouchi K, Standifer KM, Pasternak GW (1990) Modulation of-1,-2,-opioidbinding by divalent cations. Biochem Pharmacol 40:382-384.
73. Standifer KM, Clark JA, Pasternak GW (1993) Modulation of-1 opioid bindingby magnesium: Evidence for multiple receptor conformations. J Pharm Exp Ther266:106-113.
74. Holst B, Elling CE, Schwartz TW (2002) Metal ion-mediated agonism and agonistenhancement in melanocortin MC1 and MC4 receptors. J Biol Chem 277:47662-47670.
75. Li S, et al. (2016) Smelling sulfur: Copper and silver regulate the response of humanodorant receptor OR2T11 to low-molecular-weight thiols. J Am Chem Soc 138:13281-13288.
76. Block E (2017) Fifty years of smelling sulfur: From the chemistry of garlic to the molecularbasis for olfaction. Phosphorus Sulfur Silicon Relat Elem 192:141-144.
77. Duan X, et al. (2012) Crucial role of copper in detection of metal-coordinating odorants. Proc Natl Acad Sci USA 109:3492-3497.
78. Gerlach LO, et al. (2003) Metal ion enhanced binding of AMD3100 to Asp262 in theCXCR4 receptor. Biochemistry 42:710-717.
79. Rodŕguez FI, et al. (1999) A copper cofactor for the ethylene receptor ETR1 fromArabidopsis. Science 283:996-998.
80. Solov'yov IA, Chang PY, Schulten K (2012) Vibrationally assisted electron transfermechanism of olfaction: Myth or reality Phys Chem Chem Phys 14:13861-13871.
81. Reese A, List NH, Kongsted J, Solov'yov IA (2016) How far does a receptor influencevibrational properties of an odorant PLoS One 11:1-21.
82. Checiń ska A, Pollock FA, Heaney L, Nazir A (2015) Dissipation enhanced vibrationalsensing in an olfactory molecular switch. J Chem Phys 142:025102.
83. Tirandaz A, Taher Ghahramani F, Shafiee A (2015) Dissipative vibrational model forchiral recognition in olfaction. Phys Rev E 92:032724.
84. Bittner ER, Madalan A, Czader A, Roman G (2012) Quantum origins of molecularrecognition and olfaction in Drosophila. J Chem Phys 137:22A551.
85. Rakowski K, Paneth P (1996) Isotope effects on binding. J Mol Struct 378:35-43.
86. Swiderek K, Paneth P (2013) Binding isotope effects. Chem Rev 113:7851-7879.
87. Mathis CA, Hoffman AJ, Nichols DE, Shulgin AT (1988) Synthesis of high specific activity125I-A nd 123I-labelled enantiomers of 2, 5-dimethoxy-4-iodophenylisopropylamine(DOI). J Labelled Comp Radiopharm 25:1255-1265.
88. Besnard J, et al. (2012) Automated design of ligands to polypharmacological profiles. Nature 492:215-220.
89. Zhang Z, Wu J, Yu J, Xiao J (2012) A brief review on the evolution of GPCR: Conservationand diversification. Open J Genet 2:11-17.
90. Brookes JC, Horsfield AP, Stoneham AM (2012) The swipe card model of odorantrecognition. Sensors 12:15709-15749.
91. Saberi M, Seyed-allaei H (2016) Odorant receptors of Drosophila are sensitive to themolecular volume of odorants. Sci Rep 6:25103.
92. Curphey TJ (1979) Trifluoroacetylation of amino acids and peptides by ethyl trifluoroacetate. J Org Chem 44:2805-2807.
93. Chambers JJ, Kurrasch-Orbaugh DM, Parker MA, Nichols DE (2001) Enantiospecificsynthesis and pharmacological evaluation of a series of super-potent, conformationallyrestricted 5-HT2A=2C receptor agonists. J Med Chem 44:1003-1010.
94. Stoll A, Hofmann A (1955) Amide der stereoisomeren lysergsaüren und dihydrolysergsaüren. 38. Mitteilung ü ber mutterkornalkaloide [Amides of the stereoisomersof lysergic acid and dihydrolysergic acid. 38. Report about Ergot alkaloids]. Helv ChimActa 38:421-433. German.