How far does a receptor influence vibrational properties of an odorant?

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Reese, Anna ^a   List, Nanna Holmgaard ^a   Kongsted, Jacob ^a   Solov’yov, Ilia A ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACETOPHENONE; ACETOPHENONE DERIVATIVE; CYSTEINE; FRAGRANCE; OLFACTORY RECEPTOR; OPSIN; PENTANOL; TYROSINE;

CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; ELECTRON; HUMAN; INFRARED SPECTROPHOTOMETRY; METABOLISM; MOLECULAR DYNAMICS; ODOR; OLFACTORY RECEPTOR; OLFACTORY RECEPTOR NEURON; PHYSIOLOGY; VIBRATION; X RAY CRYSTALLOGRAPHY;

ACETOPHENONES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; ELECTRONS; HUMANS; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; ODORANTS; OLFACTORY RECEPTOR NEURONS; OPSINS; PENTANOLS; RECEPTORS, ODORANT; SMELL; SPECTROPHOTOMETRY, INFRARED; TYROSINE; VIBRATION;

EID: 85020016015     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0152345     Document Type: Article

References (70)

1. Nelson DL, Cox MM, Lehninger AL. Lehninger principles of biochemistry. 6th ed. New York: W.H. Freeman and Company; 2013.
2. Pfaff DW, editor. Neuroscience in the 21st Century. New York, NY: Springer New York; 2013.
3. Turin L. Rational Odorant Design. In: Rowe DJ, editor. Chemistry and Techonolgy of Flavors and Fragrances. Blackwell Publishing Ltd; 2005. p. 261–273.
4. Brookes JC, Hartoutsiou F, Horsfield AP, Stoneham AM. Could humans recognize odor by phonon assisted tunneling? Phys Rev Lett. 2007; 98:038101–(1–4). doi: 10.1103/PhysRevLett.98.038101 PMID: 17358733
5. Brookes JC, Horsfield AP, Stoneham AM. The swipe card model of odorant recognition. Sensors (Basel, Switzerland). 2012; 12(11):15709–15749. doi: 10.3390/s121115709
6. Franco MI, Turin L, Mershin A, Skoulakis EMC. Molecular vibration-sensing component in Drosophila melanogaster olfaction. Proc Natl Acad Sci USA. 2011; 108:3797–3802. doi: 10.1073/pnas. 1012293108 PMID: 21321219
7. Gane S, Georganakis D, Maniati K, Vamvakias M, Ragoussis N, Skoulakis EMC, et al. Molecular Vibration-Sensing Component in Human Olfaction. PLoS ONE. 2013; 8:e55780. doi: 10.1371/journal.pone. 0055780 PMID: 23372854
8. Checińska A, Pollock FA, Heaney L, Nazir A. Dissipation enhanced vibrational sensing in an olfactory molecular switch. J Chem Phys. 2015; 142(2):025102. doi: 10.1063/1.4905377 PMID: 25591386
9. Hettinger TP. Olfaction is a chemical sense, not a spectral sense. Proc Natl Acad Sci USA. 2011; 108 (31):E349. doi: 10.1073/pnas.1103992108 PMID: 21737743
10. Moncrieff RW. A New Theory of Odor. Perf Essent Oil Rec. 1949; 40:279–285.
11. Moncrieff RW. What is Odor? A New Theory. Am Perf Essent Oil Rev. 1949; 54:453–454.
12. de March CA, Yu Y, Ni MJ, Adipietro KA, Matsunami H, Ma M, et al. Conserved Residues Control Activation of Mammalian G Protein-Coupled Odorant Receptors. J Am Chem Soc. 2015; 137:8611–8616. doi: 10.1021/jacs.5b04659 PMID: 26090619
13. Dyson MG. The scientific basis of odour. J Soc Chem Ind. 1938; 57(28):647–651. doi: 10.1002/jctb. 5000572802
14. Wright RH. Odor and molecular vibration: Neural coding of olfactory information. J Theor Biol. 1977; 64 (3):473–502. doi: 10.1016/0022-5193(77)90283-1 PMID: 839817
15. Turin L. A spectroscopic mechanism for primary olfactory reception. Chem Senses. 1996; 21:773–791. doi: 10.1093/chemse/21.6.773 PMID: 8985605
16. Solov’yov IA, Chang PY, Schulten K. Vibrationally Assisted Electron Transfer Mechanism of Olfaction: Myth or Reality? Phys Chem Chem Phys. 2012; 14:13861–13871. doi: 10.1039/c2cp41436h PMID: 22899100
17. Bittner ER, Madalan A, Czader A, Roman G. Quantum origins of molecular recognition and olfaction in Drosophila. J Chem Phys. 2012; 137(22):22A551. doi: 10.1063/1.4767067 PMID: 23249088
18. Block E, Jang S, Matsunami H, Sekharan S, Dethier B, Ertem MZ, et al. Implausibility of the vibrational theory of olfaction. Proc Natl Acad Sci USA. 2015; 112(21):E2766–E2774. doi: 10.1073/pnas. 1503054112 PMID: 25901328
19. Block E, Jang S, Matsunami H, Batista VS, Zhuang H. Reply to Turin et al.: Vibrational theory of olfaction is implausible. Proc Natl Acad Sci USA. 2015; 112:E3155. doi: 10.1073/pnas.1508443112 PMID: 26045493
20. Turin L, Gane S, Georganakis D, Maniati K, Skoulakis EMC. Plausibility of the vibrational theory of olfaction. Proc Natl Acad Sci USA. 2015; 112:E3154. doi: 10.1073/pnas.1508035112 PMID: 26045494
21. Buck LB, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991; 65:175–187. doi: 10.1016/0092-8674(91)90418-X PMID: 1840504
22. Schmiedeberg K, Shirokova E, Weber HP, Schilling B, Meyerhof W, Krautwurst D. Structural determinants of odorant recognition by the human olfactory receptors OR1A1 and OR1A2. J Struct Biol. 2007; 159(3):400–412. doi: 10.1016/j.jsb.2007.04.013 PMID: 17601748
23. Lai PC, Singer MS, Crasto CJ. Structural activation pathways from dynamic olfactory receptor-odorant interactions. Chem Senses. 2005; 30(9):781–792. doi: 10.1093/chemse/bji070 PMID: 16243965
24. Lupieri P, Nguyen Chuong Ha Hung, Bafghi ZG, Giorgetti A, Carloni P. Computational molecular biology approaches to ligand-target interactions. HFSP journal. 2009; 3(4):228–239. doi: 10.2976/1. 3092784 PMID: 20119480
25. Gelis L, Wolf S, Hatt H, Neuhaus EM, Gerwert K. Prediction of a ligand-binding niche within a human olfactory receptor by combining site-directed mutagenesis with dynamic homology modeling. Ange Chem Int Ed Engl. 2012; 51(5):1274–1278. doi: 10.1002/anie.201103980
26. de March CA, Kim SK, Antonczak S, Goddard WA, Golebiowski J. G protein-coupled odorant receptors: From sequence to structure. Protein Sci. 2015; 24(6):1543–1548. doi: 10.1002/pro.2717 PMID: 26044705
27. 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. 2005; 25 (7):1806–1815. doi: 10.1523/JNEUROSCI.4723-04.2005 PMID: 15716417
28. Baud O, Etter S, Spreafico M, Bordoli L, Schwede T, Vogel H, et al. The mouse eugenol odorant receptor: structural and functional plasticity of a broadly tuned odorant binding pocket. Biochemistry. 2011; 50(5):843–853. doi: 10.1021/bi1017396 PMID: 21142015
29. Park JH, Morizumi T, Li Y, Hong JE, Pai EF, Hofmann KP, et al. Opsin, a structural model for olfactory receptors? Angew Chem Int Ed Engl. 2013; 52(42):11021–11024. doi: 10.1002/anie.201302374 PMID: 24038729
30. Huang K, Rhys A. Theory of Light Absorption and Non-Radiative Transitions in F-Centres. Proc R Soc A. 1950; 204(1078):406–423. doi: 10.1098/rspa.1950.0184
31. Olsen JM, Aidas K, Kongsted J. Excited States in Solution through Polarizable Embedding. J Chem Theory Comput. 2010; 6:3721–3734. doi: 10.1021/ct1003803
32. Olsen JMH, Kongsted J. Molecular Properties through Polarizable Embedding. Adv Quantum Chem. 2011; 61:107–143. doi: 10.1016/B978-0-12-386013-2.00003-6
33. List NH, Beerepoot MTP, Olsen JMH, Gao B, Ruud K, Jensen HJA, et al. Molecular quantum mechanical gradients within the polarizable embedding approach–application to the internal vibrational Stark shift of acetophenone. J Chem Phys. 2015; 142(3):034119. doi: 10.1063/1.4905909 PMID: 25612701
34. Schrödinger Suite 2009 Protein Preparation Wizard; Epik version 2.0, Schrödinger, LLC, New York, NY, 2009; Impact version 5.5, Schrödinger, LLC, New York, NY, 2009; Prime version 2.1, Schrödinger, LLC, New York, NY, 2009.;.
35. Maestro, version 9.0, Schrödinger, LLC, New York, NY, 2009.;.
36. Kaminski GA, Friesner RA, Tirado-Rives J, Jorgensen WL. Evaluation and Reparameterization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides. J Phys Chem B. 2001; 105:6474–6487. doi: 10.1021/jp003919d
37. Small-Molecule Drug Discovery Suite 2014-3; 2014. Glide v, Schrödinger, LLC, New York, NY,.
38. Barragan AM, Crofts AR, Schulten K, Solov’yov IA. Identification of Ubiquinol Binding Motifs at the Qo-Site of the Cytochrome bc1 Complex. J Phys Chem B. 2015; 119:433–447. doi: 10.1021/jp510022w PMID: 25372183
39. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, et al. Scalable Molecular Dynamics with NAMD. J Comp Chem. 2005; 26:1781–1802. doi: 10.1002/jcc.20289
40. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack RL Jr, Evanseck JD, Field MJ, et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B. 1998; 102:3586–3616. doi: 10.1021/jp973084f PMID: 24889800
41. MacKerell AD Jr, Feig M, Brooks CL III. Extending the Treatment of Backbone Energetics in Protein Force Fields: Limitations of Gas-Phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations. J Comp Chem. 2004; 25:1400–1415. doi: 10.1002/ jcc.20065
42. Feller SE, Yin D, Pastor RW, MacKerell A. Molecular dynamics simulation of unsaturated lipid bilayers at low hydration: parameterization and comparison with diffraction studies. Biophys J. 1997; 73:2269–2279. doi: 10.1016/S0006-3495(97)78259-6 PMID: 9370424
43. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of Simple Potential Functions for Simulating Liquid Water. J Chem Phys. 1983; 79:926–935. doi: 10.1063/1.445869
44. Vanommeslaeghe K, Hatcher E, Acharya C, Kundu S, Zhong S, Shim J, et al. CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J Comput Chem. 2010; 31:671–690. doi: 10.1002/jcc.21367 PMID: 19575467
45. Feller SE, Zhang YH, Pastor RW, Brooks BR. Constant pressure molecular dynamics simulation—the Langevin piston method. J Chem Phys. 1995; 103(11):4613–4621. doi: 10.1063/1.470648
46. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, et al. A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules. J Am Chem Soc. 1995; 117 (19):5179–5197. doi: 10.1021/ja00124a002
47. Gagliardi L, Lindh R, Karlström G. Local Properties of Quantum Chemical Systems: The LoProp Approach. J Chem Phys. 2004; 121(10):4494–4500. doi: 10.1063/1.1778131 PMID: 15332879
48. Söderhjelm P, Ryde U. How Accurate Can a Force Field Become? A Polarizable Multipole Model Combined with Fragment-wise Quantum-Mechanical Calculations. J Phys Chem A. 2009; 113:617–627. doi: 10.1021/jp8073514 PMID: 19093829
49. Karlström G, Lindh R, Malmqvist PÅ, Roos BO, Ryde U, Veryazov V, et al. Molcas: A Program Package for Computational Chemistry. Comput Mater Sci. 2003; 28:222–239. doi: 10.1016/S0927-0256(03) 00109-5
50. Aquilante F, Vico LD, Ferré N, Ghigo G, åke Malmqvist P, Neogrády P, et al. MOLCAS 7: The Next Generation. J Comp Chem. 2010; 31:224–247. doi: 10.1002/jcc.21318
51. Zhang DW, Zhang JZH. Molecular fractionation with conjugate caps for full quantum mechanical calculation of protein–molecule interaction energy. J Chem Phys. 2003; 119(7):3599–3605. doi: 10.1063/1. 1591727
52. Becke AD. Density-Functional Thermochemistry. III. The Role of Exact Exchange. J Chem Phys. 1993; 98(7):5648–5652. doi: 10.1063/1.464913
53. Vosko SH, Wilk L, Nusair M. Accurate Spin-Dependent Electron Liquid Correlation Energies for Local Spin Density Calculations: a Critical Analysis. Can J Phys. 1980; 58(8):1200–1211. doi: 10.1139/p80-159
54. Lee C, Yang W, Parr RG. Development of the Colle-Salvetti Correlation-Energy Formula Into a Functional of the Electron Density. Phys Rev. 1988; 37(2):785–789. doi: 10.1103/PhysRevB.37.785
55. Dunning TH. Gaussian Basis Sets for Use in Correlated Molecular Calculations. I. The Atoms Boron through Neon and Hydrogen. J Chem Phys. 1989; 90(2):1007–1023. doi: 10.1063/1.456153
56. Olsen JMH. Development of Quantum Chemical Methods towards Rationalization and Optimal Design of Photoactive Proteins. University of Southern Denmark. Odense, Denmark; 2012.
57. Aidas K, Angeli C, Bak KL, Bakken V, Bast R, Boman L, et al. The Dalton quantum chemistry program system. Wiley Interdisciplinary Reviews: Computational Molecular Science. 2014; 4:269–284. doi: 10. 1002/wcms.1172 PMID: 25309629
58. Dalton, a molecular electronic structure program, Release Dalton2013 4; 2013. http://daltonprogram. org.
59. Freindorf M, Shao Y, Furlani TR, Kong J. Lennard–Jones Parameters for the Combined QM/MM Method using the B3LYP/6-31G*/AMBER Potential. J Comput Chem. 2005; 26(12):1270–1278. doi: 10.1002/jcc.20264 PMID: 15965971
60. Pilmé J, Luppi E, Bergés J, Houée-Lévin C, de la Lande A. Topological analyses of time-dependent electronic structures: application to electron-transfers in methionine enkephalin. J Mol Model. 2014; 20:2368. doi: 10.1007/s00894-014-2368-4 PMID: 25060148
61. Mayne CG, Saam J, Schulten K, Tajkhorshid E, Gumbart JC. Rapid parameterization of small molecules using the force field toolkit. J Comp Chem. 2013; 34:2757–2770. doi: 10.1002/jcc.23422
62. Humphrey W, Dalke A, Schulten K. VMD—Visual Molecular Dynamics. J Molec Graphics. 1996; 14:33–38. doi: 10.1016/0263-7855(96)00018-5
63. Stoneham AM. Phonon coupling and photoionisation cross-sections in semiconductors. J Phys C. 1979; 12(5):891–897. doi: 10.1088/0022-3719/12/5/018
64. Sjulstok E, Olsen JMH, Solov’yov IA. Quantifying electron transfer reactions in biological systems: what interactions play the major role? Scientific Reports. 2015; 5:18446. doi: 10.1038/srep18446 PMID: 26689792
65. Solov’yov IA, Domratcheva T, Schulten K. Separation of photo-induced radical pair in cryptochrome to a functionally critical distance. Scientific Reports. 2014; 4:3845. PMID: 24457842
66. Solov’yov IA, Domratcheva T, Moughal Shahi AR, Schulten K. Decrypting Cryptochrome: Revealing the Molecular Identity of the Photoactivation Reaction. J Am Chem Soc. 2012; 134:18046–18052. doi: 10.1021/ja3074819 PMID: 23009093
67. Marcus RA, Sutin N. Electron transfer in chemistry and biology. Biochim Biophys Acta. 1985; 811:265–322. doi: 10.1016/0304-4173(85)90014-X
68. Zou X, Ma W, Solov’yov IA, Chipot C, Schulten K. Recognition of methylated DNA through methyl-CpG binding domain proteins. Nucleic Acids Research. 2012; 40:2747–2758. doi: 10.1093/nar/gkr1057 PMID: 22110028
69. Chipot C, Pohorille A, editors. Free Energy Calculations. Springer-Verlag Berlin Heidelberg; 2007.
70. Wang M, Gao J, Müller P, Giese B. Electron Transfer in Peptides with Cysteine and Methionine as Relay Amino Acids. Angewandte Chemie International Edition. 2009; 48:4232–4234. doi: 10.1002/ anie.200900827