Light activation of the isomerization and deprotonation of the protonated Schiff base retinal

Journal of Molecular Modeling

Volumn 17, Issue 10, 2011, Pages 2539-2547

  Kubli Garfias, Carlos ^a,b   Salazar Salinas, Karim ^a   Perez Angel, Emily C ^a   Seminario, Jorge M ^a  

^a Texas AandM University   (United States)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Deprotonation; DFT; Excited state potential energy; Isomerization; Light activation; Retinal; Schiff base; TD DFT

Indexed keywords

RETINAL; RHODOPSIN; SCHIFF BASE;

AB INITIO CALCULATION; ABSORPTION; ARTICLE; BINDING KINETICS; CHEMICAL BOND; CHROMATOPHORE; ENERGY; ISOMERIZATION; LIGHT; MOLECULAR ELECTRONICS; PRIORITY JOURNAL; PROTON TRANSPORT; ROTATION;

ISOMERISM; LIGHT; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PHOTOCHEMICAL PROCESSES; PROTEIN BINDING; PROTONS; RETINALDEHYDE; RHODOPSIN; SCHIFF BASES;

EID: 80255127570     PISSN: 16102940     EISSN: 09485023     Source Type: Journal    
DOI: 10.1007/s00894-010-0927-x     Document Type: Article

References (73)

1. MV Trushin 2004 Light-mediated "conversation" among microorganisms Microbiol Res 159 1 10 10.1016/j.micres.2003.11.001 (Pubitemid 38642098)
2. D Fels 2009 Cellular communication through light PLoS ONE 4 1 8 10.1371/journal.pone.0005086
3. G Jékely 2009 Evolution of phototaxis Phil Trans R Soc B 364 2795 2808 10.1098/rstb.2009.0072
4. OA Sytina DJ Heyes CN Hunter ML Groot 2009 Ultrafast catalytic processes and conformational changes in the light-driven enzyme protochlorophyllide oxidoreductase (POR) Biochem Soc Trans 37 387 391 10.1042/BST0370387 1:CAS:528:DC%2BD1MXjsFSmtLo%3D
5. NL Rangel KS Williams JM Seminario 2009 Light-Activated Molecular Conductivity in the Photoreactions of Vitamin D3 J Phys Chem A 113 6740 6744 10.1021/jp811224h 1:CAS:528:DC%2BD1MXmt1Sjsrg%3D
6. Kim TY, Uji-i H, Möller M, Muls B, Hofkens J, Alexiev U (2009) Monitoring the Interaction of a Single G-Protein Key Binding Site with Rhodopsin Disk Membranes upon Light Activation. Biochemistry 48
7. JA Gascón EM Sproviero VS Batista 2006 Computational studies of the primary phototransduction event in visual rhodopsin Acc Chem Res 39 184 193 10.1021/ar050027t
8. T Kakitani H Kakitani 1975 Molecular mechanism for the initial process of visual excitation. I. Model of photoisomerization in rhodopsin and its theoretical basis by quantum mechanical calculation of adiabatic potential J Phys Soc Jpn 38 1455 1463 10.1143/JPSJ.38.1455 1:CAS:528:DyaE2MXlsVehsLk%3D
9. A Warshel 1976 Bicycle-pedal model for the first step in the vision process Nature 260 679 683 10.1038/260679a0 1:CAS:528:DyaE28Xkslertbk%3D
10. RSH Liu GS Hammond 2000 The case of medium-dependent dual mechanisms for photoisomerization: One-bond-flip and Hula-Twist PNAS 97 11153 11158 10.1073/pnas.210323197 1:CAS:528:DC%2BD3cXnsF2rt7k%3D
11. A Yamada T Yamato T Kakitani S Yamamoto 2002 Analysis of Cis-Trans Photoisomerization Mechanism of Rhodopsin Based on the Tertiary Structure of Rhodopsin J Photosci 9 51 54 1:CAS:528:DC%2BD38XpsVyitLs%3D
12. LM Frutos T Andruniów F Santoro N Ferreé M Olivucci 2007 Tracking the excited-state time evolution of the visual pigment with multiconfigurational quantum chemistry PNAS 104 7764 7769 10.1073/pnas. 0701732104 1:CAS:528:DC%2BD2sXmtFCitr0%3D (Pubitemid 47185825)
13. I Schapiro O Weingart V Buss 2009 Bycicle-pedal in a rhodopsin chromophore model J Am Chem Soc 131 16 17 10.1021/ja805586z 1:CAS:528: DC%2BD1cXhsFSjur7M
14. E Jardón-Valadez AN Bondar DJ Tobias 2009 Dynamics of internal water molecules in squid rhodopsin Biophys J 96 2572 2576 10.1016/j.bpj.2008.12. 3927
15. TJA Craddock C Beauchemin JA Tucszynski 2009 Information processing mechanisms in microtubules at physiological temperature: Model predctions for experimetal tests BioSystems 97 28 34 10.1016/j.biosystems.2009.04.001 1:STN:280:DC%2BD1Mvgt1ylsQ%3D%3D
16. K Palczewski T Kumasaka T Hori CA Behnke H Motoshima BA Fox IL Trong DC Teller T Okada RE Stenkamp M Yamamoto M Miyano 2000 Crystal structure of rhodopsin: A G protein-coupled receptor Science 289 739 745 10.1126/science.289. 5480.739 1:CAS:528:DC%2BD3cXlslOqs78%3D (Pubitemid 30650186)
17. V Hornak S Ahuja M Eilers JA Goncalves M Sheves PJ Reeves SO Smith 2010 Light activation of rhodopsin: insights from molecular dynamics simulations guided by solid-state NMR distance restraints J Mol Biol 396 510 527 10.1016/j.jmb.2009.12.003 1:CAS:528:DC%2BC3cXhs1ymu7k%3D
18. E Crocker M Eilers S Ahuja V Hornak A Hirshfeld M Sheves SO Smith 2006 Location of Trp265 in Metarhodopsin II: Implictions for the Activation mehanism of the visual receptor rhodopsin J Mol Biol 357 163 172 10.1016/j.jmb.2005.12. 046 1:CAS:528:DC%2BD28XitlGgsLk%3D (Pubitemid 43339322)
19. AB Patel E Crocker M Eilers A Hirshfeld M Sheves SO Smith 2004 Coupling of retinal isomerization to the activation of rhodopsin PNAS 101 10048 10053 10.1073/pnas.0402848101 1:CAS:528:DC%2BD2cXlvFOhsro%3D (Pubitemid 38891192)
20. EC Yan MA Kazmin Z Ganim JM Hou D Pan BS Chang TP Sakmar RA Mathies 2003 Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin Proc Natl Acad Sci 100 9105 9107 10.1073/pnas.1733801100 (Pubitemid 37033888)
21. OA Smitienko MN Mozgovaya IV Shelaev FE Gostev TB Feldman VA Nadtochenko OM Sarkisov MA Ostrovsky 2010 Femtosecond formation dynamics of primary photoproducts of visual pigment rhodopsin Biochemistry 75 34 45
22. P Kukumura DW McCamant S Yoon DB Wandschneider RA Mathies 2005 Structural observation of the primary isomerization in vision with femtosecond-stimulated Raman Science 310 1006 1009 10.1126/science.1118379 (Pubitemid 41611910)
23. ME Estevez AV Kolesnikov P Ala-Laurila RK Crouch VI Govardovskii MC Cornwall 2009 The 9-methy group of retinal is essential for rapid Meta II decay and phototransduction quenching n red cones J Gen Physiol 134 137 150 10.1085/jgp.200910232 1:CAS:528:DC%2BD1MXhtVKgsbjF
24. NS Vassilieva-Vashakmadze RA Gakhokidze AR Gakhokidze 2008 Mechanism of Photoisomerization of the Rhodopsin Chromophore Biochemistry 73 730 732 1:CAS:528:DC%2BD1cXnvFGnsbk%3D (Pubitemid 351931573)
25. R Vogel M Mahalingam S Lüdeke T Huber F Siebert TP Sakmar 2008 Functional role of the "Ionic Lock" An interhelical hydrogen-bond netwerok in Family a heptahelical rcepetors J Mol Biol 380 648 655 10.1016/j.jmb.2008.05.022 1:CAS:528:DC%2BD1cXnvVKgt70%3D
26. B Isin K Schulten E Tajkhorshid I Bahar 2008 Mechanism of signal propagation upon retinal isomerization: insights from molecular dynamics simulations of rhodopsin restrained by normal modes Biophys J 95 789 803 10.1529/biophysj.107.120691 1:CAS:528:DC%2BD1cXotlKhsL0%3D
27. TE Angel MR Chance K Palczewski 2009 Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G-protein-coupled receptors PNAS 106 8555 8560 10.1073/pnas.0903545106 1:CAS:528: DC%2BD1MXnt1SqsrY%3D
28. JM Seminario L Yan Y Ma 2005 Transmission of vibronic signals in molecular circuits J Phys Chem A 109 9712 9715 10.1021/jp054995p 1:CAS:528:DC%2BD2MXhtV2jsb%2FE (Pubitemid 41609697)
29. JM Seminario L Yan Y Ma 2005 Scenarios for molecular-level signal processing Proc IEEE 93 753 1764 10.1109/JPROC.2005.853541 (Pubitemid 41417794)
30. JM Seminario L Yan 2007 Cascade configuration of logical gates processing information encoded in molecular potentials Int J Quantum Chem 107 754 761 10.1002/qua.21173 1:CAS:528:DC%2BD28XhtlejsbvO (Pubitemid 46114097)
31. JM Seminario L Yan Y Ma 2006 Encoding and Transport of Information in Molecular and Biomolecular Systems IEEE Transact Nanotechnol 5 436 440 10.1109/TNANO.2006.880905 (Pubitemid 44444381)
32. K Salazar-Salinas JM Seminario 2010 Energetics and vibronics analyses of the enzymatic coupled electron-proton transfer from nfsa nitroreductase to trinitrotoluene IEEE Transact Nanotechnol 9 543 553 10.1109/TNANO.2010.2058814
33. PF Salazar JM Seminario 2008 Identifying receptor-ligand interactions through an ab initio approach J Phys Chem B 112 1290 1292 10.1021/jp0768569 1:CAS:528:DC%2BD1cXivFylsQ%3D%3D (Pubitemid 351257497)
34. D Cristancho JM Seminario 2010 Polypeptides in alpha-helix conformation perform as diodes J Chem Phys 132 065102-1 065102-5 10.1063/1.3310387
35. W Kohn 1996 Density functional and density matrix method scaling linearly with the number of atoms Phys Rev Lett 76 3168 3171 10.1103/PhysRevLett.76.3168 1:CAS:528:DyaK28XisVKntb0%3D (Pubitemid 126631441)
36. W Kohn LJ Sham 1965 Self-consistent equations including exchange and correlation effects Phys Rev 140 A1133 A1138 10.1103/PhysRev.140.A1133
37. W Kohn LJ Sham 1965 Quantum density oscillations in an inhomogeneous electron gas Phys Rev 137 A1697 A1705 10.1103/PhysRev.137.A1697
38. Luo Y, Gelmont BL, Woolard DL (2006) In: Seminario JM (ed) "Bio-molecular devices for terahertz frequency sensing," in molecular and nano electronics: analysis, design and simulation, vol 17. Elsevier, Amsterdam, pp 96-140
39. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA, Vreven TJ, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA (2003) Gaussian-2003, Revision C.2. Gaussian Inc, Pittsburgh, PA
40. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery JA Jr, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas O, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ (2009) Gaussian 09, Revision A.02. Gaussian Inc, Wallingford, CT
41. AD Becke 1993 A new mixing of Hartree-Fock and local density-functional theories J Chem Phys 98 1372 1377 10.1063/1.464304 1:CAS:528:DyaK3sXhtlagt7o%3D
42. JP Perdew JA Chevary SH Vosko KA Jackson MR Pederson DJ Singh C Fiolhais 1992 Atoms, molecules, solids, and surfaces: applications of the generalized gradient approximation for exchange and correlation Phys Rev B 46 6671 6687 10.1103/PhysRevB.46.6671 1:CAS:528:DyaK38XlvFyks7c%3D
43. JP Perdew 1986 Density-functional approximation for the correlation energy of the inhomogeneous electron gas Phys Rev B 33 8822 8824 10.1103/PhysRevB.33.8822
44. PC Hariharan JA Pople 1973 The influence of polarization functions on molecular orbital hydrogenation energies Theor Chim Acta 28 213 222 10.1007/BF00533485 1:CAS:528:DyaE3sXhtFGnsL4%3D
45. WJ Hehre R Dithfield JA Pople 1972 Self-Consistent Molecular Orbital Methods. XII. Further Extensions of Gaussian-Type Basis Set for Use in Molecular Orbital Studies of Organic Molecules J Chem Phys 56 2257 2261 10.1063/1.1677527 1:CAS:528:DyaE38XptVemsw%3D%3D
46. VA Rassolov MA Ratner JA Pople PC Redfern LA Curtiss 2001 6-31 G basis set for third-row atoms J Comput Chem 22 976 984 10.1002/jcc.1058 1:CAS:528:DC%2BD3MXjtlGntrk%3D (Pubitemid 32455735)
47. NL Rangel JM Seminario 2006 Molecular electrostatic potential devices on graphite and silicon surfaces J Phys Chem A 110 12298 12302 10.1021/jp064766i 1:CAS:528:DC%2BD28XhtVKqsLbM (Pubitemid 44806875)
48. L Yan Y Ma JM Seminario 2006 Terahertz signal transmission in molecular systems International J High Speed Electron Syst 16 669 675 10.1142/ S0129156406003928 1:CAS:528:DC%2BD28XptlSiurw%3D (Pubitemid 44352519)
49. L Yan Y Ma JM Seminario 2006 Encoding information using molecular vibronics J Nanosci Nanotechnol 6 1 10
50. JM Seminario L Yan Y Ma 2005 Nano-Detectors Using Molecular Circuits Operating at THz Frequencies Proc SPIE 5995 59950R-1 59950R-15
51. JM Seminario L Yan Y Ma 2005 Encoding and transport of information in molecular and biomolecular systems Proc 2005 5th IEEE Conf Nanotechnol 1 65 68
52. JM Seminario C de la Cruz PA Derosa L Yan 2004 Nanometer-size conducting and insulating molecular devices J Phys Chem B 108 17879 17885 10.1021/jp046554w 1:CAS:528:DC%2BD2cXosFSjt7o%3D
53. PA Derosa S Guda JM Seminario 2003 A programmable molecular diode driven by charge-induced conformational changes J Am Chem Soc 125 14240 14241 10.1021/ja035071n 1:CAS:528:DC%2BD3sXosVOgtLc%3D (Pubitemid 37452339)
54. K Wang NL Rangel S Kundu JC Sotelo RM Tovar JM Seminario H Liang 2009 Switchable molecular conductivity J Am Chem Soc 131 10447 10451 10.1021/ja901156x 1:CAS:528:DC%2BD1MXlsFCnu7c%3D
55. JC Sotelo JM Seminario 2007 Biatomic substrates for bulk-molecule interfaces: The PtCo-oxygen interface J Chem Phys 127 244706-1 244706-13 10.1063/1.2799997
56. JC Sotelo JM Seminario 2008 Local reactivity of O2 with Pt3 on Co3Pt and related backgrounds J Chem Phys 128 204701-1 204701-11 10.1063/1.2908824 (Pubitemid 351770640)
57. PA Derosa JM Seminario PB Balbuena 2001 Properties of small bimetallic Ni-Cu clusters J Phys Chem A 105 7917 7925 10.1021/jp0104637 1:CAS:528:DC%2BD3MXlt1Ortb8%3D (Pubitemid 35381701)
58. D Habibollahzadeh M Grodzicki JM Seminario P Politzer 1991 Computational study of the concerted gas-phase triple dissociations of 1, 3, 5-Triazacyclohexane and its 1, 3, 5-Trinitro derivative (RDX) J Phys Chem 95 7699 7702 10.1021/j100173a027 1:CAS:528:DyaK3MXlvVanu7c%3D
59. P Politzer JM Seminario 1993 Computational study of the structure of dinitraminic acid, HN(NO2)2 and the energetics of some possible decomposition steps Chem Phys Lett 216 348 352 10.1016/0009-2614(93)90107-C 1:CAS:528:DyaK2cXotVylsQ%3D%3D
60. JM Seminario MC Concha P Politzer 1995 A density functional/molecular dynamics of the structure of liquid nitromethane J Chem Phys 102 8281 8282 10.1063/1.468960 1:CAS:528:DyaK2MXlvVags7c%3D
61. P Politzer JM Seminario 1993 Energy changes associated with some decomposition steps of 1, 3, 3-trinitroazetidine - a nonlocal density-functional study Chem Phys Lett 207 27 30 10.1016/0009-2614(93)85006-A 1:CAS:528:DyaK3sXkvFCksLg%3D
62. P Politzer J Seminario P Bolduc 1989 A proposed interpretation of the destabilizing effect of hydroxyl-groups on nitroaromatic molecules Chem Phys Lett 158 463 469 10.1016/0009-2614(89)87371-3 1:CAS:528:DyaL1MXlvFersr4%3D
63. JM Seminario MC Concha P Politzer 1992 Calculated structures and relative stabilities of furoxan, some 1, 2 dinitrosoethylenes and other isomers J Comput Chem 13 177 182 10.1002/jcc.540130209 1:CAS:528:DyaK38XhvFegtL4%3D
64. J Murray P Redfern J Seminario P Politzer 1990 Anomalous energy effects in some aliphatic and Alicyclic Aza systems and their nitro-derivatives J Phys Chem A 94 2320 2323 1:CAS:528:DyaK3cXhtlygtr8%3D
65. PF Salazar JM Seminario 2007 Simple energy corrections for precise atomization energies of CHON molecules J Phys Chem A 111 11160 11165 10.1021/jp074940i 1:CAS:528:DC%2BD2sXhtFehu7jI (Pubitemid 350097576)
66. R Send D Sundholm 2007 Stairway to the conical intersection: A computational study of the retinal isomerization J Phys Chem A 111 8766 8773 10.1021/jp073908l 1:CAS:528:DC%2BD2sXpt1OjtLo%3D (Pubitemid 47497590)
67. A Muñoz-Loza IF Galván MA Aguilar ME Martín 2008 Retinal models: Comparison electronic absorption spectra in the gas phase and in methanol solution J Phys Chem B 112 8815 8823 10.1021/jp800244h
68. M Wanko M Hoffmann P Strodel A Koslowski W Thiel F Neese T Frauenheim M Elstner 2005 Calculating absorption shifts for retinal proteins: computational challenges J Phys Chem B 109 3606 3615 10.1021/jp0463060 1:CAS:528: DC%2BD2MXnsVCrtw%3D%3D (Pubitemid 40352332)
69. T Andruniów N Ferré M Olivucci 2004 Structure, initial excited-state relaxation, and energy storage of rhodopsin resolved at the multiconfigurational perturbation theory level PNAS 101 17908 17913 10.1073/pnas.0407997101 (Pubitemid 40054048)
70. IV Rostov RD Amos R Kobayashi G Scalmani MJ Frisch 2010 Studies of the ground and excited-state surfaces of the retinal chromophore using CAM-B3LYP J Phys Chem B 114 5547 5555 10.1021/jp911329g 1:CAS:528:DC%2BC3cXkt1GkurY%3D
71. A Altun S Yokoyama K Morokuma 2008 Mechanism of spectral tuning going from retinal in vacuo to bovine rhodopsin and its mutants: multireference ab initio quantum mechanics/molecular mechanics studies J Phys Chem B 112 16883 16890 10.1021/jp807172h 1:CAS:528:DC%2BD1cXhsVGnsL%2FL
72. TP Sakmar RR Franke HG Khorana 1989 Glutamic acid-113 serves as the retinylidine Schiff base counterion in bovine rhodopsine Proc Natl Acad Sci 86 8309 8313 10.1073/pnas.86.21.8309 1:CAS:528:DyaK3cXnt1CltA%3D%3D (Pubitemid 19286049)
73. K Bravaya A Bochenkova A Granovsky A Nemukhin 2007 An opsin shift in rhodopsin: retinal S0∈→∈S1 excitation in protein, in solution, and in gas phase J Am Chem Soc 129 13035 13042 10.1021/ja0732126 1:CAS:528:DC%2BD2sXhtFeisbfF (Pubitemid 350058344)