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

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Abstract

We perform an ab initio analysis of the photoisomerization of the protonated Schiff base of retinal (PSB-retinal) from 11-cis to 11-trans rotating the C10-C11=C12-C13 dihedral angle from 0° (cis) to -180° (trans). We find that the retinal molecule shows the lowest rotational barrier (0.22 eV) when its charge state is zero as compared to the barrier for the protonated molecule which is ∼0.89 eV. We conclude that rotation most likely takes place in the excited state of the deprotonated retinal. The addition of a proton creates a much larger barrier implying a switching behavior of retinal that might be useful for several applications in molecular electronics. All conformations of the retinal compound absorb in the green region with small shifts following the dihedral angle rotation; however, the Schiff base of retinal (SB-retinal) at trans-conformation absorbs in the violet region. The rotation of the dihedral angle around the C11=C12 π-bond affects the absorption energy of the retinal and the binding energy of the SB-retinal with the proton at the N-Schiff; the binding energy is slightly lower at the trans-SB-retinal than at other conformations of the retinal.

a, Rhodopsin protein in cone and rod cells is able to recognize colors. b, Rhodopsin photoreceptor, a transmembrane protein, has a retinal chromophore joined covalently to Lys 296 through a protonated Schiff base linkage (cis-PSB-retinal). In dark conditions, retinal is in cis-conformation. c, Structure of PSB-retinal where the dihedral angle rotates along the orange C11=C12 bond to calculate the potential energy surface of the ground state (S0) and excited state (S1). d, Potential energy surface at ground state (S0) and excited state (S1) for ethene

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References

  1. Trushin MV (2004) Light-mediated “conversation” among microorganisms. Microbiol Res 159:1–10

    Article  Google Scholar 

  2. Fels D (2009) Cellular communication through light. PLoS ONE 4:1–8

    Article  Google Scholar 

  3. Jékely G (2009) Evolution of phototaxis. Phil Trans R Soc B 364:2795–2808

    Article  Google Scholar 

  4. Sytina OA, Heyes DJ, Hunter CN, Groot ML (2009) Ultrafast catalytic processes and conformational changes in the light-driven enzyme protochlorophyllide oxidoreductase (POR). Biochem Soc Trans 37:387–391

    Article  CAS  Google Scholar 

  5. Rangel NL, Williams KS, Seminario JM (2009) Light-Activated Molecular Conductivity in the Photoreactions of Vitamin D3. J Phys Chem A 113:6740–6744

    Article  CAS  Google Scholar 

  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. Gascón JA, Sproviero EM, Batista VS (2006) Computational studies of the primary phototransduction event in visual rhodopsin. Acc Chem Res 39:184–193

    Article  Google Scholar 

  8. Kakitani T, Kakitani H (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

    Article  CAS  Google Scholar 

  9. Warshel A (1976) Bicycle-pedal model for the first step in the vision process. Nature 260:679–683

    Article  CAS  Google Scholar 

  10. Liu RSH, Hammond GS (2000) The case of medium-dependent dual mechanisms for photoisomerization: One-bond-flip and Hula-Twist. PNAS 97:11153–11158

    Article  CAS  Google Scholar 

  11. Yamada A, Yamato T, Kakitani T, Yamamoto S (2002) Analysis of Cis-Trans Photoisomerization Mechanism of Rhodopsin Based on the Tertiary Structure of Rhodopsin. J Photosci 9:51–54

    CAS  Google Scholar 

  12. Frutos LM, Andruniów T, Santoro F, Ferreé N, Olivucci M (2007) Tracking the excited-state time evolution of the visual pigment with multiconfigurational quantum chemistry. PNAS 104:7764–7769

    Article  CAS  Google Scholar 

  13. Schapiro I, Weingart O, Buss V (2009) Bycicle-pedal in a rhodopsin chromophore model. J Am Chem Soc 131:16–17

    Article  CAS  Google Scholar 

  14. Jardόn-Valadez E, Bondar AN, Tobias DJ (2009) Dynamics of internal water molecules in squid rhodopsin. Biophys J 96:2572–2576

    Article  Google Scholar 

  15. Craddock TJA, Beauchemin C, Tucszynski JA (2009) Information processing mechanisms in microtubules at physiological temperature: Model predctions for experimetal tests. BioSystems 97:28–34

    Article  CAS  Google Scholar 

  16. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Trong IL, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289:739–745

    Article  CAS  Google Scholar 

  17. Hornak V, Ahuja S, Eilers M, Goncalves JA, Sheves M, Reeves PJ, Smith SO (2010) Light activation of rhodopsin: insights from molecular dynamics simulations guided by solid-state NMR distance restraints. J Mol Biol 396:510–527

    Article  CAS  Google Scholar 

  18. Crocker E, Eilers M, Ahuja S, Hornak V, Hirshfeld A, Sheves M, Smith SO (2006) Location of Trp265 in Metarhodopsin II: Implictions for the Activation mehanism of the visual receptor rhodopsin. J Mol Biol 357:163–172

    Article  CAS  Google Scholar 

  19. Patel AB, Crocker E, Eilers M, Hirshfeld A, Sheves M, Smith SO (2004) Coupling of retinal isomerization to the activation of rhodopsin. PNAS 101:10048–10053

    Article  CAS  Google Scholar 

  20. Yan EC, Kazmin MA, Ganim Z, Hou JM, Pan D, Chang BS, Sakmar TP, Mathies RA (2003) Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc Natl Acad Sci 100:9105–9107

    Article  Google Scholar 

  21. Smitienko OA, Mozgovaya MN, Shelaev IV, Gostev FE, Feldman TB, Nadtochenko VA, Sarkisov OM, Ostrovsky MA (2010) Femtosecond formation dynamics of primary photoproducts of visual pigment rhodopsin. Biochemistry 75:34–45

    Google Scholar 

  22. Kukumura P, McCamant DW, Yoon S, Wandschneider DB, Mathies RA (2005) Structural observation of the primary isomerization in vision with femtosecond-stimulated Raman. Science 310:1006–1009

    Article  Google Scholar 

  23. Estevez ME, Kolesnikov AV, Ala-Laurila P, Crouch RK, Govardovskii VI, Cornwall MC (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

    Article  CAS  Google Scholar 

  24. Vassilieva-Vashakmadze NS, Gakhokidze RA, Gakhokidze AR (2008) Mechanism of Photoisomerization of the Rhodopsin Chromophore. Biochemistry 73:730–732

    CAS  Google Scholar 

  25. Vogel R, Mahalingam M, Lϋdeke S, Huber T, Siebert F, Sakmar TP (2008) Functional role of the "Ionic Lock"- An interhelical hydrogen-bond netwerok in Family a heptahelical rcepetors. J Mol Biol 380:648–655

    Article  CAS  Google Scholar 

  26. Isin B, Schulten K, Tajkhorshid E, Bahar I (2008) Mechanism of signal propagation upon retinal isomerization: insights from molecular dynamics simulations of rhodopsin restrained by normal modes. Biophys J 95:789–803

    Article  CAS  Google Scholar 

  27. Angel TE, Chance MR, Palczewski K (2009) Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G-protein-coupled receptors. PNAS 106:8555–8560

    Article  CAS  Google Scholar 

  28. Seminario JM, Yan L, Ma Y (2005) Transmission of vibronic signals in molecular circuits. J Phys Chem A 109:9712–9715

    Article  CAS  Google Scholar 

  29. Seminario JM, Yan L, Ma Y (2005) Scenarios for molecular-level signal processing. Proc IEEE 93:753–1764

    Article  Google Scholar 

  30. Seminario JM, Yan L (2007) Cascade configuration of logical gates processing information encoded in molecular potentials. Int J Quantum Chem 107:754–761

    Article  CAS  Google Scholar 

  31. Seminario JM, Yan L, Ma Y (2006) Encoding and Transport of Information in Molecular and Biomolecular Systems. IEEE Transact Nanotechnol 5:436–440

    Article  Google Scholar 

  32. Salazar-Salinas K, Seminario JM (2010) Energetics and vibronics analyses of the enzymatic coupled electron-proton transfer from nfsa nitroreductase to trinitrotoluene. IEEE Transact Nanotechnol 9:543–553

    Article  Google Scholar 

  33. Salazar PF, Seminario JM (2008) Identifying receptor-ligand interactions through an ab initio approach. J Phys Chem B 112:1290–1292

    Article  CAS  Google Scholar 

  34. Cristancho D, Seminario JM (2010) Polypeptides in alpha-helix conformation perform as diodes. J Chem Phys 132:065102-1–065102-5

    Article  Google Scholar 

  35. Kohn W (1996) Density functional and density matrix method scaling linearly with the number of atoms. Phys Rev Lett 76:3168–3171

    Article  CAS  Google Scholar 

  36. Kohn W, Sham LJ (1965) Self-consistent equations including exchange and correlation effects. Phys Rev 140:A1133–A1138

    Article  Google Scholar 

  37. Kohn W, Sham LJ (1965) Quantum density oscillations in an inhomogeneous electron gas. Phys Rev 137:A1697–A1705

    Article  Google Scholar 

  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

    Google Scholar 

  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

    Google Scholar 

  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

    Google Scholar 

  41. Becke AD (1993) A new mixing of Hartree-Fock and local density-functional theories. J Chem Phys 98:1372–1377

    Article  CAS  Google Scholar 

  42. Perdew JP, Chevary JA, Vosko SH, Jackson KA, Pederson MR, Singh DJ, Fiolhais C (1992) Atoms, molecules, solids, and surfaces: applications of the generalized gradient approximation for exchange and correlation. Phys Rev B 46:6671–6687

    Article  CAS  Google Scholar 

  43. Perdew JP (1986) Density-functional approximation for the correlation energy of the inhomogeneous electron gas. Phys Rev B 33:8822–8824

    Article  Google Scholar 

  44. Hariharan PC, Pople JA (1973) The influence of polarization functions on molecular orbital hydrogenation energies. Theor Chim Acta 28:213–222

    Article  CAS  Google Scholar 

  45. Hehre WJ, Dithfield R, Pople JA (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

    Article  CAS  Google Scholar 

  46. Rassolov VA, Ratner MA, Pople JA, Redfern PC, Curtiss LA (2001) 6-31 G* basis set for third-row atoms. J Comput Chem 22:976–984

    Article  CAS  Google Scholar 

  47. Rangel NL, Seminario JM (2006) Molecular electrostatic potential devices on graphite and silicon surfaces. J Phys Chem A 110:12298–12302

    Article  CAS  Google Scholar 

  48. Yan L, Ma Y, Seminario JM (2006) Terahertz signal transmission in molecular systems. International J High Speed Electron Syst 16:669–675

    Article  CAS  Google Scholar 

  49. Yan L, Ma Y, Seminario JM (2006) Encoding information using molecular vibronics. J Nanosci Nanotechnol 6:1–10

    Google Scholar 

  50. Seminario JM, Yan L, Ma Y (2005) Nano-Detectors Using Molecular Circuits Operating at THz Frequencies. Proc SPIE 5995:59950R-1–59950R-15

    Google Scholar 

  51. Seminario JM, Yan L, Ma Y (2005) Encoding and transport of information in molecular and biomolecular systems. Proc 2005 5th IEEE Conf Nanotechnol 1:65–68

    Google Scholar 

  52. Seminario JM, de la Cruz C, Derosa PA, Yan L (2004) Nanometer-size conducting and insulating molecular devices. J Phys Chem B 108:17879–17885

    Article  CAS  Google Scholar 

  53. Derosa PA, Guda S, Seminario JM (2003) A programmable molecular diode driven by charge-induced conformational changes. J Am Chem Soc 125:14240–14241

    Article  CAS  Google Scholar 

  54. Wang K, Rangel NL, Kundu S, Sotelo JC, Tovar RM, Seminario JM, Liang H (2009) Switchable molecular conductivity. J Am Chem Soc 131:10447–10451

    Article  CAS  Google Scholar 

  55. Sotelo JC, Seminario JM (2007) Biatomic substrates for bulk-molecule interfaces: The PtCo-oxygen interface. J Chem Phys 127:244706-1–244706-13

    Article  Google Scholar 

  56. Sotelo JC, Seminario JM (2008) Local reactivity of O2 with Pt3 on Co3Pt and related backgrounds. J Chem Phys 128:204701-1–204701-11

    Article  Google Scholar 

  57. Derosa PA, Seminario JM, Balbuena PB (2001) Properties of small bimetallic Ni-Cu clusters. J Phys Chem A 105:7917–7925

    Article  CAS  Google Scholar 

  58. Habibollahzadeh D, Grodzicki M, Seminario JM, Politzer P (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

    Article  CAS  Google Scholar 

  59. Politzer P, Seminario JM (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

    Article  CAS  Google Scholar 

  60. Seminario JM, Concha MC, Politzer P (1995) A density functional/molecular dynamics of the structure of liquid nitromethane. J Chem Phys 102:8281–8282

    Article  CAS  Google Scholar 

  61. Politzer P, Seminario JM (1993) Energy changes associated with some decomposition steps of 1, 3, 3-trinitroazetidine - a nonlocal density-functional study. Chem Phys Lett 207:27–30

    Article  CAS  Google Scholar 

  62. Politzer P, Seminario J, Bolduc P (1989) A proposed interpretation of the destabilizing effect of hydroxyl-groups on nitroaromatic molecules. Chem Phys Lett 158:463–469

    Article  CAS  Google Scholar 

  63. Seminario JM, Concha MC, Politzer P (1992) Calculated structures and relative stabilities of furoxan, some 1, 2 dinitrosoethylenes and other isomers. J Comput Chem 13:177–182

    Article  CAS  Google Scholar 

  64. Murray J, Redfern P, Seminario J, Politzer P (1990) Anomalous energy effects in some aliphatic and Alicyclic Aza systems and their nitro-derivatives. J Phys Chem A 94:2320–2323

    CAS  Google Scholar 

  65. Salazar PF, Seminario JM (2007) Simple energy corrections for precise atomization energies of CHON molecules. J Phys Chem A 111:11160–11165

    Article  CAS  Google Scholar 

  66. Send R, Sundholm D (2007) Stairway to the conical intersection: A computational study of the retinal isomerization. J Phys Chem A 111:8766–8773

    Article  CAS  Google Scholar 

  67. Muñoz-Loza A, Galván IF, Aguilar MA, Martín ME (2008) Retinal models: Comparison electronic absorption spectra in the gas phase and in methanol solution. J Phys Chem B 112:8815–8823

    Article  Google Scholar 

  68. Wanko M, Hoffmann M, Strodel P, Koslowski A, Thiel W, Neese F, Frauenheim T, Elstner M (2005) Calculating absorption shifts for retinal proteins: computational challenges. J Phys Chem B 109:3606–3615

    Article  CAS  Google Scholar 

  69. Andruniów T, Ferré N, Olivucci M (2004) Structure, initial excited-state relaxation, and energy storage of rhodopsin resolved at the multiconfigurational perturbation theory level. PNAS 101:17908–17913

    Article  Google Scholar 

  70. Rostov IV, Amos RD, Kobayashi R, Scalmani G, Frisch MJ (2010) Studies of the ground and excited-state surfaces of the retinal chromophore using CAM-B3LYP. J Phys Chem B 114:5547–5555

    Article  CAS  Google Scholar 

  71. Altun A, Yokoyama S, Morokuma K (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

    Article  CAS  Google Scholar 

  72. Sakmar TP, Franke RR, Khorana HG (1989) Glutamic acid-113 serves as the retinylidine Schiff base counterion in bovine rhodopsine. Proc Natl Acad Sci 86:8309–8313

    Article  CAS  Google Scholar 

  73. Bravaya K, Bochenkova A, Granovsky A, Nemukhin A (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

    Article  CAS  Google Scholar 

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Acknowledgments

We acknowledge financial support from the U. S. Defense Threat Reduction Agency DTRA through the U. S. Army Research Office, Projects Nos. W91NF-06-1-0231 and W91NF-07-1-0199.

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  1. Department of Chemical Engineering, Texas A&M University, College Station, TX, USA

    Carlos Kubli-Garfias, Karim Salazar-Salinas, Emily C. Perez-Angel & Jorge M. Seminario

  2. Department of Electrical and Computer Engineering, Texas A&M University, College Station, TX, USA

    Carlos Kubli-Garfias, Karim Salazar-Salinas, Emily C. Perez-Angel & Jorge M. Seminario

  3. Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, México, DF, Mexico

    Carlos Kubli-Garfias

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Kubli-Garfias, C., Salazar-Salinas, K., Perez-Angel, E.C. et al. Light activation of the isomerization and deprotonation of the protonated Schiff base retinal. J Mol Model 17, 2539–2547 (2011). https://doi.org/10.1007/s00894-010-0927-x

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