Русская версия English version   
Том 13   Выпуск 1   Год 2018
Шигаев А.С., Фельдман Т.Б., Надточенко В.А., Островский М.А., Лахно В.Д.

Исследование фотоизомеризации хромофора родопсина на основе квантово-классической модели

Математическая биология и биоинформатика. 2018;13(1):169-186.

doi: 10.17537/2018.13.169.

Список литературы

 

  1. Lamb T.D., Collin S.P., Pugh E.N.Jr. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat. Rev. Neurosci. 2007;8:960–976. doi: 10.1038/nrn2283
  2. Menon S.T., Han M., Sakmar T.P. Rhodopsin: Structural Basis of Molecular Physiology. Physiol. Rev. 2001;81:1659–1688. doi: 10.1152/physrev.2001.81.4.1659
  3. Spudich J.L., Yang C.S., Jung K.H., Spudich E.N. Retinylidene Proteins: Structures and Functions from Archaea to Humans. Annu. Rev. Cell Dev. Biol. 2000;16:365–392. doi: 10.1146/annurev.cellbio.16.1.365
  4. Nadtochenko V.A., Smitienko O.A., Feldman T.B., Mozgovaya M.N., Shelaev I.V., Gostev F.E., Sarkisov O.M., Ostrovsky M.A. Conical intersection participation in femtosecond dynamics of visual pigment rhodopsin chromophore cis-trans photoisomerization. Dokl. Biochem. Biophys. 2012;446:242–246. doi: 10.1134/S1607672912050080
  5. Polli D., Altoe P., Weingart O., Spillane K.M., Manzoni C., Brida D., Tomasello G., Orlandi G., Kukura P., Mathies R.A., Garavelli M., Cerullo G. Conical intersection dynamics of the primary photoisomerization event in vision. Nature. 2010;467:440–443. doi: 10.1038/nature09346
  6. Yabushita A., Kobayashi T., Tsuda M. Time-resolved spectroscopy of ultrafast photoisomerization of octopus rhodopsin under photoexcitation. J. Phys. Chem. B. 2012;116:1920–1926. doi: 10.1021/jp209356s
  7. Dartnall H.J. The photosensitivities of visual pigments in the presence of hydroxylamine. Vision Res. 1968;8:339–358. doi: 10.1016/0042-6989(68)90104-1
  8. Kandori H., Matuoka S., Shichida Y., Yoshizawa T., Ito M., Tsukida K., Balogh-Nair V., Nakanishi K. Mechanism of isomerisation of rhodopsin studied by use of 11-cis-locked rhodopsin analogues excited with a picoseconds laser pulse. Biochemistry. 1989;28:6460–6467. doi: 10.1021/bi00441a045
  9. Mizukami T., Kandori H., Shichida Y., Chen A.-H., Derguini F., Caldwell C.G., Biffe C., Nakanishi K., Yoshizawa T. Photoisomerization mechanism of the rhodopsin chromophore: picosecond photolysis of pigment containing 11-cis-locked eight-membered ring retinal. Proc. Natl. Acad. Sci. USA. 1993;90:4072–4076. doi: 10.1073/pnas.90.9.4072
  10. Peteanu L.A., Schoenlein R.W., Wang Q., Mathies R.A., Shank C.V. The first step in vision occurs in femtoseconds: complete blue and red spectral studies. Proc. Natl. Acad. Sci. USA. 1993;90:11762–11766. doi: 10.1073/pnas.90.24.11762
  11. Schoenlein R.W., Peteanu L.A., Mathies R.A., Shank C.V. The first step in vision: femtosecond isomerization of rhodopsin. Science. 1991;254:412–415. doi: 10.1126/science.1925597
  12. Johnson P.J.M., Halpin A., Morizumi T., Prokhorenko V.I., Ernst O.P., Miller R.J.D. Local vibrational coherences drive the primary photochemistry of vision. Nat. Chem. 2015;7:980–986. doi: 10.1038/nchem.2398
  13. Schnedermann C., Liebel M., Kukura P. Mode-specificity of vibrationally coherent internal conversion in rhodopsin during the primary visual event. J. Am. Chem. Soc. 2015;137:2886–2891. doi: 10.1021/ja508941k
  14. Smitienko O., Nadtochenko V., Feldman T., Balatskaya M., Shelaev I., Gostev F., Sarkisov O., Ostrovsky M. Femtosecond laser spectroscopy of the rhodopsin photochromic reaction: a concept for ultrafast optical molecular switch creation (ultrafast reversible photoreaction of rhodopsin). Molecules. 2014;19:18351–18366. doi: 10.3390/molecules191118351
  15. Smitienko O.A., Mozgovaya M.N., Shelaev I.V., Gostev F.E., Feldman T.B., Nadtochenko V.A., Sarkisov O.M., Ostrovsky M.A. Femtosecond formation dynamics of primary photoproducts of visual pigment rhodopsin. Biochemistry (Moscow). 2010;75:25–35. doi: 10.1134/S0006297910010049
  16. Worth G.A., Cederbaum L.S. Beyond Born-Oppenheimer: molecular dynamics through a conical intersection. Annu. Rev. Phys. Chem. 2004;55:127–158. doi: 10.1146/annurev.physchem.55.091602.094335
  17. Gonzalez-Luque R., Garavelli M., Bernardi F., Merchan M., Robb M.A., Olivucci M. Computational evidence in favor of a two-state, two-mode model of the retinal chromophore photoisomerization. Proc. Natl. Acad. Sci. USA. 2000;97:9379–9384. doi: 10.1073/pnas.97.17.9379
  18. Polli D., Rivalta I., Nenov A., Weingart O., Garavelli M., Cerullo G. Tracking the primary photoconversion events in rhodopsins by ultrafast optical spectroscopy. Photochem. Photobiol. Sci. 2015;14:213–228. doi: 10.1039/C4PP00370E
  19. Schapiro I., Ryazantsev M.N., Frutos L.M., Ferre N., Lindh R., Olivucci M. The ultrafast photoisomerizations of rhodopsin and bathorhodopsin are modulated by bond length alternation and HOOP driven electronic effects. J. Am. Chem. Soc. 2011;133:3354–3364. doi: 10.1021/ja1056196
  20. Abe M., Ohtsuki Y., Fujimura Y., Domcke W. Optimal control of ultrafast cis-trans photoisomerization of retinal in rhodopsin via a conical intersection. J. Chem. Phys. 2015;123:144508. doi: 10.1063/1.2034488
  21. Levine B.G., Martinez T.M. Isomerization through conical intersections. Annu. Rev. Phys. Chem. 2008;58:613–634. doi: 10.1146/annurev.physchem.57.032905.104612
  22. Tomasello G., Olaso-Gonzalez G., Altoe P., Stenta M., Serrano-Andres L., Merchan M., Orlandi G., Bottoni A., Garavelli M. Electrostatic control of the photoisomerization efficiency and optical properties in visual pigments: on the role of counterion quenching. J. Am. Chem. Soc. 2009;131:5172–5186. doi: 10.1021/ja808424b
  23. Kochendoerfer G.G., Mathies R.A. Spontaneous emission study of the femtosecond isomerization dynamics of rhodopsin. J. Phys.Chem. 1996;100:14526–14532. doi: 10.1021/jp960509+
  24. Lakhno V.D., Shigaev A.S., Feldman T.B., Ostrovsky M.A., Nadtochenko V.A. Quantum-classical model of retinal photoisomerization reaction in visual pigment rhodopsin. Doklady Biochemistry and Biophysics. 2016;471(1):435-439. doi: 10.1134/S1607672916060168
  25. Chung W.C., Nanbu S., Ishida T. QM/MM trajectory surface hopping approach to photoisomerization of rhodopsin and isorhodopsin: the origin of faster and more efficient isomerization for rhodopsin. J. Phys. Chem. B. 2012;116:8009–8023. doi: 10.1021/jp212378u
  26. Rivalta I., Nenov A., Weingart O., Cerullo G., Garavelli M., Mukamel S. Modelling time-resolved two-dimensional electronic spectroscopy of the primary photoisomerization event in rhodopsin. J. Phys. Chem. B. 2014;118:8396–8405. doi: 10.1021/jp502538m
  27. Tscherbul T.V., Brumer P. Quantum coherence effects in natural light-induced processes: cis–trans photoisomerization of model retinal under incoherent excitation. Phys. Chem. Chem. Phys. 2015;17:30904–30913. doi: 10.1039/C5CP01388G
  28. Weingart O., Altoe P., Stenta M., Bottoni A., Orlandi G., Garavelli M. Product formation in rhodopsin by fast hydrogen motions. Phys. Chem. Chem. Phys. 2011;13:3645–3648. doi: 10.1039/c0cp02496a
  29. Weingart O., Garavelli M. Modelling vibrational coherence in the primary rhodopsin photoproduct. J. Chem. Phys. 2012;137:22A523.
  30. Honig B., Karplus M. Implications of torsional potential of retinal isomers for visual excitation. Nature. 1971;229:558–560. doi: 10.1038/229558a0
  31. Warshel A. Multiscale modeling of biological functions: from enzymes to molecular machines (Nobel Lecture). Angew. Chem. Int. Ed. Engl. 2014;53(38):10020–10031. doi: 10.1002/anie.201403689
  32. Andruniow T., Ferre N., Olivucci M. Structure, initial excited-state relaxation, and energy storage of rhodopsin resolved at the multiconfigurational perturbation theory level. Proc. Natl. Acad. Sci. USA. 2004;101:17908–17913. doi: 10.1073/pnas.0407997101
  33. Borhan B., Soutu M.L., Imai H., Shichida Y., Nakanishi K. Movement of retinal along the visual transduction path. Science. 2000;288:2209–2212. doi: 10.1126/science.288.5474.2209
  34. Liu R.S.H. Photoisomerization by hula-twist: a fundamental supramolecular photochemical reaction. Acc. Chem. Res. 2001;34:555–562. doi: 10.1021/ar000165c
  35. Liu R.S., Yang L.Y., Liu J. Mechanisms of photoisomerization of polyenes in confined media: from organic glasses to protein binding cavities. Photochem. Photobiol. 2007;83:2–10.
  36. Nakamichi H., Okada T. Crystallographic analysis of primary visual photochemistry. Angew. Chem. Int. Ed. 2006;45:4270–4273. doi: 10.1002/anie.200600595
  37. Smith S.O., Courtin J., de Groot H.J.M., Gebhard M., Lugtenburg J. 13C magic-angle spinning NMR studies of bathorhodopsin, the primary photoproduct of rhodopsin. Biochemistry. 1991;30:7409–7415. doi: 10.1021/bi00244a007
  38. Saam J., Tajkhorshid E., Hayashi S., Schulten K. Molecular dynamics investigation of primary photoinduced events in the activation of rhodopsin. Biophys. J. 2002;83:3097–3112. doi: 10.1016/S0006-3495(02)75314-9
  39. Yamada A., Yamato T., Kakitani T., Yamamoto S. Torsion potential works in rhodopsin. Photochem. Photobiol. 2014;79:476–486. doi: 10.1562/WB-03-10.1
  40. Kholmurodov Kh.T., Feldman T.B., Ostrovsky M.A. Visual pigment rhodopsin: molecular dynamics of 11-cis-retinal chromophore and amino-acid residues in the chromophore center. Computer simulation study, Mendeleev comm. 2006;1:1–8.
  41. Isin B., Schulten K., Tajkhorshid E., Bahar I. Mechanism of signal propagation upon retinal isomerization: insights from molecular dynamics simulations of rhodopsin restrained by normal modes. Biophys. J. 2008;95:789–803. doi: 10.1529/biophysj.107.120691
  42. Holstein T. Studies of polaron motion: Part I. The molecular-crystal model. Ann. Phys. 1959;8:325–342. doi: 10.1016/0003-4916(59)90002-8
  43. Davydov A.S. The theory of contraction of proteins under their excitation. J. Theor. Biology. 1973;38:559–569. doi: 10.1016/0022-5193(73)90256-7
  44. Davydov A.S. Solitons and energy transfer along protein molecules. J. Theor. Biology. 1977;66:379–387. doi: 10.1016/0022-5193(77)90178-3
  45. Physics in One Dimension. Ed. Bernassoni J. Springer-Verlag, 1981. (Springer series in solid-state sciences. Vol. 23).
  46. Okahata Y., Kobayashi T., Tanaka K., Shimomura M.J. Anisotropic Electric Conductivity in an Aligned DNA Cast Film. J. Am. Chem. Soc. 1998;120:6165–6166. doi: 10.1021/ja980165w
  47. Modern Methods for Theoretical Physical Chemistry of Biopolymers. Eds. Starikov E.B., Lewis J.P., Tanaka S. Elsevier, 2006. ISBN: 9780080461014.
  48. Cramer T., Steinbrecher T., Labahn A., Koslowski T. Static and dynamic aspects of DNA charge transfer: a theoretical perspective. Phys. Chem. Chem. Phys. 2005;7:4039–4050. doi: 10.1039/b507454a
  49. Lakhno V.D. Oscilations in the primary charge separation in bacterial photosynthesis. Phys. Chem. Chem. Phys. 2002;4:2246–2250. doi: 10.1039/b102700j
  50. Lakhno V.D. Dynamical theory of primary processes of charge separation in the photosynthetic reaction center. J. Biol. Phys. 2005;31:145–159. doi: 10.1007/s10867-005-5109-1
  51. Komineas S., Kalosakas G., Bishop A.R. Effects of intrinsic base-pair fluctuations on charge transport in DNA. Phys. Rev. E. 2002;65:061905. doi: 10.1103/PhysRevE.65.061905
  52. Maniadis P., Kalosakas G., Rasmussen K.O., Bishop A.R. AC conductivity in a DNA charge transport model. Phys. Rev. E. 2005;72:021912. doi: 10.1103/PhysRevE.72.021912
  53. Diaz E., Lima R.P.A., Dominguez-Adame F. Bloch-like oscillations in the Peyrard-Bishop-Holstein model. Phys. Rev. B. 2008;78:134303. doi: 10.1103/PhysRevB.78.134303
  54. Lakhno V.D., Sultanov V.B., Montgomery Pettitt B. Combined hopping–superexchange model of a hole transfer in DNA. Chem. Phys. Lett. 2004;400:47–53. doi: 10.1016/j.cplett.2004.10.077
  55. Shigaev A.S., Ponomarev O.A., Lakhno V.D. A new approach to microscopic modeling of a hole transfer in heteropolymer DNA. Chem. Phys. Lett. 2011;513:276–279. doi: 10.1016/j.cplett.2011.07.080
  56. Korshunova A.N., Lakhno V.D. A new type of localized fast moving electronic excitations in molecular chains. Physica E. 2014;60:206–209. doi: 10.1016/j.physe.2014.02.025
  57. Ganter U.M., Schmid E.D., Perez-Sala D., Rando R.R., Siebert F. Removal of the 9-methyl group of retinal inhibits signal transduction in the visual process. A Fourier transform infrared and biochemical investigation. Biochemistry. 1989;28:5954–5962. doi: 10.1021/bi00440a036
  58. Han M., Groesbeek M., Smith S.O., Sakmar T.P. Role of the C9 methyl group in rhodopsin activation: characterization of mutant opsins with the artificial chromophore 11-cis-9-demethylretinal. Biochemistry. 1998;37:538–545. doi: 10.1021/bi972060w
  59. Meyer C.K., Bohme M., Ockenfels A., Gartner W., Hofmann K.P, Ernst O.P. Signaling states of rhodopsin. Retinal provides a scaffold for activating proton transfer switches. J. Biol. Chem. 2000;275:19713–19718. doi: 10.1074/jbc.M000603200
  60. Lemaitre V., Yeagle P., Watts A. Molecular dynamics simulations of retinal in rhodopsin: from the dark-adapted state towards lumirhodopsin. Biochemistry. 2005;44:12667–12680. doi: 10.1021/bi0506019
  61. Kholmurodov Kh.T., Feldman T.B., Ostrovskii M.A. Molecular dynamics simulation and experimental studies of the visual pigment rhodopsin: multiple conformational states and structural changes. In: Molecular Simulation Studies in Material and Biological Sciences. Ed. Kh.T. Kholmurodov, N.Y.: Nova Science Publishers Inc., 2007. P. 85–113.
  62. Lin S.W., Groesbeek M., van der Hoef I., Verdegem P., Lugtenburg J., and Mathies R.A. Vibrational assignment of torsional normal modes of rhodopsin: probing excited-state isomerization dynamics along the reactive C11dC12 torsion coordinate. J. Phys. Chem. B. 1998;102:2787–2806. doi: 10.1021/jp972752u
  63. Kim J.E., Mathies R.A. Anti-stokes Raman study of vibrational cooling dynamics in the primary photochemistry of rhodopsin. J. Phys. Chem. A. 2002;106:8508–8515. doi: 10.1021/jp021069r
  64. Fialko N.S., Lakhno V.D. Nonlinear dynamics of excitations in DNA. Phys. Lett. A. 2000;278:108–112. doi: 10.1016/S0375-9601(00)00755-6
  65. Wang Q., Schoenlein R.W, Peteanu L.A., Mathies R.A., Shank C.V. Vibrationally coherent photochemistry in the femtosecond primary event of vision. Science. 1994;266:422–424. doi: 10.1126/science.7939680
  66. Feldman T.B., Smitienko O.A., Shelaev I.V., Gostev F.E., Nekrasova O.V., Dolgikh D.A., Nadtochenko V.A., Kirpichnikov M.P., Ostrovsky M.A. Femtosecond spectroscopic study of photochromic reactions of bacteriorhodopsin and visual rhodopsin. J. Photochem. Photobiol. B: Biology. 2016;164:296–305. doi: 10.1016/j.jphotobiol.2016.09.041
  67. Cooper A. Energy uptake in the first step of visual excitation. Nature. 1979;282:531–533. doi: 10.1038/282531a0
  68. Birge R.R., Cooper T.M. Energy storage in the primary step of the photocycle of bacteriorhodopsin. Biophys. J. 1983;42:61–69. doi: 10.1016/S0006-3495(83)84369-0
Содержание Оригинальная статья
Мат. биол. и биоинф.
2018;13(1):169-186
doi: 10.17537/2018.13.169
опубликована на рус. яз.

Аннотация (рус.)
Аннотация (англ.)
Полный текст (рус., pdf)
Список литературы

 

  Copyright ИМПБ РАН © 2005-2024