Origin of the low thermal isomerization rate of rhodopsin chromophore

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Yanagawa, Masataka ^a   Kojima, Keiichi ^b   Yamashita, Takahiro ^b   Imamoto, Yasushi ^b   Matsuyama, Take ^b   Nakanishi, Koji ^c   Yamano, Yumiko ^d   Wada, Akimori ^d   Sako, Yasushi ^a   Shichida, Yoshinori ^b  

^a RIKEN   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; PROTEIN BINDING; RHODOPSIN;

CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RETINA; THERMODYNAMICS;

AMINO ACIDS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RETINA; RHODOPSIN; THERMODYNAMICS;

EID: 84931275690     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11081     Document Type: Article

References (36)

1. Stockman, A. & Sharpe, L. T. Into the twilight zone: The complexities of mesopic vision and luminous efficiency. Ophthalmic Physiol Opt 26, 225-239 (2006).
2. Rieke, F. & Baylor, D. A. Single-photon detection by rod cells of the retina. Reviews of Modern Physics 70, 1027-1036 (1998).
3. Yau, K. W., Matthews, G. & Baylor, D. A. Thermal activation of the visual transduction mechanism in retinal rods. Nature 279, 806-7 (1979).
4. Fu, Y., Kefalov, V., Luo, D. G., Xue, T. & Yau, K. W. Quantal noise from human red cone pigment. Nat Neurosci 11, 565-71 (2008).
5. Sakurai, K. et al. Physiological properties of rod photoreceptor cells in green-sensitive cone pigment knock-in mice. J Gen Physiol 130, 21-40 (2007).
6. Shichida, Y. & Matsuyama, T. Evolution of opsins and phototransduction. Philos Trans R Soc Lond B Biol Sci 364, 2881-95 (2009).
7. Akita, H., Tanis, S. P., Adams, M., Baloghnair, V. & Nakanishi, K. Nonbleachable rhodopsins retaining the full natural chromophore. J Am Chem Soc 102, 6370-6372 (1980).
8. Kandori, H. et al. Mechanism of isomerization of rhodopsin studied by use of 11-cis-locked rhodopsin analogues excited with a picosecond laser pulse. Biochemistry 28, 6460-7 (1989).
9. Corson, D. W. et al. Sensitization of bleached rod photoreceptors by 11-cis-locked analogues of retinal. Proc Natl Acad Sci USA 87, 6823-7 (1990).
10. Mizukami, T. et al. Photoisomerization mechanism of the rhodopsin chromophore: Picosecond photolysis of pigment containing 11-cis-locked eight-membered ring retinal. Proc Natl Acad Sci USA 90, 4072-6 (1993).
11. Yanagawa, M., Yamashita, T. & Shichida, Y. Glutamate acts as a partial inverse agonist to metabotropic glutamate receptor with a single amino acid mutation in the transmembrane domain. J Biol Chem 288, 9593-601 (2013).
12. Baylor, D. A., Matthews, G. & Yau, K. W. Two components of electrical dark noise in toad retinal rod outer segments. J Physiol 309, 591-621 (1980).
13. Donner, K., Firsov, M. L. & Govardovskii, V. I. The frequency of isomerization-like 'dark' events in rhodopsin and porphyropsin rods of the bull-frog retina. J Physiol 428, 673-92 (1990).
14. Ala-Laurila, P., Donner, K., Crouch, R. K. & Cornwall, M. C. Chromophore switch from 11-cis-dehydroretinal (A2) to 11-cisretinal (A1) decreases dark noise in salamander red rods. J Physiol 585, 57-74 (2007).
15. Luo, D. G., Yue, W. W., Ala-Laurila, P. & Yau, K. W. Activation of visual pigments by light and heat. Science 332, 1307-12 (2011).
16. Matthews, G. Dark noise in the outer segment membrane current of green rod photoreceptors from toad retina. J Physiol 349, 607-18 (1984).
17. Matsuyama, T., Yamashita, T., Imai, H. & Shichida, Y. Covalent bond between ligand and receptor required for efficient activation in rhodopsin. J Biol Chem 285, 8114-21 (2010).
18. Kojima, K., Imamoto, Y., Maeda, R., Yamashita, T. & Shichida, Y. Rod visual pigment optimizes active state to achieve efficient G protein activation as compared with cone visual pigments. J Biol Chem 289, 5061-73 (2014).
19. Phillips, W. J. & Cerione, R. A. The intrinsic fluorescence of the a subunit of transducin. Measurement of receptor-dependent guanine nucleotide exchange. J Biol Chem 263, 15498-505 (1988).
20. Farrens, D. L. & Khorana, H. G. Structure and function in rhodopsin. Measurement of the rate of metarhodopsin II decay by fluorescence spectroscopy. J Biol Chem 270, 5073-6 (1995).
21. Imai, H. et al. Single amino acid residue as a functional determinant of rod and cone visual pigments. Proc Natl Acad Sci USA 94, 2322-6 (1997).
22. Kuwayama, S., Imai, H., Hirano, T., Terakita, A. & Shichida, Y. Conserved proline residue at position 189 in cone visual pigments as a determinant of molecular properties different from rhodopsins. Biochemistry 41, 15245-52 (2002).
23. Okano, T., Kojima, D., Fukada, Y., Shichida, Y. & Yoshizawa, T. Primary structures of chicken cone visual pigments: Vertebrate rhodopsins have evolved out of cone visual pigments. Proc Natl Acad Sci USA 89, 5932-6 (1992).
24. Hisatomi, O., Ishikawa, M., Tonosaki, A. & Tokunaga, F. Characterization of lamprey rhodopsin by isolation from lamprey retina and expression in mammalian cells. Photochem Photobiol 66, 792-5 (1997).
25. Mendez, A. et al. Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 28, 153-64 (2000).
26. Pepperberg, D. R. Bleaching desensitization: Background and current challenges. Vision Res 43, 3011-9 (2003).
27. Honig, B., Ebrey, T., Callender, R. H., Dinur, U. & Ottolenghi, M. Photoisomerization, energy storage, and charge separation: A model for light energy transduction in visual pigments and bacteriorhodopsin. Proc Natl Acad Sci USA 76, 2503-7 (1979).
28. Barlow, R. B., Birge, R. R., Kaplan, E. & Tallent, J. R. On the molecular origin of photoreceptor noise. Nature 366, 64-6 (1993).
29. Barlow, H. B. Purkinje shift and retinal noise. Nature 179, 255-6 (1957).
30. Gozem, S., Schapiro, I., Ferre, N. & Olivucci, M. The molecular mechanism of thermal noise in rod photoreceptors. Science 337, 1225-8 (2012).
31. Ala-Laurila, P., Donner, K. & Koskelainen, A. Thermal activation and photoactivation of visual pigments. Biophys J 86, 3653-62 (2004).
32. Okada, T. et al. The retinal conformation and its environment in rhodopsin in light of a new 2.2 Å crystal structure. J Mol Biol 342, 571-83 (2004).
33. Choe, H. W. et al. Crystal structure of metarhodopsin II. Nature 471, 651-5 (2011).
34. Lorenz-Fonfria, V. A., Furutani, Y., Ota, T., Ido, K. & Kandori, H. Protein fluctuations as the possible origin of the thermal activation of rod photoreceptors in the dark. J Am Chem Soc 132, 5693-5703 (2010).
35. Piechnick, R. et al. Effect of channel mutations on the uptake and release of the retinal ligand in opsin. Proc Natl Acad Sci USA 109, 5247-52 (2012).
36. Grell, L., Parkin, C., Slatest, L. & Craig, P. A. EZ-Viz, a tool for simplifying molecular viewing in PyMOL. Biochem Mol Biol Educ 34, 402-7 (2006).