Structural changes in the Schiff base region of squid rhodopsin upon photoisomerization studied by low-temperature FTIR spectroscopy

Biochemistry

Volumn 45, Issue 9, 2006, Pages 2845-2851

  Ota, Toru ^a   Furutani, Yuji ^a,c   Terakita, Akihisa ^b,c   Shichida, Yoshinori ^b,c   Kandori, Hideki ^a,c  

^a NAGOYA INSTITUTE OF TECHNOLOGY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; HYDROGEN BONDS; ISOMERIZATION; ISOMERS; MOLECULAR SPECTROSCOPY; RHODIUM COMPOUNDS;

LOW FREQUENCIES; O-D OR N-D STRETCHES; SCHIFF BASE REGION; SQUID RETINOCHROME; SQUID RHODOPSIN; STRUCTURAL CHANGES; WATER MOLECULES;

INFRARED SPECTROSCOPY;

9 CIS RHODOPSIN; BACTERIORHODOPSIN; BATHORHODOPSIN; ISORHODOPSIN; RHODOPSIN; SCHIFF BASE; UNCLASSIFIED DRUG; WATER;

ARTICLE; HYDROGEN BOND; INFRARED SPECTROSCOPY; ISOMERIZATION; LOW TEMPERATURE PROCEDURES; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SQUID; STRUCTURE ANALYSIS; VIBRATION;

ANIMALS; DECAPODIFORMES; HYDROGEN BONDING; ISOMERISM; MODELS, BIOLOGICAL; PHOTOCHEMISTRY; PROTEIN STRUCTURE, SECONDARY; RHODOPSIN; SCHIFF BASES; SENSORY RHODOPSINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TEMPERATURE; WATER;

BOVINAE; CEPHALOPODA; VERTEBRATA;

EID: 33644679534     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051937l     Document Type: Article

References (48)

1. Hubbard, R., and St. George, R. C. C. (1958) The rhodopsin system of the squid, J. Gen. Physiol. 41, 501-528.
2. Hofmann, K. P., and Helmreich, E. J. M. (1996) Structure and function of proteins in G-protein-coupled signal transfer, Biochim. Biophys. Acta 1286, 285-322.
3. Shichida, Y., and Imai, H. (1998) Visual pigment: G-protein-coupled receptor for light signals, Cell. Mol. Life Sci. 54, 1299-1315.
4. Terakita, A., Koyanagi, M., Tsukamoto, H., Yamashita, T., Miyata, T., and Shichida, Y. (2004) Counterion displacement in the molecular evolution of the rhodopsin family, Nat. Struct. Mol. Biol. 11, 284-289.
5. Kandori, H., Shichida, Y., and Yoshizawa, T. (2001) Photoisomerization in rhodopsin, Biochemistry (Moscow) 66, 1197-1209.
6. Hofmann, K. P. (1986) Effect of GTP on the rhodopsin-G-protein complex by transient formation of extra metarhodopsin II, Biochim. Biophys. Acta 27, 278-281.
7. Zhukovsky, E. A., and Oprian, K. K. (1989) Effect of carboxylic acid side chains on the absorption maximum of visual pigments, Science 17, 928-930.
8. Sakmar, T. P., Franke, R. R., and Khorana, H. G. (1989) Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin, Proc. Natl. Acad. Sci. U.S.A. 86, 8309-8313.
9. Nathans, J. (1990) Determinants of visual pigment absorbance: Identification for the retinylidene Schiffs base counterion in bovine rhodopsin, Biochemistry 29, 9746-9752.
10. Terakita, A., Yamashita, T., and Shichida, T. (2000) Highly conserved glutamic acid in the extracellular IV-V loop in rhodopsins acts as the counterion in retinochrome, a member of the rhodopsin family, Proc. Natl. Acad. Sci. U.S.A. 97, 14263-14267.
11. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, S. X., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor, Science 289, 739-745.
12. a of the protonated Schiff base of bovine rhodopsin. A study with artificial pigments, Biophys. J. 64, 1499-1502.
13. a of the protonated Schiff bases of gecko cone and octopus visual pigments, Biophys. J. 67, 848-854.
14. a of the retinal protonated Schiff base in retinal proteins. A study with model compounds, J. Am. Chem. Soc. 115, 3772-3773.
15. Han, M., and Smith, S. O. (1995) NMR constraints on the location of the retinal chromophore in rhodopsin and bathorhodopsin, Biochemistry 34, 1425-1432.
16. 2H NMR and optical measurements, J. Phys. Chem. A 103, 2274-2281.
17. Buss, V., Sugihara, M., Entel, P., and Hafner, J. (2003) Thr94 and Wat2b effect protonation of the retinal chromophore in rhodopsin, Angew. Chem., Int. Ed. 42, 3245-3247.
18. Sugihara, M., Buss, V., Entel, P., and Hafner, J. (2004) The nature of the complex counterion of the chromophore in rhodopsin, J. Phys. Chem. B 108, 3673-3680.
19. Kandori, H. (2000) Role of internal water molecules in bacteriorhodopsin, Biochim. Biophys. Acta 1460, 177-191.
20. Furutani, Y., and Kandori, H. (2002) Internal water molecules of archaeal rhodopsins, Mol. Membr. Biol. 19, 257-265.
21. Tanimoto, T., Furutani, Y., and Kandori, H. (2003) Structural changes of water in the Schiff base region of bacteriorhodopsin: Proposal of a hydration switch model, Biochemistry 42, 2300-2306.
22. Nagata, T., Terakita, A., Kandori, H., Kojima, D., Shichida, Y., and Maeda, A. (1998) The hydrogen-bonding network of water molecules and the peptide backbone in the region connecting Asp83, Gly120, and Glu113 in bovine rhodopsin, Biochemistry 37, 17216-17222.
23. Teller, D. C., Okada, T., Behnke, C. A., Palczewski, K., and Stenkamp, R. E. (2001) Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G-protein-coupled receptors (GPCRs), Biochemistry 40, 7761-7772.
24. Okada, T., Fujiyoshi, Y., Silow, M., Navarro, J., Landau, E. M., and Shichida, Y. (2002) Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography, Proc. Natl. Acad. Sci. U.S.A. 99, 5982-5987.
25. Furutani, Y., Shichida, Y., and Kandori, H. (2003) Structural changes of water molecules during the photoactivation processes in bovine rhodopsin, Biochemistry 42, 9619-9625.
26. Maeda, A., Shichida, Y., and Yoshizawa, T. (1979) Formation of 7-cis- and 13-cis-retinal pigments by irradiating squid rhodopsin, Biochemistry 18, 1449-1453.
27. Nishimura, S., Kandori, H., Nakagawa, M., Tsuda, M., and Maeda, A. (1997) Structural dynamics of water and the peptide backbone around the Schiff base associated with the light-activated process of octopus rhodopsin, Biochemistry 36, 864-870.
28. Kandori, H., and Shichida, Y. (2000) Direct observation of the bridged water stretching vibrations inside a protein, J. Am. Chem. Soc. 122, 11745-11746.
29. Shibata, M., Tanimoto, T., and Kandori, H. (2003) Water molecules in the Schiff base region of bacteriorhodopsin, J. Am. Chem. Soc. 125, 13312-13313.
30. Shibata, M., and Kandori, H. (2005) FTIR studies of internal water molecules in the Schiff base region of bacteriorhodopsin, Biochemistry 44, 7406-7413.
31. Furutani, Y., Terakita, A., Shichida, Y., and Kandori, H. (2005) FTIR studies of the photoactivation processes in squid retinochrome, Biochemistry 44, 7988-7997.
32. Kandori, H., Belenky, M., and Herzfeld, J. (2002) Vibrational frequency and dipolar orientation of the protonated Schiff base in bacteriorhodopsin before and after photoisomerization, Biochemistry 41, 6026-6031.
33. Shimono, K., Furutani, Y., Kamo, N., and Kandori, H. (2003) Vibrational modes of the protonated Schiff base in pharaonis phoborhodopsin, Biochemistry 42, 7801-7806.
34. Rodman-Gilson, H. S., Honig, B., Croteau, A., Zarrilli, G., and Nakanishi, K. (1998) Analysis of the factors that influence the C=N stretching frequency of polyene Schiff bases. Implications for bacteriorhodopsin and rhodopsin, Biophys. J. 53, 261-269.
35. Baasov, T., Friedman, N., and Sheves, M. (1987) Factors affecting the C=N stretching in protonated retinal Schiff base: A model study for bacteriorhodopsin and visual pigments, Biochemistry 26, 3210-3217.
36. Huang, L., Deng, H., Weng, G., Koutalos, Y., Ebrey, T., Groesbeek, M., Lugtenburg, J., Tsuda, M., and Callender, R. H. (1996) A resonance Raman study of the C=N configurations of octopus rhodopsin, bathorhodopsin, and isorhodopsin, Biochemistry 35, 8504-8510.
37. Palings, I., Pardoen, J. A., van den Berg, E., Winkel, C., Lugtenburg, J., and Mathies, R. A. (1987) Assignment of fingerprint vibrations in the resonance Raman spectra of rhodopsin, isorhodopsin, and bathorhodopsin: Implications for chromophore structure and environment, Biochemistry 26, 2544-2556.
38. Luecke, H., Schobert, B., Richter, H. T., Cartailler, J. P., and Lanyi, J. K. (1999) Structure of bacteriorhodopsin at 1.55 Å resolution, J. Mol. Biol. 297, 899-911.
39. Kolbe, M., Besir, H., Essen, L. O., and Oesterhelt, D. (2000) Structure of the light-driven chloride pump halorhodopsin at 1.8 Å resolution, Science 288, 1390-1396.
40. Luecke, H., Schobert, B., Lanyi, J. K., Spudich, E. N., and Spudich, J. L. (2001) Crystal structure of sensory rhodopsin II at 2.4 angstroms: Insights into color tuning and transducer interaction, Science 293, 1499-1503.
41. Royant, A., Nollert, P., Edman, K., Neutze, R., Landau, E. M., Pebay-Peyroula, E., and Navarro, J. (2001) X-ray structure of sensory rhodopsin II at 2.1-Å resolution, Proc. Natl. Acad. Sci. U.S.A. 98, 10131-10136.
42. Vogeley, L., Sineshchekov, O. A., Trivedi, V. D., Sasaki, J., Spudich, J. L., and Luecke, H. (2004) Anabaena sensory rhodopsin: A photochromic color sensor at 2.0 Å, Science 306, 1390-1393.
43. Mathies, R. A., and Lugtenburg, J. (2000) The primary photoreaction of rhodopsin, in Handbook of Biological Physics (Stavenga, D. G., de Grip, W. J., and Pugh, E. N., Eds.) Vol. 3, pp 55-90, Elsevier, Amsterdam.
44. Kandori, H., Furutani, Y., Shimono, K., Shichida, Y., and Kamo, N. (2001) Internal water molecules of pharaonis phoborhodopsin studied by low-temperature infrared spectroscopy, Biochemistry 40, 15693-15698.
45. Furutani, Y., Kawanabe, A., Jung, K.-H., and Kandori, H. (2005) FTIR spectroscopy of the all-trans form of Anabaena sensory rhodopsin at 77 K: Hydrogen bond of a water between the Schiff base and Asp75, Biochemistry 44, 12287-12296.
46. Druckmann, S., Ottolenghi, M., Pande, A., Pande, J., and Callender, R. H. (1982) Acid-base equilibrium of the Schiff base in bacteriorhodopsin, Biochemistry 21, 4953-4959.
47. Iwamoto, M., Furutani, Y., Sudo, Y., Shimono, K., Kandori, H., and Kamo, N. (2002) Role of Asp193 in chromophore-protein interaction of pharaonis phoborhodopsin (sensory rhodopsin II), Biophys. J. 83, 1130-1135.
48. Janz, J. M., and Farrens, D. L. (2004) Role of the retinal hydrogen bond network in rhodopsin Schiff base stability and hydrolysis, J. Biol. Chem. 279, 55886-55894.