Deactivation of rhodopsin in the transition from the signaling state Meta II to Meta III involves a thermal isomerization of the retinal chromophore C = N double bond

Biochemistry

Volumn 42, Issue 33, 2003, Pages 9863-9874

  Vogel, Reiner ^a   Siebert, Friedrich ^a   Mathias, Gerald ^b   Tavan, Paul ^b   Fan, Guibao ^c   Sheves, Mordechai ^c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CHEMICAL BONDS; CHROMOPHORES; DISSOCIATION; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROLYSIS; ISOMERIZATION; LIPIDS; PH EFFECTS; PROBABILITY DENSITY FUNCTION;

RECEPTOR STATES;

PROTEINS;

HYDROXYLAMINE; OPSIN; RHODOPSIN; SCHIFF BASE;

ARTICLE; BINDING KINETICS; CALCULATION; CATALYSIS; CHROMATOPHORE; DISSOCIATION; HYDROLYSIS; INFRARED SPECTROSCOPY; ISOMERISM; PH; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTON TRANSPORT; QUANTUM CHEMISTRY; QUANTUM MECHANICS; SIGNAL TRANSDUCTION; THERMAL ANALYSIS;

ANIMALS; CATTLE; KINETICS; LIGHT; MODELS, BIOLOGICAL; MODELS, CHEMICAL; PHOTOCHEMISTRY; PROTEIN BINDING; RHODOPSIN; RODS (RETINA); SCHIFF BASES; SIGNAL TRANSDUCTION; SPECTROPHOTOMETRY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STEREOISOMERISM;

EID: 0042473251     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi034684+     Document Type: Article

References (58)

1. Menon, S. T., Han, M., and Sakmar, T. P. (2001) Rhodopsin: structural basis of molecular physiology, Physiol. Rev. 81, 1659-1688.
2. Vogel, R., and Siebert, F. (2003) New insights from FTIR spectroscopy into molecular properties and activation mechanisms of the visual pigment rhodopsin, Biospectroscopy 72, 133-148.
3. Okada, T., Ernst, O. P., Palczewski, K., and Hofmann, K. P. (2001) Activation of rhodopsin: new insights from structural and biochemical studies, Trends Biochem. Sci. 26, 318-324.
4. Shichida, Y., and Imai, H. (1998) Visual pigment: G-protein-coupled receptor for light signals, Cell. Mol. Life Sci. 54, 1299-1315.
5. Schoenlein, R. W., Peteanu, L. A., Mathies, R. A., and Shank, C. V. (1991) The first step in vision: femtosecond isomerization of rhodopsin, Science 254, 412-415.
6. Helmreich, E. J. M., and Hofmann, K. P. (1996) Structure and function of proteins in G protein-coupled signal transfer, Biochim. Biophys. Acta 1286, 285-322.
7. Fain, G. L., Matthews, H. R., Cornwall, M. C., and Koutalos, Y. (2001) Adaptation in vertebrate photoreceptors. Physiol. Rev. 81, 117-151.
8. Papermaster, D. S. (1982) Preparation of retinal rod outer segments, Methods Enzymol. 81, 48-52.
9. Melia, T. J., Cowan, C. W., Angleson, J. K., and Wensel, T. G. (1997) A comparison of the efficiency of G protein activation by ligand-free and light-activated forms of rhodopsin, Biophys. J. 73, 3182-3191.
10. Rothschild, K. J., Gillespie, J., and DeGrip, W. J. (1987) Evidence for rhodopsin refolding during the decay of Meta II, Biophys. J. 51, 345-350.
11. Klinger, A. L., and Braiman, M. S. (1992) Structural comparison of metarhodopsin II, metarhodopsin III, and opsin based on kinetic analysis of Fourier transform infrared difference spectra, Biophys. J. 63, 1244-1255.
12. Vogel, R., and Siebert, F. (2001) Conformations of the active and inactive states of opsin, J. Biol. Chem. 276, 38487-38493.
13. Ostroy, S. E., Erhardt, F., and Abrahamson, E. W. (1966) Protein configuration changes in the photolysis of rhodopsin. II. The sequence of intermediates in thermal decay of cattle metarhodopsin in vitro, Biochim. Biophys. Acta 112, 265-277.
14. 1-activating form of photolyzed bovine rhodopsin, Biochemistry 30, 6761-6768.
15. Lewis, J., W., van Kuijk, F. J., Carruthers, J. A., and Kliger, D. S. (1997) Metarhodopsin III formation and decay kinetics: comparison of bovine and human rhodopsin, Vision Res. 37, 1-8.
16. Chabre, M., and Breton, J. (1979) The orientation of the chromophore of vertebrate rhodopsin in the "Meta" intermediate states and the reversibility of the Meta II-Meta III transition, Vision Res. 19, 1005-1018.
17. van Breugel, P. J., Bovee-Geurts, P. H., Bonting, S. L., and Daemen, F. J. (1979) Biochemical aspects of the visual process. XL. Spectral and chemical analysis of metarhodopsin III in photoreceptor membrane suspensions. Biochim. Biophys. Acta 557, 188-198.
18. Reuter, T. (1976) Photoregeneration of rhodopsin and isorhodopsin from metarhodopsin III in the frog retina, Vision Res. 16, 909-917.
19. Heck, M., Schädel, S. A., Maretzki, D., Bartl, F. J., Ritter, E., Palczewski, K., and Hofmann, K. P. (2003) Signaling states of rhodopsin. Formation of the storage form, metarhodopsin III, from active metarhodopsin II, J. Biol. Chem. 278, 3162-3169.
20. Bartl, F. J., Ritter, E., and Hofmann, K. P. (2001) Signaling states of rhodopsin: absorption of light in active Metarhodopsin II generates an all-trans-retinal bound inactive state, J. Biol. Chem. 276, 30161-30166.
21. Vogel, R., Fan, G. B., Sheves, M., and Siebert, F. (2000) The molecular origin of the inhibition of transducin activation in rhodopsin lacking the 9-methyl group of the retinal chromophore: A UV-vis and FTIR spectroscopic study, Biochemistry 39, 8895-8908.
22. Fan, G. B., Siebert, F., Sheves, M., and Vogel, R. (2002) Rhodopsin with 11-cis-locked chromophore is capable of forming an active state photoproduct, J. Biol. Chem. 277, 40229-40234.
23. Delange, F., Bovee-Geurts, P. H., Vanoostrum, J., Portier, M. D., Verdegem, P. J., Lugtenburg, J., and DeGrip, W. J. (1998) An additional methyl group at the 10-position of retinal dramatically slows down the kinetics of the rhodopsin photocascade, Biochemistry 37, 1411-1420.
24. Longstaff, C., and Rando, R. R. (1985) Methylation of the activesite lysine of rhodopsin, Biochemistry 24, 8137-8145.
25. DeGrip, W. J. (1982) Purification of bovine rhodopsin over cancanavalin A-Sepharose, Methods Enzymol. 81, 197-207.
26. Becke, A. D. (1993) Density-Functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98, 5648-5652.
27. Lee, C., Yang, W., and Parr, R. C. (1988) Development of the Colle-Salvetti correlation energy formula into a functional of the electron density, Phys. Rev. B 37, 785-789.
28. Frisch, M. J. (1998) Gaussian 98, Gaussian, Inc., Pittsburgh, PA.
29. Foresman, J. B., and Frisch, Æ. (1996) Exploring chemistry with electronic structure methods, Gaussian, Inc., Pittsburgh, PA.
30. Matthews, R. G., Hubbard, R., Brown, P. K., and Wald, G. (1963) Tautomeric forms of Metarhodopsin, J. Gen. Physiol. 47, 215-240.
31. Siebert, F. (1995) Application of FTIR spectroscopy to the investigation of dark structures and photoreactions of visual pigments, Isr. J. Chem. 35, 309-323.
32. 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.
33. Jäger, F., Fahmy, K., Sakmar, T. P., and Siebert, F. (1994) Identification of glutamic acid 113 as the Schiff base proton acceptor in the Metarhodopsin II photointermediate of rhodopsin, Biochemistry 33, 10878-10882.
34. Rath, P., DeCaluwe, L. L., Bovee-Geurts, P. H., DeGrip, W. J., and Rothschild, K. J. (1993) Fourier transform infrared difference spectroscopy of rhodopsin mutants: light activation of rhodopsin causes hydrogen-bonding change in residue aspartic acid-83 during Meta II formation, Biochemistry 32, 10277-10282.
35. Fahmy, K., Jäger, F., Beck, M., Zvyaga, T. A., Sakmar, T. P., and Siebert, F. (1993) Protonation states of membrane-embedded carboxylic acid groups in rhodopsin and Metarhodopsin II: a Fourier transform infrared spectroscopy study of site-directed mutants. Proc. Natl. Acad. Sci. U.S.A. 90, 10206-10210.
36. Palings, I., Pardoen, J. A., van den Berg, E. M., 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.
37. Siebert, F., and Mäntele, W. (1980) Investigations of the rhodopsin/ Meta I and rhodopsin/Meta II transitions of bovine rod outer segments by means of kinetic infrared spectroscopy, Biophys. Struct. Mech. 6, 147-164.
38. Smith, S. O., Myers, A. B., Pardoen, J. A., Winkel, C., Mulder, P. P. J., Lugtenburg, J., and Mathies, R. (1984) Determination of retinal Schiff base configuration in bacteriorhodopsin, Proc. Natl. Acad. Sci. U.S.A. 81, 2055-2059.
39. Smith, S. O., Pardoen, J. A., Lugtenburg, J., and Mathies, R. A. (1987) Vibrational analysis of the 13-cis-retinal chromophore in dark-adapted bacteriorhodopsin, J. Phys. Chem. 91, 804-819.
40. Nonella, M., and Tavan, P. (1995) An unscaled quantum mechanical force field for p-benzoquinone, Chem. Phys. 199, 19-32.
41. Zhou, X., Mole, S. J., and Liu, R. (1996) Density functional theory of vibrational spectra. 4. Comparison of experimental and calculated frequencies of all-trans-1,3,5,7-octatetraene - The end of normal coordinate analysis? Vib. Spectrosc. 12, 73-79.
42. Nonella, M., Mathias, G., Eichinger, M., and Tavan, P. (2003) Structures of vibrational frequencies of the quinones in Rb. sphaeroides derived by a combined density functional/molecular mechanics approach, J. Phys. Chem. B 107, 316-322.
43. Grossjean, M. F., Tavan, P., and Schulten, K. (1990) Quantum chemical vibrational analysis of the chromophore of bacteriorhodopsin, J. Phys. Chem. 94, 8059-8069.
44. Smith, S. O., Braiman, M. S., Myers, A. B., Pardoen, J. A., Courtin, J. M. L., Winkel, C., Lugtenburg, J., and Mathies, R. A. (1987) Vibrational analysis of the all-trans-retinal chromophore in light-adapted bacteriorhodopsin, J. Am. Chem. Soc. 109, 3108-3125.
45. Groenendijk, G. W., De Grip, W. J., and Daemen, F. J. (1980) Quantitative determination of retinals with complete retention of their geometric configuration, Biochim. Biophys. Acta 617, 430-438.
46. Vogel, R., and Siebert, F. (2002) Conformation and stability of α-helical membrane proteins. 2. Influence of pH and salts on stability and unfolding of rhodopsin, Biochemistry 41, 3536-3545.
47. Vogel, R., Fan, G. B., Siebert, F., and Sheves, M. (2001) Anions stabilize a Metarhodopsin II-like photoproduct with a protonated Schiff base, Biochemistry 40, 13342-13352.
48. Bagley, K. A., Balogh-Nair, V., Croteau, A. A., Dollinger, G., Ebrey, T. G., Eisenstein, L., Hong, M. K., Nakanishi, K., and Vittitow, J. (1985) Fourier transform infrared difference spectroscopy of rhodopsin and its photoproducts at low temperature, Biochemistry 24, 6055-6071.
49. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor, Science 289, 739-745.
50. 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.
51. Pan, D., and Mathies, R. A. (2001) Chromophore structure in Lumirhodopsin and Metarhodopsin I by time-resolved resonance Raman microchip spectroscopy, Biochemistry 40, 7929-7936.
52. Groenendijk, G. W., Jacobs, C. W., Bonting, S. L., and Daemen, F. J. (1980) Dark isomerization of retinals in the presence of phosphatidylethanolamine, Eur. J. Biochem. 106, 119-128.
53. Livnah, N., and Sheves, M. (1993) The Schiff base bond configuration in bacteriorhodopsin and in model compounds, Biochemistry 32, 7223-7228.
54. Parkes, J. H., and Liebman, P. A. (1984) Temperature and pH dependence of the Metarhodopsin I-Metarhodopsin II kinetics and equilibria in bovine rod disk membrane suspensions, Biochemistry 23, 5054-5061.
55. Nishimura, S., Sasaki, J., Kandori, H., Lugtenburg, J., and Maeda, A. (1995) Structural changes in the lumirhodopsin-to-metarhodopsin I conversion of air-dried bovine rhodopsin, Biochemistry 34, 16758-16763.
56. Kuksa, V., Bartl, F., Maeda, T., Jang, G. F., Ritter, E., Heck, M., Van Hooser, J. P., Liang, Y., Filipek, S., Gelb, M. H., Hofmann, K. P., and Palczewski, K. (2002) Biochemical and physiological properties of rhodopsin regenerated with 11-cis-6-ring and 7-ring-retinals, J. Biol. Chem. 277, 42315-42324.
57. Jang, G. F., Kuksa, V., Filipek, S., Bartl, F., Ritter, E., Gelb, M. H., Hofmann, K. P., and Palczewski, K. (2001) Mechanism of rhodopsin activation as examined with ring-constrained retinal analogues and the crystal structure of the ground-state protein, J. Biol. Chem. 276, 26148-26153.
58. Vogel, R., Fan, G. B., Lüdeke, S., Siebert, F., and Sheves, M. (2002) A nonbleachable rhodopsin analogue with a slow photocycle, J. Biol. Chem. 277, 40222-40228.