The steric trigger in rhodopsin activation

Journal of Molecular Biology

Volumn 269, Issue 3, 1997, Pages 373-384

  Shieh, Ted ^a   Han, May ^b   Sakmar, Thomas P ^b   Smith, Steven O ^a  

^a YALE UNIVERSITY   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

G protein coupled receptor; Membrane protein; Retinal; Rhodopsin; Visual pigment

Indexed keywords

BATHORHODOPSIN; MEMBRANE RECEPTOR; RECEPTOR BLOCKING AGENT; RETINAL; RHODOPSIN; VISUAL PIGMENT;

ARTICLE; BINDING SITE; CHROMATOPHORE; ISOMERISM; LIGHT; NUCLEAR MAGNETIC RESONANCE; PHOTOACTIVATION; PRIORITY JOURNAL; RECEPTOR BINDING; STRUCTURE ACTIVITY RELATION;

VERTEBRATA;

EID: 0031566429     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1035     Document Type: Article

References (80)

1. Altenbach C., Yang K., Farrens D. L., Farahbaksh Z. T., Khorana H. G., Hubbell W. L. Structural features and light-dependent changes in the cytoplasmic interhelical E-F loop region of rhodopsin: a site-directed spin-labeling study. Biochemistry. 35:1996;12470-12478.
2. Arnis S., Hofmann K. P. Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling state. Proc. Natl Acad. Sci. USA. 90:1993;7849-7853.
3. Arnis S., Fahmy K., Hofmann K. P., Sakmar T. P. A conserved carboxylic acid group mediates light-dependent proton uptake and signaling by rhodopsin. J. Biol. Chem. 269:1994;23879-23881.
4. Asato A. E., Zhang B.-W., Denny M., Mirzadegan T., Seff K., Liu R. S. H. A study of the binding site requirements of rhodopsin using isomers of α-retinal and 5-substituted α-retinal analogs. J. Biorgan. Chem. 17:1989;410-417.
5. Baldwin J. M. The probable arrangement of the helices in G protein-coupled receptors. EMBO J. 12:1993;1693-1703.
6. Barlow R. B., Birge R. R., Kaplan E., Tallent J. R. On the molecular origin of photoreceptor noise. Nature. 366:1993;64-66.
7. Beppu Y., Kakitani T., Tokunaga F. Energetics of protonation-deprotonation of the chromophore in retinal proteins. Photochem. Photobiol. 56:1992;1113-1117.
8. Birge R. R. Nature of the primary photochemical events in rhodopsin and bacteriorhodopsin. Biochim. Biophys. Acta. 1016:1990;293-327.
9. aof the rhodopsin chromphore. Is this how nature minimizes photoreceptor noise? Biophys. J. 64:1993;1371-1372.
10. Brooks B., Bruccoleri R., Olafson D., States D., Swaminathan S., Karplus M. CHARMM: a program for macromolecular energy minimization and dynamics calculations. J. Comput. Chem. 4:1983;187-217.
11. Brünger A. X-PLOR Version 3.1. 1992;Yale University Press, New Haven.
12. Chan T., Lee M., Sakmar T. P. Introduction of hydroxyl-bearing amino acids causes bathochromic spectral shifts in rhodopsin. J. Biol. Chem. 267:1992;9478-9480.
13. Cohen G. B., Oprian D. D., Robinson P. R. Mechanism of activation and inactivation of opsin: role of Glu113 and Lys296. Biochemistry. 31:1992;12592-12601.
14. Cooper A., Converse C. A. Energetics of primary processes in visual excitation: photocalorimetry of rhodopsin in rod outer segment membranes. Biochemistry. 15:1976;2970-2978.
15. DeGrip W. J., Gray D., Gillespie J., Bovee P. H., van den Berg E. M., Lugtenburg J., Rothschild K. J. Photoexcitation of rhodopsin: conformation changes in the chromophore, protein and associated lipids as determined by FTIR difference spectroscopy. Photochem. Photobiol. 48:1988;497-504.
16. Drikos G., Rüppel H. Polarized UV-absorption spectra of retinal isomers - II. On the assignment of the low and high energy absorption bands. Photochem. Photobiol. 40:1984;93-104.
17. Eyring G., Curry B., Mathies R., Fransen R., Palings I., Lugtenburg J. Interpretation of the resonance Raman spectrum of bathorhodopsin based on visual pigment analogues. Biochemistry. 19:1980;2410-2418.
18. Eyring G., Curry B., Broek A., Lugtenburg J., Mathies R. Assignment and interpretation of hydrogen out-of-plane vibrations in the resonance Raman spectra of rhodopsin and bathorhodopsin. Biochemistry. 21:1982;384-393.
19. Fahmy K., Sakmar T. P. Light-dependent transducin activation by an ultraviolet-absorbing rhodopsin mutant. Biochemistry. 32:1993a;9165-9171.
20. Fahmy K., Sakmar T. P. Regulation of the rhodopsin-transducin interaction by a highly conserved carboxylic acid group. Biochemistry. 32:1993b;7229-7236.
21. Fahmy K., Siebert F., Sakmar T. P. A mutant rhodopsin photoproduct with a protonated Schiff base displays an active-state conformation: a Fourier-transform infrared spectroscopy study. Biochemistry. 33:1994;13700-13705.
22. Fahmy K., Siebert F., Sakmar T. P. Photoactivated state of rhodopsin and how it can form. Biophys. Chem. 56:1995;171-181.
23. Farahbakhsh Z. T., Hideg K., Hubbell W. L. Photoactivated conformational changes in rhodopsin: a time-resolved spin label study. Science. 262:1993;1416-1419.
24. Farrens D. L., Altenbach C., Yang K., Hubbell W. L., Khorana H. G. Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science. 274:1996;768-770.
25. Franke R. R., Konig B., Sakmar T. P., Khorana H. G., Hofmann K. P. Rhodopsin mutants that bind but fail to activate transducin. Science. 250:1990;123-125.
26. Franke R. R., Sakmar T. P., Graham R. M., Khorana H. G. Structure and function in rhodopsin. Studies of the interaction between the rhodopsin cytoplasmic domain and transducin. J. Biol. Chem. 267:1992;14767-14774.
27. Fu D., Ballesteros J. A., Weinstein H., Chen J., Javitch J. A. Residues in the seventh membrane-spanning segment of the dopamine D2 receptor accessible in the binding-site crevice. Biochemistry. 35:1996;11278-11285.
28. 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. 28:1989;5954-5962.
29. Gärtner W., Ullrich D., Vogt K. Quantum yield of CHAPSO-solubilized rhodopsin and 3-hydroxy retinal containing bovine opsin. Photochem. Photobiol. 54:1991;1047-1055.
30. aof the retinal protonated Schiff base in retinal proteins. a study with model compounds. J. Am. Chem. Soc. 115:1993;3772-3773.
31. Gerstein M., Lesk A. M., Chothia C. Structural mechanisms of domain movements in proteins. Biochemistry. 33:1994;6739-6749.
32. Han M., Smith S. O. NMR constraints on the location of the retinal chromophore in rhodopsin and bathorhodopsin. Biochemistry. 34:1995;1425-1432.
33. Han M., DeDecker B. S., Smith S. O. Localization of the retinal protonated Schiff base counterion in rhodopsin. Biophys. J. 65:1993;899-906.
34. Han M., Lin S. W., Minkova M., Smith S. O., Sakmar T. P. Functional helix-helix interactions in rhodopsin: replacement of phenylalanine 261 by alanine causes reversion of phenotype of a glycine 121 replacement mutant. J. Biol. Chem. 271:1996a;32337-32342.
35. Han M., Lin S. W., Smith S. O., Sakmar T. P. The effects of amino acid replacements of glycine 121 on transmembrane helix 3 of rhodopsin. J. Biol. Chem. 271:1996b;32330-32336.
36. 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. 76:1979;2503-2507.
37. Hubbard R., Wald G. Cis-trans isomers of vitamin A and retinene in the rhodopsin system. J. Gen. Physiol. 31-32:1952;268-313.
38. Humphrey W., Logunov I., Schulten K., Sheves M. Molecular dynamics study of bacteriorhodopsin and artificial pigments. Biochemistry. 33:1994;3668-3678.
39. Jäger F., Jäger S., Kräutle O., Friedman N., Sheves M., Hofmann K. P., Siebert F. Interaction of the β-ionone ring with the protein in the visual pigment rhodopsin control the activation mechanism. An FTIR and fluorescence study on artificial vertebrate rhodopsins. Biochemistry. 33:1994;7389-7397.
40. Kibelbek J., Mitchell D. C., Beach J. M., Litman B. J. Functional equivalence of metarhodopsin II and the Gt-activating form of photolyzed bovine rhodopsin. Biochemistry. 30:1991;6761-6768.
41. Lamola A. A., Yamane T., Zipp A. Effects of detergents and high pressure upon the metarhodopsin I - metarhodopsin II equilibrium. Biochemistry. 13:1974;738-745.
42. Lewis J. W., Einterz C. M., Hug S. J., Kliger D. S. Transition dipole orientations in the early photolysis intermediates of rhodopsin. Biophys. J. 56:1989;1101-1111.
43. Liebman P. A. In situ microspectrophotometric studies on the pigments of single retinal rods. Biophys. J. 2:1962;161-178.
44. Lin S. W., Sakmar T. P. Specific tryptophan UV-absorbance changes are probes of the transition of rhodopsin to its active state. Biochemistry. 35:1996;11149-11159.
45. Liu R. S. H., Asato A. E., Denny M., Mead D. The nature of restrictions in the binding site of rhodopsin. A model study. J. Am. Chem. Soc. 106:1984;8298-8300.
46. Longstaff C., Calhoon R. D., Rando R. R. Deprotonation of the Schiff base of rhodopsin is obligate in the activation of the G protein. Proc. Natl Acad. Sci. USA. 83:1986;4209-4213.
47. Marr K., Peters K. S. Photoacoustic calorimetric study of the conversion of rhodopsin and isorhodopsin to lumirhodopsin. Biochemistry. 30:1991;1254-1258.
48. Mathies R. A., Oseroff R., Stryer L. Rapid-flow resonance Raman spectroscopy of photolabile molecules: rhodopsin and isorhodopsin. Proc. Natl Acad. Sci. USA. 73:1976;1-5.
49. Matsumoto H., Yoshizawa T. Recognition of opsin to the longitudinal length of retinal isomers in the formation of rhodopsin. Vision Res. 18:1978;607-609.
50. Michel-Villaz M., Roche C., Chabre M. Orientational changes of the absorbing dipole of retinal upon conversion of rhodopsin to bathorhodopsin, lumirhodopsin and isorhodopsin. Biophys. J. 37:1982;603-616.
51. Mirzadegan T., Humblet C., Ripka W. C., Colmenares L. U., Liu R. S. H. Modeling rhodopsin, a member of G-protein coupled receptors, by computer graphics. Interpretation of chemical shifts of fluorinated rhodopsins. Photochem. Photobiol. 56:1992;883-893.
52. Nakanishi K. Bioorganic studies with rhodopsin. Pure Appl. Chem. 57:1985;769-776.
53. Nakayama T. A., Khorana H. G. Orientation of retinal in bovine rhodopsin determined by cross-linking using a photoactivatable analog of 11-cis -retinal. J. Biol. Chem. 265:1990;15762-15769.
54. Nakayama T. A., Khorana H. G. Mapping of the amino acids in membrane-embedded helices that interact with the retinal chromophore in bovine rhodopsin. J. Biol. Chem. 266:1991;4269-4275.
55. Nathans J. Determinants of visual pigment absorbance: role of charged amino acids in the putative transmembrane segments. Biochemistry. 29:1990;937-942.
56. Nathans J., Hogness D. S. Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell. 34:1983;807-814.
57. Rao V. R., Cohen G. B., Oprian D. D. Rhodopsin mutation G90D and a molecular mechanism for congenital night blindness. Nature. 367:1994;639-642.
58. Robinson P. R., Cohen G. B., Zhukovsky E. A., Oprian D. D. Constitutively active mutants of rhodopsin. Neuron. 9:1992;719-725.
59. Sakmar T. P., Franke R. R., Khorana H. G. Glutamic acid 113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc. Natl Acad. Sci. USA. 86:1989;8309.
60. Sakmar T. P., Franke R. R., Khorana H. G. The role of the retinylidene Schiff base counterion in rhodopsin in determining wavelength absorbance and Schiff base pKa. Proc. Natl Acad. Sci. USA. 88:1991;3079-3083.
61. Schertler G. F. X., Hargrave P. A. Projection structure of frog rhodopsin in two crystal forms. Proc. Natl Acad. Sci. USA. 92:1995;11578-11582.
62. Schertler G. F., Villa C., Henderson R. Projection structure of rhodopsin. Nature. 362:1993;770-772.
63. Schick G. A., Cooper T. M., Holloway R. A., Murray L. P., Birge R. R. Energy storage in the primary photochemical events of rhodopsin and isorhodopsin. Biochemistry. 26:1987;2556-2562.
64. Schoenlein R. W., Peteanu L. A., Mathies R. A., Shank C. V. The first step in vision: femtosecond isomerization of rhodopsin. Science. 254:1991;412-415.
65. Schulten K., Dinur U., Honig B. The spectra of carbonium ions, cyanine dyes, and protonated Schiff base polyenes. J. Chem. Phys. 73:1980;3927-3935.
66. Sheikh S., Zvyaga T. A., Lichtarge O., Sakmar T. P., Bourne H. R. Rhodopsin activation blocked by metal-ion-binding sites linking transmembrane helices C and F. Nature. 383:1996;347-350.
67. Siebert F., Måntele W., Gerwert K. Fourier-transform infrared spectroscopy applied to rhodopsin. The problem of the protonation state of the retinylidene Schiff base re-investigated. Eur. J. Biochem. 136:1983;119-127.
68. 13C magic angle spinning NMR studies of bathorhodopsin the primary photoproduct of rhodopsin. Biochemistry. 30:1991;7409-7415.
69. Smith S. O., De Groot H. J. M., Gebhard R., Lugtenburg J. Magic angle spinning NMR studies on the metarhodopsin II intermediate of bovine rhodopsin: evidence for an unprotonated Schiff base. Photochem. Photobiol. 56:1992;1035-1039.
70. aof the protonated Schiff base of bovine rhodopsin. A study with artificial pigments. Biophys. J. 64:1993;1499-1502.
71. Strader C. D., Fong T. M., Tota M. R., Underwood D. Structure and function of G protein-coupled receptors. Annu. Rev. Biochem. 63:1994;101-132.
72. Stryer L. Cyclic GMP cascade of vision. Annu. Rev. Neurosci. 9:1986;87-119.
73. Stryer L. Visual excitation and recovery. J. Biol. Chem. 266:1991;10711-10714.
74. Warshel A., Barboy N. Energy storage and reaction pathways in the first steps of vision process. J. Am. Chem. Soc. 104:1982;1469-1476.
75. Warshel A., Karplus M. Calculation of ππ* excited state conformations and vibronic structure of retinal and related molecules. J. Am. Chem. Soc. 96:1974;5677-5689.
76. Wynn R., Harkins P. C., Richards F. M., Fox R. O. Mobile unnatural amino acid side-chains in the core of staphylococcal nuclease. Protein Sci. 5:1996;1026-1031.
77. Yoshizawa T., Wald G. Pre-lumirhodopsin and the bleaching of visual pigments. Nature. 197:1963;1279-1286.
78. Zhang H., Lerro K. A., Yamamoto T., Lien T. H., Sastry L., Gawinowicz M. A., Nakanishi K. The location of the chromophore in rhodopsin: a photoaffinity study. J. Am. Chem. Soc. 116:1994;10165-10173.
79. Zhukovsky E. A., Oprian D. D. Effect of carboxylic acid side-chains on the absorption maximum of visual pigments. Science. 246:1989;928-930.
80. Zvyaga T. A., Fahmy K., Sakmar T. P. Characterization of rhodopsin-transducin interaction: a mutant rhodopsin photoproduct with a protonated Schiff base activates transducin. Biochemistry. 33:1994;9753-9761.