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Department of Biology, University of Washington, Seattle, Washington 98195
Correspondence: Address reprint requests and inquiries to Thomas G. Ebrey, Tel: 206-685-3550; E-mail: tebrey{at}u.washington.edu.
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ABSTRACT |
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max = 571 nm), which has polar residues in the ring binding site that interact with the ring, with that for three pigments, which do not. We conclude that by the time the Lumi product of the pigment is formed, the ring has moved away from the ring binding site.
What is the action of light on the chromophore of rhodopsin? There is agreement that light causes a rapid cis-trans isomerization (reviewed in (1
)), but does this lead to large movements of the chromophore itself with respect to its binding site? Recently Borhan et al. (2) has presented evidence from photoaffinity labeling experiments that the ß-ionone ring of the retinylidene chromophore of rhodopsin (see Fig. 1) moves substantially in going from the initial, unphotolyzed state of the pigment to an early photointermediate, lumirhodopsin (Lumi).
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,4). These changes are primarily responsible for the spectral shift from a "green cone" pigment (for humans 531 nm) to that of a "red cone" (561 nm) pigment. When these residues are changed from an apolar residue to a polar one, Ala-164-Ser, Phe-261-Tyr, and Ala-269-Thr, the spectrum is red shifted by 
1070 cm–1 (average of seven pairs of pigments). Changes at two of the three residues, 261 and 269, account for most of the change (5,6).
The x-ray structure of rhodopsin (7,8) showed that these two residues were part of the retinal binding site and close to the ß-ionone ring (see Fig. 1). The shift to longer wavelengths depends on the strength of interaction and so the distance between the ring and the two polar residues. If the ring moves away from its usual binding site in forming its Lumi intermediate, there should be an anomalous blue spectral shift for this intermediate compared to a visual pigment that does not rely on the two residues to shift its absorption spectrum. Bovine rhodopsin (max = 498 nm) is an example of the type where both residues are in their nonpolar form and so their interaction with the ring is less important. Another example is a chicken pigment, P508, in the RH2 family (for visual pigment families see (9,10)). The chicken long-wavelength sensitive cone pigment iodopsin is an example of the type where both residues are in their polar form, and that, along with the effect of chloride binding, shifts the spectrum out to 571 nm. A third example with nonpolar residues is a mid-wavelength pigment from gecko, P521, which is in the same visual pigment family as iodopsin (9,11). The gecko pigment, like iodopsin, binds a chloride ion to help shift its absorption maxima to longer wavelengths (reviewed in (10,11)).
We first calculated the wavelength shift upon the formation of the first photointermediate, bathorhodopsin, for these four pigments using the data presented in references (12,13). In all four pigments the bathoproduct is shifted 1400 cm–1 to the red of the unphotolyzed pigment and so there is no anomalous difference in the spectral shifts for the two types of pigments, suggesting that the ring had not moved away from the two residues at this stage. In forming the next photointermediate, Lumi, bovine rhodopsin is shifted back to a value near its initial absorption maximum (497 nm, so almost no net shift) and the Lumi's of the chicken P508 and the gecko P521 pigments had very similar small shifts when they were formed. However, the Lumi product of iodopsin (535 nm) is shifted by a much larger amount, 1510 cm–1, and to the blue of its initial absorption maximum. This is the result predicted if the ring moved away from the two hydroxyl-containing residues in forming Lumi. Such a large shift might also occur if the chloride were to be released when the Lumi intermediate of iodopsin is formed, but this cause is excluded because the gecko pigment has the chloride, but not the binding site shifting residues, and its Lumi shifts just like the nonchloride binding pigments.
These results imply a striking difference between the effects of light on visual pigments compared to bacteriorhodopsin. There are several similarities in the photochemistry of these two classes of retinal pigments such as photoisomerization, in a temperature-independent process, leading to a high free-energy, red-shifted primary photoproduct. However, for bacteriorhodopsin x-ray structures of its primary bathoproduct, K, and the product formed by warming K, L, and L's thermal decay product M, all have the ß-ionone ring unmoved from its initial site in the pigment (14). Thus the movement of the ß-ionone ring of a visual pigment as lumirhodopsin is formed represents a fundamental difference between these two types of retinal-based pigments in the steps that occur after photoisomerization.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTACKNOWLEDGEMENTSREFERENCES |
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Submitted on January 28, 2005; accepted for publication March 2, 2005.
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REFERENCES |
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(2) Borhan, B., M. Souto, H. Imai, Y. Shichida, and K. Nakanishi. 2000. Movement of retinal along the visual transduction path. Science. 288:2209–2212.
(3) Yokoyama, R., and S. Yokoyama. 1990. Convergent evolution of the red and green-like visual pigment genes in fish, Astyanax fasciatus, and human. Proc. Natl. Acad. Sci. USA. 87:9315–9318.
(4) Neitz, M., J. Neitz, and G. Jacobs. 1991. Spectral tuning of pigments underlying red-green color vision. Science. 252:971–974.
(5) Asenjo, A., J. Rim, and D. Oprian. 1994. Molecular determinants of human red/green color discrimination. Neuron. 12:1131–1138.[CrossRef][Medline]
(6) Chan, T., M. Lee, and T. Sakmar. 1992. Introduction of hydroxyl-bearing amino acids causes bathochromic spectral shifts in rhodopsin. J. Biol. Chem. 267:9478–9480.
(7) Palczewski, K., T. Kumasaka, T. Hori, C. Behnke, H. Motoshima, B. Fox, I. Le Trong, D. Teller, T. Okada, R. Stenkamp, M. Yamamoto, and M. Miyano. 2000. Crystal structure of rhodopsin: a G protein-coupled receptor. Science. 289:739–745.
(8) Okada, Y., Y. Fujiyoshi, M. Solow, J. Navarro, E. Landau, and Y. Shichida. 2002. Functional role of internal water molecules in rhodopsin revealed by x-ray crystallography. Proc. Natl. Acad. Sci. USA. 99:5982–5987.
(9) Ebrey, T. G., and Y. Koutalos. 2001. Vertebrate photoreceptors. Prog. Retin. Eye Res. 20:49–94.[CrossRef][Medline]
(10) Kumauchi, M., and T. Ebrey. 2005. Visual pigments as photoreceptors. In Handbook of Photosensory Receptors. W. Briggs and J. Spudich, editors. John Wiley & Sons, Hoboken, NJ. 43–76.
(11) Ebrey, T. G., and Y. Takahashi. 2001. Photobiology of retinal proteins. In Photobiology for the 21st Century. T. P. Coohill and D. P. Velenzeno, editors. Valdenmar Publishing, Overland Park, KS. 101–133.
(12) Shichida, Y., and H. Imai. 1999. Amino acid residues controlling the properties and functions of rod and cone visual pigments. In Rhodopsins and Phototransduction. John Wiley & Sons, Hoboken, NJ. 142–157.
(13) Lewis, J., J. Liang, T. Ebrey, M. Sheves, N. Livnah, O. Kuwata, S. Jager, and D. Kliger. 1997. Early photolysis intermediates of gecko and bovine artificial visual pigments. Biochemistry. 36:14593–14600.[CrossRef][Medline]
(14) Lanyi, J. K. 2004. Bacteriorhodopsin. Annu. Rev. Physiol. 66:665–688.[CrossRef][Medline]
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