Hostname: page-component-7b7567c8c-mnklg Total loading time: 0 Render date: 2026-11-12T07:21:16.854Z Has data issue: false hasContentIssue false
  • English
  • Français

Differences in the pharmacological activation of visual opsins

Published online by Cambridge University Press:  30 January 2007

T. ISAYAMA,
Y. CHEN,
M. KONO,
W.J. DEGRIP,
J.-X. MA,
R.K. CROUCH and
C.L. MAKINO
T. ISAYAMA
Affiliation:
Department of Ophthalmology, Massachusetts Eye & Ear Infirmary, Harvard Medical School, Boston, Massachusetts
Y. CHEN
Affiliation:
Department of Cell Biology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
M. KONO
Affiliation:
Department of Ophthalmology, Storm Eye Research Institute, Medical University of South Carolina, Charleston, South Carolina
W.J. DEGRIP
Affiliation:
Department of Biochemistry, NCMLS, University of Nijmegen, Nijmegen, The Netherlands
J.-X. MA
Affiliation:
Department of Cell Biology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
R.K. CROUCH
Affiliation:
Department of Ophthalmology, Storm Eye Research Institute, Medical University of South Carolina, Charleston, South Carolina
C.L. MAKINO
Affiliation:
Department of Ophthalmology, Massachusetts Eye & Ear Infirmary, Harvard Medical School, Boston, Massachusetts
Get accessRights & Permissions [Opens in a new window]

Abstract

Opsins, like many other G-protein-coupled receptors, sustain constitutive activity in the absence of ligand. In partially bleached rods and cones, opsin's activity closes cGMP-gated channels and produces a state of “pigment adaptation” with reduced sensitivity to light and accelerated flash response kinetics. The truncated retinal analogue, β-ionone, further desensitizes partially bleached green-sensitive salamander rods, but enables partially bleached red-sensitive cones to recover dark-adapted physiology. Structural differences between rod and cone opsins were proposed to explain the effect. Rods and cones, however, also contain different transducins, raising the possibility that G-protein type determines the photoreceptor-specific effects of β-ionone. To test the two hypotheses, we applied β-ionone to partially bleached blue-sensitive rods and cones of salamander, two cells that couple the same cone-like opsin to either rod or cone transducin, respectively. Immunocytochemistry confirmed that all salamander rods contain one form of transducin, whereas all cones contain another. β-Ionone enhanced pigment adaptation in blue-sensitive rods, but it also did so in blue- and UV-sensitive cones. Furthermore, all recombinant salamander rod and cone opsins, with the exception of the red-sensitive cone opsin, activated rod transducin upon the addition of β-ionone. Thus opsin structure determines the identity of β-ionone as an agonist or an inverse agonist and in that respect distinguishes the red-sensitive cone opsin from all others.

Keywords

RodConeRhodopsinTransducinPhototransduction

Information

Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 6 , November 2006, pp. 899 - 908
Copyright
© 2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

REFERENCES

Attwell, D.I., Werblin, F.S., Wilson, M., & Wu, S.M. (1983). Properties of double cones in the larval salamander retina. Journal of Physiology (London) 341, 74.Google Scholar
Baehr, W., Morita, E.A., Swanson, R.J., & Applebury, M.L. (1982). Characterization of bovine rod outer segment G-protein. Journal of Biological Chemistry 257, 6452–6460.Google Scholar
Chen, N., Ma, J.-X., Corson, D.W., Hazard, E.S., & Crouch, R.K. (1996). Molecular cloning of a rhodopsin gene from salamander rods. Investigative Ophthalmology and Visual Science 37, 1907–1913.Google Scholar
Clapham, D.E. & Neer, E.J. (1997). G protein βγ subunits. Annual Review of Pharmacology and Toxicology 37, 167–203.CrossRefGoogle Scholar
Corson, D.W., Kefalov, V.J., Cornwall, M.C., & Crouch, R.K. (2000). Effect of 11-cis 13-demethylretinal on phototransduction in bleach-adapted rod and cone photoreceptors. Journal of General Physiology 116, 283–297.CrossRefGoogle Scholar
Craft, C.M., Whitmore, D.H., & Weichmann, A.F. (1994). Cone arrestin identified by targeting expression of a functional family. Journal of Biological Chemistry 269, 4613–4619.Google Scholar
Das, J., Crouch, R.K., Ma, J.-X., Oprian, D.D., & Kono, M. (2004). Role of the 9-methyl group of retinal in cone visual pigments. Biochemistry 43, 5532–5538.CrossRefGoogle Scholar
Dean, D.M., Nguitragool, W., Miri, A., McCabe, S.L., & Zimmerman, A.L. (2002). All-trans-retinal shuts down rod cyclic nucleotide-gated ion channels: A novel role for photoreceptor retinoids in the response to bright light? Proceedings of the National Academy of Science USA 99, 8372–8377.Google Scholar
Downes, G.B. & Gautam, N. (1999). The G protein subunit gene families. Genomics 62, 544–552.CrossRefGoogle Scholar
Ebrey, T. & Koutalos, Y. (2001). Vertebrate photoreceptors. Progress in Retinal and Eye Research 20, 49–94.CrossRefGoogle Scholar
Fain, G.L., Matthews, H.R., Cornwall, M.C., & Koutalos, Y. (2001). Adaptation in vertebrate photoreceptors. Physiological Reviews 81, 117–151.Google Scholar
Fung, B.K.-K., Lieberman, B.S., & Lee, R.H. (1992). A third form of the G protein β subunit. 2. Purification and biochemical properties. Journal of Biological Chemistry 267, 24782–24788.Google Scholar
Hisatomi, O., Matsuda, S., Satoh, T., Kotaka, S., Imanishi, Y., & Tokunaga, F. (1998). A novel subtype of G-protein-coupled receptor kinase, GRK7, in teleost cone photoreceptors. Federation of European Biochemical Societies Letters 424, 159–164.CrossRefGoogle Scholar
Horrigan, D.M., Tetreault, M.L., Tsomaia, N., Vasileiou, C., Borhan, B., Mierke, D.F., Crouch, R.K., & Zimmerman, A.L. (2005). Defining the retinoid binding site in the rod cyclic nucleotide-gated channel. Journal of General Physiology 126, 453–460.CrossRefGoogle Scholar
Jin, J., Crouch, R.K., Corson, D.W., Katz, B.M., MacNichol, E.F., & Cornwall, M.C. (1993). Noncovalent occupancy of the retinal-binding pocket of opsin diminishes bleaching adaptation of retinal cones. Neuron 11, 513–522.CrossRefGoogle Scholar
Jones, G.J., Crouch, R.K., Wiggert, B., Cornwall, M.C., & Chader, G.J. (1989). Retinoid requirements for recovery of sensitivity after visual-pigment bleaching in isolated photoreceptors. Proceedings of the National Academy of Science USA 86, 9606–9610.CrossRefGoogle Scholar
Kefalov, V.J., Cornwall, M.C., & Crouch, R.K. (1999). Occupancy of the chromophore binding site of opsin activates visual transduction in rod photoreceptors. Journal of General Physiology 113, 491–503.CrossRefGoogle Scholar
Kefalov, V.J., Crouch, R.K., & Cornwall, M.C. (2001). Role of noncovalent binding of 11-cis-retinal to opsin in dark adaptation of rod and cone photoreceptors. Neuron 29, 749–755.CrossRefGoogle Scholar
Kefalov, V.J., Estevez, M.E., Kono, M., Goletz, P.W., Crouch, R.K., Cornwall, M.C., & Yau, K.-W. (2005). Breaking the covalent bond—A pigment property that contributes to desensitization in cones. Neuron 46, 879–890.CrossRefGoogle Scholar
Kono, M. (2006). Constitutive activity of a UV cone opsin. Federation of European Biochemical Societies Letters 580, 229–232.CrossRefGoogle Scholar
Lee, R.H., Lieberman, B.S., Yamane, H.K., Bok, D., & Fung, B.K.-K. (1992). A third form of the G protein β subunit. 1. Immunochemical identification and localization to cone photoreceptors. Journal of Biological Chemistry 267, 24776–24781.Google Scholar
Ma, J.-X., Kono, M., Xu, L., Das, J., Ryan, J.C., Hazard, E.S.III, Oprian, D.D., & Crouch, R.K. (2001a). Salamander UV cone pigment: Sequence, expression, and spectral properties. Visual Neuroscience 18, 393–399.Google Scholar
Ma, J.-X., Znoiko, S., Othersen, K.L., Ryan, J.C., Das, J., Isayama, T., Kono, M., Oprian, D.D., Corson, D.W., Cornwall, M.C., Cameron, D.A., Harosi, F.I., Makino, C.L., & Crouch, R.K. (2001b). A visual pigment expressed in both rod and cone photoreceptors. Neuron 32, 451–461.Google Scholar
Makino, C.L. & Dodd, R.L. (1996). Multiple visual pigments in a photoreceptor of the salamander retina. Journal of General Physiology 108, 27–34.CrossRefGoogle Scholar
Makino, C.L., Groesbeek, M., Lugtenburg, J., & Baylor, D.A. (1999). Spectral tuning in salamander visual pigments studied with dihydroretinal chromophores. Biophysical Journal 77, 1024–1035.CrossRefGoogle Scholar
Makino, C.L., Taylor, W.R., & Baylor, D.A. (1991). Rapid charge movements and photosensitivity of visual pigments in salamander rods and cones. Journal of Physiology (London) 442, 761–780.CrossRefGoogle Scholar
Matsumoto, H., Tokunaga, F., & Yoshizawa, T. (1975). Accessibility of the iodopsin chromophore. Biochimica et Biophysica Acta 404, 300–308.CrossRefGoogle Scholar
McBee, J.K., Palczewski, K., Baehr, W., & Pepperberg, D.R. (2001). Confronting complexity: The interlink of phototransduction and retinoid metabolism in the vertebrate retina. Progress in Retinal and Eye Research 20, 469–529.CrossRefGoogle Scholar
Moench, S.J., Terry, C.E., & Dewey, T.G. (1994a). Fluoresence labeling of the palmitoylation sites of rhodopsin. Biochemistry 33, 5783–5790.Google Scholar
Moench, S.J., Moreland, J., Stewart, D.H., & Dewey, T.G. (1994b). Fluorescence studies of the location and membrane accessibility of the palmitoylation sites of rhodopsin. Biochemistry 33, 5791–5796.Google Scholar
Nir, I. & Ransom, N. (1992). S-antigen in rods and cones of the primate retina: Different labeling patterns are revealed with antibodies directed against specific domains in the molecule. Journal of Histochemistry and Cytochemistry 40, 343–352.CrossRefGoogle Scholar
Ong, O.C., Yamane, H.K., Phan, K.B., Fong, H.K.W., Bok, D., Lee, R.H., & Fung, B.K.-K. (1995). Molecular cloning and characterization of the G protein γ subunit of cone photoreceptors. Journal of Biological Chemistry 270, 8495–8500.CrossRefGoogle Scholar
Ovchinnikov, Y.A., Abdulaev, N.G., & Bogachuk, A.S. (1988). Two adjacent cysteine residues in the C-terminal cytoplasmic fragment of bovine rhodopsin are palmitylated. Federation of European Biochemical Societies Letters 230, 1–5.Google Scholar
Peng, Y.-W., Robishaw, J.D., Levine, M.A., & Yau, K.-W. (1992). Retinal rods and cones have distinct G protein β and γ subunits. Proceedings of the National Academy of Science USA 89, 10882–10886.CrossRefGoogle Scholar
Pittler, S.J., Fliesler, S.J., & Baehr, W. (1992). Primary structure of frog rhodopsin. Federation of European Biochemical Societies Letters 313, 103–108.CrossRefGoogle Scholar
Rieke, F. & Baylor, D.A. (2000). Origin and functional impact of dark noise in retinal cones. Neuron 26, 181–186.CrossRefGoogle Scholar
Robinson, P.R. (2000). Assays for detection of constitutively active opsins. Methods in Enzymology 315, 207–218.CrossRefGoogle Scholar
Robinson, P.R., Cohen, G.B., Zhukovsky, E.A., & Oprian, D.D. (1992). Constitutively active mutants of rhodopsin. Neuron 9, 719–725.CrossRefGoogle Scholar
Ryan, J.C., Znoiko, S., Xu, L., Crouch, R.K., & Ma, J.-X. (2000). Salamander rods and cones contain distinct transducin alpha subunits. Visual Neuroscience 17, 847–854.CrossRefGoogle Scholar
Ryan, J.C., Crouch, R.K., & Ma, J.-X. (2001). Cloning and characterization of three salamander retinal G-protein beta subunits. Molecular Vision 7, 222–227.Google Scholar
Sachs, K., Maretzki, D., Meyer, C.K., & Hofmann, K.P. (2000). Diffusible ligand all-trans-retinal activates opsin via a palmitoylation-dependent mechanism. Journal of Biological Chemistry 275, 6189–6194.CrossRefGoogle Scholar
Sakuma, H., Inana, G., Murakami, A., Higashide, T., & McLaren, M.J. (1996). Immunolocalization of X-arrestin in human cone photoreceptors. Federation of European Biochemical Societies Letters 382, 105–110.CrossRefGoogle Scholar
Sherry, D.M., Bui, D.D., & DeGrip, W.J. (1998). Identification and distribution of photoreceptor subtypes in the neotenic tiger salamander retina. Visual Neuroscience 15, 1175–1187.Google Scholar
Smith, W.C., Gurevich, E.V., Dugger, D.R., Vishnivetskiy, S.A., Shelamer, C.L., McDowell, J.H., & Gurevich, V.V. (2000). Cloning and functional characterization of salamander rod and cone arrestins. Investigative Ophthalmology and Visual Science 41, 2445–2455.Google Scholar
Vissers, P.M.A.M. & DeGrip, W.J. (1996). Functional expression of human cone pigments using recombinant baculovirus: Compatibility with histidine tagging and evidence for N-glycosylation. Federation of European Biochemical Societies Letters 396, 26–30.CrossRefGoogle Scholar
Weiss, E.R., Raman, D., Shirakawa, S., Ducceschi, M.H., Bertram, P.T., Wong, F., Kraft, T.W., & Osawa, S. (1998). The cloning of GRK7, a candidate cone opsin kinase, from cone- and rod-dominant mammalian retinas. Molecular Vision 4, 27–34.Google Scholar
Weiss, E.R., Ducceschi, M.H., Horner, T.J., Li, A., Craft, C.M., & Osawa, S. (2001). Species-specific differences in expression of G-protein-coupled receptor kinase (GRK) 7 and GRK1 in mammalian cone photoreceptor cells: Implications for cone cell phototransduction. Journal of Neuroscience 21, 9175–9184.Google Scholar
Wessling-Resnick, M. & Johnson, G.L. (1987). Allosteric behavior in transducin activation mediated by rhodopsin. Initial rate analysis of guanine nucleotide exchange. Journal of Biological Chemistry 262, 3697–3705.Google Scholar
Xu, L., Hazard, E.S.III, Lockman, D.K., Crouch, R.K., & Ma, J.-X. (1998). Molecular cloning of the salamander red and blue cone visual pigments. Molecular Vision 4, 10–15.Google Scholar
Yokoyama, S. (2000). Molecular evolution of vertebrate visual pigments. Progress in Retinal and Eye Research 19, 385–419.CrossRefGoogle Scholar