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Evidence for the prolonged photoactivated lifetime of an analogue visual pigment containing 11 -cis 9-desmethylretinal

Published online by Cambridge University Press:  02 June 2009

D. Wesley Corson ,
M. Carter Cornwall  and
David R. Pepperberg
D. Wesley Corson
Affiliation:
Department of Pathology and Laboratory Medicine, Medical University of South Carolina, Charleston Department of Ophthalmology, Medical University of South Carolina, Charleston
M. Carter Cornwall
Affiliation:
Department of Physiology, Boston University School of Medicine, Boston
David R. Pepperberg
Affiliation:
Lions of Illinois Eye Research Institute, Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago College of Medicine, Chicago
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Abstract

Following bright flashes, rod photoreceptors exhibit a period of photocurrent saturation that increases linearly with the logarithm of flash intensity. In a recent report, Pepperberg et al. (1992) presented evidence that the slope of the function relating the saturation period (T) to the natural logarithm of flash intensity (In If) represents the exponential lifetime (τ) of photoactivated visual pigment: τ = ΔT/Δ[ln If]. In salamander rods, 11 -cis 9-desmethylretinal combines with opsin to form 9-desmethyl rhodopsin. Dim flash responses mediated by this analogue visual pigment exhibited slow recovery kinetics relative to those of native pigment (Corson et al., 1991). This observation raises the hypothesis that the physiological lifetime of photoactivated 9-desmethyl rhodopsin is substantially longer than that of native visual pigment. To test this hypothesis, we have examined the relation between the period of photocurrent saturation and flash intensity in salamander rods containing a mixture of the two pigments. Brief stimuli at two widely separated wavelengths (440 and 640 nm) elicited saturating photocurrent responses that were preferentially mediated by 9-desmethyl rhodopsin or residual native pigment, respectively. Plots of T vs. In If revealed a linear increase in the period of response saturation over a large range of saturating intensities at both wavelengths. However, the slope of the relation between T and In If with 440-nm flashes was more than twice as large (4.1 ± 0.5 s, n = 5) as that measured with 640-nm flashes (1.7 ± 0.4 s). For rods subjected only to bleaching of the native pigment, or to bleaching and resensitization with 11-cis retinal, the slope of the relation between T and In If remained independent of wavelength and indistinguishable from that of native pigment in unbleached cells. The data provide support for the hypothesis that the slope parameter τ represents the lifetime of photoactivated pigment, and specifically suggest that the lifetime of photoactivated 9-desmethyl rhodopsin is abnormally long.

Keywords

RhodopsinRetinoidsPhototransductionVisual pigmentRetinal
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 91 - 98
Copyright
Copyright © Cambridge University Press 1994

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References

Baylor, D.A., Lamb, T.D. & Yau, K.-W. (1979 a). The membrane current of single rod outer segments. Journal of Physiology 288, 589–611.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.-W. (1979 b). Responses of retinal rods to single photons. Journal of Physiology 288, 613–634.CrossRefGoogle ScholarPubMed
Baylor, D.A., Matthews, G. & Nunn, B.J. (1984 a). Location and function of voltage-sensitive conductances in retinal rods of the salamander, Ambystoma tigrinum. Journal of Physiology 354, 203–223.CrossRefGoogle ScholarPubMed
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984 b). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaco fascicularis. Journal of Physiology 357, 575–607.CrossRefGoogle Scholar
Baylor, D.A., Matthews, G. & Yau, K.-W. (1983). Temperature effects on the membrane current of retinal rods of the toad. Journal of Physiology 337, 723–734.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Nunn, B.J. (1986). Electrical properties of the light sensitive conductances of rods of the salamander Ambystoma tigrinum. Journal of Physiology 371, 115–145.CrossRefGoogle ScholarPubMed
Bridges, C.D.B. (1976). 11-cis Vitamin A in dark-adapted rod outer segments is a probable source of prosthetic groups for rhodopsin biosynthesis. Nature (London) 259, 247–248.CrossRefGoogle ScholarPubMed
Cobbs, W.H. (1991). Light and dark active phosphodiesterase regulation in salamander rods. Journal of General Physiology 98, 575–614.CrossRefGoogle ScholarPubMed
Cobbs, W.H. & Pugh, E.N. Jr (1987). Kinetics and components of the flash photocurrent of isolated retinal rods of the larval salamander, Ambystoma tigrinum. Journal of Physiology 394, 529–572.CrossRefGoogle ScholarPubMed
Cocozza, J.D. & Ostroy, S.E. (1987). Factors affecting the regeneration of rhodopsin in the isolated amphibian retina. Vision Research 27, 1085–1091.CrossRefGoogle ScholarPubMed
Chabre, M. & Vuong, T.M. (1992). Kinetics and energetics of the rho-dopsin-transducin-cGMP phosphodiesterase cascade of visual transduction. Biochimica Biophysica Acta 1101, 260–263.CrossRefGoogle ScholarPubMed
Cornwall, M.C., Fein, A. & Macnichol, E.F., Jr. (1990). Cellular mechanisms that underlie bleaching and background adaptation. Journal of General Physiology 96, 345–372.CrossRefGoogle ScholarPubMed
Cornwall, M.C., Ripps, C., Chappell, G.L. & Jones, G.J. (1989). Membrane current responses of skate photoreceptors. Journal of General Physiology 94, 633–647.CrossRefGoogle ScholarPubMed
Corson, D.W., Derguini, F., Nakanishi, K., Crouch, R.K., Macnichol, E.F. & Cornwall, M.C. (1991). Partial relief of bleaching adaptation and induction of wavelength dependent response shapes by 9-desmethyl retinal in rods. Investigative Ophthalmology and Visual Science 32, 670.Google Scholar
Corson, D.W., Cornwall, M.C., Macnichol, E.F., Jin, J., Johnson, R., Derguini, F., Crouch, R.K. & Nakanishi, K. (1990). Sensitization of bleached rod photoreceptors by 1 1-cis-locked analogues of retinal. Proceedings of the National Academy of Sciences of the U.S.A. 87, 6823–6827.CrossRefGoogle Scholar
Corson, D.W., Derguini, F., Nakanishi, K., Crouch, R.K., Cornwall, M.C. & Pepperberg, D.R. (1992). Evidence for a long-lived photoactivated state of 1 11-cis 9-desmethyl rhodopsin in salamander rod photoreceptors. Biophysical Journal 61, A9.Google Scholar
Ernst, W., Kemp, C. M. & Price, D.E. (1978). Studies on the effects of bleaching amphibian rod pigments in situ. I. The absorbance spectra of axolotl and tiger salamander rhodopsin and porphyropsin. Experimental Eye Research 26, 329–336.CrossRefGoogle ScholarPubMed
Forti, S., Menini, A., Rispoli, G. & Torre, V. (1989). Kinetics of phototransduction in retinal rods of the newt Triturus cristatus. Journal of Physiology 419, 265–295.CrossRefGoogle ScholarPubMed
Ganter, U.M., Schmidt, E.D., Peres-Sala, D., Rando, R.R. & Sie-bert, F. (1989). Removal of the 9-methyl group of retinal inhibits signal transduction in the visual process. A Fourier transform infrared and biochemical investigation. Biochemistry 28, 5954–5962.CrossRefGoogle ScholarPubMed
Hárosi, F.I. (1975). Absorption spectra and linear dichroism of some amphibian photoreceptors. Journal of General Physiology 66, 357–382.CrossRefGoogle ScholarPubMed
Hodgkin, A.L., McNaughton, P.A., Nunn, B.J. & Yau, K.-W. (1984). Effect of ions on retinal rods from Bufo marinus. Journal of Physiology 350, 649–680.CrossRefGoogle ScholarPubMed
Köhler, A. (1893). Ein neues Beleuchtungsverfahren für mikrophoto- graphische Zweeke. Zeitschrift Wissenschaften Mikroskopie 10, 433–440.Google 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 442, 761–780.CrossRefGoogle ScholarPubMed
Morrison, D.F., Ting, T.D., Ho, Y.-K., Crouch, R.K., Corson, D.W. & Pepperberg, D.R. (1993). Reduced activity of 9-desmethylrho-dopsin in light-dependent phosphorylation. Biophysical Journal 64, A211.Google Scholar
Palczewski, K., Rispoli, G. & Detwiler, P.B. (1992). The influence of arrestin (48k protein) and rhodopsin kinase on visual transduction. Neuron 8, 117–126.CrossRefGoogle ScholarPubMed
Pepperberg, D.R., Lurie, M., Brown, P.K. & Dowling, J.E. (1976). Visual adaptation: Effects of externally applied retinal on the light-adapted, isolated skate retina. Science 191, 394–396.CrossRefGoogle ScholarPubMed
Pepperberg, D.R., Brown, P.K., Lurie, M. & Dowling, J.E. (1978). Visual pigment and photoreceptor sensitivity in the isolated skate retina. Journal of General Physiology 71, 369–396.CrossRefGoogle ScholarPubMed
Pepperberg, D.R., Cornwall, M.C., Kahlert, M., Hofmann, K.P., Jin, J., Jones, G.J. & Ripps, H. (1992). Light-dependent delay in the falling phase of the retinal rod photoresponse. Visual Neuro-science 8, 9–18.CrossRefGoogle ScholarPubMed
Vuong, T.M. & Chabre, M. (1991). Deactivation kinetics of the transduction cascade of vision. Proceedings of the National Academy of Sciences of the U.S.A. 88, 9813–9817.CrossRefGoogle ScholarPubMed
Wilden, U., Hall, S.W. & Kühn, H. (1986). Phosphodiesterase activation of photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48-kDa protein of rod outer segments. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1174–1178.CrossRefGoogle ScholarPubMed