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The 9-methyl group of retinal is essential for rapid Meta II decay and phototransduction quenching in red cones.

Estevez ME, Kolesnikov AV, Ala-Laurila P, Crouch RK, Govardovskii VI, Cornwall MC - J. Gen. Physiol. (2009)

Bottom Line: In all cases, cones were bleached and their visual pigment was regenerated with either 11-cis retinal or with 11-cis 9-demethyl retinal, an analogue of retinal lacking the 9-methyl group.This was accompanied by a significant slowing of the recovery from saturation in cones lacking the 9-methyl group after exposure to bright (>0.1% visual pigment photoactivated) but not dim light.These results demonstrate that the 9-methyl group of retinal is required for steric chromophore-opsin interactions that favor both the rapid decay of Meta II and the rapid response recovery after exposure to bright light in red-sensitive cones.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118, USA. estevez@bu.edu

ABSTRACT
Cone photoreceptors of the vertebrate retina terminate their response to light much faster than rod photoreceptors. However, the molecular mechanisms underlying this rapid response termination in cones are poorly understood. The experiments presented here tested two related hypotheses: first, that the rapid decay rate of metarhodopsin (Meta) II in red-sensitive cones depends on interactions between the 9-methyl group of retinal and the opsin part of the pigment molecule, and second, that rapid Meta II decay is critical for rapid recovery from saturation of red-sensitive cones after exposure to bright light. Microspectrophotometric measurements of pigment photolysis, microfluorometric measurements of retinol production, and single-cell electrophysiological recordings of flash responses of salamander cones were performed to test these hypotheses. In all cases, cones were bleached and their visual pigment was regenerated with either 11-cis retinal or with 11-cis 9-demethyl retinal, an analogue of retinal lacking the 9-methyl group. Meta II decay was four to five times slower and subsequent retinol production was three to four times slower in red-sensitive cones lacking the 9-methyl group of retinal. This was accompanied by a significant slowing of the recovery from saturation in cones lacking the 9-methyl group after exposure to bright (>0.1% visual pigment photoactivated) but not dim light. A mathematical model of the turn-off process of phototransduction revealed that the slower recovery of photoresponse can be explained by slower Meta decay of 9-demethyl visual pigment. These results demonstrate that the 9-methyl group of retinal is required for steric chromophore-opsin interactions that favor both the rapid decay of Meta II and the rapid response recovery after exposure to bright light in red-sensitive cones.

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Comparison of quenching of the phototransduction cascade in salamander red cones containing different visual pigments. Experimental points for 11-cis–regenerated cones are shown in black; those for 9-DM cones are in red. The solid line is drawn as a five-exponential least-square approximation with four free parameters. It yields the time course of quenching of flash-induced PDE activity for red cones of Ambystoma mexicanum containing 11-cis (black) or 9-DM (red) visual pigment, as follows from the theoretical prediction of the kinetic scheme of Fig. 7. Numbers near the curves show coefficient of determination of the model fits. The fits were further used to obtain the parameters of reactions given in Table I, as explained in the text.
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fig8: Comparison of quenching of the phototransduction cascade in salamander red cones containing different visual pigments. Experimental points for 11-cis–regenerated cones are shown in black; those for 9-DM cones are in red. The solid line is drawn as a five-exponential least-square approximation with four free parameters. It yields the time course of quenching of flash-induced PDE activity for red cones of Ambystoma mexicanum containing 11-cis (black) or 9-DM (red) visual pigment, as follows from the theoretical prediction of the kinetic scheme of Fig. 7. Numbers near the curves show coefficient of determination of the model fits. The fits were further used to obtain the parameters of reactions given in Table I, as explained in the text.

Mentions: Data from six cones regenerated with 11-cis retinal and four cones regenerated with 9-DM retinal processed this way are shown in Fig. 8. It is seen that up to ∼2 s, the PDE quenching with both types of the chromophore follow a common curve. At longer times, however, PDE activity decays substantially more slowly in cells containing 9-DM visual pigment (red symbols) compared with cells containing normal visual pigment (black symbols).


The 9-methyl group of retinal is essential for rapid Meta II decay and phototransduction quenching in red cones.

Estevez ME, Kolesnikov AV, Ala-Laurila P, Crouch RK, Govardovskii VI, Cornwall MC - J. Gen. Physiol. (2009)

Comparison of quenching of the phototransduction cascade in salamander red cones containing different visual pigments. Experimental points for 11-cis–regenerated cones are shown in black; those for 9-DM cones are in red. The solid line is drawn as a five-exponential least-square approximation with four free parameters. It yields the time course of quenching of flash-induced PDE activity for red cones of Ambystoma mexicanum containing 11-cis (black) or 9-DM (red) visual pigment, as follows from the theoretical prediction of the kinetic scheme of Fig. 7. Numbers near the curves show coefficient of determination of the model fits. The fits were further used to obtain the parameters of reactions given in Table I, as explained in the text.
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2717693&req=5

fig8: Comparison of quenching of the phototransduction cascade in salamander red cones containing different visual pigments. Experimental points for 11-cis–regenerated cones are shown in black; those for 9-DM cones are in red. The solid line is drawn as a five-exponential least-square approximation with four free parameters. It yields the time course of quenching of flash-induced PDE activity for red cones of Ambystoma mexicanum containing 11-cis (black) or 9-DM (red) visual pigment, as follows from the theoretical prediction of the kinetic scheme of Fig. 7. Numbers near the curves show coefficient of determination of the model fits. The fits were further used to obtain the parameters of reactions given in Table I, as explained in the text.
Mentions: Data from six cones regenerated with 11-cis retinal and four cones regenerated with 9-DM retinal processed this way are shown in Fig. 8. It is seen that up to ∼2 s, the PDE quenching with both types of the chromophore follow a common curve. At longer times, however, PDE activity decays substantially more slowly in cells containing 9-DM visual pigment (red symbols) compared with cells containing normal visual pigment (black symbols).

Bottom Line: In all cases, cones were bleached and their visual pigment was regenerated with either 11-cis retinal or with 11-cis 9-demethyl retinal, an analogue of retinal lacking the 9-methyl group.This was accompanied by a significant slowing of the recovery from saturation in cones lacking the 9-methyl group after exposure to bright (>0.1% visual pigment photoactivated) but not dim light.These results demonstrate that the 9-methyl group of retinal is required for steric chromophore-opsin interactions that favor both the rapid decay of Meta II and the rapid response recovery after exposure to bright light in red-sensitive cones.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118, USA. estevez@bu.edu

ABSTRACT
Cone photoreceptors of the vertebrate retina terminate their response to light much faster than rod photoreceptors. However, the molecular mechanisms underlying this rapid response termination in cones are poorly understood. The experiments presented here tested two related hypotheses: first, that the rapid decay rate of metarhodopsin (Meta) II in red-sensitive cones depends on interactions between the 9-methyl group of retinal and the opsin part of the pigment molecule, and second, that rapid Meta II decay is critical for rapid recovery from saturation of red-sensitive cones after exposure to bright light. Microspectrophotometric measurements of pigment photolysis, microfluorometric measurements of retinol production, and single-cell electrophysiological recordings of flash responses of salamander cones were performed to test these hypotheses. In all cases, cones were bleached and their visual pigment was regenerated with either 11-cis retinal or with 11-cis 9-demethyl retinal, an analogue of retinal lacking the 9-methyl group. Meta II decay was four to five times slower and subsequent retinol production was three to four times slower in red-sensitive cones lacking the 9-methyl group of retinal. This was accompanied by a significant slowing of the recovery from saturation in cones lacking the 9-methyl group after exposure to bright (>0.1% visual pigment photoactivated) but not dim light. A mathematical model of the turn-off process of phototransduction revealed that the slower recovery of photoresponse can be explained by slower Meta decay of 9-demethyl visual pigment. These results demonstrate that the 9-methyl group of retinal is required for steric chromophore-opsin interactions that favor both the rapid decay of Meta II and the rapid response recovery after exposure to bright light in red-sensitive cones.

Show MeSH
Related in: MedlinePlus