Our ability to see in bright light depends critically on the rapid rate at which cone photoreceptors detect and adapt to changes in illumination. This is achieved, in part, by their rapid response termination. In this study, we investigate the hypothesis that this rapid termination of the response in red cones is dependent on interactions between the 9-methyl group of retinal and red cone opsin, which are required for timely metarhodopsin (Meta) II decay. We used single-cell electrical recordings of flash responses to assess the kinetics of response termination and to calculate guanylyl cyclase (GC) rates in salamander red cones containing native visual pigment as well as visual pigment regenerated with 11-cis 9-demethyl retinal, an analogue of retinal in which the 9-methyl group is missing. After exposure to bright light that photoactivated more than ∼0.2% of the pigment, red cones containing the analogue pigment had a slower recovery of both flash response amplitudes and GC rates (up to 10 times slower at high bleaches) than red cones containing 11-cis retinal. This finding is consistent with previously published biochemical data demonstrating that red cone opsin regenerated in vitro with 11-cis 9-demethyl retinal exhibited prolonged activation as a result of slowed Meta II decay. Our results suggest that two different mechanisms regulate the recovery of responsiveness in red cones after exposure to light. We propose a model in which the response recovery in red cones can be regulated (particularly at high light intensities) by the Meta II decay rate if that rate has been inhibited. In red cones, the interaction of the 9-methyl group of retinal with opsin promotes efficient Meta II decay and, thus, the rapid rate of recovery.
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1 December 2006
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November 13 2006
Turning Cones Off: the Role of the 9-Methyl Group of Retinal in Red Cones
Maureen E. Estevez,
Maureen E. Estevez
1Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118
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Petri Ala-Laurila,
Petri Ala-Laurila
1Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118
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Rosalie K. Crouch,
Rosalie K. Crouch
2Department of Ophthalmology, Medical University of South Carolina, Charleston, SC 29425
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M. Carter Cornwall
M. Carter Cornwall
1Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118
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Maureen E. Estevez
1Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118
Petri Ala-Laurila
1Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118
Rosalie K. Crouch
2Department of Ophthalmology, Medical University of South Carolina, Charleston, SC 29425
M. Carter Cornwall
1Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118
Correspondence to Maureen E. Estevez: [email protected]
Abbreviations used in this paper: cGMP, cyclic guanosine monophosphate; GC, guanylyl cyclase; GTP, guanosine triphosphate; IBMX, 3-isobutyl-1-methylxanthine; Meta, metarhodopsin; PDE, phosphodiesterase.
Received:
July 17 2006
Accepted:
October 23 2006
Online ISSN: 1540-7748
Print ISSN: 0022-1295
The Rockefeller University Press
2006
J Gen Physiol (2006) 128 (6): 671–685.
Article history
Received:
July 17 2006
Accepted:
October 23 2006
Citation
Maureen E. Estevez, Petri Ala-Laurila, Rosalie K. Crouch, M. Carter Cornwall; Turning Cones Off: the Role of the 9-Methyl Group of Retinal in Red Cones . J Gen Physiol 1 December 2006; 128 (6): 671–685. doi: https://doi.org/10.1085/jgp.200609630
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