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β-ionone activates and bleaches visual pigment in salamander photoreceptors

Published online by Cambridge University Press:  01 May 2009

TOMOKI ISAYAMA ,
S.L. McCABE ENGLAND ,
R.K. CROUCH ,
A.L. ZIMMERMAN  and
C.L. MAKINO
TOMOKI ISAYAMA*
Affiliation:
Department of Ophthalmology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, Massachusetts
S.L. McCABE ENGLAND
Affiliation:
Department of Molecular Pharmacology, Physiology and Biotechnology, Brown University, Providence, Rhode Island
R.K. CROUCH
Affiliation:
Department of Ophthalmology, Storm Eye Research Institute, Medical University of South Carolina, Charleston, South Carolina
A.L. ZIMMERMAN
Affiliation:
Department of Molecular Pharmacology, Physiology and Biotechnology, Brown University, Providence, Rhode Island
C.L. MAKINO
Affiliation:
Department of Ophthalmology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, Massachusetts
*
*Address correspondence and reprint requests to: Tomoki Isayama, Department of Ophthalmology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, 243 Charles Street, Boston, MA 02114. E-mail: tomoki_isayama@meei.harvard.edu
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Abstract

Vision begins with photoisomerization of 11-cis retinal to the all-trans conformation within the chromophore-binding pocket of opsin, leading to activation of a biochemical cascade. Release of all-trans retinal from the binding pocket curtails but does not fully quench the ability of opsin to activate transducin. All-trans retinal and some other analogs, such as β-ionone, enhance opsin’s activity, presumably on binding the empty chromophore-binding pocket. By recording from isolated salamander photoreceptors and from patches of rod outer segment membrane, we now show that high concentrations of β-ionone suppressed circulating current in dark-adapted green-sensitive rods by inhibiting the cyclic nucleotide-gated channels. There were also decreases in circulating current and flash sensitivity, and accelerated flash response kinetics in dark-adapted blue-sensitive (BS) rods and cones, and in ultraviolet-sensitive cones, at concentrations too low to inhibit the channels. These effects persisted in BS rods even after incubation with 9-cis retinal to ensure complete regeneration of their visual pigment. After long exposures to high concentrations of β-ionone, recovery was incomplete unless 9-cis retinal was given, indicating that visual pigment had been bleached. Therefore, we propose that β-ionone activates and bleaches some types of visual pigments, mimicking the effects of light.

Keywords

RetinoidsPhototransductionRhodopsinCyclic nucleotide-gated channelNeurophysiology
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 267 - 274
Copyright
Copyright © Cambridge University Press 2009

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