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J. Biol. Chem., Vol. 282, Issue 9, 6677-6684, March 2, 2007

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Molecular Properties of Rhodopsin and Rod Function^*

Hiroo Imai¹², Vladimir Kefalov¹³, Keisuke Sakurai¹, Osamu Chisaka^¶, Yoshiki Ueda^||4, Akishi Onishi⁵, Takefumi Morizumi, Yingbin Fu, Kazuhisa Ichikawa^**, Kei Nakatani, Yoshihito Honda^||6, Jeannie Chen, King-Wai Yau, and Yoshinori Shichida⁷

From the Department of Biophysics, Graduate School of Science, Kyoto University and Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Kyoto 606-8502, Japan, the Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, the Departments of ^¶Cell and Developmental Biology, Graduate School of Biostudies, and ^||Ophthalmology and Visual Science, Graduate School of Medicine, Kyoto University, Kyoto 606-8507, Japan, the ^**Department of Brain and Bioinformation Science, Kanazawa Institute of Technology, Ishikawa 924-0838, Japan, the Graduate School of Life and Environmental Sciences, University of Tsukuba and Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Ibaraki 305-8572, Japan, and the The Mary D. Allen Laboratory for Vision Research, Doheny Eye Institute, Keck School of Medicine, University of Southern California, Los Angeles, California 90033

Signal transduction in rod cells begins with photon absorption by rhodopsin and leads to the generation of an electrical response. The response profile is determined by the molecular properties of the phototransduction components. To examine how the molecular properties of rhodopsin correlate with the rod-response profile, we have generated a knock-in mouse with rhodopsin replaced by its E122Q mutant, which exhibits properties different from those of wild-type (WT) rhodopsin. Knock-in mouse rods with E122Q rhodopsin exhibited a photosensitivity about 70% of WT. Correspondingly, their single-photon response had an amplitude about 80% of WT, and a rate of decline from peak about 1.3 times of WT. The overall 30% lower photosensitivity of mutant rods can be explained by a lower pigment photosensitivity (0.9) and the smaller single-photon response (0.8). The slower decline of the response, however, did not correlate with the 10-fold shorter lifetime of the meta-II state of E122Q rhodopsin. This shorter lifetime became evident in the recovery phase of rod cells only when arrestin was absent. Simulation analysis of the photoresponse profile indicated that the slower decline and the smaller amplitude of the single-photon response can both be explained by the shift in the meta-I/meta-II equilibrium of E122Q rhodopsin toward meta-I. The difference in meta-III lifetime between WT and E122Q mutant became obvious in the recovery phase of the dark current after moderate photobleaching of rod cells. Thus, the present study clearly reveals how the molecular properties of rhodopsin affect the amplitude, shape, and kinetics of the rod response.

Received for publication, October 27, 2006 , and in revised form, December 27, 2006.

^* This work was supported in part by grants-in-aid for Scientific Research from the Japanese Ministry of Education, Science, Sports and Culture (to Y. S. and H. I.) and United States National Eye Institute Grant EY 06837 (to K.-W. Y.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ These authors contributed equally to this work.

² Present address: Dept. of Cellular and Molecular Biology, Primate Research Institute, Kyoto University, Aichi 484-8506, Japan.

³ Present address: Dept. of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, MO 63110.

⁴ Present address: Nagahama City Hospital, Nagahama, Shiga 526-8380, Japan.

⁵ Present address: Dept. of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205.

⁶ Present address: Osaka Red Cross Hospital, Osaka 543-5111, Japan.

⁷ To whom correspondence should be addressed. Tel.: 81-75-753-4213; Fax: 81-75-753-4210; E-mail: shichida{at}vision-kyoto-u.jp.

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