The Journal of General Physiology
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Published online June 25, 2007
doi:10.1085/jgp.200609729
The Journal of General Physiology, Vol. 130, No. 1, 21-40
The Rockefeller University Press, 0022-1295 $30.00
© 2007 Sakurai et al.
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ARTICLE

 Physiological Properties of Rod Photoreceptor Cells in Green-sensitive Cone Pigment Knock-in Mice



Keisuke Sakurai1, Akishi Onishi1, Hiroo Imai1, Osamu Chisaka2, Yoshiki Ueda3, Jiro Usukura4, Kei Nakatani5, and Yoshinori Shichida1

1 Department of Biophysics, Graduate School of Science, Kyoto University and Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, Kyoto 606-8502, Japan
2 Department of Cell and Developmental Biology, Graduate School of Biostudies, Kyoto University, Kyoto 606-8501, Japan
3 Department of Ophthalmology, School of Medicine, Kyoto University, Kyoto 606-8501, Japan
4 Department of Anatomy and Cell Biology, School of Medicine, Nagoya University, Nagoya 466-8550, Japan
5 Graduate School of Life and Environmental Science, University of Tsukuba and Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, Tsukuba, Ibaraki 305-8572, Japan

Correspondence to Yoshinori Shichida: shichida{at}vision-kyoto-u.jp

Rod and cone photoreceptor cells that are responsible for scotopic and photopic vision, respectively, exhibit photoresponses different from each other and contain similar phototransduction proteins with distinctive molecular properties. To investigate the contribution of the different molecular properties of visual pigments to the responses of the photoreceptor cells, we have generated knock-in mice in which rod visual pigment (rhodopsin) was replaced with mouse green-sensitive cone visual pigment (mouse green). The mouse green was successfully transported to the rod outer segments, though the expression of mouse green in homozygous retina was ~11% of rhodopsin in wild-type retina. Single-cell recordings of wild-type and homozygous rods suggested that the flash sensitivity and the single-photon responses from mouse green were three to fourfold lower than those from rhodopsin after correction for the differences in cell volume and levels of several signal transduction proteins. Subsequent measurements using heterozygous rods expressing both mouse green and rhodopsin E122Q mutant, where these pigments in the same rod cells can be selectively irradiated due to their distinctive absorption maxima, clearly showed that the photoresponse of mouse green was threefold lower than that of rhodopsin. Noise analysis indicated that the rate of thermal activations of mouse green was 1.7 x 10–7 s–1, about 860-fold higher than that of rhodopsin. The increase in thermal activation of mouse green relative to that of rhodopsin results in only 4% reduction of rod photosensitivity for bright lights, but would instead be expected to severely affect the visual threshold under dim-light conditions. Therefore, the abilities of rhodopsin to generate a large single photon response and to retain high thermal stability in darkness are factors that have been necessary for the evolution of scotopic vision.

A. Onishi's present address is Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205.

H. Imai's present address is Department of Cellular and Molecular Biology, Primate Research Institute, Kyoto University, Aichi 484-8506, Japan.

Y. Ueda's present address is Nagahama City Hospital, Nagahama, Shiga 526-8380, Japan.

Abbreviations used in this paper: ES, embryonic stem; GRK, G protein–coupled receptor kinase; GTP{gamma}S, guanosine 5'-O-(3-thiotriphosphate); ROS, rod outer segment.


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