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Role of visual pigment properties in rod and cone phototransduction

Nature volume 425, pages 526–531 (2003)Cite this article

Abstract

Retinal rods and cones share a phototransduction pathway involving cyclic GMP1. Cones are typically 100 times less photosensitive than rods and their response kinetics are several times faster2, but the underlying mechanisms remain largely unknown. Almost all proteins involved in phototransduction have distinct rod and cone variants. Differences in properties between rod and cone pigments have been described, such as a 10-fold shorter lifetime of the meta-II state (active conformation) of cone pigment3,4,5,6 and its higher rate of spontaneous isomerization7,8, but their contributions to the functional differences between rods and cones remain speculative. We have addressed this question by expressing human or salamander red cone pigment in Xenopus rods, and human rod pigment in Xenopus cones. Here we show that rod and cone pigments when present in the same cell produce light responses with identical amplification and kinetics, thereby ruling out any difference in their signalling properties. However, red cone pigment isomerizes spontaneously 10,000 times more frequently than rod pigment. This high spontaneous activity adapts the native cones even in darkness, making them less sensitive and kinetically faster than rods. Nevertheless, additional factors are probably involved in these differences.

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Figure 1: Xenopus rods expressing transgenic human and salamander red cone pigments.
Figure 2: Spectral shift and dim-flash responses in rods expressing transgenic cone pigment.
Figure 3: Analysis of dark-current noise.
Figure 4: Xenopus red cones expressing transgenic human rod pigment.

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Acknowledgements

We thank J. Lai, Y. Liang and R. Bruno for help with generating transgenic frogs; J. Nathans for the human rhodopsin and red cone opsin cDNAs and the antibody to red opsin; V. Bhandawat for suggesting the program for computer simulations of random events; and D. A. Baylor, M. E. Burns, S. Kawamura, E. N. Pugh Jr, F. Rieke, J. L. Schnapf, Y. Shichida and members of the Yau laboratory for discussions and comments on the manuscript. This work was supported by the US National Eye Institute.

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Author notes

  1. Vladimir Kefalov and Yingbin Fu: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, Maryland, 21205, USA

    Vladimir Kefalov, Nicholas Marsh-Armstrong & King-Wai Yau

  2. Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland, 21205, USA

    Yingbin Fu & King-Wai Yau

  3. Kennedy-Krieger Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland, 21205, USA

    Nicholas Marsh-Armstrong

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  1. Vladimir Kefalov
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Correspondence to King-Wai Yau.

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Kefalov, V., Fu, Y., Marsh-Armstrong, N. et al. Role of visual pigment properties in rod and cone phototransduction. Nature 425, 526–531 (2003). https://doi.org/10.1038/nature01992

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