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The Journal of Neuroscience, October 7, 2009, 29(40):12401-12411; doi:10.1523/JNEUROSCI.0951-09.2009

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Development/Plasticity/Repair
The Spatial Patterning of Mouse Cone Opsin Expression Is Regulated by Bone Morphogenetic Protein Signaling through Downstream Effector COUP-TF Nuclear Receptors

Shinya Satoh,¹ Ke Tang,² Atsumi Iida,¹ Mariko Inoue,¹ Tatsuhiko Kodama,³ Sophia Y. Tsai,² Ming-Jer Tsai,² Yasuhide Furuta,⁴ and Sumiko Watanabe¹

¹Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, Tokyo, 108-8639 Japan, ²Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas 77030, ³Research Center for Advanced Science and Technology, University of Tokyo, Tokyo, 153-8904 Japan, and ⁴Department of Biochemistry and Molecular Biology, The University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030

Correspondence should be addressed to Sumiko Watanabe, Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan. Email: sumiko{at}ims.u-tokyo.ac.jp

Cone photopigments, known as opsins, are pivotal elements and the first detection module used in color vision. In mice, cone photoreceptors are distributed throughout the retina, and short-wavelength (S) and medium-wavelength (M) opsins have unique expression patterns in the retina with a gradient along the dorsoventral axis; however, the mechanisms regulating the spatial patterning of cone opsin expression have not been well documented. The purpose of this study was to define the mechanisms regulating the spatial patterning of cone opsin expression. By analyzing knock-outs for bone morphogenetic protein (BMP) signaling, we found an essential role for BMP in forming cone opsin expression patterns in the retina; however, BMP signaling is activated only transiently in the dorsal half of the retina during early retinal development. Thus, BMP is not likely to play a direct role in opsin gene expression, which starts at a later stage of retinal development. We identified the chicken ovalbumin upstream promoter-transcription factor (COUP-TF) nuclear receptor as a link between BMP and opsin expression. BMP signaling is essential for the correct dorsoventral spatial expression of COUP-TFI and COUP-TFII. Through gain- and loss-of-function analyses, we found that both COUP-TFI and COUP-TFII are required to suppress S-opsin expression in the dorsal retina but that only COUP-TFI plays an essential role in suppressing M-opsin expression in the ventral retina. Based on these findings, we propose a new molecular cascade involving BMP and COUP-TFs that conveys dorsoventral information to direct the expression of cone opsins during retinal development.

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Received Feb. 25, 2009; revised July 2, 2009; accepted Aug. 17, 2009.

Correspondence should be addressed to Sumiko Watanabe, Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan. Email: sumiko{at}ims.u-tokyo.ac.jp

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