Evolution and the origin of the visual retinoid cycle in vertebrates
Open accessAbstract
Absorption of a photon by visual pigments induces isomerization of 11- cis -retinaldehyde (RAL) chromophore to all- trans -RAL. Since the opsins lacking 11- cis -RAL lose light sensitivity, sustained vision requires continuous regeneration of 11- cis -RAL via the process called ‘visual cycle’. Protostomes and vertebrates use essentially different machinery of visual pigment regeneration, and the origin and early evolution of the vertebrate visual cycle is an unsolved mystery. Here we compare visual retinoid cycles between different photoreceptors of vertebrates, including rods, cones and non-visual photoreceptors, as well as between vertebrates and invertebrates. The visual cycle systems in ascidians, the closest living relatives of vertebrates, show an intermediate state between vertebrates and non-chordate invertebrates. The ascidian larva may use retinochrome-like opsin as the major isomerase. The entire process of the visual cycle can occur inside the photoreceptor cells with distinct subcellular compartmentalization, although the visual cycle components are also present in surrounding non-photoreceptor cells. The adult ascidian probably uses RPE65 isomerase, and trans -to- cis isomerization may occur in distinct cellular compartments, which is similar to the vertebrate situation. The complete transition to the sophisticated retinoid cycle of vertebrates may have required acquisition of new genes, such as interphotoreceptor retinoid-binding protein, and functional evolution of the visual cycle genes.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Visual perception starts with the absorption of a photon, which induces isomerization of 11cRAL to 11-trans retinaldehyde; then 11tRAL is released from opsin and the 11-cis chromophore is regenerated for sustained vision.
“Visual perception starts with the absorption of a photon, which induces isomerization of 11cRAL to 11-trans retinaldehyde (11tRARL).Then 11tRAL is released from opsin and the 11-cis chromophore is regenerated for sustained vision.”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [8]
11cRAL works as a chromophore and binds opsin, a G protein.
“11cRAL works as a chromophore and binds opsin, a G protein.”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [8]
Vitamin A is essential for vision.
“Vitamin A is essential for vision.”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [8]
In the eye, the active metabolite of vitamin A is 11-cis-retinaldehyde (11cRAL).
“In the eye, its active metabolite is 11-cis -retinaldehyde (11cRAL) (for review, see Ref. 8 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [8]
Cites
Tunicates and not cephalochordates are the closest living relatives of vertebrates
Delsuc, F., Brinkmann, H., Chourrout, D., & Philippe, H. (2006) · Nature · doi:10.1038/nature04336 · Cited by 1,651 · see citing works
The amphioxus genome and the evolution of the chordate karyotype
Putnam, N. H., Butts, T., Ferrier, D. E. K., Furlong, R. F., Hellsten, U., Kawashima, T., Robinson‐Rechavi, M., Shoguchi, E., Terry, A. Y., Yu, J., et al. (2008) · Nature · doi:10.1038/nature06967 · Cited by 1,568 · see citing works
Ciabarra, A., Sullivan, J., Gahn, L. G., Pecht, G., Heinemann, S., & Sevarino, K. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06498.1995 · Cited by 1,254 · see citing works
Hattar, S., Lucas, R. J., Mrosovsky, N., Thompson, S., Douglas, R. H., Hankins, M. W., Lem, J., Biel, M., Hofmann, F., Foster, R. G., et al. (2003) · Nature · doi:10.1038/nature01761 · Cited by 1,245 · see citing works
Melanopsin: An opsin in melanophores, brain, and eye
Provencio, I., Jiang, G., De Grip, W. J., Hayes, W. P., & Rollag, M. D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.1.340 · Cited by 975 · see citing works
Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle
Redmond., T. M., Yu, S., Lee, E., Bok, D., Hamasaki, D., Chen, N., Goletz, P., Ma, J.-X., Crouch, R. K., & Pfeifer, K. (1998) · Nature Genetics · doi:10.1038/3813 · Cited by 929 · see citing works
Gossip in Evolutionary Perspective
Dunbar, R. I. M. (2004) · Review of General Psychology · doi:10.1037/1089-2680.8.2.100 · Cited by 920 · see citing works
Nrl is required for rod photoreceptor development
Mears, A. J., Kondo, M., Swain, P. K., Takada, Y., Bush, R. A., Saunders, T. L., Sieving, P. A., & Swaroop, A. (2001) · Nature Genetics · doi:10.1038/ng774 · Cited by 912 · see citing works
Diminished Pupillary Light Reflex at High Irradiances in Melanopsin-Knockout Mice
Lucas, R. J., Hattar, S. S., Takao, M., Berson, D. M., Foster, F., & Yau, K. (2003) · Science · doi:10.1126/science.1077293 · Cited by 835 · see citing works
Dark adaptation and the retinoid cycle of vision
Lamb, T. D., & Pugh, E. N. (2004) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2004.03.001 · Cited by 725 · see citing works
RPE65 is the isomerohydrolase in the retinoid visual cycle
Moiseyev, G., Chen, Y., Takahashi, Y., Wu, B. X., & Ma, J.-X. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503460102 · Cited by 536 · see citing works
Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina.
Bunt-Milam, A. H., & Saari, J. C. (1983) · The Journal of cell biology · doi:10.1083/jcb.97.3.703 · Cited by 455 · see citing works
Kiefer, C., Hessel, S., Lampert, J. M., Vogt, K., Lederer, M. O., Breithaupt, D. E., & Lintig, J. V. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011510200 · Cited by 453 · see citing works
Filling the Gap in Vitamin A Research
von Lintig, J., & Vogt, K. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.16.11915 · Cited by 449 · see citing works
Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium
Jin, M., Li, S., Moghrabi, W. N., Sun, H., & Travis, G. H. (2005) · Cell · doi:10.1016/j.cell.2005.06.042 · Cited by 424 · see citing works
Self-citationDiseases Caused by Defects in the Visual Cycle: Retinoids as Potential Therapeutic Agents
Travis, G. H., Golczak, M., Moise, A. R., & Palczewski, K. (2007) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.47.120505.105225 · Cited by 419 · see citing works
Redmond, T. M., Poliakov, E., Yu, S., Tsai, J.-Y., Lu, Z., & Gentleman, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504167102 · Cited by 409 · see citing works
Isomerization and Oxidation of Vitamin A in Cone-Dominant Retinas
Mata, N. L., Radu, R. A., Clemmons, R. S., & Travis, G. H. (2002) · Neuron · doi:10.1016/s0896-6273(02)00912-1 · Cited by 382 · see citing works
Batten, M. L., Imanishi, Y., Maeda, T., Tu, D. C., Moise, A. R., Bronson, D., Possin, D., Van Gelder, R. N., Baehr, W., & Palczewski, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312410200 · Cited by 368 · see citing works
Hamel, C., Tsilou, E. T., Pfeffer, B. A., Hooks, J. J., Detrick, B., & Redmond, T. M. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)82319-5 · Cited by 334 · see citing works
Maw, M. A., Kennedy, B. N., Knight, A., Bridges, R., Roth, K. E., Mani, E. J., Mukkadan, J. K., Nancarrow, D. J., Crabb, J. W., & Denton, M. J. (1997) · Nature Genetics · doi:10.1038/ng1097-198 · Cited by 327 · see citing works
CAROTENOIDS AND THE VISUAL CYCLE
Wald, G. (1935) · The Journal of General Physiology · doi:10.1085/jgp.19.2.351 · Cited by 302 · see citing works
Identification, Expression, and Substrate Specificity of a Mammalian β-Carotene 15,15′-Dioxygenase
Redmond, T. M., Gentleman, S., Duncan, T. E., Yu, S., Wiggert, B. O., Gantt, E., & Cunningham, F. X. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009030200 · Cited by 279 · see citing works
Molecular and Biochemical Characterization of Lecithin Retinol Acyltransferase
Ruiz, A., Winston, A., Lim, Y.-H., Gilbert, B. A., Rando, R. R., & Bok, D. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.6.3834 · Cited by 265 · see citing works
The Structure of a Retinal-Forming Carotenoid Oxygenase
Kloer, D. P., Ruch, S., Al‐Babili, S., Beyer, P., & Schulz, G. E. (2005) · Science · doi:10.1126/science.1108965 · Cited by 261 · see citing works
Saari, J. C., Nawrot, M., Kennedy, B. N., Garwin, G. G., Hurley, J. B., Huang, J., Possin, D. E., & Crabb, J. W. (2001) · Neuron · doi:10.1016/s0896-6273(01)00248-3 · Cited by 251 · see citing works
Biochemistry of visual pigment regeneration: the Friedenwald lecture.
Saari, J. C. (2000) · PubMed · Cited by 244 · see citing works
Jones, G. J., Crouch, R. K., Wiggert, B., Cornwall, M. C., & Chader, G. J. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.23.9606 · Cited by 244 · see citing works
Biochemical Properties of Purified Recombinant Human β-Carotene 15,15′-Monooxygenase
Lindqvist, A., & Andersson, S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202756200 · Cited by 239 · see citing works
Koyanagi, M., Kubokawa, K., Tsukamoto, H., Shichida, Y., & Terakita, A. (2005) · Current Biology · doi:10.1016/j.cub.2005.04.063 · Cited by 237 · see citing works
Dual-substrate Specificity Short Chain Retinol Dehydrogenases from the Vertebrate Retina
Haeseleer, F., Jang, G.-F., Imanishi, Y., Driessen, C. A. G. G., Matsumura, M., Nelson, P. S., & Palczewski, K. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m208882200 · Cited by 214 · see citing works
A photic visual cycle of rhodopsin regeneration is dependent on Rgr
Chen, P., Hao, W., Rife, L. L., Wang, X. P., Shen, D., Chen, J., Ogden, T. E., Boemel, G. B. V., Wu, L., Yang, M., et al. (2001) · Nature Genetics · doi:10.1038/90089 · Cited by 208 · see citing works
Rattner, A., Smallwood, P. M., & Nathans, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.15.11034 · Cited by 207 · see citing works
Liou, G. I., Bridges, C. D. B., Fong, S. –., Alvarez, R., & Gonzalez–Fernandez, F. (1982) · Vision Research · doi:10.1016/0042-6989(82)90210-3 · Cited by 205 · see citing works
The photoreceptor array of the dipteran retina
Hardie, R. (1986) · Trends in Neurosciences · doi:10.1016/0166-2236(86)90136-0 · Cited by 205 · see citing works
Non-rod, non-cone photoreception in the vertebrates
Foster, F., & Hankins, M. W. (2002) · Progress in Retinal and Eye Research · doi:10.1016/s1350-9462(02)00036-8 · Cited by 191 · see citing works
The Biochemistry of the Visual Cycle
Rando, R. R. (2001) · Chemical Reviews · doi:10.1021/cr960141c · Cited by 163 · see citing works
Bistable UV pigment in the lamprey pineal
Koyanagi, M., Kawano‐Yamashita, E., Kinugawa, Y., Oishi, T., Shichida, Y., Tamotsu, S., & Terakita, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400819101 · Cited by 163 · see citing works
Membranes as the Energy Source in the Endergonic Transformation of Vitamin A to 11- cis -Retinol
Deigner, P. S., Law, W. C., Cañada, F. J., & Rando, R. R. (1989) · Science · doi:10.1126/science.2727688 · Cited by 162 · see citing works
Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo
Maeda, A., Maeda, T., Imanishi, Y., Kuksa, V., Alekseev, A., Bronson, J. D., Zhang, H., Zhu, L., Sun, W., Saperstein, D. A., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m501757200 · Cited by 159 · see citing works
Palczewski, K., Hooser, J. P. V., Garwin, G. G., Chen, J., Liou, G. I., & Saari, J. C. (1999) · Biochemistry · doi:10.1021/bi990504d · Cited by 157 · see citing works
Kojima, D., Mano, H., & Fukada, Y. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-08-02845.2000 · Cited by 154 · see citing works
Sun, H., Gilbert, D. J., Copeland, N. G., Jenkins, N. A., & Nathans, J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.18.9893 · Cited by 153 · see citing works
Yan, W., Jang, G.-F., Haeseleer, F., Esumi, N., Chang, J. T., Kerrigan, M., Campochiaro, M., Campochiaro, P. A., Palczewski, K., & Zack, D. J. (2001) · Genomics · doi:10.1006/geno.2000.6476 · Cited by 152 · see citing works
Morimura, H., Berson, E. L., & Dryja, T. P. (1999) · PubMed · Cited by 147 · see citing works
Redmond, T. M., Wiggert, B. O., Robey, F. A., Yen, N. N., Lewis, M. S., Lee, L., & Chader, G. J. (1985) · Biochemistry · doi:10.1021/bi00324a038 · Cited by 145 · see citing works
A Palmitoylation Switch Mechanism in the Regulation of the Visual Cycle
Xue, L., Gollapalli, D. R., Maiti, P., Jahng, W. J., & Rando, R. R. (2004) · Cell · doi:10.1016/j.cell.2004.05.016 · Cited by 141 · see citing works
Soni, B. G., Philp, A. R., Foster, F., & Knox, B. E. (1998) · Nature · doi:10.1038/27794 · Cited by 138 · see citing works
Lampert, J. M., Holzschuh, J., Hessel, S., Driever, W., Vogt, K., & Lintig, J. V. (2003) · Development · doi:10.1242/dev.00437 · Cited by 137 · see citing works
Muller cells of chicken retina synthesize 11- <i>cis</i> -retinol
Das, S. R., Bhardwaj, N., Kjeldbye, H., & Gouras, P. (1992) · Biochemical Journal · doi:10.1042/bj2850907 · Cited by 135 · see citing works
Interphotoreceptor Retinoid-binding Protein
Borst, D. E., Redmond, T. M., Elser, J. E., Gonda, M. A., Wiggert, B. O., Chader, G. J., & Nickerson, J. M. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)85061-5 · Cited by 133 · see citing works
Driessen, C. A. G. G., Winkens, H. J., Hoffmann, K., Kuhlmann, L. D., Janssen, B. P. M., Van Vugt, A. H. M., Van Hooser, J. P., Wieringa, B. E., Deutman, A. F., Palczewski, K., et al. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.12.4275-4287.2000 · Cited by 132 · see citing works
Båvik, C., Busch, C., & Eriksson, U. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)50052-1 · Cited by 129 · see citing works
The distribution and proportions of vitamin A compounds during the visual cycle in the rat
Zimmerman, W. F. (1974) · Vision Research · doi:10.1016/0042-6989(74)90143-6 · Cited by 126 · see citing works
Burstedt, M. S. I., Sandgren, O., Holmgren, G., & Forsman‐Semb, K. (1999) · PubMed · Cited by 126 · see citing works
Mata, N. L., Moghrabi, W. N., Lee, J. S., Bui, T. V., Radu, R. A., Horwitz, J., & Travis, G. H. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m310042200 · Cited by 123 · see citing works
Terakita, A., Hara, R., & Hara, T. (1989) · Vision Research · doi:10.1016/0042-6989(89)90026-6 · Cited by 118 · see citing works
Nonvisual photoreceptors of the deep brain, pineal organs and retina.
Béla, V. I. G. H., Silva, M. J. M. E., Zádori, A., Frank, C. L., Lukáts, Á., Röhlich, P., Szél, Á., & Dávid, C. (2002) · PubMed · doi:10.14670/hh-17.555 · Cited by 114 · see citing works
Koyanagi, M., Terakita, A., Kubokawa, K., & Shichida, Y. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)03616-5 · Cited by 114 · see citing works
van Veen, T., Katial, A., Shinohara, T., Barrett, D. J., Wiggert, B., Chader, G., & Nickerson, J. M. (1986) · FEBS Letters · doi:10.1016/0014-5793(86)81547-2 · Cited by 112 · see citing works
Carotene Oxygenases: A New Family of Double Bond Cleavage Enzymes
Wyss, A. (2004) · Journal of Nutrition · doi:10.1093/jn/134.1.246s · Cited by 112 · see citing works
(1984) · PubMed · Cited by 112 · see citing works
Carlson, A., & Bok, D. (1992) · Biochemistry · doi:10.1021/bi00152a049 · Cited by 111 · see citing works
Photochemistry of retinal chromophore in mouse melanopsin
Walker, M., Brown, R. L., Cronin, T. W., & Robinson, P. R. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711397105 · Cited by 109 · see citing works
Delayed Dark Adaptation in 11-cis-Retinol Dehydrogenase-deficient Mice
Kim, T. S., Maeda, A., Maeda, T., Heinlein, C. A., Kedishvili, N. Y., Palczewski, K., & Nelson, P. S. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m413172200 · Cited by 108 · see citing works
Identification of the RPE65 protein in mammalian cone photoreceptors.
Znoiko, S. L., Crouch, R. K., Moiseyev, G. P., & Xing, J. (2002) · PubMed · Cited by 107 · see citing works
Crouch, R. K., Hazard, E. S., Lind, T., Wiggert, B., Chader, G., & Corson, D. W. (1992) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1992.tb02154.x · Cited by 105 · see citing works
Kusakabe, T. G., Kusakabe, R., Kawakami, I., Satou, Y., Satoh, N., & Tsuda, M. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02877-0 · Cited by 100 · see citing works
Self-citationRipps, H., Peachey, N. S., Xu, X., Nozell, S. E., Smith, S. B., & Liou, G. I. (2000) · Visual Neuroscience · doi:10.1017/s095252380017110x · Cited by 96 · see citing works
The Retinal G Protein-coupled Receptor (RGR) Enhances Isomerohydrolase Activity Independent of Light
Wenzel, A., Oberhauser, V., Pugh, E. N., Lamb, T. D., Grimm, C., Samardzija, M., Fahl, E., Seeliger, M. W., Remé, C. E., & von Lintig, J. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m503603200 · Cited by 92 · see citing works
Regeneration of Squid Retinochrome
Hara, T., & Hara, R. (1968) · Nature · doi:10.1038/219450a0 · Cited by 90 · see citing works
Blue and Ultraviolet Light-Absorbing Opsin from the Retinal Pigment Epithelium
Hao, W., & Fong, H. K. W. (1996) · Biochemistry · doi:10.1021/bi952420k · Cited by 83 · see citing works
Mata, N. L., Ruiz, A., Radu, R. A., Bui, T. V., & Travis, G. H. (2005) · Biochemistry · doi:10.1021/bi050942m · Cited by 80 · see citing works
Interphotoreceptor retinoid-binding protein in retinal rod cells and pineal gland.
Rodrigues, M. M., Hackett, J., Gaskins, H. R., Wiggert, B. O., Lee, L., Redmond, T. M., & Chader, G. J. (1986) · PubMed · Cited by 78 · see citing works
Maeda, T., Van Hooser, J. P., Driessen, C. A. G. G., Filipek, S., Janssen, J. J. M., & Palczewski, K. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01741.x · Cited by 75 · see citing works
β-Carotene Conversion into Vitamin A in Human Retinal Pigment Epithelial Cells
Chichili, G. R., Nöhr, D., ̈ffer, M. S., Lintig, J. V., & Biesalski, H. K. (2005) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.05-0089 · Cited by 72 · see citing works
A Median Third Eye: Pineal Gland Retraces Evolution of Vertebrate Photoreceptive Organs †
Mano, H., & Fukada, Y. (2006) · Photochemistry and Photobiology · doi:10.1562/2006-02-24-ir-813 · Cited by 71 · see citing works
Fleisch, V. C., Schonthaler, H. B., von Lintig, J., & Neuhauss, S. C. F. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2367-08.2008 · Cited by 68 · see citing works
Transcriptional Profiling of Circadian Patterns of mRNA Expression in the Chick Retina
Bailey, M. J., Beremand, P. D., Hammer, R., Reidel, E., Thomas, T. L., & Cassone, V. M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405679200 · Cited by 66 · see citing works
RPE65 is essential for the function of cone photoreceptors in NRL-deficient mice
Wenzel, A., von Lintig, J., Oberhauser, V., Tanimoto, N., Grimm, C., & Seeliger, M. W. (2007) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.06-0652 · Cited by 66 · see citing works
PHOTORECEPTION AND PHOTOTRANSDUCTION IN INVERTEBRATE PHOTORECEPTORS
Tsuda, M. (1987) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1987.tb07903.x · Cited by 65 · see citing works
Self-citationDriessen, C. A. G. G. (1995) · Vision Research · doi:10.1016/0042-6989(95)98273-c · Cited by 63 · see citing works
A novel cone visual cycle in the cone-dominated retina
Muniz, A., Villazana-Espinoza, E. T., Hatch, A. L., Trevino, S. G., Allen, D. M., & Tsin, A. T. C. (2007) · Experimental Eye Research · doi:10.1016/j.exer.2007.05.003 · Cited by 60 · see citing works
Expression, purification, and MALDI analysis of RPE65.
X., J., Zhang, J., Othersen, K. L., Moiseyev, G. P., Ablonczy, Z., Redmond, T. M., Chen, Y.-J., & Crouch, R. K. (2001) · PubMed · Cited by 58 · see citing works
Luo, W., Marsh-Armstrong, N., Rattner, A., & Nathans, J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5302-03.2004 · Cited by 58 · see citing works
Isomerization of Retinal catalysed by Retinochrome in the Light
Hara, T., & Hara, R. (1973) · Nature New Biology · doi:10.1038/newbio242039a0 · Cited by 57 · see citing works
Pigmented and nonpigmented ocelli in the brain vesicle of the ascidian larva
Horie, T., Sakurai, D., Ohtsuki, H., Terakita, A., Shichida, Y., Usukura, J., Kusakabe, T. G., & Tsuda, M. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21733 · Cited by 56 · see citing works
Self-citationCollery, R., McLoughlin, S., Vendrell, V., Finnegan, J., Crabb, J. W., Saari, J. C., & Kennedy, B. N. (2008) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.08-1957 · Cited by 56 · see citing works
Bailey, M. J., & Cassone, V. M. (2004) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.03-1125 · Cited by 55 · see citing works
Highly efficient retinal metabolism in cones
Miyazono, S., Shimauchi-Matsukawa, Y., Tachibanaki, S., & Kawamura, S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806593105 · Cited by 55 · see citing works
Evidence for RPE65‐independent vision in the cone‐dominated zebrafish retina
Schönthaler, H. B., Lampert, J. M., Isken, A., Rinner, O., Mader, A., Gesemann, M., Oberhauser, V., Golczak, M., Biehlmaier, O., Palczewski, K., et al. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05801.x · Cited by 52 · see citing works
A Cleavable Affinity Biotinylating Agent Reveals a Retinoid Binding Role for RPE65
Jahng, W. J., David, C. J., Nesnas, N., Nakanishi, K., & Rando, R. R. (2003) · Biochemistry · doi:10.1021/bi034002i · Cited by 52 · see citing works
Retinoid Specificity of Interphotoreceptor Retinoid-Binding Protein
Chen, Y., & Noy, N. (1994) · Biochemistry · doi:10.1021/bi00201a013 · Cited by 51 · see citing works
Role of LRAT on the Retinoid Isomerase Activity and Membrane Association of Rpe65
Jin, M., Yuan, Q., Li, S., & Travis, G. H. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701432200 · Cited by 47 · see citing works
Self-citationChen, P., Lee, T. D., & Fong, H. K. W. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010441200 · Cited by 47 · see citing works
Tsuda, M., Kusakabe, T. G., Iwamoto, H., Horie, T., Nakashima, Y., Nakagawa, M., & Okunou, K. (2003) · Vision Research · doi:10.1016/j.visres.2003.09.012 · Cited by 46 · see citing works
Self-citationManning, T. J., & Sontheimer, H. W. (1997) · Glia · doi:10.1002/(sici)1098-1136(199711)21:3 · Cited by 46 · see citing works
Sensitization and Habituation of the Swimming Behavior in Ascidian Larvae to Light
Tsuda, M., Kawakami, I., & Shiraishi, S. (2003) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.20.13 · Cited by 45 · see citing works
Self-citationEvolution of the visual cycle: the role of retinoid-binding proteins
Gonzalez–Fernandez, F. (2002) · Journal of Endocrinology · doi:10.1677/joe.0.1750075 · Cited by 44 · see citing works
Nrl -Knockout Mice Deficient in Rpe65 Fail to Synthesize 11- cis Retinal and Cone Outer Segments
Feathers, K. L., Lyubarsky, A., Khan, N. W., Teofilo, K., Swaroop, A., Williams, D. S., Pugh, E. N., & Thompson, D. A. (2008) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.07-1234 · Cited by 44 · see citing works
Deyts, C., Casañe, D., Vernier, P., Bourrat, F., & Joly, J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05073.x · Cited by 42 · see citing works
Photoreceptive Systems in Ascidians†
Kusakabe, T. G., & Tsuda, M. (2007) · Photochemistry and Photobiology · doi:10.1562/2006-07-11-ir-965 · Cited by 41 · see citing works
Self-citationNakashima, Y., Kusakabe, T. G., Kusakabe, R., Terakita, A., Shichida, Y., & Tsuda, M. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10645 · Cited by 41 · see citing works
Self-citationTargeted knockdown of an opsin gene inhibits the swimming behaviour photoresponse of ascidian larvae
Inada, K., Horie, T., Kusakabe, T. G., & Tsuda, M. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00689-x · Cited by 40 · see citing works
Self-citationDabestani, R., & Ivanov, I. N. (1999) · Photochemistry and Photobiology · doi:10.1562/0031-8655(1999)070 · Cited by 38 · see citing works
Self-citationInterstitial retinol-binding protein and cellular retinal-binding protein in the mammalian pineal
Bridges, C. D. B., Foster, F., Landers, R. A., & Fong, S. –. (1987) · Vision Research · doi:10.1016/0042-6989(87)90119-2 · Cited by 34 · see citing works
Qtaishat, N. M., Wiggert, B. O., & Pepperberg, D. R. (2005) · Experimental Eye Research · doi:10.1016/j.exer.2005.03.005 · Cited by 33 · see citing works
SHARMA, H. S. (1973) · Nature · doi:10.1038/242039a0 · Cited by 33 · see citing works
Acyl CoA:retinol acyltransferase (ARAT) activity is present in bovine retinal pigment epithelium
Kaschula, C. H., Jin, M., Desmond-Smith, N. S., & Travis, G. H. (2005) · Experimental Eye Research · doi:10.1016/j.exer.2005.05.010 · Cited by 28 · see citing works
Self-citationHara, T., & Hara, R. (1991) · Progress in Retinal Research · doi:10.1016/0278-4327(91)90013-r · Cited by 27 · see citing works
Origin of the Vertebrate Visual Cycle†
Takimoto, N., Kusakabe, T. G., & Tsuda, M. (2007) · Photochemistry and Photobiology · doi:10.1562/2006-06-30-ir-957 · Cited by 26 · see citing works
Self-citationInterphotoreceptor retinoid-binding protein gene structure in tetrapods and teleost fish.
Nickerson, J. M., Frey, R. A., Ciavatta, V. T., & Stenkamp, D. L. (2006) · PubMed · Cited by 23 · see citing works
Rhodopsin, vitamin A, and interstitial retinol-binding protein in the rd chicken.
Bridges, C. D. B., Alvarez, R., Fong, S. –., Liou, G. I., & Ulshafer, R. J. (1987) · PubMed · Cited by 22 · see citing works
Takimoto, N., Kusakabe, T. G., Horie, T., Miyamoto, Y., & Tsuda, M. (2006) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2006.tb09801.x · Cited by 20 · see citing works
Self-citationVisualization of Retinal Proteins in the Cerebral Ganglion of Ascidian, Halocynthia roretzi
Ohkuma, M., & Tsuda, M. (2000) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.17.161 · Cited by 20 · see citing works
Self-citationOhkuma, M., Katagiri, Y., Nakagawa, M., & Tsuda, M. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01481-6 · Cited by 20 · see citing works
Self-citationTakahashi, Y., Moiseyev, G. P., Chen, Y., & Ma, J. (2006) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.06-0614 · Cited by 19 · see citing works
Choo, D. W., Cheung, E. C., & Rando, R. R. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)01459-8 · Cited by 18 · see citing works
Tsutsui, H., & Oka, Y. (2000) · Biological Bulletin · doi:10.2307/1542800 · Cited by 18 · see citing works
Dynamic Uplift of Andean Mountains and Island Arcs
Gough, D. I. (1973) · Nature Physical Science · doi:10.1038/physci242039a0 · Cited by 16 · see citing works
Molecular Logic of 11-cis-Retinoid Biosynthesis in a Cone-Dominated Species
Gollapalli, D. R., & Rando, R. R. (2003) · Biochemistry · doi:10.1021/bi0356505 · Cited by 14 · see citing works
A Purified Agonist-Activated G-Protein Coupled Receptor: Truncated Octopus Acid Metarhodopsin
Ashida, A., Matsumoto, K., Ebrey, T. G., & Tsuda, M. (2004) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.21.245 · Cited by 14 · see citing works
Self-citationRetinal isomers in the cerebral ganglion of the ascidian,Halocynthia roretzi
Kajiwara, S., Tamotsu, S., Morita, Y., & Numakunai, T. (1990) · Invertebrate Reproduction & Development · doi:10.1080/07924259.1990.9672104 · Cited by 11 · see citing works
Peterson, P. L. (1995) · Journal of Philosophical Logic · doi:10.1007/bf01048531 · Cited by 4 · see citing works
New Paradigms for Organic Catalysts: The First Organocatalytic Living Polymerization
Nederberg, F., Connor, E. F., Möller, M., Glauser, T., & Hedrick, J. L. (2001) · Angewandte Chemie International Edition · doi:10.1002/1521-3773(20010716)40:14
Flagged first, then by citations
1 of the 126 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Vitamin E: Emerging aspects and new directions
Galli, F., Azzi, A., Birringer, M., Cook‐Mills, J. M., Eggersdorfer, M. L., Frank, J., Cruciani, G., Stefan Lorkowski, A., & Özer, N. K. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.09.017 · Cited by 455 · see citing works
Evolution of phototransduction, vertebrate photoreceptors and retina
Lamb, T. D. (2013) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2013.06.001 · Cited by 399 · see citing works
Vitamin A and retinoid signaling: genomic and nongenomic effects
Al Tanoury, Z., Piskunov, A., & Rochette-Egly, C. (2013) · Journal of Lipid Research · doi:10.1194/jlr.r030833 · Cited by 408 · see citing works
Chemistry of the Retinoid (Visual) Cycle
Kiser, P. D., Golczak, M., & Palczewski, K. (2014) · Chemical Reviews · doi:10.1021/cr400107q · Cited by 353 · see citing works
Eye evolution and its functional basis
NILSSON, D.-E. (2013) · Visual Neuroscience · doi:10.1017/s0952523813000035 · Cited by 267 · see citing works
The evolution of eyes and visually guided behaviour
Nilsson, D.-E. (2009) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0083 · Cited by 258 · see citing works
Avian Coloration Genetics: Recent Advances and Emerging Questions
Price-Waldman, R., & Stoddard, M. C. (2021) · Journal of Heredity · doi:10.1093/jhered/esab015 · Cited by 118 · see citing works
Kefalov, V. J. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.r111.303008 · Cited by 114 · see citing works
Vertebrate ancient opsin and melanopsin: divergent irradiance detectors
Davies, W. L., Hankins, M. W., & Foster, R. G. (2010) · Photochemical & Photobiological Sciences · doi:10.1039/c0pp00203h · Cited by 100 · see citing works
How Complexity Originates: The Evolution of Animal Eyes
Oakley, T. H., & Speiser, D. I. (2015) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-110512-135907 · Cited by 82 · see citing works
Akhtar, T., Xie, H., Khan, M. I., Zhao, H., Bao, J., Zhang, M., & Xue, T. (2019) · Stem Cell Research · doi:10.1016/j.scr.2019.101491 · Cited by 76 · see citing works
Evolution of vertebrate retinal photoreception
Lamb, T. D. (2009) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0102 · Cited by 73 · see citing works
Lrat-specific domain facilitates Vitamin A metabolism by domain swapping in HRASLS3
Golczak, M., Sears, A. E., Kiser, P. D., & Palczewski, K. (2015) · Nature Chemical Biology · doi:10.1038/nchembio.1687 · Cited by 58 · see citing works
Single-cell transcriptome profiling of the Ciona larval brain
Sharma, S., Wang, W., & Stolfi, A. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.09.023 · Cited by 43 · see citing works
Poliakov, E., Gubin, A. N., Stearn, O., Li, Y., Campos, M. M., Gentleman, S., Rogozin, I. B., & Redmond, T. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049975 · Cited by 40 · see citing works
Evolution of the Genetic Machinery of the Visual Cycle: A Novelty of the Vertebrate Eye?
Albalat, R. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr313 · Cited by 40 · see citing works
Interphotoreceptor Retinoid-Binding Protein (IRBP) in Retinal Health and Disease
Zeng, S., Zhang, T., Madigan, M. C., Fernando, N., Aggio-Bruce, R., Zhou, F., Pierce, M., Chen, Y., Huang, L., Natoli, R., et al. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.577935 · Cited by 37 · see citing works
Oonuma, K., Tanaka, M., Nishitsuji, K., KATO, Y. O., Shimai, K., & Kusakabe, T. G. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.10.014 · Cited by 37 · see citing works
Self-citationThe evolution of phototransduction and eyes
Lamb, T. D., Arendt, D., & Collin, S. P. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0106 · Cited by 27 · see citing works
Axon ensheathment and metabolic supply by glial cells in Drosophila
Schirmeier, S., Matzat, T., & Klämbt, C. (2015) · Brain Research · doi:10.1016/j.brainres.2015.09.003 · Cited by 24 · see citing works
Okawa, N., Shimai, K., Ohnishi, K., Ohkura, M., Nakai, J., Horie, T., Kuhara, A., & Kusakabe, T. G. (2020) · Scientific Reports · doi:10.1038/s41598-020-75344-7 · Cited by 21 · see citing works
Self-citationThe ascidian pigmented sensory organs: structures and developmental programs
Esposito, R., Racioppi, C., Pezzotti, M. R., Branno, M., Locascio, A., Ristoratore, F., & Spagnuolo, A. (2014) · genesis · doi:10.1002/dvg.22836 · Cited by 19 · see citing works
The chromophore structure of the long-lived intermediate of the C128T channelrhodopsin-2 variant
Bruun, S., Naumann, H., Kuhlmann, U., Schulz, C., Stehfest, K., Hegemann, P., & Hildebrandt, P. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.11.007 · Cited by 19 · see citing works
Kaushik, V., Gessa, L., Kumar, N., & Fernandes, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054408 · Cited by 19 · see citing works
Bacterial origin of a key innovation in the evolution of the vertebrate eye
Kalluraya, C. A., Weitzel, A. J., Tsu, B. V., & Daugherty, M. D. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2214815120 · Cited by 17 · see citing works
Vöcking, O., Leclère, L., & Hausen, H. (2021) · BMC Ecology and Evolution · doi:10.1186/s12862-021-01939-x · Cited by 15 · see citing works
Enhancing Understanding of the Visual Cycle by Applying CRISPR/Cas9 Gene Editing in Zebrafish
Ward, R. H. R., Sundaramurthi, H., Giacomo, V. D., & Kennedy, B. N. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00037 · Cited by 13 · see citing works
Identifying Vertebrate Brain Prototypes in Deuterostomes
Kusakabe, T. G. (2017) · Diversity and commonality in animals · doi:10.1007/978-4-431-56469-0_7 · Cited by 10 · see citing works
Self-citationOonuma, K., & Kusakabe, T. G. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.11.011 · Cited by 8 · see citing works
Self-citationEvolution of the vertebrate retina by repurposing of a composite ancestral median eye
Kafetzis, G., Bok, M. J., Baden, T., & Nilsson, D.-E. (2026) · Current Biology · doi:10.1016/j.cub.2025.12.028 · Cited by 7 · see citing works
Getz, T. E., Chrenek, M. A., Papania, J. T., Shelton, D. A., Markand, S., Iuvone, P. M., Kozmík, Z., Boatright, J. H., & Nickerson, J. M. (2024) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.65.6.32 · Cited by 7 · see citing works
Regeneration of 11-cis-Retinal in Visual Systems with Monostable and Bistable Visual Pigments
Saari, J. C. (2014) · Springer eBooks · doi:10.1007/978-4-431-54880-5_3 · Cited by 4 · see citing works
河村, 正. (2017) · JAPANESE ORTHOPTIC JOURNAL · doi:10.4263/jorthoptic.046i001 · Cited by 1 · see citing works
Encoding the Photoreceptors of the Human Eye
Roy, S., & Nagrale, P. (2022) · Cureus · doi:10.7759/cureus.30125 · Cited by 6 · see citing works
A study of the regulatory role of retinoic acid receptor gamma in Zebrafish development
Wai, H. A. (2015) · Aston Publications Explorer (Aston University) · doi:10.48780/publications.aston.ac.uk.00027207 · Cited by 1 · see citing works
Concentrazione plasmatica e produzione extrapineale di melatonina nel tursiope (Tursiops truncatus)
Panin, M. (2012) · Padua Research Archive (University of Padova)
A systemically-delivered stem cell therapy for dry age related macular degeneration
Pay, S. L. (2017) · IUScholarWorks (Indiana University) · doi:10.7912/c2006q
Understanding retinal diseases with genotypic and transcriptomic data analysis
Manda, S. A. P. (2021) · Minerva Access (University of Melbourne)
Teikari, P. (2012) · theses.fr (ABES) · doi:10.70675/96362824z0120z4ed7z94c7zb60f3d7e5f50 · Cited by 2 · see citing works
Li, M., Liang, R., Guo, S., & Zhou, X. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1865865
Huang, J., Ren, C., Qin, Z., Cui, Y., Zhang, B., Luo, P., Wang, X., Xie, Y., Zhang, X., Yan, A., et al. (2026) · Advanced Science · doi:10.1002/advs.202512095
- Authors
- Kusakabe, T. G., Takimoto, N., Jin, M., & Tsuda, M.
- Affiliations
- Konan University (JP)
- University of Hyogo (JP)
- Louisiana State University (US)
- Tokushima Bunri University (JP)
- Corresponding author
- Tsuda, Motoyuki
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2009-10-12
- Volume
- 364
- Issue
- 1531
- Pages
- 2897-2910
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC2781855
- OpenAlex
- W2102212845
- Cited by
- 41
- References
- 126
- Citations by year
- 2026: 3 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 1 · 2018: 3 · 2017: 3 · 2016: 2 · 2015: 3 · 2014: 3 · 2013: 4 · 2012: 3
- FWCI
- 1.34
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology (17018018)
- Japan Society for the Promotion of Science (21570174, 18370089, 16370075, 17018018)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Photoreceptor and optogenetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
- Keywords
- visual cycle, retinoid cycle, 11-cis-retinal regeneration, visual pigment regeneration, opsin evolution, retinochrome, RPE65, interphotoreceptor retinoid-binding protein, photoreceptors, rods and cones, ascidians, vertebrate evolution, subcellular compartmentalization, gene acquisition
- MeSH terms
- Animals, Phylogeny, Retinaldehyde, Vertebrates, Vision, Ocular, Photoreceptor Cells, Invertebrate, Evolution, Molecular, Photoreceptor Cells, Vertebrate
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review