Distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.

Mammals contain 1 melanopsin (Opn4) gene that is expressed in a subset of retinal ganglion cells to serve as a photopigment involved in non-image-forming vision such as photoentrainment of circadian rhythms. In contrast, most nonmammalian vertebrates possess multiple melanopsins that are distributed...

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Main Authors: Lanfang Sun, Emi Kawano-Yamashita, Takashi Nagata, Hisao Tsukamoto, Yuji Furutani, Mitsumasa Koyanagi, Akihisa Terakita
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4177573?pdf=render
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spelling doaj-56c9b67e66de422c9ebd4c8360beaac32020-11-25T01:46:09ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0199e10820910.1371/journal.pone.0108209Distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.Lanfang SunEmi Kawano-YamashitaTakashi NagataHisao TsukamotoYuji FurutaniMitsumasa KoyanagiAkihisa TerakitaMammals contain 1 melanopsin (Opn4) gene that is expressed in a subset of retinal ganglion cells to serve as a photopigment involved in non-image-forming vision such as photoentrainment of circadian rhythms. In contrast, most nonmammalian vertebrates possess multiple melanopsins that are distributed in various types of retinal cells; however, their functions remain unclear. We previously found that the lamprey has only 1 type of mammalian-like melanopsin gene, which is similar to that observed in mammals. Here we investigated the molecular properties and localization of melanopsin in the lamprey and other cyclostome hagfish retinas, which contribute to visual functions including image-forming vision and mainly to non-image-forming vision, respectively. We isolated 1 type of mammalian-like melanopsin cDNA from the eyes of each species. We showed that the recombinant lamprey melanopsin was a blue light-sensitive pigment and that both the lamprey and hagfish melanopsins caused light-dependent increases in calcium ion concentration in cultured cells in a manner that was similar to that observed for mammalian melanopsins. We observed that melanopsin was distributed in several types of retinal cells, including horizontal cells and ganglion cells, in the lamprey retina, despite the existence of only 1 melanopsin gene in the lamprey. In contrast, melanopsin was almost specifically distributed to retinal ganglion cells in the hagfish retina. Furthermore, we found that the melanopsin-expressing horizontal cells connected to the rhodopsin-containing short photoreceptor cells in the lamprey. Taken together, our findings suggest that in cyclostomes, the global distribution of melanopsin in retinal cells might not be related to the melanopsin gene number but to the extent of retinal contribution to visual function.http://europepmc.org/articles/PMC4177573?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Lanfang Sun
Emi Kawano-Yamashita
Takashi Nagata
Hisao Tsukamoto
Yuji Furutani
Mitsumasa Koyanagi
Akihisa Terakita
spellingShingle Lanfang Sun
Emi Kawano-Yamashita
Takashi Nagata
Hisao Tsukamoto
Yuji Furutani
Mitsumasa Koyanagi
Akihisa Terakita
Distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.
PLoS ONE
author_facet Lanfang Sun
Emi Kawano-Yamashita
Takashi Nagata
Hisao Tsukamoto
Yuji Furutani
Mitsumasa Koyanagi
Akihisa Terakita
author_sort Lanfang Sun
title Distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.
title_short Distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.
title_full Distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.
title_fullStr Distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.
title_full_unstemmed Distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.
title_sort distribution of mammalian-like melanopsin in cyclostome retinas exhibiting a different extent of visual functions.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2014-01-01
description Mammals contain 1 melanopsin (Opn4) gene that is expressed in a subset of retinal ganglion cells to serve as a photopigment involved in non-image-forming vision such as photoentrainment of circadian rhythms. In contrast, most nonmammalian vertebrates possess multiple melanopsins that are distributed in various types of retinal cells; however, their functions remain unclear. We previously found that the lamprey has only 1 type of mammalian-like melanopsin gene, which is similar to that observed in mammals. Here we investigated the molecular properties and localization of melanopsin in the lamprey and other cyclostome hagfish retinas, which contribute to visual functions including image-forming vision and mainly to non-image-forming vision, respectively. We isolated 1 type of mammalian-like melanopsin cDNA from the eyes of each species. We showed that the recombinant lamprey melanopsin was a blue light-sensitive pigment and that both the lamprey and hagfish melanopsins caused light-dependent increases in calcium ion concentration in cultured cells in a manner that was similar to that observed for mammalian melanopsins. We observed that melanopsin was distributed in several types of retinal cells, including horizontal cells and ganglion cells, in the lamprey retina, despite the existence of only 1 melanopsin gene in the lamprey. In contrast, melanopsin was almost specifically distributed to retinal ganglion cells in the hagfish retina. Furthermore, we found that the melanopsin-expressing horizontal cells connected to the rhodopsin-containing short photoreceptor cells in the lamprey. Taken together, our findings suggest that in cyclostomes, the global distribution of melanopsin in retinal cells might not be related to the melanopsin gene number but to the extent of retinal contribution to visual function.
url http://europepmc.org/articles/PMC4177573?pdf=render
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