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Neurosensory and neuromuscular organization in tube feet of the sea urchin Strongylocentrotus purpuratus
Several behavioral and electrophysiological studies indicate that all classes of echinoderms, including Echinoidia, the class to which sea urchins belong, are photosensitive and exhibit complex behavioral responses to light or changes in light intensity. However, no discrete photosensitive structure...
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Published in: | Journal of comparative neurology (1911) 2011-12, Vol.519 (17), p.3566-3579 |
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container_title | Journal of comparative neurology (1911) |
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creator | Agca, Cavit Elhajj, Milad C. Klein, William H. Venuti, Judith M. |
description | Several behavioral and electrophysiological studies indicate that all classes of echinoderms, including Echinoidia, the class to which sea urchins belong, are photosensitive and exhibit complex behavioral responses to light or changes in light intensity. However, no discrete photosensitive structure has been identified in sea urchins. The purpose of this study was to provide new insights into eye evolution by determining whether distinct photosensory structures are present in adult sea urchins. Recently, we showed that the Strongylocentrotus purpuratus genome contains orthologs of many mammalian retinal genes and that these genes are expressed in tube feet, suggesting the presence of photoreceptor neurons. To determine whether this is so, we identified several features of tube feet that relate to a possible invertebrate phototransduction system. We show that rhabdomeric opsin is expressed severalfold higher within the disk region of the tube feet and is the most abundant opsin. Immunostaining identified βIII‐tubulin‐expressing cells at the periphery of disk in the vicinity of the synaptotagmin‐expressing nerve fibers. We also showed that Pax6 expression in the disk was restricted to the periphery, where small clusters of putative sensory neurons reside. Our results reveal neuromuscular organization of the tube foot neuromuscular system. They further support earlier studies suggesting the presence of a photosensory system in tube feet. J. Comp. Neurol. 519:3566–3579, 2011. © 2011 Wiley‐Liss, Inc. |
doi_str_mv | 10.1002/cne.22724 |
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However, no discrete photosensitive structure has been identified in sea urchins. The purpose of this study was to provide new insights into eye evolution by determining whether distinct photosensory structures are present in adult sea urchins. Recently, we showed that the Strongylocentrotus purpuratus genome contains orthologs of many mammalian retinal genes and that these genes are expressed in tube feet, suggesting the presence of photoreceptor neurons. To determine whether this is so, we identified several features of tube feet that relate to a possible invertebrate phototransduction system. We show that rhabdomeric opsin is expressed severalfold higher within the disk region of the tube feet and is the most abundant opsin. Immunostaining identified βIII‐tubulin‐expressing cells at the periphery of disk in the vicinity of the synaptotagmin‐expressing nerve fibers. We also showed that Pax6 expression in the disk was restricted to the periphery, where small clusters of putative sensory neurons reside. Our results reveal neuromuscular organization of the tube foot neuromuscular system. They further support earlier studies suggesting the presence of a photosensory system in tube feet. J. Comp. Neurol. 519:3566–3579, 2011. © 2011 Wiley‐Liss, Inc.</description><identifier>ISSN: 0021-9967</identifier><identifier>ISSN: 1096-9861</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.22724</identifier><identifier>PMID: 21800307</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc., A Wiley Company</publisher><subject>Animals ; Echinoidea ; locomotory tube feet ; Marine ; Neuromuscular Junction - cytology ; Neuromuscular Junction - growth & development ; Photoreceptor Cells, Invertebrate - physiology ; photoreceptors ; Sea Urchins ; sensory neurons ; Sensory Receptor Cells - physiology ; Strongylocentrotus purpuratus ; Strongylocentrotus purpuratus - cytology ; Strongylocentrotus purpuratus - growth & development ; synaptotagmin</subject><ispartof>Journal of comparative neurology (1911), 2011-12, Vol.519 (17), p.3566-3579</ispartof><rights>Copyright © 2011 Wiley‐Liss, Inc.</rights><rights>Copyright © 2011 Wiley-Liss, Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4894-85ca6666999e8a62f311fac1b6c5a9e5810d73b4ad139cab639d78377dea97003</citedby><cites>FETCH-LOGICAL-c4894-85ca6666999e8a62f311fac1b6c5a9e5810d73b4ad139cab639d78377dea97003</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21800307$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Agca, Cavit</creatorcontrib><creatorcontrib>Elhajj, Milad C.</creatorcontrib><creatorcontrib>Klein, William H.</creatorcontrib><creatorcontrib>Venuti, Judith M.</creatorcontrib><title>Neurosensory and neuromuscular organization in tube feet of the sea urchin Strongylocentrotus purpuratus</title><title>Journal of comparative neurology (1911)</title><addtitle>J. Comp. Neurol</addtitle><description>Several behavioral and electrophysiological studies indicate that all classes of echinoderms, including Echinoidia, the class to which sea urchins belong, are photosensitive and exhibit complex behavioral responses to light or changes in light intensity. However, no discrete photosensitive structure has been identified in sea urchins. The purpose of this study was to provide new insights into eye evolution by determining whether distinct photosensory structures are present in adult sea urchins. Recently, we showed that the Strongylocentrotus purpuratus genome contains orthologs of many mammalian retinal genes and that these genes are expressed in tube feet, suggesting the presence of photoreceptor neurons. To determine whether this is so, we identified several features of tube feet that relate to a possible invertebrate phototransduction system. We show that rhabdomeric opsin is expressed severalfold higher within the disk region of the tube feet and is the most abundant opsin. Immunostaining identified βIII‐tubulin‐expressing cells at the periphery of disk in the vicinity of the synaptotagmin‐expressing nerve fibers. We also showed that Pax6 expression in the disk was restricted to the periphery, where small clusters of putative sensory neurons reside. Our results reveal neuromuscular organization of the tube foot neuromuscular system. They further support earlier studies suggesting the presence of a photosensory system in tube feet. J. Comp. Neurol. 519:3566–3579, 2011. © 2011 Wiley‐Liss, Inc.</description><subject>Animals</subject><subject>Echinoidea</subject><subject>locomotory tube feet</subject><subject>Marine</subject><subject>Neuromuscular Junction - cytology</subject><subject>Neuromuscular Junction - growth & development</subject><subject>Photoreceptor Cells, Invertebrate - physiology</subject><subject>photoreceptors</subject><subject>Sea Urchins</subject><subject>sensory neurons</subject><subject>Sensory Receptor Cells - physiology</subject><subject>Strongylocentrotus purpuratus</subject><subject>Strongylocentrotus purpuratus - cytology</subject><subject>Strongylocentrotus purpuratus - growth & development</subject><subject>synaptotagmin</subject><issn>0021-9967</issn><issn>1096-9861</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNp9kU1v1DAQhi0EokvhwB9AljgUDmk9cRLbR7rqB6IsUgvq0XKcSTclay92LFh-fb1s2wMSWJY88jzzjscvIa-BHQJj5ZF1eFiWoqyekBkw1RRKNvCUzHIOCqUasUdexHjLGFOKy-dkrwTJGGdiRpYLTMFHdNGHDTWuo257sUrRptEE6sONccNvMw3e0cHRKbVIe8SJ-p5OS6QRDU3BLnPuagre3WxGb9HlcEqRrlPI2-TwJXnWmzHiq_tzn3w7Pfk6Py8uvpx9nH-4KGwlVVXI2pomL6UUStOUPQfojYW2sbVRWEtgneBtZTrgypq24aoTkgvRoVEiD7VPDna66-B_JIyTXg3R4jgahz5FnZtIEHWlMvnuvyQwEKqRvNyib_9Cb30KLs-hoa5qBpAflqn3O8rmH40Be70Ow8qETZbSW6N0Nkr_MSqzb-4VU7vC7pF8cCYDRzvg5zDi5t9Ker44eZAsdhVDnPDXY4UJ33UjuKj19eJMX16ewufjq2v9id8Bmyes2A</recordid><startdate>20111201</startdate><enddate>20111201</enddate><creator>Agca, Cavit</creator><creator>Elhajj, Milad C.</creator><creator>Klein, William H.</creator><creator>Venuti, Judith M.</creator><general>Wiley Subscription Services, Inc., A Wiley Company</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7TN</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>7X8</scope></search><sort><creationdate>20111201</creationdate><title>Neurosensory and neuromuscular organization in tube feet of the sea urchin Strongylocentrotus purpuratus</title><author>Agca, Cavit ; 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subjects | Animals Echinoidea locomotory tube feet Marine Neuromuscular Junction - cytology Neuromuscular Junction - growth & development Photoreceptor Cells, Invertebrate - physiology photoreceptors Sea Urchins sensory neurons Sensory Receptor Cells - physiology Strongylocentrotus purpuratus Strongylocentrotus purpuratus - cytology Strongylocentrotus purpuratus - growth & development synaptotagmin |
title | Neurosensory and neuromuscular organization in tube feet of the sea urchin Strongylocentrotus purpuratus |
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