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Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors
The outer segment (OS) of the rod photoreceptor is a light-sensing cilium containing ∼1,000 membrane-bound discs. Each day, discs constituting the distal tenth of the OS are shed, whereas nascent discs are formed at the base of the OS through the incorporation of molecules transported from the inner...
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| Published in: | Developmental cell 2015-03, Vol.32 (6), p.731-742 |
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| container_title | Developmental cell |
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| creator | Hsu, Ya-Chu Chuang, Jen-Zen Sung, Ching-Hwa |
| description | The outer segment (OS) of the rod photoreceptor is a light-sensing cilium containing ∼1,000 membrane-bound discs. Each day, discs constituting the distal tenth of the OS are shed, whereas nascent discs are formed at the base of the OS through the incorporation of molecules transported from the inner segment. The mechanisms regulating these processes remain elusive. Here, we show that rhodopsin preferentially enters the OS in the dark. Photoexcitation of post-Golgi rhodopsins retains them in the inner segment. Disc-rim protein peripherin2/rds enters the OS following a rhythm complementary to that of rhodopsin. Light-dark cycle-regulated protein trafficking serves as a mechanism to segregate rhodopsin-rich and peripherin2/rds-rich discs into alternating stacks, which are flanked by characteristic cytoplasmic pockets. This periodic cytostructure divides the OS into approximately ten fractions, each containing discs synthesized in a single day. This mechanism may explain how the rod photoreceptor balances the quantity of discs added and removed daily.
•Light regulates the rod OS entry of rhodopsin•PRPH2 enters the OS following a rhythm complementary to that of rhodopsin•Rod OS discs formed during the day and night have distinct composition and morphology•Cyclic light governs the periodicity of the OS disc arrangement and cytostructure
The light-sensing cilium (outer segment) of each rod photoreceptor contains ∼1,000 discs that undergo constant renewal. Hsu et al. show that that light, beyond its recognized role in triggering phototransduction, also regulates the ciliary entry of rhodopsin, the morphology of the discs, and their arrangement within the outer segment. |
| doi_str_mv | 10.1016/j.devcel.2015.01.027 |
| format | article |
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•Light regulates the rod OS entry of rhodopsin•PRPH2 enters the OS following a rhythm complementary to that of rhodopsin•Rod OS discs formed during the day and night have distinct composition and morphology•Cyclic light governs the periodicity of the OS disc arrangement and cytostructure
The light-sensing cilium (outer segment) of each rod photoreceptor contains ∼1,000 discs that undergo constant renewal. Hsu et al. show that that light, beyond its recognized role in triggering phototransduction, also regulates the ciliary entry of rhodopsin, the morphology of the discs, and their arrangement within the outer segment.</description><identifier>ISSN: 1534-5807</identifier><identifier>EISSN: 1878-1551</identifier><identifier>DOI: 10.1016/j.devcel.2015.01.027</identifier><identifier>PMID: 25805137</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Cilia ; Light ; Mice ; Mice, Inbred C57BL ; Peripherins ; Protein Transport - physiology ; Rats ; Rats, Sprague-Dawley ; Retinal Photoreceptor Cell Inner Segment - physiology ; Retinal Rod Photoreceptor Cells - metabolism ; Rhodopsin - biosynthesis ; Rhodopsin - metabolism ; Rod Cell Outer Segment - physiology</subject><ispartof>Developmental cell, 2015-03, Vol.32 (6), p.731-742</ispartof><rights>2015 Elsevier Inc.</rights><rights>Copyright © 2015 Elsevier Inc. All rights reserved.</rights><rights>2015 Elsevier Inc. All rights reserved. 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c463t-80a9babb17543fd430600833952e9a98702369bb1350ceaf8b09b3a623f6d1bd3</citedby><cites>FETCH-LOGICAL-c463t-80a9babb17543fd430600833952e9a98702369bb1350ceaf8b09b3a623f6d1bd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25805137$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hsu, Ya-Chu</creatorcontrib><creatorcontrib>Chuang, Jen-Zen</creatorcontrib><creatorcontrib>Sung, Ching-Hwa</creatorcontrib><title>Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors</title><title>Developmental cell</title><addtitle>Dev Cell</addtitle><description>The outer segment (OS) of the rod photoreceptor is a light-sensing cilium containing ∼1,000 membrane-bound discs. Each day, discs constituting the distal tenth of the OS are shed, whereas nascent discs are formed at the base of the OS through the incorporation of molecules transported from the inner segment. The mechanisms regulating these processes remain elusive. Here, we show that rhodopsin preferentially enters the OS in the dark. Photoexcitation of post-Golgi rhodopsins retains them in the inner segment. Disc-rim protein peripherin2/rds enters the OS following a rhythm complementary to that of rhodopsin. Light-dark cycle-regulated protein trafficking serves as a mechanism to segregate rhodopsin-rich and peripherin2/rds-rich discs into alternating stacks, which are flanked by characteristic cytoplasmic pockets. This periodic cytostructure divides the OS into approximately ten fractions, each containing discs synthesized in a single day. This mechanism may explain how the rod photoreceptor balances the quantity of discs added and removed daily.
•Light regulates the rod OS entry of rhodopsin•PRPH2 enters the OS following a rhythm complementary to that of rhodopsin•Rod OS discs formed during the day and night have distinct composition and morphology•Cyclic light governs the periodicity of the OS disc arrangement and cytostructure
The light-sensing cilium (outer segment) of each rod photoreceptor contains ∼1,000 discs that undergo constant renewal. Hsu et al. show that that light, beyond its recognized role in triggering phototransduction, also regulates the ciliary entry of rhodopsin, the morphology of the discs, and their arrangement within the outer segment.</description><subject>Animals</subject><subject>Cilia</subject><subject>Light</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Peripherins</subject><subject>Protein Transport - physiology</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Retinal Photoreceptor Cell Inner Segment - physiology</subject><subject>Retinal Rod Photoreceptor Cells - metabolism</subject><subject>Rhodopsin - biosynthesis</subject><subject>Rhodopsin - metabolism</subject><subject>Rod Cell Outer Segment - physiology</subject><issn>1534-5807</issn><issn>1878-1551</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNp9UcFu1DAQtRCIlpY_QMhHLkntOHacC1K1QKm0qBUtZ8txJhuvEntrO4v693W1pYULpxnNzHszbx5CHygpKaHibFv2sDcwlRWhvCS0JFXzCh1T2ciCck5f55yzuuCSNEfoXYxbkmFUkrfoqMpFTllzjMa13YwJ_4TNMukEEacR8MpOVod7fB18AuvwbdAu7nxIWLseXy0JAr6BzQwu4S82mgx38FtP2A_4h55nneEOX48--QAGdjnEU_Rm0FOE90_xBP369vV29b1YX11crs7XhakFS4Ukuu1019GG12zoa0YEIZKxllfQ6lY2pGKizX3GiQE9yI60HdOiYoPoadezE_T5wLtbuhl6k28MelK7YOcsSXlt1b8dZ0e18XtVs6amFcsEn54Igr9bICY1Z4kwTdqBX6KiQohWClq3ebQ-jJrgYwwwPK-hRD2apLbqYJJ6NEkRqrJJGfbx7xOfQX9cedEA-VF7C0FFY8EZ6G3-Z1K9t__f8AAaEqa1</recordid><startdate>20150323</startdate><enddate>20150323</enddate><creator>Hsu, Ya-Chu</creator><creator>Chuang, Jen-Zen</creator><creator>Sung, Ching-Hwa</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20150323</creationdate><title>Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors</title><author>Hsu, Ya-Chu ; Chuang, Jen-Zen ; Sung, Ching-Hwa</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-80a9babb17543fd430600833952e9a98702369bb1350ceaf8b09b3a623f6d1bd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Cilia</topic><topic>Light</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Peripherins</topic><topic>Protein Transport - physiology</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Retinal Photoreceptor Cell Inner Segment - physiology</topic><topic>Retinal Rod Photoreceptor Cells - metabolism</topic><topic>Rhodopsin - biosynthesis</topic><topic>Rhodopsin - metabolism</topic><topic>Rod Cell Outer Segment - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hsu, Ya-Chu</creatorcontrib><creatorcontrib>Chuang, Jen-Zen</creatorcontrib><creatorcontrib>Sung, Ching-Hwa</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hsu, Ya-Chu</au><au>Chuang, Jen-Zen</au><au>Sung, Ching-Hwa</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors</atitle><jtitle>Developmental cell</jtitle><addtitle>Dev Cell</addtitle><date>2015-03-23</date><risdate>2015</risdate><volume>32</volume><issue>6</issue><spage>731</spage><epage>742</epage><pages>731-742</pages><issn>1534-5807</issn><eissn>1878-1551</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Equal contribution</notes><abstract>The outer segment (OS) of the rod photoreceptor is a light-sensing cilium containing ∼1,000 membrane-bound discs. Each day, discs constituting the distal tenth of the OS are shed, whereas nascent discs are formed at the base of the OS through the incorporation of molecules transported from the inner segment. The mechanisms regulating these processes remain elusive. Here, we show that rhodopsin preferentially enters the OS in the dark. Photoexcitation of post-Golgi rhodopsins retains them in the inner segment. Disc-rim protein peripherin2/rds enters the OS following a rhythm complementary to that of rhodopsin. Light-dark cycle-regulated protein trafficking serves as a mechanism to segregate rhodopsin-rich and peripherin2/rds-rich discs into alternating stacks, which are flanked by characteristic cytoplasmic pockets. This periodic cytostructure divides the OS into approximately ten fractions, each containing discs synthesized in a single day. This mechanism may explain how the rod photoreceptor balances the quantity of discs added and removed daily.
•Light regulates the rod OS entry of rhodopsin•PRPH2 enters the OS following a rhythm complementary to that of rhodopsin•Rod OS discs formed during the day and night have distinct composition and morphology•Cyclic light governs the periodicity of the OS disc arrangement and cytostructure
The light-sensing cilium (outer segment) of each rod photoreceptor contains ∼1,000 discs that undergo constant renewal. Hsu et al. show that that light, beyond its recognized role in triggering phototransduction, also regulates the ciliary entry of rhodopsin, the morphology of the discs, and their arrangement within the outer segment.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25805137</pmid><doi>10.1016/j.devcel.2015.01.027</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Cilia Light Mice Mice, Inbred C57BL Peripherins Protein Transport - physiology Rats Rats, Sprague-Dawley Retinal Photoreceptor Cell Inner Segment - physiology Retinal Rod Photoreceptor Cells - metabolism Rhodopsin - biosynthesis Rhodopsin - metabolism Rod Cell Outer Segment - physiology |
| title | Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors |
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