Proprioceptive Opsin Functions in Drosophila Larval Locomotion
Animals rely on mechanosensory feedback from proprioceptors to control locomotory body movements. Unexpectedly, we found that this movement control requires visual opsins. Disrupting the Drosophila opsins NINAE or Rh6 impaired larval locomotion and body contractions, independently of light and visio...
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| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2018-04, Vol.98 (1), p.67-74.e4 |
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| container_title | Neuron (Cambridge, Mass.) |
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| creator | Zanini, Damiano Giraldo, Diego Warren, Ben Katana, Radoslaw Andrés, Marta Reddy, Suneel Pauls, Stephanie Schwedhelm-Domeyer, Nicola Geurten, Bart R.H. Göpfert, Martin C. |
| description | Animals rely on mechanosensory feedback from proprioceptors to control locomotory body movements. Unexpectedly, we found that this movement control requires visual opsins. Disrupting the Drosophila opsins NINAE or Rh6 impaired larval locomotion and body contractions, independently of light and vision. Opsins were detected in chordotonal proprioceptors along the larval body, localizing to their ciliated dendrites. Loss of opsins impaired mechanically evoked proprioceptor spiking and cilium ultrastructure. Without NINAE or Rh6, NOMPC mechanotransduction channels leaked from proprioceptor cilia and ciliary Inactive (Iav) channels partly disappeared. Locomotion is shown to require opsins in proprioceptors, and the receptors are found to express the opsin gene Rh7, in addition to ninaE and Rh6. Besides implicating opsins in movement control, this documents roles of non-ciliary, rhabdomeric opsins in cilium organization, providing a model for a key transition in opsin evolution and suggesting that structural roles of rhabdomeric opsins preceded their use for light detection.
•Drosophila larval locomotion requires the visual opsins NINAE and Rh6•NINAE and Rh6 occur in ciliated proprioceptor dendrites along the larval body•Loss of NINAE or Rh6 impairs proprioceptor function and TRP channel localization•NINAE and Rh6, though rhabdomeric, contribute to cilium integrity
Zanini et al. report that locomotion in Drosophila larvae requires rhabdomeric visual opsins in ciliated proprioceptors where they contribute to mechanosensation and cilium organization. |
| doi_str_mv | 10.1016/j.neuron.2018.02.028 |
| format | Article |
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•Drosophila larval locomotion requires the visual opsins NINAE and Rh6•NINAE and Rh6 occur in ciliated proprioceptor dendrites along the larval body•Loss of NINAE or Rh6 impairs proprioceptor function and TRP channel localization•NINAE and Rh6, though rhabdomeric, contribute to cilium integrity
Zanini et al. report that locomotion in Drosophila larvae requires rhabdomeric visual opsins in ciliated proprioceptors where they contribute to mechanosensation and cilium organization.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2018.02.028</identifier><identifier>PMID: 29551493</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; chordotonal organ ; Cilia ; cilium maintenance ; Defects ; Dendrites ; Drosophila ; Inactive (Iav) channel ; Insects ; Locomotion ; mechanosensory transduction ; Mechanotransduction ; Microscopy ; movement control ; Nanchung (Nan) ; Nervous system ; NOMPC ; Opsins ; Proprioception ; Proprioceptors ; Proteins ; rhabdomeric opsin evolution ; sensory dendrite organization ; TRP cation channel ; Ultrastructure</subject><ispartof>Neuron (Cambridge, Mass.), 2018-04, Vol.98 (1), p.67-74.e4</ispartof><rights>2018 Elsevier Inc.</rights><rights>Copyright © 2018 Elsevier Inc. All rights reserved.</rights><rights>2018. Elsevier Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c436t-f66f57d3cfa09a0125cf3ba389baef83b965253e4ba32ed3d197d9401c3cd01e3</citedby><cites>FETCH-LOGICAL-c436t-f66f57d3cfa09a0125cf3ba389baef83b965253e4ba32ed3d197d9401c3cd01e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuron.2018.02.028$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29551493$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zanini, Damiano</creatorcontrib><creatorcontrib>Giraldo, Diego</creatorcontrib><creatorcontrib>Warren, Ben</creatorcontrib><creatorcontrib>Katana, Radoslaw</creatorcontrib><creatorcontrib>Andrés, Marta</creatorcontrib><creatorcontrib>Reddy, Suneel</creatorcontrib><creatorcontrib>Pauls, Stephanie</creatorcontrib><creatorcontrib>Schwedhelm-Domeyer, Nicola</creatorcontrib><creatorcontrib>Geurten, Bart R.H.</creatorcontrib><creatorcontrib>Göpfert, Martin C.</creatorcontrib><title>Proprioceptive Opsin Functions in Drosophila Larval Locomotion</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Animals rely on mechanosensory feedback from proprioceptors to control locomotory body movements. Unexpectedly, we found that this movement control requires visual opsins. Disrupting the Drosophila opsins NINAE or Rh6 impaired larval locomotion and body contractions, independently of light and vision. Opsins were detected in chordotonal proprioceptors along the larval body, localizing to their ciliated dendrites. Loss of opsins impaired mechanically evoked proprioceptor spiking and cilium ultrastructure. Without NINAE or Rh6, NOMPC mechanotransduction channels leaked from proprioceptor cilia and ciliary Inactive (Iav) channels partly disappeared. Locomotion is shown to require opsins in proprioceptors, and the receptors are found to express the opsin gene Rh7, in addition to ninaE and Rh6. Besides implicating opsins in movement control, this documents roles of non-ciliary, rhabdomeric opsins in cilium organization, providing a model for a key transition in opsin evolution and suggesting that structural roles of rhabdomeric opsins preceded their use for light detection.
•Drosophila larval locomotion requires the visual opsins NINAE and Rh6•NINAE and Rh6 occur in ciliated proprioceptor dendrites along the larval body•Loss of NINAE or Rh6 impairs proprioceptor function and TRP channel localization•NINAE and Rh6, though rhabdomeric, contribute to cilium integrity
Zanini et al. report that locomotion in Drosophila larvae requires rhabdomeric visual opsins in ciliated proprioceptors where they contribute to mechanosensation and cilium organization.</description><subject>Animals</subject><subject>chordotonal organ</subject><subject>Cilia</subject><subject>cilium maintenance</subject><subject>Defects</subject><subject>Dendrites</subject><subject>Drosophila</subject><subject>Inactive (Iav) channel</subject><subject>Insects</subject><subject>Locomotion</subject><subject>mechanosensory transduction</subject><subject>Mechanotransduction</subject><subject>Microscopy</subject><subject>movement control</subject><subject>Nanchung (Nan)</subject><subject>Nervous system</subject><subject>NOMPC</subject><subject>Opsins</subject><subject>Proprioception</subject><subject>Proprioceptors</subject><subject>Proteins</subject><subject>rhabdomeric opsin evolution</subject><subject>sensory dendrite organization</subject><subject>TRP cation channel</subject><subject>Ultrastructure</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp9kE1LJDEQhoO46Dj6D0QavHjp2VS-unMRRFddGJg9rOeQSVdjhp5Om3QP-O83w7gePAgFIcVTb1IPIZdAF0BB_dwsepxi6BeMQr2gLFd9RGZAdVUK0PqYzGitValYxU_JWUobSkFIDSfklGkpQWg-I7d_YhiiDw6H0e-wWA3J98Xj1LvRhz4V-fIQQwrDq-9ssbRxZ7tiGVzYhj1wTn60tkt48XHOycvjr7_3z-Vy9fT7_m5ZOsHVWLZKtbJquGst1ZYCk67la8trvbbY1nytlWSSo8g9hg1vQFeNFhQcdw0F5HNyc8gdYnibMI1m65PDrrM9himZ7EAKqECLjF5_QTdhin3-XaYYKM2kqjMlDpTL26WIrckWtja-G6Bm79dszMHvPrs2lOXaj119hE_rLTafQ_-FZuD2AGC2sfMYTXIee4eNj-hG0wT__Qv_ANJMjZA</recordid><startdate>20180404</startdate><enddate>20180404</enddate><creator>Zanini, Damiano</creator><creator>Giraldo, Diego</creator><creator>Warren, Ben</creator><creator>Katana, Radoslaw</creator><creator>Andrés, Marta</creator><creator>Reddy, Suneel</creator><creator>Pauls, Stephanie</creator><creator>Schwedhelm-Domeyer, Nicola</creator><creator>Geurten, Bart R.H.</creator><creator>Göpfert, Martin C.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20180404</creationdate><title>Proprioceptive Opsin Functions in Drosophila Larval Locomotion</title><author>Zanini, Damiano ; Giraldo, Diego ; Warren, Ben ; Katana, Radoslaw ; Andrés, Marta ; Reddy, Suneel ; Pauls, Stephanie ; Schwedhelm-Domeyer, Nicola ; Geurten, Bart R.H. ; Göpfert, Martin C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c436t-f66f57d3cfa09a0125cf3ba389baef83b965253e4ba32ed3d197d9401c3cd01e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>chordotonal organ</topic><topic>Cilia</topic><topic>cilium maintenance</topic><topic>Defects</topic><topic>Dendrites</topic><topic>Drosophila</topic><topic>Inactive (Iav) channel</topic><topic>Insects</topic><topic>Locomotion</topic><topic>mechanosensory transduction</topic><topic>Mechanotransduction</topic><topic>Microscopy</topic><topic>movement control</topic><topic>Nanchung (Nan)</topic><topic>Nervous system</topic><topic>NOMPC</topic><topic>Opsins</topic><topic>Proprioception</topic><topic>Proprioceptors</topic><topic>Proteins</topic><topic>rhabdomeric opsin evolution</topic><topic>sensory dendrite organization</topic><topic>TRP cation channel</topic><topic>Ultrastructure</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zanini, Damiano</creatorcontrib><creatorcontrib>Giraldo, Diego</creatorcontrib><creatorcontrib>Warren, Ben</creatorcontrib><creatorcontrib>Katana, Radoslaw</creatorcontrib><creatorcontrib>Andrés, Marta</creatorcontrib><creatorcontrib>Reddy, Suneel</creatorcontrib><creatorcontrib>Pauls, Stephanie</creatorcontrib><creatorcontrib>Schwedhelm-Domeyer, Nicola</creatorcontrib><creatorcontrib>Geurten, Bart R.H.</creatorcontrib><creatorcontrib>Göpfert, Martin C.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zanini, Damiano</au><au>Giraldo, Diego</au><au>Warren, Ben</au><au>Katana, Radoslaw</au><au>Andrés, Marta</au><au>Reddy, Suneel</au><au>Pauls, Stephanie</au><au>Schwedhelm-Domeyer, Nicola</au><au>Geurten, Bart R.H.</au><au>Göpfert, Martin C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Proprioceptive Opsin Functions in Drosophila Larval Locomotion</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2018-04-04</date><risdate>2018</risdate><volume>98</volume><issue>1</issue><spage>67</spage><epage>74.e4</epage><pages>67-74.e4</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>Animals rely on mechanosensory feedback from proprioceptors to control locomotory body movements. Unexpectedly, we found that this movement control requires visual opsins. Disrupting the Drosophila opsins NINAE or Rh6 impaired larval locomotion and body contractions, independently of light and vision. Opsins were detected in chordotonal proprioceptors along the larval body, localizing to their ciliated dendrites. Loss of opsins impaired mechanically evoked proprioceptor spiking and cilium ultrastructure. Without NINAE or Rh6, NOMPC mechanotransduction channels leaked from proprioceptor cilia and ciliary Inactive (Iav) channels partly disappeared. Locomotion is shown to require opsins in proprioceptors, and the receptors are found to express the opsin gene Rh7, in addition to ninaE and Rh6. Besides implicating opsins in movement control, this documents roles of non-ciliary, rhabdomeric opsins in cilium organization, providing a model for a key transition in opsin evolution and suggesting that structural roles of rhabdomeric opsins preceded their use for light detection.
•Drosophila larval locomotion requires the visual opsins NINAE and Rh6•NINAE and Rh6 occur in ciliated proprioceptor dendrites along the larval body•Loss of NINAE or Rh6 impairs proprioceptor function and TRP channel localization•NINAE and Rh6, though rhabdomeric, contribute to cilium integrity
Zanini et al. report that locomotion in Drosophila larvae requires rhabdomeric visual opsins in ciliated proprioceptors where they contribute to mechanosensation and cilium organization.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>29551493</pmid><doi>10.1016/j.neuron.2018.02.028</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals chordotonal organ Cilia cilium maintenance Defects Dendrites Drosophila Inactive (Iav) channel Insects Locomotion mechanosensory transduction Mechanotransduction Microscopy movement control Nanchung (Nan) Nervous system NOMPC Opsins Proprioception Proprioceptors Proteins rhabdomeric opsin evolution sensory dendrite organization TRP cation channel Ultrastructure |
| title | Proprioceptive Opsin Functions in Drosophila Larval Locomotion |
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