Nogo‐A does not inhibit retinal axon regeneration in the lizard Gallotia galloti
ABSTRACT The myelin‐associated protein Nogo‐A contributes to the failure of axon regeneration in the mammalian central nervous system (CNS). Inhibition of axon growth by Nogo‐A is mediated by the Nogo‐66 receptor (NgR). Nonmammalian vertebrates, however, are capable of spontaneous CNS axon regenerat...
Gespeichert in:
| Veröffentlicht in: | Journal of comparative neurology (1911) 2017-03, Vol.525 (4), p.936-954 |
|---|---|
| Hauptverfasser: | , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 954 |
|---|---|
| container_issue | 4 |
| container_start_page | 936 |
| container_title | Journal of comparative neurology (1911) |
| container_volume | 525 |
| creator | Lang, Dirk M. Romero‐Alemán, Maria del Mar Dobson, Bryony Santos, Elena Monzón‐Mayor, Maximina |
| description | ABSTRACT
The myelin‐associated protein Nogo‐A contributes to the failure of axon regeneration in the mammalian central nervous system (CNS). Inhibition of axon growth by Nogo‐A is mediated by the Nogo‐66 receptor (NgR). Nonmammalian vertebrates, however, are capable of spontaneous CNS axon regeneration, and we have shown that retinal ganglion cell (RGC) axons regenerate in the lizard Gallotia galloti. Using immunohistochemistry, we observed spatiotemporal regulation of Nogo‐A and NgR in cell bodies and axons of RGCs during ontogeny. In the adult lizard, expression of Nogo‐A was associated with myelinated axon tracts and upregulated in oligodendrocytes during RGC axon regeneration. NgR became upregulated in RGCs following optic nerve injury. In in vitro studies, Nogo‐A‐Fc failed to inhibit growth of lizard RGC axons. The inhibitor of protein kinase A (pkA) activity KT5720 blocked growth of lizard RGC axons on substrates of Nogo‐A‐Fc, but not laminin. On patterned substrates of Nogo‐A‐Fc, KT5720 caused restriction of axon growth to areas devoid of Nogo‐A‐Fc. Levels of cyclic adenosine monophosphate (cAMP) were elevated over sustained periods in lizard RGCs following optic nerve lesion. We conclude that Nogo‐A and NgR are expressed in a mammalian‐like pattern and are upregulated following optic nerve injury, but the presence of Nogo‐A does not inhibit RGC axon regeneration in the lizard visual pathway. The results of outgrowth assays suggest that outgrowth‐promoting substrates and activation of the cAMP/pkA signaling pathway play a key role in spontaneous lizard retinal axon regeneration in the presence of Nogo‐A. Restriction of axon growth by patterned Nogo‐A‐Fc substrates suggests that Nogo‐A may contribute to axon guidance in the lizard visual system. J. Comp. Neurol. 525:936–954, 2017. © 2016 Wiley Periodicals, Inc.
The authors show that the neurite growth inhibitory protein Nogo‐A and its receptor, NgR, are expressed in a mammalian‐like pattern in the lizard visual system, but Nogo‐A does not inhibit lizard retinal axon regeneration. The findings indicate a crucial role for cAMP/pkA signaling in enabling axon regrowth in the lizard. |
| doi_str_mv | 10.1002/cne.24112 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_1859491954</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1835359671</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3862-34d522f06efea9f4088e5c9d97d50afb68ad50119db13117b5829de86d138e073</originalsourceid><addsrcrecordid>eNqNkc9O3DAQh60KVLbbHvoClSUu5RDw2IljH1cr_lRCi1S158iJJ7tG2Xixs6Jw4hF4Rp6kZkM5VELiNL_RfPoO8yPkK7BjYIyfND0e8xyAfyATYFpmWknYI5N0g0xrWR6QTzFeM8a0FuojOeClBCkFm5CfC7_0Tw-PM2o9Rtr7gbp-5Wo30ICD601HzR_fp2WJPQYzuLS4ng4rpJ27N8HSc9N1fnCGLsfwmey3pov45WVOye-z01_zi-zy6vzHfHaZNUJJnoncFpy3TGKLRrc5UwqLRltd2oKZtpbKpACgbQ0CoKwLxbVFJS0IhawUU_J99G6Cv9liHKq1iw12nenRb2MFqtC5Bl3k70BFIYr0KEjo4X_otd-G9IedUOZcgxSJOhqpJvgYA7bVJri1CXcVsOq5kyp1Uu06Sey3F-O2XqN9Jf-VkICTEbh1Hd69barmi9NR-RcIvpR2</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1856429163</pqid></control><display><type>article</type><title>Nogo‐A does not inhibit retinal axon regeneration in the lizard Gallotia galloti</title><source>Wiley Online Library - AutoHoldings Journals</source><source>MEDLINE</source><creator>Lang, Dirk M. ; Romero‐Alemán, Maria del Mar ; Dobson, Bryony ; Santos, Elena ; Monzón‐Mayor, Maximina</creator><creatorcontrib>Lang, Dirk M. ; Romero‐Alemán, Maria del Mar ; Dobson, Bryony ; Santos, Elena ; Monzón‐Mayor, Maximina</creatorcontrib><description>ABSTRACT
The myelin‐associated protein Nogo‐A contributes to the failure of axon regeneration in the mammalian central nervous system (CNS). Inhibition of axon growth by Nogo‐A is mediated by the Nogo‐66 receptor (NgR). Nonmammalian vertebrates, however, are capable of spontaneous CNS axon regeneration, and we have shown that retinal ganglion cell (RGC) axons regenerate in the lizard Gallotia galloti. Using immunohistochemistry, we observed spatiotemporal regulation of Nogo‐A and NgR in cell bodies and axons of RGCs during ontogeny. In the adult lizard, expression of Nogo‐A was associated with myelinated axon tracts and upregulated in oligodendrocytes during RGC axon regeneration. NgR became upregulated in RGCs following optic nerve injury. In in vitro studies, Nogo‐A‐Fc failed to inhibit growth of lizard RGC axons. The inhibitor of protein kinase A (pkA) activity KT5720 blocked growth of lizard RGC axons on substrates of Nogo‐A‐Fc, but not laminin. On patterned substrates of Nogo‐A‐Fc, KT5720 caused restriction of axon growth to areas devoid of Nogo‐A‐Fc. Levels of cyclic adenosine monophosphate (cAMP) were elevated over sustained periods in lizard RGCs following optic nerve lesion. We conclude that Nogo‐A and NgR are expressed in a mammalian‐like pattern and are upregulated following optic nerve injury, but the presence of Nogo‐A does not inhibit RGC axon regeneration in the lizard visual pathway. The results of outgrowth assays suggest that outgrowth‐promoting substrates and activation of the cAMP/pkA signaling pathway play a key role in spontaneous lizard retinal axon regeneration in the presence of Nogo‐A. Restriction of axon growth by patterned Nogo‐A‐Fc substrates suggests that Nogo‐A may contribute to axon guidance in the lizard visual system. J. Comp. Neurol. 525:936–954, 2017. © 2016 Wiley Periodicals, Inc.
The authors show that the neurite growth inhibitory protein Nogo‐A and its receptor, NgR, are expressed in a mammalian‐like pattern in the lizard visual system, but Nogo‐A does not inhibit lizard retinal axon regeneration. The findings indicate a crucial role for cAMP/pkA signaling in enabling axon regrowth in the lizard.</description><identifier>ISSN: 0021-9967</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.24112</identifier><identifier>PMID: 27616630</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>AB_2314901 ; Animals ; axon regeneration ; Axons - physiology ; Blotting, Western ; development ; Gallotia galloti ; Image Processing, Computer-Assisted ; Immunohistochemistry ; Lacertilia ; Lizards ; Nerve Regeneration - physiology ; neurite growth inhibitor ; Nogo Proteins - metabolism ; optic pathway ; reptile ; Retinal Ganglion Cells - physiology ; RRID: AB_10000211 ; RRID: AB_11211656 ; RRID: AB_1620281 ; RRID: AB_257899 ; RRID: AB_2619717 ; RRID: AB_357520 ; RRID: AB_477010 ; RRID: SCR_002078 ; RRID: SCR_002677 ; Time-Lapse Imaging</subject><ispartof>Journal of comparative neurology (1911), 2017-03, Vol.525 (4), p.936-954</ispartof><rights>2016 Wiley Periodicals, Inc.</rights><rights>2017 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3862-34d522f06efea9f4088e5c9d97d50afb68ad50119db13117b5829de86d138e073</citedby><cites>FETCH-LOGICAL-c3862-34d522f06efea9f4088e5c9d97d50afb68ad50119db13117b5829de86d138e073</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fcne.24112$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fcne.24112$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27616630$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lang, Dirk M.</creatorcontrib><creatorcontrib>Romero‐Alemán, Maria del Mar</creatorcontrib><creatorcontrib>Dobson, Bryony</creatorcontrib><creatorcontrib>Santos, Elena</creatorcontrib><creatorcontrib>Monzón‐Mayor, Maximina</creatorcontrib><title>Nogo‐A does not inhibit retinal axon regeneration in the lizard Gallotia galloti</title><title>Journal of comparative neurology (1911)</title><addtitle>J Comp Neurol</addtitle><description>ABSTRACT
The myelin‐associated protein Nogo‐A contributes to the failure of axon regeneration in the mammalian central nervous system (CNS). Inhibition of axon growth by Nogo‐A is mediated by the Nogo‐66 receptor (NgR). Nonmammalian vertebrates, however, are capable of spontaneous CNS axon regeneration, and we have shown that retinal ganglion cell (RGC) axons regenerate in the lizard Gallotia galloti. Using immunohistochemistry, we observed spatiotemporal regulation of Nogo‐A and NgR in cell bodies and axons of RGCs during ontogeny. In the adult lizard, expression of Nogo‐A was associated with myelinated axon tracts and upregulated in oligodendrocytes during RGC axon regeneration. NgR became upregulated in RGCs following optic nerve injury. In in vitro studies, Nogo‐A‐Fc failed to inhibit growth of lizard RGC axons. The inhibitor of protein kinase A (pkA) activity KT5720 blocked growth of lizard RGC axons on substrates of Nogo‐A‐Fc, but not laminin. On patterned substrates of Nogo‐A‐Fc, KT5720 caused restriction of axon growth to areas devoid of Nogo‐A‐Fc. Levels of cyclic adenosine monophosphate (cAMP) were elevated over sustained periods in lizard RGCs following optic nerve lesion. We conclude that Nogo‐A and NgR are expressed in a mammalian‐like pattern and are upregulated following optic nerve injury, but the presence of Nogo‐A does not inhibit RGC axon regeneration in the lizard visual pathway. The results of outgrowth assays suggest that outgrowth‐promoting substrates and activation of the cAMP/pkA signaling pathway play a key role in spontaneous lizard retinal axon regeneration in the presence of Nogo‐A. Restriction of axon growth by patterned Nogo‐A‐Fc substrates suggests that Nogo‐A may contribute to axon guidance in the lizard visual system. J. Comp. Neurol. 525:936–954, 2017. © 2016 Wiley Periodicals, Inc.
The authors show that the neurite growth inhibitory protein Nogo‐A and its receptor, NgR, are expressed in a mammalian‐like pattern in the lizard visual system, but Nogo‐A does not inhibit lizard retinal axon regeneration. The findings indicate a crucial role for cAMP/pkA signaling in enabling axon regrowth in the lizard.</description><subject>AB_2314901</subject><subject>Animals</subject><subject>axon regeneration</subject><subject>Axons - physiology</subject><subject>Blotting, Western</subject><subject>development</subject><subject>Gallotia galloti</subject><subject>Image Processing, Computer-Assisted</subject><subject>Immunohistochemistry</subject><subject>Lacertilia</subject><subject>Lizards</subject><subject>Nerve Regeneration - physiology</subject><subject>neurite growth inhibitor</subject><subject>Nogo Proteins - metabolism</subject><subject>optic pathway</subject><subject>reptile</subject><subject>Retinal Ganglion Cells - physiology</subject><subject>RRID: AB_10000211</subject><subject>RRID: AB_11211656</subject><subject>RRID: AB_1620281</subject><subject>RRID: AB_257899</subject><subject>RRID: AB_2619717</subject><subject>RRID: AB_357520</subject><subject>RRID: AB_477010</subject><subject>RRID: SCR_002078</subject><subject>RRID: SCR_002677</subject><subject>Time-Lapse Imaging</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc9O3DAQh60KVLbbHvoClSUu5RDw2IljH1cr_lRCi1S158iJJ7tG2Xixs6Jw4hF4Rp6kZkM5VELiNL_RfPoO8yPkK7BjYIyfND0e8xyAfyATYFpmWknYI5N0g0xrWR6QTzFeM8a0FuojOeClBCkFm5CfC7_0Tw-PM2o9Rtr7gbp-5Wo30ICD601HzR_fp2WJPQYzuLS4ng4rpJ27N8HSc9N1fnCGLsfwmey3pov45WVOye-z01_zi-zy6vzHfHaZNUJJnoncFpy3TGKLRrc5UwqLRltd2oKZtpbKpACgbQ0CoKwLxbVFJS0IhawUU_J99G6Cv9liHKq1iw12nenRb2MFqtC5Bl3k70BFIYr0KEjo4X_otd-G9IedUOZcgxSJOhqpJvgYA7bVJri1CXcVsOq5kyp1Uu06Sey3F-O2XqN9Jf-VkICTEbh1Hd69barmi9NR-RcIvpR2</recordid><startdate>20170301</startdate><enddate>20170301</enddate><creator>Lang, Dirk M.</creator><creator>Romero‐Alemán, Maria del Mar</creator><creator>Dobson, Bryony</creator><creator>Santos, Elena</creator><creator>Monzón‐Mayor, Maximina</creator><general>Wiley Subscription Services, Inc</general><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>7X8</scope></search><sort><creationdate>20170301</creationdate><title>Nogo‐A does not inhibit retinal axon regeneration in the lizard Gallotia galloti</title><author>Lang, Dirk M. ; Romero‐Alemán, Maria del Mar ; Dobson, Bryony ; Santos, Elena ; Monzón‐Mayor, Maximina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3862-34d522f06efea9f4088e5c9d97d50afb68ad50119db13117b5829de86d138e073</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>AB_2314901</topic><topic>Animals</topic><topic>axon regeneration</topic><topic>Axons - physiology</topic><topic>Blotting, Western</topic><topic>development</topic><topic>Gallotia galloti</topic><topic>Image Processing, Computer-Assisted</topic><topic>Immunohistochemistry</topic><topic>Lacertilia</topic><topic>Lizards</topic><topic>Nerve Regeneration - physiology</topic><topic>neurite growth inhibitor</topic><topic>Nogo Proteins - metabolism</topic><topic>optic pathway</topic><topic>reptile</topic><topic>Retinal Ganglion Cells - physiology</topic><topic>RRID: AB_10000211</topic><topic>RRID: AB_11211656</topic><topic>RRID: AB_1620281</topic><topic>RRID: AB_257899</topic><topic>RRID: AB_2619717</topic><topic>RRID: AB_357520</topic><topic>RRID: AB_477010</topic><topic>RRID: SCR_002078</topic><topic>RRID: SCR_002677</topic><topic>Time-Lapse Imaging</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lang, Dirk M.</creatorcontrib><creatorcontrib>Romero‐Alemán, Maria del Mar</creatorcontrib><creatorcontrib>Dobson, Bryony</creatorcontrib><creatorcontrib>Santos, Elena</creatorcontrib><creatorcontrib>Monzón‐Mayor, Maximina</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</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>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of comparative neurology (1911)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lang, Dirk M.</au><au>Romero‐Alemán, Maria del Mar</au><au>Dobson, Bryony</au><au>Santos, Elena</au><au>Monzón‐Mayor, Maximina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nogo‐A does not inhibit retinal axon regeneration in the lizard Gallotia galloti</atitle><jtitle>Journal of comparative neurology (1911)</jtitle><addtitle>J Comp Neurol</addtitle><date>2017-03-01</date><risdate>2017</risdate><volume>525</volume><issue>4</issue><spage>936</spage><epage>954</epage><pages>936-954</pages><issn>0021-9967</issn><eissn>1096-9861</eissn><abstract>ABSTRACT
The myelin‐associated protein Nogo‐A contributes to the failure of axon regeneration in the mammalian central nervous system (CNS). Inhibition of axon growth by Nogo‐A is mediated by the Nogo‐66 receptor (NgR). Nonmammalian vertebrates, however, are capable of spontaneous CNS axon regeneration, and we have shown that retinal ganglion cell (RGC) axons regenerate in the lizard Gallotia galloti. Using immunohistochemistry, we observed spatiotemporal regulation of Nogo‐A and NgR in cell bodies and axons of RGCs during ontogeny. In the adult lizard, expression of Nogo‐A was associated with myelinated axon tracts and upregulated in oligodendrocytes during RGC axon regeneration. NgR became upregulated in RGCs following optic nerve injury. In in vitro studies, Nogo‐A‐Fc failed to inhibit growth of lizard RGC axons. The inhibitor of protein kinase A (pkA) activity KT5720 blocked growth of lizard RGC axons on substrates of Nogo‐A‐Fc, but not laminin. On patterned substrates of Nogo‐A‐Fc, KT5720 caused restriction of axon growth to areas devoid of Nogo‐A‐Fc. Levels of cyclic adenosine monophosphate (cAMP) were elevated over sustained periods in lizard RGCs following optic nerve lesion. We conclude that Nogo‐A and NgR are expressed in a mammalian‐like pattern and are upregulated following optic nerve injury, but the presence of Nogo‐A does not inhibit RGC axon regeneration in the lizard visual pathway. The results of outgrowth assays suggest that outgrowth‐promoting substrates and activation of the cAMP/pkA signaling pathway play a key role in spontaneous lizard retinal axon regeneration in the presence of Nogo‐A. Restriction of axon growth by patterned Nogo‐A‐Fc substrates suggests that Nogo‐A may contribute to axon guidance in the lizard visual system. J. Comp. Neurol. 525:936–954, 2017. © 2016 Wiley Periodicals, Inc.
The authors show that the neurite growth inhibitory protein Nogo‐A and its receptor, NgR, are expressed in a mammalian‐like pattern in the lizard visual system, but Nogo‐A does not inhibit lizard retinal axon regeneration. The findings indicate a crucial role for cAMP/pkA signaling in enabling axon regrowth in the lizard.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>27616630</pmid><doi>10.1002/cne.24112</doi><tpages>19</tpages></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0021-9967 |
| ispartof | Journal of comparative neurology (1911), 2017-03, Vol.525 (4), p.936-954 |
| issn | 0021-9967 1096-9861 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_1859491954 |
| source | Wiley Online Library - AutoHoldings Journals; MEDLINE |
| subjects | AB_2314901 Animals axon regeneration Axons - physiology Blotting, Western development Gallotia galloti Image Processing, Computer-Assisted Immunohistochemistry Lacertilia Lizards Nerve Regeneration - physiology neurite growth inhibitor Nogo Proteins - metabolism optic pathway reptile Retinal Ganglion Cells - physiology RRID: AB_10000211 RRID: AB_11211656 RRID: AB_1620281 RRID: AB_257899 RRID: AB_2619717 RRID: AB_357520 RRID: AB_477010 RRID: SCR_002078 RRID: SCR_002677 Time-Lapse Imaging |
| title | Nogo‐A does not inhibit retinal axon regeneration in the lizard Gallotia galloti |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-21T04%3A07%3A40IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Nogo%E2%80%90A%20does%20not%20inhibit%20retinal%20axon%20regeneration%20in%20the%20lizard%20Gallotia%20galloti&rft.jtitle=Journal%20of%20comparative%20neurology%20(1911)&rft.au=Lang,%20Dirk%20M.&rft.date=2017-03-01&rft.volume=525&rft.issue=4&rft.spage=936&rft.epage=954&rft.pages=936-954&rft.issn=0021-9967&rft.eissn=1096-9861&rft_id=info:doi/10.1002/cne.24112&rft_dat=%3Cproquest_cross%3E1835359671%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1856429163&rft_id=info:pmid/27616630&rfr_iscdi=true |