Critical role of CRAG, a splicing variant of centaurin-γ3/AGAP3, in ELK1-dependent SRF activation at PML bodies
CRMP-5-associated GTPase (CRAG), a short splicing variant of centaurin-γ3/AGAP3, is predominantly expressed in the developing brain. We previously demonstrated that CRAG, but not centaurin-γ3, translocates to the nucleus and activates the serum response factor (SRF)-c-Fos pathway in cultured neurona...
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| Veröffentlicht in: | Scientific reports 2019-12, Vol.9 (1), p.20107-10, Article 20107 |
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| creator | Nagashima, Shun Takeda, Keisuke Shiiba, Isshin Higashi, Mizuho Fukuda, Toshifumi Tokuyama, Takeshi Matsushita, Nobuko Nagano, Seiichi Araki, Toshiyuki Kaneko, Mari Shioi, Go Inatome, Ryoko Yanagi, Shigeru |
| description | CRMP-5-associated GTPase (CRAG), a short splicing variant of centaurin-γ3/AGAP3, is predominantly expressed in the developing brain. We previously demonstrated that CRAG, but not centaurin-γ3, translocates to the nucleus and activates the serum response factor (SRF)-c-Fos pathway in cultured neuronal cells. However, the physiological relevance of CRAG
in vivo
is unknown. Here, we found that CRAG/centaurin-γ3–knockout mice showed intensively suppressed kainic acid-induced c-fos expression in the hippocampus. Analyses of molecular mechanisms underlying CRAG-mediated SRF activation revealed that CRAG has an essential role in GTPase activity, interacts with ELK1 (a co-activator of SRF), and activates SRF in an ELK1-dependent manner. Furthermore, CRAG and ELK1 interact with promyelocytic leukaemia bodies through SUMO-interacting motifs, which is required for SRF activation. These results suggest that CRAG plays a critical role in ELK1-dependent SRF-c-fos activation at promyelocytic leukaemia bodies in the developing brain. |
| doi_str_mv | 10.1038/s41598-019-56559-9 |
| format | Article |
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in vivo
is unknown. Here, we found that CRAG/centaurin-γ3–knockout mice showed intensively suppressed kainic acid-induced c-fos expression in the hippocampus. Analyses of molecular mechanisms underlying CRAG-mediated SRF activation revealed that CRAG has an essential role in GTPase activity, interacts with ELK1 (a co-activator of SRF), and activates SRF in an ELK1-dependent manner. Furthermore, CRAG and ELK1 interact with promyelocytic leukaemia bodies through SUMO-interacting motifs, which is required for SRF activation. These results suggest that CRAG plays a critical role in ELK1-dependent SRF-c-fos activation at promyelocytic leukaemia bodies in the developing brain.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-019-56559-9</identifier><identifier>PMID: 31882856</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/1 ; 13/109 ; 13/44 ; 13/51 ; 14/19 ; 14/35 ; 14/63 ; 38/70 ; 631/378/1934 ; 631/80/83 ; 64/60 ; Alternative Splicing ; Animals ; c-Fos protein ; ets-Domain Protein Elk-1 - genetics ; GTP-Binding Proteins - genetics ; GTPase-Activating Proteins - genetics ; Guanosine triphosphatases ; Hippocampus - metabolism ; Humanities and Social Sciences ; Kainic acid ; Kainic Acid - pharmacology ; Leukemia ; Mice ; Mice, Knockout ; Molecular modelling ; multidisciplinary ; Neurons - metabolism ; Promyelocytic Leukemia Protein - metabolism ; Proto-Oncogene Proteins c-fos - genetics ; Proto-Oncogene Proteins c-fos - metabolism ; Science ; Science (multidisciplinary) ; Serum response factor ; Serum Response Factor - metabolism ; Splicing ; Sumoylation</subject><ispartof>Scientific reports, 2019-12, Vol.9 (1), p.20107-10, Article 20107</ispartof><rights>The Author(s) 2019</rights><rights>2019. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c540t-e6fc91504f8d683a48edd880343c30d71625c2ec514e72f92efab53cf4a3db2e3</citedby><cites>FETCH-LOGICAL-c540t-e6fc91504f8d683a48edd880343c30d71625c2ec514e72f92efab53cf4a3db2e3</cites><orcidid>0000-0003-3625-2042 ; 0000-0002-1392-8663</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6934726/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6934726/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,41096,42165,51551,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31882856$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nagashima, Shun</creatorcontrib><creatorcontrib>Takeda, Keisuke</creatorcontrib><creatorcontrib>Shiiba, Isshin</creatorcontrib><creatorcontrib>Higashi, Mizuho</creatorcontrib><creatorcontrib>Fukuda, Toshifumi</creatorcontrib><creatorcontrib>Tokuyama, Takeshi</creatorcontrib><creatorcontrib>Matsushita, Nobuko</creatorcontrib><creatorcontrib>Nagano, Seiichi</creatorcontrib><creatorcontrib>Araki, Toshiyuki</creatorcontrib><creatorcontrib>Kaneko, Mari</creatorcontrib><creatorcontrib>Shioi, Go</creatorcontrib><creatorcontrib>Inatome, Ryoko</creatorcontrib><creatorcontrib>Yanagi, Shigeru</creatorcontrib><title>Critical role of CRAG, a splicing variant of centaurin-γ3/AGAP3, in ELK1-dependent SRF activation at PML bodies</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>CRMP-5-associated GTPase (CRAG), a short splicing variant of centaurin-γ3/AGAP3, is predominantly expressed in the developing brain. We previously demonstrated that CRAG, but not centaurin-γ3, translocates to the nucleus and activates the serum response factor (SRF)-c-Fos pathway in cultured neuronal cells. However, the physiological relevance of CRAG
in vivo
is unknown. Here, we found that CRAG/centaurin-γ3–knockout mice showed intensively suppressed kainic acid-induced c-fos expression in the hippocampus. Analyses of molecular mechanisms underlying CRAG-mediated SRF activation revealed that CRAG has an essential role in GTPase activity, interacts with ELK1 (a co-activator of SRF), and activates SRF in an ELK1-dependent manner. Furthermore, CRAG and ELK1 interact with promyelocytic leukaemia bodies through SUMO-interacting motifs, which is required for SRF activation. These results suggest that CRAG plays a critical role in ELK1-dependent SRF-c-fos activation at promyelocytic leukaemia bodies in the developing brain.</description><subject>13/1</subject><subject>13/109</subject><subject>13/44</subject><subject>13/51</subject><subject>14/19</subject><subject>14/35</subject><subject>14/63</subject><subject>38/70</subject><subject>631/378/1934</subject><subject>631/80/83</subject><subject>64/60</subject><subject>Alternative Splicing</subject><subject>Animals</subject><subject>c-Fos protein</subject><subject>ets-Domain Protein Elk-1 - genetics</subject><subject>GTP-Binding Proteins - genetics</subject><subject>GTPase-Activating Proteins - genetics</subject><subject>Guanosine triphosphatases</subject><subject>Hippocampus - metabolism</subject><subject>Humanities and Social Sciences</subject><subject>Kainic acid</subject><subject>Kainic Acid - pharmacology</subject><subject>Leukemia</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Molecular modelling</subject><subject>multidisciplinary</subject><subject>Neurons - 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genetics</topic><topic>GTP-Binding Proteins - genetics</topic><topic>GTPase-Activating Proteins - genetics</topic><topic>Guanosine triphosphatases</topic><topic>Hippocampus - metabolism</topic><topic>Humanities and Social Sciences</topic><topic>Kainic acid</topic><topic>Kainic Acid - pharmacology</topic><topic>Leukemia</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Molecular modelling</topic><topic>multidisciplinary</topic><topic>Neurons - metabolism</topic><topic>Promyelocytic Leukemia Protein - metabolism</topic><topic>Proto-Oncogene Proteins c-fos - genetics</topic><topic>Proto-Oncogene Proteins c-fos - metabolism</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Serum response factor</topic><topic>Serum Response Factor - metabolism</topic><topic>Splicing</topic><topic>Sumoylation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nagashima, Shun</creatorcontrib><creatorcontrib>Takeda, Keisuke</creatorcontrib><creatorcontrib>Shiiba, Isshin</creatorcontrib><creatorcontrib>Higashi, Mizuho</creatorcontrib><creatorcontrib>Fukuda, Toshifumi</creatorcontrib><creatorcontrib>Tokuyama, Takeshi</creatorcontrib><creatorcontrib>Matsushita, Nobuko</creatorcontrib><creatorcontrib>Nagano, Seiichi</creatorcontrib><creatorcontrib>Araki, Toshiyuki</creatorcontrib><creatorcontrib>Kaneko, Mari</creatorcontrib><creatorcontrib>Shioi, Go</creatorcontrib><creatorcontrib>Inatome, Ryoko</creatorcontrib><creatorcontrib>Yanagi, Shigeru</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nagashima, Shun</au><au>Takeda, Keisuke</au><au>Shiiba, Isshin</au><au>Higashi, Mizuho</au><au>Fukuda, Toshifumi</au><au>Tokuyama, Takeshi</au><au>Matsushita, Nobuko</au><au>Nagano, Seiichi</au><au>Araki, Toshiyuki</au><au>Kaneko, Mari</au><au>Shioi, Go</au><au>Inatome, Ryoko</au><au>Yanagi, Shigeru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Critical role of CRAG, a splicing variant of centaurin-γ3/AGAP3, in ELK1-dependent SRF activation at PML bodies</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2019-12-27</date><risdate>2019</risdate><volume>9</volume><issue>1</issue><spage>20107</spage><epage>10</epage><pages>20107-10</pages><artnum>20107</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>CRMP-5-associated GTPase (CRAG), a short splicing variant of centaurin-γ3/AGAP3, is predominantly expressed in the developing brain. We previously demonstrated that CRAG, but not centaurin-γ3, translocates to the nucleus and activates the serum response factor (SRF)-c-Fos pathway in cultured neuronal cells. However, the physiological relevance of CRAG
in vivo
is unknown. Here, we found that CRAG/centaurin-γ3–knockout mice showed intensively suppressed kainic acid-induced c-fos expression in the hippocampus. Analyses of molecular mechanisms underlying CRAG-mediated SRF activation revealed that CRAG has an essential role in GTPase activity, interacts with ELK1 (a co-activator of SRF), and activates SRF in an ELK1-dependent manner. Furthermore, CRAG and ELK1 interact with promyelocytic leukaemia bodies through SUMO-interacting motifs, which is required for SRF activation. These results suggest that CRAG plays a critical role in ELK1-dependent SRF-c-fos activation at promyelocytic leukaemia bodies in the developing brain.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31882856</pmid><doi>10.1038/s41598-019-56559-9</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0003-3625-2042</orcidid><orcidid>https://orcid.org/0000-0002-1392-8663</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Nature Free; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry; Springer Nature OA Free Journals |
| subjects | 13/1 13/109 13/44 13/51 14/19 14/35 14/63 38/70 631/378/1934 631/80/83 64/60 Alternative Splicing Animals c-Fos protein ets-Domain Protein Elk-1 - genetics GTP-Binding Proteins - genetics GTPase-Activating Proteins - genetics Guanosine triphosphatases Hippocampus - metabolism Humanities and Social Sciences Kainic acid Kainic Acid - pharmacology Leukemia Mice Mice, Knockout Molecular modelling multidisciplinary Neurons - metabolism Promyelocytic Leukemia Protein - metabolism Proto-Oncogene Proteins c-fos - genetics Proto-Oncogene Proteins c-fos - metabolism Science Science (multidisciplinary) Serum response factor Serum Response Factor - metabolism Splicing Sumoylation |
| title | Critical role of CRAG, a splicing variant of centaurin-γ3/AGAP3, in ELK1-dependent SRF activation at PML bodies |
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