Activation of ADF/cofilin by phosphorylation-regulated Slingshot phosphatase is required for the meiotic spindle assembly in Xenopus laevis oocytes
We identify Xenopus ADF/cofilin (XAC) and its activator, Slingshot phosphatase (XSSH), as key regulators of actin dynamics essential for spindle microtubule assembly during Xenopus oocyte maturation. Phosphorylation of XSSH at multiple sites within the tail domain occurs just after germinal vesicle...
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| Veröffentlicht in: | Molecular biology of the cell 2013-06, Vol.24 (12), p.1933-1946 |
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| container_title | Molecular biology of the cell |
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| creator | Iwase, Shohei Sato, Ryuhei De Bock, Pieter-Jan Gevaert, Kris Fujiki, Saburo Tawada, Toshinobu Kuchitsu, Miyako Yamagishi, Yuka Ono, Shoichiro Abe, Hiroshi |
| description | We identify Xenopus ADF/cofilin (XAC) and its activator, Slingshot phosphatase (XSSH), as key regulators of actin dynamics essential for spindle microtubule assembly during Xenopus oocyte maturation. Phosphorylation of XSSH at multiple sites within the tail domain occurs just after germinal vesicle breakdown (GVBD) and is accompanied by dephosphorylation of XAC, which was mostly phosphorylated in immature oocytes. This XAC dephosphorylation after GVBD is completely suppressed by latrunculin B, an actin monomer-sequestering drug. On the other hand, jasplakinolide, an F-actin-stabilizing drug, induces dephosphorylation of XAC. Effects of latrunculin B and jasplakinolide are reconstituted in cytostatic factor-arrested extracts (CSF extracts), and XAC dephosphorylation is abolished by depletion of XSSH from CSF extracts, suggesting that XSSH functions as an actin filament sensor to facilitate actin filament dynamics via XAC activation. Injection of anti-XSSH antibody, which blocks full phosphorylation of XSSH after GVBD, inhibits both meiotic spindle formation and XAC dephosphorylation. Coinjection of constitutively active XAC with the antibody suppresses this phenotype. Treatment of oocytes with jasplakinolide also impairs spindle formation. These results strongly suggest that elevation of actin dynamics by XAC activation through XSSH phosphorylation is required for meiotic spindle assembly in Xenopus laevis. |
| doi_str_mv | 10.1091/mbc.E12-12-0851 |
| format | Article |
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Phosphorylation of XSSH at multiple sites within the tail domain occurs just after germinal vesicle breakdown (GVBD) and is accompanied by dephosphorylation of XAC, which was mostly phosphorylated in immature oocytes. This XAC dephosphorylation after GVBD is completely suppressed by latrunculin B, an actin monomer-sequestering drug. On the other hand, jasplakinolide, an F-actin-stabilizing drug, induces dephosphorylation of XAC. Effects of latrunculin B and jasplakinolide are reconstituted in cytostatic factor-arrested extracts (CSF extracts), and XAC dephosphorylation is abolished by depletion of XSSH from CSF extracts, suggesting that XSSH functions as an actin filament sensor to facilitate actin filament dynamics via XAC activation. Injection of anti-XSSH antibody, which blocks full phosphorylation of XSSH after GVBD, inhibits both meiotic spindle formation and XAC dephosphorylation. Coinjection of constitutively active XAC with the antibody suppresses this phenotype. Treatment of oocytes with jasplakinolide also impairs spindle formation. These results strongly suggest that elevation of actin dynamics by XAC activation through XSSH phosphorylation is required for meiotic spindle assembly in Xenopus laevis.</description><identifier>ISSN: 1059-1524</identifier><identifier>EISSN: 1939-4586</identifier><identifier>DOI: 10.1091/mbc.E12-12-0851</identifier><identifier>PMID: 23615437</identifier><language>eng</language><publisher>United States: The American Society for Cell Biology</publisher><subject>Actin Cytoskeleton - drug effects ; Actin Cytoskeleton - metabolism ; Actin Depolymerizing Factors - genetics ; Actin Depolymerizing Factors - metabolism ; Actins - metabolism ; Animals ; Binding Sites - genetics ; Bridged Bicyclo Compounds, Heterocyclic - pharmacology ; Depsipeptides - pharmacology ; Electrophoresis, Polyacrylamide Gel ; Female ; Immunoblotting ; Meiosis ; Microscopy, Fluorescence ; Mutation ; Oocytes - drug effects ; Oocytes - metabolism ; Phosphoprotein Phosphatases - genetics ; Phosphoprotein Phosphatases - metabolism ; Phosphorylation - drug effects ; Spindle Apparatus - metabolism ; Thiazolidines - pharmacology ; Xenopus laevis - genetics ; Xenopus laevis - metabolism ; Xenopus Proteins - genetics ; Xenopus Proteins - metabolism</subject><ispartof>Molecular biology of the cell, 2013-06, Vol.24 (12), p.1933-1946</ispartof><rights>2013 Iwase This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License ( ). 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c352t-2598e3c26be094e87f2459ce4e41d93eb9b4498baf55ebf4c9e63181d399c5f63</citedby><cites>FETCH-LOGICAL-c352t-2598e3c26be094e87f2459ce4e41d93eb9b4498baf55ebf4c9e63181d399c5f63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3681698/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3681698/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,725,778,782,883,27907,27908,53774,53776</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23615437$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Chang, Fred</contributor><creatorcontrib>Iwase, Shohei</creatorcontrib><creatorcontrib>Sato, Ryuhei</creatorcontrib><creatorcontrib>De Bock, Pieter-Jan</creatorcontrib><creatorcontrib>Gevaert, Kris</creatorcontrib><creatorcontrib>Fujiki, Saburo</creatorcontrib><creatorcontrib>Tawada, Toshinobu</creatorcontrib><creatorcontrib>Kuchitsu, Miyako</creatorcontrib><creatorcontrib>Yamagishi, Yuka</creatorcontrib><creatorcontrib>Ono, Shoichiro</creatorcontrib><creatorcontrib>Abe, Hiroshi</creatorcontrib><title>Activation of ADF/cofilin by phosphorylation-regulated Slingshot phosphatase is required for the meiotic spindle assembly in Xenopus laevis oocytes</title><title>Molecular biology of the cell</title><addtitle>Mol Biol Cell</addtitle><description>We identify Xenopus ADF/cofilin (XAC) and its activator, Slingshot phosphatase (XSSH), as key regulators of actin dynamics essential for spindle microtubule assembly during Xenopus oocyte maturation. Phosphorylation of XSSH at multiple sites within the tail domain occurs just after germinal vesicle breakdown (GVBD) and is accompanied by dephosphorylation of XAC, which was mostly phosphorylated in immature oocytes. This XAC dephosphorylation after GVBD is completely suppressed by latrunculin B, an actin monomer-sequestering drug. On the other hand, jasplakinolide, an F-actin-stabilizing drug, induces dephosphorylation of XAC. Effects of latrunculin B and jasplakinolide are reconstituted in cytostatic factor-arrested extracts (CSF extracts), and XAC dephosphorylation is abolished by depletion of XSSH from CSF extracts, suggesting that XSSH functions as an actin filament sensor to facilitate actin filament dynamics via XAC activation. Injection of anti-XSSH antibody, which blocks full phosphorylation of XSSH after GVBD, inhibits both meiotic spindle formation and XAC dephosphorylation. Coinjection of constitutively active XAC with the antibody suppresses this phenotype. Treatment of oocytes with jasplakinolide also impairs spindle formation. These results strongly suggest that elevation of actin dynamics by XAC activation through XSSH phosphorylation is required for meiotic spindle assembly in Xenopus laevis.</description><subject>Actin Cytoskeleton - drug effects</subject><subject>Actin Cytoskeleton - metabolism</subject><subject>Actin Depolymerizing Factors - genetics</subject><subject>Actin Depolymerizing Factors - metabolism</subject><subject>Actins - metabolism</subject><subject>Animals</subject><subject>Binding Sites - genetics</subject><subject>Bridged Bicyclo Compounds, Heterocyclic - pharmacology</subject><subject>Depsipeptides - pharmacology</subject><subject>Electrophoresis, Polyacrylamide Gel</subject><subject>Female</subject><subject>Immunoblotting</subject><subject>Meiosis</subject><subject>Microscopy, Fluorescence</subject><subject>Mutation</subject><subject>Oocytes - drug effects</subject><subject>Oocytes - metabolism</subject><subject>Phosphoprotein Phosphatases - genetics</subject><subject>Phosphoprotein Phosphatases - metabolism</subject><subject>Phosphorylation - drug effects</subject><subject>Spindle Apparatus - metabolism</subject><subject>Thiazolidines - pharmacology</subject><subject>Xenopus laevis - genetics</subject><subject>Xenopus laevis - metabolism</subject><subject>Xenopus Proteins - genetics</subject><subject>Xenopus Proteins - metabolism</subject><issn>1059-1524</issn><issn>1939-4586</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkU2LFDEQhhtR3HX17E1y9NI7Sedjkosw7IcKCx5U8BaSdGUm0t3pTdID_Tv8w2bdcVGoogrqqbcK3qZ5S_AlwYpsRusub0jX1sCSk2fNOVFUtYxL8bz2mKuW8I6dNa9y_okxYUxsXzZnHRWEM7o9b37tXAlHU0KcUPRod327cdGHIUzIrmg-xFwzrcMfok2wX2oLPfpaiX0-xHJiTDEZUMgowf0SUiV8TKgcAI0QYgkO5TlM_QDI5AyjHVZUT_yAKc5LRoOBY92N0a0F8uvmhTdDhjenetF8v735dvWpvfvy8fPV7q51lHel7biSQF0nLGDFQG59x7hywICRXlGwyjKmpDWec7CeOQWCEkl6qpTjXtCL5sOj7rzYEXoHU0lm0HMKo0mrjibo_ydTOOh9PGoqJBFKVoH3J4EU7xfIRY8hOxgGM0FcsiZUbKVkBHcV3TyiLsWcE_inMwTrByt1tVID6XSNByvrxrt_v3vi_3pHfwNODZ_p</recordid><startdate>20130615</startdate><enddate>20130615</enddate><creator>Iwase, Shohei</creator><creator>Sato, Ryuhei</creator><creator>De Bock, Pieter-Jan</creator><creator>Gevaert, Kris</creator><creator>Fujiki, Saburo</creator><creator>Tawada, Toshinobu</creator><creator>Kuchitsu, Miyako</creator><creator>Yamagishi, Yuka</creator><creator>Ono, Shoichiro</creator><creator>Abe, Hiroshi</creator><general>The American Society for Cell Biology</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20130615</creationdate><title>Activation of ADF/cofilin by phosphorylation-regulated Slingshot phosphatase is required for the meiotic spindle assembly in Xenopus laevis oocytes</title><author>Iwase, Shohei ; Sato, Ryuhei ; De Bock, Pieter-Jan ; Gevaert, Kris ; Fujiki, Saburo ; Tawada, Toshinobu ; Kuchitsu, Miyako ; Yamagishi, Yuka ; Ono, Shoichiro ; Abe, Hiroshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c352t-2598e3c26be094e87f2459ce4e41d93eb9b4498baf55ebf4c9e63181d399c5f63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Actin Cytoskeleton - drug effects</topic><topic>Actin Cytoskeleton - metabolism</topic><topic>Actin Depolymerizing Factors - genetics</topic><topic>Actin Depolymerizing Factors - metabolism</topic><topic>Actins - metabolism</topic><topic>Animals</topic><topic>Binding Sites - genetics</topic><topic>Bridged Bicyclo Compounds, Heterocyclic - pharmacology</topic><topic>Depsipeptides - pharmacology</topic><topic>Electrophoresis, Polyacrylamide Gel</topic><topic>Female</topic><topic>Immunoblotting</topic><topic>Meiosis</topic><topic>Microscopy, Fluorescence</topic><topic>Mutation</topic><topic>Oocytes - drug effects</topic><topic>Oocytes - metabolism</topic><topic>Phosphoprotein Phosphatases - genetics</topic><topic>Phosphoprotein Phosphatases - metabolism</topic><topic>Phosphorylation - drug effects</topic><topic>Spindle Apparatus - metabolism</topic><topic>Thiazolidines - pharmacology</topic><topic>Xenopus laevis - genetics</topic><topic>Xenopus laevis - metabolism</topic><topic>Xenopus Proteins - genetics</topic><topic>Xenopus Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Iwase, Shohei</creatorcontrib><creatorcontrib>Sato, Ryuhei</creatorcontrib><creatorcontrib>De Bock, Pieter-Jan</creatorcontrib><creatorcontrib>Gevaert, Kris</creatorcontrib><creatorcontrib>Fujiki, Saburo</creatorcontrib><creatorcontrib>Tawada, Toshinobu</creatorcontrib><creatorcontrib>Kuchitsu, Miyako</creatorcontrib><creatorcontrib>Yamagishi, Yuka</creatorcontrib><creatorcontrib>Ono, Shoichiro</creatorcontrib><creatorcontrib>Abe, Hiroshi</creatorcontrib><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>Molecular biology of the cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Iwase, Shohei</au><au>Sato, Ryuhei</au><au>De Bock, Pieter-Jan</au><au>Gevaert, Kris</au><au>Fujiki, Saburo</au><au>Tawada, Toshinobu</au><au>Kuchitsu, Miyako</au><au>Yamagishi, Yuka</au><au>Ono, Shoichiro</au><au>Abe, Hiroshi</au><au>Chang, Fred</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Activation of ADF/cofilin by phosphorylation-regulated Slingshot phosphatase is required for the meiotic spindle assembly in Xenopus laevis oocytes</atitle><jtitle>Molecular biology of the cell</jtitle><addtitle>Mol Biol Cell</addtitle><date>2013-06-15</date><risdate>2013</risdate><volume>24</volume><issue>12</issue><spage>1933</spage><epage>1946</epage><pages>1933-1946</pages><issn>1059-1524</issn><eissn>1939-4586</eissn><abstract>We identify Xenopus ADF/cofilin (XAC) and its activator, Slingshot phosphatase (XSSH), as key regulators of actin dynamics essential for spindle microtubule assembly during Xenopus oocyte maturation. Phosphorylation of XSSH at multiple sites within the tail domain occurs just after germinal vesicle breakdown (GVBD) and is accompanied by dephosphorylation of XAC, which was mostly phosphorylated in immature oocytes. This XAC dephosphorylation after GVBD is completely suppressed by latrunculin B, an actin monomer-sequestering drug. On the other hand, jasplakinolide, an F-actin-stabilizing drug, induces dephosphorylation of XAC. Effects of latrunculin B and jasplakinolide are reconstituted in cytostatic factor-arrested extracts (CSF extracts), and XAC dephosphorylation is abolished by depletion of XSSH from CSF extracts, suggesting that XSSH functions as an actin filament sensor to facilitate actin filament dynamics via XAC activation. Injection of anti-XSSH antibody, which blocks full phosphorylation of XSSH after GVBD, inhibits both meiotic spindle formation and XAC dephosphorylation. Coinjection of constitutively active XAC with the antibody suppresses this phenotype. Treatment of oocytes with jasplakinolide also impairs spindle formation. These results strongly suggest that elevation of actin dynamics by XAC activation through XSSH phosphorylation is required for meiotic spindle assembly in Xenopus laevis.</abstract><cop>United States</cop><pub>The American Society for Cell Biology</pub><pmid>23615437</pmid><doi>10.1091/mbc.E12-12-0851</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Actin Cytoskeleton - drug effects Actin Cytoskeleton - metabolism Actin Depolymerizing Factors - genetics Actin Depolymerizing Factors - metabolism Actins - metabolism Animals Binding Sites - genetics Bridged Bicyclo Compounds, Heterocyclic - pharmacology Depsipeptides - pharmacology Electrophoresis, Polyacrylamide Gel Female Immunoblotting Meiosis Microscopy, Fluorescence Mutation Oocytes - drug effects Oocytes - metabolism Phosphoprotein Phosphatases - genetics Phosphoprotein Phosphatases - metabolism Phosphorylation - drug effects Spindle Apparatus - metabolism Thiazolidines - pharmacology Xenopus laevis - genetics Xenopus laevis - metabolism Xenopus Proteins - genetics Xenopus Proteins - metabolism |
| title | Activation of ADF/cofilin by phosphorylation-regulated Slingshot phosphatase is required for the meiotic spindle assembly in Xenopus laevis oocytes |
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