KATNB1 is a master regulator of multiple katanin enzymes in male meiosis and haploid germ cell development
Katanin microtubule-severing enzymes are crucial executers of microtubule regulation. Here, we have created an allelic loss-of-function series of the katanin regulatory B-subunit KATNB1 in mice. We reveal that KATNB1 is the master regulator of all katanin enzymatic A-subunits during mammalian sperma...
Gespeichert in:
| Veröffentlicht in: | Development (Cambridge) 2021-12, Vol.148 (24) |
|---|---|
| Hauptverfasser: | , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | |
|---|---|
| container_issue | 24 |
| container_start_page | |
| container_title | Development (Cambridge) |
| container_volume | 148 |
| creator | Dunleavy, Jessica E M O'Connor, Anne E Okuda, Hidenobu Merriner, D Jo O'Bryan, Moira K |
| description | Katanin microtubule-severing enzymes are crucial executers of microtubule regulation. Here, we have created an allelic loss-of-function series of the katanin regulatory B-subunit KATNB1 in mice. We reveal that KATNB1 is the master regulator of all katanin enzymatic A-subunits during mammalian spermatogenesis, wherein it is required to maintain katanin A-subunit abundance. Our data shows that complete loss of KATNB1 from germ cells is incompatible with sperm production, and we reveal multiple new spermatogenesis functions for KATNB1, including essential roles in male meiosis, acrosome formation, sperm tail assembly, regulation of both the Sertoli and germ cell cytoskeletons during sperm nuclear remodelling, and maintenance of seminiferous epithelium integrity. Collectively, our findings reveal that katanins are able to differentially regulate almost all key microtubule-based structures during mammalian male germ cell development, through the complexing of one master controller, KATNB1, with a 'toolbox' of neofunctionalised katanin A-subunits. |
| doi_str_mv | 10.1242/dev.199922 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2604020874</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2604020874</sourcerecordid><originalsourceid>FETCH-LOGICAL-c323t-1475e056fd5ba9dad3c230ff962dbe4b6c1c1bb07ac89d630c8e81a1e415e4e73</originalsourceid><addsrcrecordid>eNo9kMtOwzAQRS0EglLY8AHIS4SU4lfieFkqXqKCTVlHjj0pKXEc7ASpfD2pCqxmNHPm6s5F6IKSGWWC3Vj4mlGlFGMHaEKFlImiTB2iCVEpScYNPUGnMW4IITyT8hidcJEzJmk-QZvn-erlluI6Yo2djj0EHGA9NLr3AfsKu6Hp664B_KF73dYthvZ76yDisXV6nDuofdydtxa_667xtcVrCA4baBo8eoPGdw7a_gwdVbqJcP5bp-jt_m61eEyWrw9Pi_kyMZzxPhkfSIGkWWXTUiurLTeMk6pSGbMliDIz1NCyJFKbXNmME5NDTjUFQVMQIPkUXe11u-A_B4h94eq4M6Nb8EMsWEYEYSSXYkSv96gJPsYAVdGF2umwLSgpdtkWo_9in-0IX_7qDqUD-4_-hcl_ANT0dag</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2604020874</pqid></control><display><type>article</type><title>KATNB1 is a master regulator of multiple katanin enzymes in male meiosis and haploid germ cell development</title><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Alma/SFX Local Collection</source><source>Company of Biologists</source><creator>Dunleavy, Jessica E M ; O'Connor, Anne E ; Okuda, Hidenobu ; Merriner, D Jo ; O'Bryan, Moira K</creator><creatorcontrib>Dunleavy, Jessica E M ; O'Connor, Anne E ; Okuda, Hidenobu ; Merriner, D Jo ; O'Bryan, Moira K</creatorcontrib><description>Katanin microtubule-severing enzymes are crucial executers of microtubule regulation. Here, we have created an allelic loss-of-function series of the katanin regulatory B-subunit KATNB1 in mice. We reveal that KATNB1 is the master regulator of all katanin enzymatic A-subunits during mammalian spermatogenesis, wherein it is required to maintain katanin A-subunit abundance. Our data shows that complete loss of KATNB1 from germ cells is incompatible with sperm production, and we reveal multiple new spermatogenesis functions for KATNB1, including essential roles in male meiosis, acrosome formation, sperm tail assembly, regulation of both the Sertoli and germ cell cytoskeletons during sperm nuclear remodelling, and maintenance of seminiferous epithelium integrity. Collectively, our findings reveal that katanins are able to differentially regulate almost all key microtubule-based structures during mammalian male germ cell development, through the complexing of one master controller, KATNB1, with a 'toolbox' of neofunctionalised katanin A-subunits.</description><identifier>ISSN: 0950-1991</identifier><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.199922</identifier><identifier>PMID: 34822718</identifier><language>eng</language><publisher>England</publisher><subject>Acrosome - metabolism ; Animals ; Cytoskeleton - genetics ; Germ Cells - cytology ; Germ Cells - growth & development ; Haploidy ; Katanin - genetics ; Male ; Meiosis - genetics ; Mice ; Microtubules - genetics ; Sertoli Cells - cytology ; Sperm Tail - metabolism ; Spermatogenesis - genetics ; Spermatozoa - growth & development ; Spermatozoa - metabolism</subject><ispartof>Development (Cambridge), 2021-12, Vol.148 (24)</ispartof><rights>2021. Published by The Company of Biologists Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c323t-1475e056fd5ba9dad3c230ff962dbe4b6c1c1bb07ac89d630c8e81a1e415e4e73</citedby><cites>FETCH-LOGICAL-c323t-1475e056fd5ba9dad3c230ff962dbe4b6c1c1bb07ac89d630c8e81a1e415e4e73</cites><orcidid>0000-0003-2009-0165 ; 0000-0001-7298-4940 ; 0000-0001-9334-4256 ; 0000-0003-3975-3205 ; 0000-0001-5953-2421</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,3665,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34822718$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dunleavy, Jessica E M</creatorcontrib><creatorcontrib>O'Connor, Anne E</creatorcontrib><creatorcontrib>Okuda, Hidenobu</creatorcontrib><creatorcontrib>Merriner, D Jo</creatorcontrib><creatorcontrib>O'Bryan, Moira K</creatorcontrib><title>KATNB1 is a master regulator of multiple katanin enzymes in male meiosis and haploid germ cell development</title><title>Development (Cambridge)</title><addtitle>Development</addtitle><description>Katanin microtubule-severing enzymes are crucial executers of microtubule regulation. Here, we have created an allelic loss-of-function series of the katanin regulatory B-subunit KATNB1 in mice. We reveal that KATNB1 is the master regulator of all katanin enzymatic A-subunits during mammalian spermatogenesis, wherein it is required to maintain katanin A-subunit abundance. Our data shows that complete loss of KATNB1 from germ cells is incompatible with sperm production, and we reveal multiple new spermatogenesis functions for KATNB1, including essential roles in male meiosis, acrosome formation, sperm tail assembly, regulation of both the Sertoli and germ cell cytoskeletons during sperm nuclear remodelling, and maintenance of seminiferous epithelium integrity. Collectively, our findings reveal that katanins are able to differentially regulate almost all key microtubule-based structures during mammalian male germ cell development, through the complexing of one master controller, KATNB1, with a 'toolbox' of neofunctionalised katanin A-subunits.</description><subject>Acrosome - metabolism</subject><subject>Animals</subject><subject>Cytoskeleton - genetics</subject><subject>Germ Cells - cytology</subject><subject>Germ Cells - growth & development</subject><subject>Haploidy</subject><subject>Katanin - genetics</subject><subject>Male</subject><subject>Meiosis - genetics</subject><subject>Mice</subject><subject>Microtubules - genetics</subject><subject>Sertoli Cells - cytology</subject><subject>Sperm Tail - metabolism</subject><subject>Spermatogenesis - genetics</subject><subject>Spermatozoa - growth & development</subject><subject>Spermatozoa - metabolism</subject><issn>0950-1991</issn><issn>1477-9129</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kMtOwzAQRS0EglLY8AHIS4SU4lfieFkqXqKCTVlHjj0pKXEc7ASpfD2pCqxmNHPm6s5F6IKSGWWC3Vj4mlGlFGMHaEKFlImiTB2iCVEpScYNPUGnMW4IITyT8hidcJEzJmk-QZvn-erlluI6Yo2djj0EHGA9NLr3AfsKu6Hp664B_KF73dYthvZ76yDisXV6nDuofdydtxa_667xtcVrCA4baBo8eoPGdw7a_gwdVbqJcP5bp-jt_m61eEyWrw9Pi_kyMZzxPhkfSIGkWWXTUiurLTeMk6pSGbMliDIz1NCyJFKbXNmME5NDTjUFQVMQIPkUXe11u-A_B4h94eq4M6Nb8EMsWEYEYSSXYkSv96gJPsYAVdGF2umwLSgpdtkWo_9in-0IX_7qDqUD-4_-hcl_ANT0dag</recordid><startdate>20211215</startdate><enddate>20211215</enddate><creator>Dunleavy, Jessica E M</creator><creator>O'Connor, Anne E</creator><creator>Okuda, Hidenobu</creator><creator>Merriner, D Jo</creator><creator>O'Bryan, Moira K</creator><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><orcidid>https://orcid.org/0000-0003-2009-0165</orcidid><orcidid>https://orcid.org/0000-0001-7298-4940</orcidid><orcidid>https://orcid.org/0000-0001-9334-4256</orcidid><orcidid>https://orcid.org/0000-0003-3975-3205</orcidid><orcidid>https://orcid.org/0000-0001-5953-2421</orcidid></search><sort><creationdate>20211215</creationdate><title>KATNB1 is a master regulator of multiple katanin enzymes in male meiosis and haploid germ cell development</title><author>Dunleavy, Jessica E M ; O'Connor, Anne E ; Okuda, Hidenobu ; Merriner, D Jo ; O'Bryan, Moira K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c323t-1475e056fd5ba9dad3c230ff962dbe4b6c1c1bb07ac89d630c8e81a1e415e4e73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Acrosome - metabolism</topic><topic>Animals</topic><topic>Cytoskeleton - genetics</topic><topic>Germ Cells - cytology</topic><topic>Germ Cells - growth & development</topic><topic>Haploidy</topic><topic>Katanin - genetics</topic><topic>Male</topic><topic>Meiosis - genetics</topic><topic>Mice</topic><topic>Microtubules - genetics</topic><topic>Sertoli Cells - cytology</topic><topic>Sperm Tail - metabolism</topic><topic>Spermatogenesis - genetics</topic><topic>Spermatozoa - growth & development</topic><topic>Spermatozoa - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dunleavy, Jessica E M</creatorcontrib><creatorcontrib>O'Connor, Anne E</creatorcontrib><creatorcontrib>Okuda, Hidenobu</creatorcontrib><creatorcontrib>Merriner, D Jo</creatorcontrib><creatorcontrib>O'Bryan, Moira K</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><jtitle>Development (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dunleavy, Jessica E M</au><au>O'Connor, Anne E</au><au>Okuda, Hidenobu</au><au>Merriner, D Jo</au><au>O'Bryan, Moira K</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>KATNB1 is a master regulator of multiple katanin enzymes in male meiosis and haploid germ cell development</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2021-12-15</date><risdate>2021</risdate><volume>148</volume><issue>24</issue><issn>0950-1991</issn><eissn>1477-9129</eissn><abstract>Katanin microtubule-severing enzymes are crucial executers of microtubule regulation. Here, we have created an allelic loss-of-function series of the katanin regulatory B-subunit KATNB1 in mice. We reveal that KATNB1 is the master regulator of all katanin enzymatic A-subunits during mammalian spermatogenesis, wherein it is required to maintain katanin A-subunit abundance. Our data shows that complete loss of KATNB1 from germ cells is incompatible with sperm production, and we reveal multiple new spermatogenesis functions for KATNB1, including essential roles in male meiosis, acrosome formation, sperm tail assembly, regulation of both the Sertoli and germ cell cytoskeletons during sperm nuclear remodelling, and maintenance of seminiferous epithelium integrity. Collectively, our findings reveal that katanins are able to differentially regulate almost all key microtubule-based structures during mammalian male germ cell development, through the complexing of one master controller, KATNB1, with a 'toolbox' of neofunctionalised katanin A-subunits.</abstract><cop>England</cop><pmid>34822718</pmid><doi>10.1242/dev.199922</doi><orcidid>https://orcid.org/0000-0003-2009-0165</orcidid><orcidid>https://orcid.org/0000-0001-7298-4940</orcidid><orcidid>https://orcid.org/0000-0001-9334-4256</orcidid><orcidid>https://orcid.org/0000-0003-3975-3205</orcidid><orcidid>https://orcid.org/0000-0001-5953-2421</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0950-1991 |
| ispartof | Development (Cambridge), 2021-12, Vol.148 (24) |
| issn | 0950-1991 1477-9129 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_2604020874 |
| source | MEDLINE; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection; Company of Biologists |
| subjects | Acrosome - metabolism Animals Cytoskeleton - genetics Germ Cells - cytology Germ Cells - growth & development Haploidy Katanin - genetics Male Meiosis - genetics Mice Microtubules - genetics Sertoli Cells - cytology Sperm Tail - metabolism Spermatogenesis - genetics Spermatozoa - growth & development Spermatozoa - metabolism |
| title | KATNB1 is a master regulator of multiple katanin enzymes in male meiosis and haploid germ cell development |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-17T12%3A09%3A20IST&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=KATNB1%20is%20a%20master%20regulator%20of%20multiple%20katanin%20enzymes%20in%20male%20meiosis%20and%20haploid%20germ%20cell%20development&rft.jtitle=Development%20(Cambridge)&rft.au=Dunleavy,%20Jessica%20E%20M&rft.date=2021-12-15&rft.volume=148&rft.issue=24&rft.issn=0950-1991&rft.eissn=1477-9129&rft_id=info:doi/10.1242/dev.199922&rft_dat=%3Cproquest_cross%3E2604020874%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=2604020874&rft_id=info:pmid/34822718&rfr_iscdi=true |