Initiation of Meiotic Development Is Controlled by Three Post-transcriptional Pathways in Caenorhabditis elegans
A major event in germline development is the transition from stem/progenitor cells to entry into meiosis and gametogenesis. This transition requires downregulation of mitotic cell cycle activity and upregulation of processes associated with meiosis. We identify the SCF E3 ubiquitin-ligase complex as...
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| Veröffentlicht in: | Genetics (Austin) 2018-08, Vol.209 (4), p.1197-1224 |
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| creator | Mohammad, Ariz Vanden Broek, Kara Wang, Christopher Daryabeigi, Anahita Jantsch, Verena Hansen, Dave Schedl, Tim |
| description | A major event in germline development is the transition from stem/progenitor cells to entry into meiosis and gametogenesis. This transition requires downregulation of mitotic cell cycle activity and upregulation of processes associated with meiosis. We identify the
SCF
E3 ubiquitin-ligase complex as functioning to downregulate mitotic cell cycle protein levels including cyclin E, WAPL-1, and KNL-2 at meiotic entry and, independently, promoting homologous chromosome pairing as a positive regulator of the CHK-2 kinase. SCF
is thus a novel regulator of meiotic entry, coordinating downregulation of mitotic cell cycle proteins and promoting homolog pairing. We further show that SCF
functions redundantly, in parallel to the previously described GLD-1 and GLD-2 meiotic entry pathways, downstream of and inhibited by GLP-1 Notch signaling, which specifies the stem cell fate. Accordingly,
employs three post-transcriptional pathways, SCF
-mediated protein degradation, GLD-1-mediated translational repression, and GLD-2-mediated translational activation, to control and coordinate the initiation of meiotic development. |
| doi_str_mv | 10.1534/genetics.118.300985 |
| format | Article |
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SCF
E3 ubiquitin-ligase complex as functioning to downregulate mitotic cell cycle protein levels including cyclin E, WAPL-1, and KNL-2 at meiotic entry and, independently, promoting homologous chromosome pairing as a positive regulator of the CHK-2 kinase. SCF
is thus a novel regulator of meiotic entry, coordinating downregulation of mitotic cell cycle proteins and promoting homolog pairing. We further show that SCF
functions redundantly, in parallel to the previously described GLD-1 and GLD-2 meiotic entry pathways, downstream of and inhibited by GLP-1 Notch signaling, which specifies the stem cell fate. Accordingly,
employs three post-transcriptional pathways, SCF
-mediated protein degradation, GLD-1-mediated translational repression, and GLD-2-mediated translational activation, to control and coordinate the initiation of meiotic development.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.118.300985</identifier><identifier>PMID: 29941619</identifier><language>eng</language><publisher>United States: Genetics Society of America</publisher><subject>Animals ; Caenorhabditis elegans ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - physiology ; Caenorhabditis elegans Proteins - genetics ; Cell cycle ; Cell Cycle Proteins - genetics ; Cell fate ; Cells (biology) ; Checkpoint Kinase 2 - genetics ; Chromosomes ; Cycle protein ; Cyclin E ; Drosophila Proteins - genetics ; F-Box Proteins - genetics ; Gametogenesis ; Gene Expression Regulation ; Gene Regulatory Networks ; Genes ; Genetics ; Homology ; Investigations ; Kinases ; Meiosis ; Nematodes ; Polynucleotide Adenylyltransferase - genetics ; Post-transcription ; Progenitor cells ; Protein Biosynthesis ; Proteins ; Proteolysis ; Receptors, Notch - genetics ; RNA polymerase ; Signal Transduction ; Stem cells ; Translation ; Ubiquitin ; Ubiquitin-protein ligase ; Worms</subject><ispartof>Genetics (Austin), 2018-08, Vol.209 (4), p.1197-1224</ispartof><rights>Copyright © 2018 by the Genetics Society of America.</rights><rights>Copyright Genetics Society of America Aug 2018</rights><rights>Copyright © 2018 by the Genetics Society of America 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c433t-965e8a033008e8a3260b10c33a3f9bc30d038953d3a0778fc06277c461aa7acc3</citedby><cites>FETCH-LOGICAL-c433t-965e8a033008e8a3260b10c33a3f9bc30d038953d3a0778fc06277c461aa7acc3</cites><orcidid>0000-0002-1978-682X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,777,781,882,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29941619$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mohammad, Ariz</creatorcontrib><creatorcontrib>Vanden Broek, Kara</creatorcontrib><creatorcontrib>Wang, Christopher</creatorcontrib><creatorcontrib>Daryabeigi, Anahita</creatorcontrib><creatorcontrib>Jantsch, Verena</creatorcontrib><creatorcontrib>Hansen, Dave</creatorcontrib><creatorcontrib>Schedl, Tim</creatorcontrib><title>Initiation of Meiotic Development Is Controlled by Three Post-transcriptional Pathways in Caenorhabditis elegans</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>A major event in germline development is the transition from stem/progenitor cells to entry into meiosis and gametogenesis. This transition requires downregulation of mitotic cell cycle activity and upregulation of processes associated with meiosis. We identify the
SCF
E3 ubiquitin-ligase complex as functioning to downregulate mitotic cell cycle protein levels including cyclin E, WAPL-1, and KNL-2 at meiotic entry and, independently, promoting homologous chromosome pairing as a positive regulator of the CHK-2 kinase. SCF
is thus a novel regulator of meiotic entry, coordinating downregulation of mitotic cell cycle proteins and promoting homolog pairing. We further show that SCF
functions redundantly, in parallel to the previously described GLD-1 and GLD-2 meiotic entry pathways, downstream of and inhibited by GLP-1 Notch signaling, which specifies the stem cell fate. Accordingly,
employs three post-transcriptional pathways, SCF
-mediated protein degradation, GLD-1-mediated translational repression, and GLD-2-mediated translational activation, to control and coordinate the initiation of meiotic development.</description><subject>Animals</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans - physiology</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Cell cycle</subject><subject>Cell Cycle Proteins - genetics</subject><subject>Cell fate</subject><subject>Cells (biology)</subject><subject>Checkpoint Kinase 2 - genetics</subject><subject>Chromosomes</subject><subject>Cycle protein</subject><subject>Cyclin E</subject><subject>Drosophila Proteins - genetics</subject><subject>F-Box Proteins - genetics</subject><subject>Gametogenesis</subject><subject>Gene Expression Regulation</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Genetics</subject><subject>Homology</subject><subject>Investigations</subject><subject>Kinases</subject><subject>Meiosis</subject><subject>Nematodes</subject><subject>Polynucleotide Adenylyltransferase - genetics</subject><subject>Post-transcription</subject><subject>Progenitor cells</subject><subject>Protein Biosynthesis</subject><subject>Proteins</subject><subject>Proteolysis</subject><subject>Receptors, Notch - genetics</subject><subject>RNA polymerase</subject><subject>Signal Transduction</subject><subject>Stem cells</subject><subject>Translation</subject><subject>Ubiquitin</subject><subject>Ubiquitin-protein ligase</subject><subject>Worms</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpdkU9r3DAQxUVpaNK0n6BQBL304o3ksWXrUijbfwsJySE9C1ke7ypoJVfSJuy3r5ZNQtqTBvTmN_PmEfKBswVvoblYo8dsTVpw3i-AMdm3r8gZlw1UtQD--kV9St6mdMcYE7Lt35DTWsqGCy7PyLzyNludbfA0TPQKbShM-g3v0YV5iz7TVaLL4HMMzuFIhz293UREehNSrnLUPplo5wNAO3qj8-ZB7xO1ni41-hA3ehjLhETR4bqI35GTSbuE7x_fc_L7x_fb5a_q8vrnavn1sjINQK6kaLHXDIqvvhRQCzZwZgA0THIwwEYGvWxhBM26rp8ME3XXmUZwrTttDJyTL0fuvBu2OJriJGqn5mi3Ou5V0Fb9--PtRq3DvRJMQF13BfD5ERDDnx2mrLY2GXROewy7pGrWylY0vG6K9NN_0ruwi-UeRcUZrzsO7QEIR5WJIaWI0_MynKlDouopUVUSVcdES9fHlz6ee54ihL_5C6CP</recordid><startdate>20180801</startdate><enddate>20180801</enddate><creator>Mohammad, Ariz</creator><creator>Vanden Broek, Kara</creator><creator>Wang, Christopher</creator><creator>Daryabeigi, Anahita</creator><creator>Jantsch, Verena</creator><creator>Hansen, Dave</creator><creator>Schedl, Tim</creator><general>Genetics Society of America</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>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1978-682X</orcidid></search><sort><creationdate>20180801</creationdate><title>Initiation of Meiotic Development Is Controlled by Three Post-transcriptional Pathways in Caenorhabditis elegans</title><author>Mohammad, Ariz ; Vanden Broek, Kara ; Wang, Christopher ; Daryabeigi, Anahita ; Jantsch, Verena ; Hansen, Dave ; Schedl, Tim</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c433t-965e8a033008e8a3260b10c33a3f9bc30d038953d3a0778fc06277c461aa7acc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Caenorhabditis elegans</topic><topic>Caenorhabditis elegans - genetics</topic><topic>Caenorhabditis elegans - physiology</topic><topic>Caenorhabditis elegans Proteins - genetics</topic><topic>Cell cycle</topic><topic>Cell Cycle Proteins - genetics</topic><topic>Cell fate</topic><topic>Cells (biology)</topic><topic>Checkpoint Kinase 2 - genetics</topic><topic>Chromosomes</topic><topic>Cycle protein</topic><topic>Cyclin E</topic><topic>Drosophila Proteins - genetics</topic><topic>F-Box Proteins - genetics</topic><topic>Gametogenesis</topic><topic>Gene Expression Regulation</topic><topic>Gene Regulatory Networks</topic><topic>Genes</topic><topic>Genetics</topic><topic>Homology</topic><topic>Investigations</topic><topic>Kinases</topic><topic>Meiosis</topic><topic>Nematodes</topic><topic>Polynucleotide Adenylyltransferase - genetics</topic><topic>Post-transcription</topic><topic>Progenitor cells</topic><topic>Protein Biosynthesis</topic><topic>Proteins</topic><topic>Proteolysis</topic><topic>Receptors, Notch - genetics</topic><topic>RNA polymerase</topic><topic>Signal Transduction</topic><topic>Stem cells</topic><topic>Translation</topic><topic>Ubiquitin</topic><topic>Ubiquitin-protein ligase</topic><topic>Worms</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mohammad, Ariz</creatorcontrib><creatorcontrib>Vanden Broek, Kara</creatorcontrib><creatorcontrib>Wang, Christopher</creatorcontrib><creatorcontrib>Daryabeigi, Anahita</creatorcontrib><creatorcontrib>Jantsch, Verena</creatorcontrib><creatorcontrib>Hansen, Dave</creatorcontrib><creatorcontrib>Schedl, Tim</creatorcontrib><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>Docstoc</collection><collection>University Readers</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Agricultural Science Collection</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 Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</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>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</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>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>SciTech Premium Collection</collection><collection>Consumer Health Database (Alumni Edition)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Consumer Health Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</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 China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mohammad, Ariz</au><au>Vanden Broek, Kara</au><au>Wang, Christopher</au><au>Daryabeigi, Anahita</au><au>Jantsch, Verena</au><au>Hansen, Dave</au><au>Schedl, Tim</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Initiation of Meiotic Development Is Controlled by Three Post-transcriptional Pathways in Caenorhabditis elegans</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2018-08-01</date><risdate>2018</risdate><volume>209</volume><issue>4</issue><spage>1197</spage><epage>1224</epage><pages>1197-1224</pages><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><abstract>A major event in germline development is the transition from stem/progenitor cells to entry into meiosis and gametogenesis. This transition requires downregulation of mitotic cell cycle activity and upregulation of processes associated with meiosis. We identify the
SCF
E3 ubiquitin-ligase complex as functioning to downregulate mitotic cell cycle protein levels including cyclin E, WAPL-1, and KNL-2 at meiotic entry and, independently, promoting homologous chromosome pairing as a positive regulator of the CHK-2 kinase. SCF
is thus a novel regulator of meiotic entry, coordinating downregulation of mitotic cell cycle proteins and promoting homolog pairing. We further show that SCF
functions redundantly, in parallel to the previously described GLD-1 and GLD-2 meiotic entry pathways, downstream of and inhibited by GLP-1 Notch signaling, which specifies the stem cell fate. Accordingly,
employs three post-transcriptional pathways, SCF
-mediated protein degradation, GLD-1-mediated translational repression, and GLD-2-mediated translational activation, to control and coordinate the initiation of meiotic development.</abstract><cop>United States</cop><pub>Genetics Society of America</pub><pmid>29941619</pmid><doi>10.1534/genetics.118.300985</doi><tpages>28</tpages><orcidid>https://orcid.org/0000-0002-1978-682X</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection |
| subjects | Animals Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - physiology Caenorhabditis elegans Proteins - genetics Cell cycle Cell Cycle Proteins - genetics Cell fate Cells (biology) Checkpoint Kinase 2 - genetics Chromosomes Cycle protein Cyclin E Drosophila Proteins - genetics F-Box Proteins - genetics Gametogenesis Gene Expression Regulation Gene Regulatory Networks Genes Genetics Homology Investigations Kinases Meiosis Nematodes Polynucleotide Adenylyltransferase - genetics Post-transcription Progenitor cells Protein Biosynthesis Proteins Proteolysis Receptors, Notch - genetics RNA polymerase Signal Transduction Stem cells Translation Ubiquitin Ubiquitin-protein ligase Worms |
| title | Initiation of Meiotic Development Is Controlled by Three Post-transcriptional Pathways in Caenorhabditis elegans |
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